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Parasitism, Host Immune Function, and Sexual Selection
Abstract
Parasite-mediated sexual selection may arise as a consequence of 1) females avoiding mates with directly transmitted parasites, 2) females choosing less-parasitized males that provide parental care of superior quality, or 3) females choosing males with few parasites in order to obtain genes for parasite resistance in their offspring. Studies of specific host-parasite systems and comparative analyses have revealed both supportive and conflicting evidence for these hypotheses. A meta-analysis of the available evidence revealed a negative relationship between parasite load and the expression of male secondary sexual characters. Experimental studies yielded more strongly negative relationships than observations did, and the relationships were more strongly negative for ectoparasites than for endoparasites. There was no significant difference in the magnitude of the negative effect for species with and without male parental care, or between behavioral and morphological secondary sexual characters. There was a significant difference between studies based on host immune function and those based on parasite loads, with stronger effects for measures of immune function, suggesting that the many negative results from previous analyses of parasite-mediated sexual selection may be explained because relatively benign parasites were studied. The multivariate analyses demonstrating strong effect sizes of immune function in relation to the expression of secondary sexual characters, and for species with male parental care as compared to those without, suggest that parasite resistance may be a general determinant of parasite-mediated sexual selection.
... Parasites reduce the ability of their host to perform fitness-enhancing functions, such as attracting a mate (Hamilton and Zuk 1982;McLennan and Brooks 1991;Møller et al. 1999), delivering oxygen to muscle tissue (Dunlap and Mathies 1993), sprinting (Garrido and Pérez-Mellado 2014), gaining mass (Klukowski and Nelson 2001), and defending a territory (Rau 1984;Schall and Dearing 1987;Maksimowich and Mathis 2000). But what determines which individuals in a host population acquire parasites, the intensity of those parasites on their host, and where on their hosts the parasites settle? ...
... Competitive social behaviors often involve the display of sexual characters that are informative to conspecifics precisely because they are costly to produce and maintain (Zahavi 1975). Because parasites are almost ubiquitous in nature, a primary function of sexual displays may be to demonstrate the signaler's ability to efficiently handle common infections (Hamilton and Zuk 1982;reviews in Clayton 1991;Møller et al. 1999). Over evolutionary time, sexual selection translates the lesions and anemia produced by parasites into hosts bearing colorful badges and other expensive advertisements of genetic quality (Clayton 1991), and the presence of an elaborate display may therefore indicate that a species is under selection pressure from parasites (Hamilton and Zuk 1982). ...
... Over evolutionary time, sexual selection translates the lesions and anemia produced by parasites into hosts bearing colorful badges and other expensive advertisements of genetic quality (Clayton 1991), and the presence of an elaborate display may therefore indicate that a species is under selection pressure from parasites (Hamilton and Zuk 1982). Although numerous studies have found that the quality of the badge displayed to conspecifics reflects the parasite infection status of the bearer (e.g., Ressel and Schall 1989;Torio 1992;Megía-Palma et al. 2016a), behavior may be an even more sensitive indicator of the magnitude of the fitness costs incurred by infection (Folstad and Karter 1992, but see Møller et al. 1999). ...
Parasites often have profound effects on the survival and evolution of their hosts, and hence on the structure and health of entire ecosystems. Yet basic questions, such as the degree of virulence of a given parasite on its host, and factors influencing which hosts in a population are at the greatest risk of infection, are vexingly difficult to resolve. The western blacklegged tick-western fence lizard (Ixodes pacificus-Sceloporus occidentalis) system is important, primarily because I. pacificus, a vector of the Lyme disease spirochete Borrelia burgdorferi, is dependent on S. occidentalis for blood meals in its subadult stages, and this lizard possesses an innate immune response that removes the Lyme disease pathogen from attached ticks. My study focused on two aspects of the I. pacificus-S. occidentalis interaction. In Chapter 1, I investigated factors correlating with the intensity of I. pacificus infestations on S. occidentalis. Infection intensity (parasites per host) is often highly variable within a host population, though certain individuals, such as males, tend to be more heavily infected. Previous work in the I. pacificus-S. occidentalis system suggests that differences in behavior, such as the frequency of territorial patrols, may contribute to variation in tick intensity among lizards. I therefore hypothesized that lizard traits that correlate with dominance would also correlate with infestation intensity. Specifically, I predicted that larger and more colorful males would have higher infestation intensities than less impressive animals. In this chapter, I also focused on site selection by ticks infesting S. occidentalis. Skin folds on the necks of these lizards (nuchal pockets) may function to divert ectoparasites away from eyes, ears, and other potentially vulnerable structures. I therefore also looked for factors correlating with tick attachment in these pockets. I sampled ticks on adult male S. occidentalis in the spring and summer, which is the seasonal peak for both S. occidentalis territorial behavior and subadult I. pacificus abundance. After determining the site of infestation and intensity of ticks on these lizards, I re-infested lizards with laboratory-reared I. pacificus larvae, and again quantified tick intensity and attachment location. Contrary to expectation, no host traits correlated with tick intensity among ticks naturally infesting lizards, and lab-reared larval intensity was negatively correlated with lizard body size. As expected, ticks acquired by lizards naturally concentrated inside nuchal pockets, and I also observed this site preference among ticks in lab-based experimental infestations. Although the general pattern, lab-reared ticks were more varied in the sites on which they fed. There was a negative correlation between infestation intensity and the proportion of ticks attached in nuchal pockets. Unsurprisingly, the most reliable predictor of tick intensity and site selection was the season. In Chapter 2, I explored how tick attachment affects male S. occidentalis contest behavior. I. pacificus infestation has been shown to have negative physiological impacts on S. occidentalis, but mechanisms linking physiological changes to ultimate fitness consequences have been largely underexplored. I hypothesized that tick infestation reduces male S. occidentalis fighting ability by reducing O2 carrying capacity, or by obstructing or damaging vulnerable structures on their hosts. I held fifty half-hour trials between pairs of size- and ventral badge-matched male S. occidentalis, with one male in each pair infested with lab-reared I. pacificus larvae. I found that tick infestation negatively correlated with aggressive behavior in these staged contests. In support of reduced O2 capacity as the mechanism of reduced aggression, my ecologically relevant infestation intensities seemed to cause significant declines in hematocrit among experimentally infested lizards relative to controls. However, the site at which ticks attached did not significantly correlate with the aggressiveness of their lizard hosts. This is one of only a handful of studies to address the direct effect of I. pacificus on S. occidentalis. My study demonstrates that tick infestation can be detrimental to the fitness of their lizard hosts even without the transmission of pathogens. This insight may prove informative in future work on the ecology of I. pacificus-borne diseases in the western United States. This study is also one of only a few to use parasite infection to induce an asymmetry in fighting ability in intrasexual contests.
... Hamilton and Zuk further suggested that through mating with these resistant males, females have offspring with geneticallydetermined resistance to local parasite strains and, because of the co-adaptational cycles between hosts and parasites, heritable genetic variation in dynamic ornaments is maintained (Hamilton and Zuk 1982). Since it was proposed, the predictions made by the Hamilton-Zuk hypothesis have been tested many times across animal taxa, but the evidence remains mixed (reviewed by Hamilton and Poulin 1997;Møller et al. 1999;Weaver et al. 2018). ...
... e ab e f a ab a a e a a e e a ce than his dynamic traits. Because, by definition, they do not reflect recent changes in male condition, static ornaments are less sensitive to stochastic factors a d a e c e ef ec a a e ge e c a (Hill et al. 1999;Møller et al. 1999). In particular, static ornaments are not vulnerable to e e introduced by parasite distribution in natural conditions: given the typically aggregated distribution of parasites among their hosts (Shaw and Dobson 1995), relatively few males in any population will be infected and, among these, infection loads may rarely reach levels that affect dynamic male ornaments (Poulin and Vickery 1993). ...
... .e. f c a g a e , arises during the development of morphological structures, and tends to be highest in secondary sexual traits (Møller et al. 1999;Palmer and Strobeck 1986;Sheridan and Pomiankowski 1997b). Fluctuating asymmetry in secondary sexual traits may be dynamic, for example if these traits are renewed between breeding seasons (e.g. ...
Sexually selected ornaments range from highly dynamic traits to those that are fixed during development and relatively static throughout sexual maturity. Ornaments along this continuum differ in the information they provide about the qualities of potential mates, such as their parasite resistance. Dynamic ornaments enable real-time assessment of the bearer's condition: they can reflect an individual's current infection status, or they can reflect resistance to recent infections. Static ornaments, however, are not affected by recent infection but may instead indicate an individual's genetically determined resistance, even in the absence of infection. Given the typically aggregated distribution of parasites among hosts, infection is unlikely to affect the ornaments of the vast majority of individuals in a population: static ornaments may therefore be the more reliable indicators of parasite resistance. To test this hypothesis, we quantified the ornaments of male guppies (Poecilia reticulata) before experimentally infecting them with Gyrodactylus turnbulli. Males with more left-right symmetrical black coloration and those with larger areas of orange coloration, both static ornaments, were more resistant. However, males with more saturated orange coloration, a dynamic ornament, were less resistant. Female guppies often prefer symmetrical males with larger orange ornaments, suggesting that parasite-mediated natural and sexual selection act in concert on these traits.
... Hamilton & Zuk (1982) proposed that sexual signals might provide reliable information about the health status of signalers because only healthy individuals in prime condition would be able to develop and maintain exaggerated secondary sexual characters without compromising their health status. Numerous studies have since investigated the relationship between level of parasitism and expression of secondary sexual characters, showing an overall weak, but highly significant negative relationship across studies and different taxa (Møller, Christe & Lux, 1999). An increasing number of studies have shown that the ability to raise an immune response is positively related to the expression of secondary sexual characters, with a mean effect size that is large (Møller et al., 1999). ...
... Numerous studies have since investigated the relationship between level of parasitism and expression of secondary sexual characters, showing an overall weak, but highly significant negative relationship across studies and different taxa (Møller, Christe & Lux, 1999). An increasing number of studies have shown that the ability to raise an immune response is positively related to the expression of secondary sexual characters, with a mean effect size that is large (Møller et al., 1999). This suggests that females or other receivers may gain reliable information on health status and ability to cope with parasites from inspection of secondary sexual characters. ...
... This opens up the possibility for efficient transmission of infectious disease (Hamilton, 1990). While comparative studies and meta-analyses have found mixed evidence consistent with this hypothesis (Able, 1996;Møller et al., 1999), currently available evidence almost exclusively concerns secondary sexual characters involved in female choice. An exception to this generalization is spur length and immunity in pheasants Phasianus colchicus (von Schantz et al., 1996). ...
Canines in wild boar Sus scrofa constitute weapons used in male–male conflict. We analyzed extensive data for the ecological correlates of canine size in several study sites in Extremadura, Spain, to determine their degree of condition‐dependence and their relationship with health status. Boars with relatively large body size had larger canines than small boars. Canine size was larger in estates without livestock, in estates with low population density, and in estates with rich holmoak forest. These findings are consistent with predictions for condition‐dependent secondary sexual characters. Boars with relatively large canines had large spleens for their body size, higher prevalence of Aujeszky's disease and higher prevalence of macroscopic lesions compatible with Bovine Tuberculosis than boars with relatively small canines. Thus, boars with large canines that were likely to be dominant and have differential access to females were in poorer health than boars with small canines. Since the virus responsible for Aujeszky's disease and Mycobacterium bovis are readily transmitted through direct contact during mating, we suggest that there is a sexual conflict over mating. Boars with large canines that are most likely to copulate with sows are also more likely to be a direct cause of transmission of disease to the sows.
... Finally, we did not find evidence to suggest that host sex affected the probability of infection by microfilariae, contrasting with the general acceptance that males are more susceptible to parasites and diseases than females, mainly due to physiological causes (e.g., interaction between immune system and testosterone; reviewed in [89,90]). However, in parasite-host systems formed by filarioids and birds, no differences in the parasite's susceptibility between sexes have been reported in a wide variety of bird species, such as the purple martin (Progne subis) [50], the Northern cardinal (Cardinalis cardinalis) [78], the Galápagos cormorant (Phalacrocorax harrisi) [37], the village weaver (Ploceus cucullatus) [47], or the blue tit (in this study). ...
... Moreover, most of these bird species exhibit moderate to high degrees of sexual dichromatism, with males being typically brighter and more colored than females. Because the expression of secondary sexual characters is related to infection susceptibility and immune function [89], males are expected to suffer more from parasitism [91]. However, this scenario has not been observed in the present study, nor in other filarioid-bird systems worldwide. ...
Filarioid nematodes (commonly known as filarial worms) are known to impact human and domestic animal health, but studies examining their ecological relevance and impacts on wildlife are still underrepresented. In the case of birds, microfilariae are typically found at low prevalence, but they may negatively affect some fitness-related traits. Here, we study the prevalence and associations of microfilariae in a wild population of blue tits (Cyanistes caeruleus) inhabiting a woodland comprising different forestry formations. In addition, we characterize the filarioid lineages through the cytochrome c oxidase subunit I (COI) gene sequence. We found a moderate prevalence of microfilariae in the blue tit population (9.4%) and that the presence of such parasites was negatively associated with host body mass. Neither forest type nor host sex influenced microfilariae presence. Phylogenetic analyses revealed the presence of five filarioid lineages clustered in the Onchocercidae family-four out of five lineages clustered in the Splendidofilaria clade, while the remaining lineage could not be clearly assigned to a genus. In addition, this is the first study examining the filarioid lineages infecting the blue tit. Our results suggest that hosts in poorer body condition, in terms of lower body mass, are more susceptible to be parasitized by filarioid nematodes and call for further genetic studies of these parasites.
... The distribution and abundance of ticks in host populations can be influenced by various factors, both intrinsic to the hosts (sex, social organization, abundance, community structure) and extrinsic or environmental ones (temperature, precipitation, habitat structure) (Altizer et al., 2003;Estrada-Peña et al., 2012). Among intrinsic factors, the ethological and physiological differences between host males and females affect their corresponding vulnerability to tick infestation (Moller et al., 1999;Moore and Wilson 2002;Ottova et al., 2005;Ruiz-Fons et al., 2013). For example, in several vertebrate species males are more prone to tick infestation due to the immunomodulatory effect of testosterone ("immunocompetence handicap hypothesis", e.g. ...
... Furthermore, many vertebrate species exhibit a sexual selection towards larger or more ornamented males (Perez-Orella and Schulte-Hostedde 2005; Deviche and Parris 2006;Hoby et al., 2006). This strong tendency of males to compete for females leads to an increased susceptibility to predators or ticks (Folstad and Karter, 1992;Moller et al., 1999;Moore and Wilson, 2002;Rolff, 2002;Ottova et al., 2005). However, in the two studied hedgehog species no sexual dimorphism is apparent. ...
The availability of data regarding population abundance and dynamics of ticks in wild vertebrate populations is crucial to understand the host-tick relationship and to assess the risk for domestic animals and humans from possible zoonotic diseases. In this study we analyse several host-intrinsic and environmental factors affecting the tick population of two sympatric hedgehog species (the European and the Algerian hedgehog) in two differently anthropized habitats in eastern Spain. We captured 215 hedgehogs and sampled 356 adult ticks of four different species (Rhipicephalus sanguineus, R. turanicus, R. bursa and R. pusillus). We analysed by General Linear Mixed Models how the hosts’ species, sex, capture month and site and their interactions affected tick presence and tick load. Further, we carried out Spearman correlation tests to analyse how environmental temperature and precipitation affect tick presence and load on hedgehogs. We found that, in general, male hedgehogs were more infested than females. However, the effects of the different factors depended on the tick species, especially related to their endophilic or exophilic character. High values of general tick infestation can be explained by the coincidence of tick activity peaks and higher male host activity levels, especially within areas with higher habitat diversity and species richness. We also discuss how the potential immunosuppressive effect of testosterone could be affecting our results. Our results show that in highly anthropized environments hedgehogs potentially act as important mixing vessels for tick-borne zoonotic pathogens and that monitoring ticks in periurban wildlife is important to assess potential health risks for pets and humans.
... Parasite infections are another well-recognised agent driving the evolution of exaggerated secondary sexual traits (Hamilton and Zuk 1982;Møller et al. 1999). Hamilton and Zuk (1982) proposed that males in better condition could express larger secondary sexual traits because they are more likely to carry genes for parasite resistance (i.e., requiring fewer resources to fight parasite infections). ...
... When considering multiple parasites simultaneously, the evidence suggests that sexual traits can respond in different directions (Doucet and Montgomery 2003;Martin and Johnsen 2007;Hund et al. 2021). Therefore, a better understanding of how sexual traits evolve under multiple parasite infections would require studying trait responses to parasite co-infections (Møller et al. 1999;Karvonen and Seehausen 2012). ...
... Furthermore, it has been showed that once introduced in Europe, the yellow-legged hornet has experienced a strong bottleneck and this might have selected only the most immunocompetent females (Prenter et al. 2004;Dunn et al. 2012;White & Perkins 2012;Arca et al. 2015). Similarly, also the invasion dynamics and polyandry documented in foundresses of V. velutina in the invasive range could play a role in the higher immunity observed in reproductive females of the yellow-legged hornet (Moller et al. 1999;Arca et al. 2015;Simone-Finstorm et al. 2016). In fact, it has been inferred that the invasion of Europe by V. velutina started with a single queen that had mated with multiple males (around 3-4 according to Arca et al. 2015) and subsequent studies confirmed this single introduction for the European population Granato et al. 2019); it is therefore likely that the immunocompetence of the resulting European population might be impacted by the genetic background and strongly depends on the immune abilities of the first invasive foundress and its mates (Moller et al. 1999;Arca et al. 2015;Simone-Finstorm et al. 2016). ...
... Similarly, also the invasion dynamics and polyandry documented in foundresses of V. velutina in the invasive range could play a role in the higher immunity observed in reproductive females of the yellow-legged hornet (Moller et al. 1999;Arca et al. 2015;Simone-Finstorm et al. 2016). In fact, it has been inferred that the invasion of Europe by V. velutina started with a single queen that had mated with multiple males (around 3-4 according to Arca et al. 2015) and subsequent studies confirmed this single introduction for the European population Granato et al. 2019); it is therefore likely that the immunocompetence of the resulting European population might be impacted by the genetic background and strongly depends on the immune abilities of the first invasive foundress and its mates (Moller et al. 1999;Arca et al. 2015;Simone-Finstorm et al. 2016). The difference between gynes and foundresses of the two species is quite intriguing and further research, for example by evaluating the individual immunocompetence in the native range of the yellow-legged hornet or assessing the effects of mating on immunity (Baer et al. 2006), is required to unveil the mechanisms responsible for the change in individual immunocompetence from gynes to foundresses of V. crabro and for the strong resistance to bacterial pathogens in reproductive females of V. velutina and the weak antibacterial response of V. crabro gynes. ...
Abstract: Understanding the major mechanisms that allow an alien species to become invasive is crucial for limiting the impact of such species, and individual immunity seems to be a crucial trait for their large range colonization when introduced to a new area. Indeed, a high resistance to pathogens and parasites could favour the establishment and proliferation of an alien species in a newly colonized region. A striking example of recent successful invasion is represented by the Asian hornet, Vespa velutina nigrithorax, which has invaded Western Europe threatening bees and beekeeping activities. Investigating the biology of this species is fundamental to understand how V. velutina has become invasive in Europe and this knowledge could be crucial for limiting its impact. Here, by performing bacterial challenge bioassays, we compare the immune competence of different castes and sex of a population of the invasive Asian hornet, V. velutina nigrithorax, and of the native European hornet, V. crabro. Our results demonstrate that the two species differ in their immunocompetence with respect to caste: a higher level of immunocompetence was found in the reproductive females of the Asian hornet which were resistant to bacterial challenge when compared to workers and males of both species and to reproductive females of the native European hornet. The high pathogen resistance in reproductive females of the Asian hornet, might therefore represent a key factor contributing to the ecological success and spread of this invader.
... Some key models for the evolution of sexually selected traits rely on the honesty of those traits as indicators of condition or some other measures of quality (Zahavi 1975;Johnstone 1995). The Hamilton-Zuk model integrates this logic with host-parasite evolutionary dynamics, suggesting that sexually selected traits reveal an individual's genetic ability either to avoid parasitism or to mitigate the detrimental effects of parasitism (Hamilton and Zuk 1982;reviews in Clayton 1991;Møller et al. 1999;Balenger and Zuk 2014). Much of this work has focused on coloration traits, which likely reflect a trade-off with immune defense (e.g., Borgia and Collis 1990;Megía-Palma et al. 2016a, b;Stephenson et al. 2020). ...
... Much of this work has focused on coloration traits, which likely reflect a trade-off with immune defense (e.g., Borgia and Collis 1990;Megía-Palma et al. 2016a, b;Stephenson et al. 2020). However, behavior may be an even more sensitive indicator of parasitism because it can change more rapidly than most morphological traits (Folstad and Karter 1992;Wingfield et al. 1998; but see Møller et al. 1999). Parasitized animals that do not appear to be impaired under less demanding circumstances may betray their infection during agonistic interactions (Schall and Dearing 1987), and this can upend social hierarchies and disrupt access to mates (Rau 1984;Maksimowich and Mathis 2000). ...
Parasites may impair host behavior in ways that reduce host fitness, especially when access to territories or mates becomes disrupted. Western fence lizards (Sceloporus occidentalis) are a key host to western blacklegged ticks (Ixodes pacificus). Males are highly aggressive during the mating season, competing with rivals through displays of color badges, pushups, and other behaviors. We hypothesized that experimental tick infestation diminishes the performance of male western fence lizards in intrasexual contests, via either blood loss, damage to sensory structures, or both. We infested adult males with larval ticks for 7 to 10 days, staged contests between infested and quality-matched control males, and measured their behavior in enclosure arenas. Infested lizards were less aggressive and exhibited decreased hematocrit, compared to non-infested animals. We found no relationships between aggression and either body size or blue ventral badge color traits, for either infested or uninfested males. There was also no effect of tick attachment location and hemoparasite infection on host contest behavior. This is the first demonstration of the impact of I. pacificus parasitism on intraspecific interactions of western fence lizards and suggests that tick infestation has substantial impacts on lizard fitness. Because I. pacificus rely heavily on these lizards for blood meals and dispersal, these impacts could also influence the abundance of ticks and the pathogens they vector.
Significance statement
Parasitism frequently impairs host behavior. We investigated the effect of blacklegged tick parasitism on western fence lizard contest behavior using a lab-based manipulation experiment. We demonstrated that tick infestation reduced lizard aggressiveness, which may lead to territory loss and reduced mating opportunities in the wild. We found no evidence that host body size or coloration are correlated with aggression. This study adds to a growing body of evidence that tick parasitism is costly for lizards, while demonstrating the usefulness of manipulation experiments to understand host-parasite interactions.
... Parasitism has usually been studied in males to evaluate its effect on their sexual ornaments, such as coloration, and their behavior, including social status and courtship displays (Clayton 1991;Moller et al. 1999;Roberts et al. 2004;Habig & Archie 2015). In females, one of the main focuses has been studying their fecundity (Hurd 2001). ...
The reproductive mode of viviparity has independently evolved in various animal taxa. It refers to the condition in which the embryos or young develop inside the female’s body during gestation, providing advantages such as protection, nutrition, and improved survival chances. However, parasites and diseases can be an evolutionary force that limit the host’s resources, leading to physiological, morphological, and behavioral changes that impose additional costs on both the pregnant female and her offspring. This review integrates the primary literature published between 1980 and 2021 on the parasitism of viviparous hosts. We describe aspects such as reproductive investment in females, offspring sex ratios, lactation investment in mammals, alterations in birth intervals, current reproductive investment, variations between environments, immune system activity in response to immunological challenges, and other factors that can influence the interaction between viviparous females and parasites. Maintaining pregnancy incurs costs in managing the mother’s resources and regulating the immune system’s responses to the offspring, while simultaneously maintaining an adequate defense against parasites and pathogens. Parasites can significantly influence this reproductive mode: parasitized females adjust their investment in survival and reproduction based on their life history, environmental factors, and the diversity of encountered parasites.
... Tracing phylogenetic patterns helps reconstruct the evolutionary origins and history of attributes and behaviors, identifying both promoting and constraining influences on excess male mortality. Females typically outlive males across most animal species (Hazzard, 1990), reflecting trade-offs that increase male reproductive success even at the expense of longevity (Møller, Christe, & Lux 1999). ...
Sex differences in human mortality rates emerge from a complex interaction of genetic heritage and developmental environment. Although mortality is not in itself a behavior, it is an indirect product of behavior and physiology and thus responsive to life history variation in resource allocation, behavioral tendencies, and relevant environmental conditions. The explanatory framework of Tinbergenʹs Four Questions is sufficiently powerful in generalization to promote understanding of this phenomenon. Excess male mortality is a result of a trade‐off between competitiveness and longevity. Male life history gives greater emphasis to reproductive effort at the expense of somatic effort, and mating effort at the expense of longevity compared to female life history. Men exhibit riskier behavioral patterns and greater physiological susceptibility, dying at higher rates from behavioral and most non‐behavioral causes across the lifespan. The magnitude of the sex difference in mortality in developed nations peaks when males sexually mature and enter into mating competition. Social and environmental conditions intensifying male competition for resources, status, and mates lead to increased male mortality.
... The consequence frequently is an evolutionary arms race between pathogens/parasites and their hosts (Gómez et al. 2010). Moreover, parasites often prove decisive in sexual selection, with females usually choosing less parasitized males (Hamilton and Zuk 1982, Able 1996, Møller et al. 1999. Therefore, both pathogens and parasites have consequences in most aspects of the host's life history (Clayton and Moore 1997, Combes 2001, Schmid-Hempel 2011. ...
... Sexual selection has long been thought to be driven by parasitism (Hamilton and Zuk 1982;Clayton 1991;Andersson 1994;Zuk and McKean 1996;Moller et al. 1999), and recent work has increasingly sought to link ecological dynamics to sexual selection (Qvarnström 2001;Gillespie et al. 2014;Miller and Svensson 2014;Moore et al. 2019;Siepielski et al. 2022) and parasitism (Pietrock and Marcogliese 2003;Poulin 2006;Wolinska and King 2009;Penczykowski et al. 2015;Hasik and Siepielski 2022). Yet evidence that directly or indirectly links ecological conditions to parasitism and sexual selection among populations is limited, especially in natural populations (Laine and Tellier 2008). ...
Parasite-driven population divergence in hosts can be exacerbated by environmental factors affecting host parasitism, as well as by increasing sexual selection against parasitized hosts. Environmental factors can influence parasitism directly by affecting parasite survival, and indirectly by affecting host condition, which can in turn shape host sexual selection. To disentangle these potential alternative paths, we used a damselfly (host) - water mite (parasite) system to examine how environmental factors directly and indirectly drive heterogeneity in parasitism across populations and influence the strength of sexual selection acting against parasitized males. We found substantial heterogeneity in parasitism across populations, driven mainly by lake pH, and damselfly density. Although this heterogeneity in parasitism did not translate directly into variation in sexual selection, the density of predatory fish increased sexual selection strength, likely through the effects on damselfly condition. These results imply that parasitism alone may not cause differences in sexual selection across populations, but when linked with underlying environmental conditions, parasitism can increase the strength of selection. More broadly, these results suggest that elucidating how parasitism may drive sexual selection requires consideration of the intwined effects of ecological processes.
... Merely formal uglinesses-such as facial asymmetries and deviations from the form of the average face and from typical secondary sexual traits-are thought to be correlated with susceptibility to disease, and as a result are honest indicators of an increased chance of carrying pathogens now, asymptomatically, or in the future (e.g., Thornhill & Gangestad 1993;Tybur & Gangestad 2011;Livshits & Kobyliansky 1991;Thornhill & Møller 1997;Møller & Swaddle 1997;Møller et al. 1999). ...
I offer the first sustained defence of the claim that ugliness is constituted by the disposition to disgust. I advance three main lines of argument in support of this thesis. First, ugliness and disgustingness tend to lie in the same kinds of things and properties (the argument from ostensions). Second, the thesis is better placed than all existing accounts to accommodate the following facts: ugliness is narrowly and systematically distributed in a heterogenous set of things, ugliness is sometimes enjoyed, and ugliness sits opposed to beauty across a neutral midpoint (the argument from proposed intensions). And third, ugliness and disgustingness function in the same way in both giving rise to representations of contamination (the argument from the law of contagion). In making these arguments, I show why prominent objections to the thesis do not succeed, cast light on some of the artistic functions of ugliness, and, in addition, demonstrate why a dispositional account of disgustingness is correct, and present a novel problem for warrant-based accounts of disgustingness (the ‘too many reasons’ problem).
... Regardless, our broad comparative analysis has revealed a consistent role for parasitism in shaping the potential for selection. These results both confirm and expand upon the findings of previous meta-analyses that demonstrated a role for parasites in shaping selection experienced by their hosts [38,39], but add to them by revealing the specific underpinnings of potential selection operating. ...
Determining the effects of parasites on host reproduction is key to understanding how parasites affect the underpinnings of selection on hosts. Although infection is expected to be costly, reducing mean fitness, infection could also increase variation in fitness costs among hosts, both of which determine the potential for selection on hosts. To test these ideas, we used a phylogenetically informed meta-analysis of 118 studies to examine how changes in the mean and variance in the outcome of reproduction differed between parasitized and non-parasitized hosts. We found that parasites had severe negative effects on mean fitness, with parasitized hosts suffering reductions in fecundity, viability and mating success. Parasite infection also increased variance in reproduction, particularly fecundity and offspring viability. Surprisingly, parasites had similar effects on viability when either the male or female was parasitized. These results not only provide the first synthetic, comparative, and quantitative summary of the strong deleterious effects of parasites on host reproductive fitness, but also reveal a consistent role for parasites in shaping the opportunity for selection.
... Thus, activation of the host immune response should have a negative effect on the exaggeration of its secondary sexual traits. Moller et al. studied this hypothesis, using meta-analysis of previous studies and concluded that there is a negative correlation between an individual's secondary sexual ornaments and its immune activation (Moller et al., 1999). ...
In host-parasite coevolution, the parasite is selected to increase its infectivity while host is selected to resist the parasite infection. It is widely held that parasite-mediated sexual selection can further amplify the selective pressure on the host to overcome parasite infection. In this paper we focus on certain types of parasites, those that can impair the activity of the host immune function to prevent signs of sickness. We show that the effect of sexual selection can actually reduce the selective pressure on the host immune response to adapt to the parasite infection. We design a simple mathematical model for a population of sexually reproducing organism in which individuals are choosy, preferring traits that are correlated negatively with immune system activity. We introduce to this population a parasite that can suppress activation of the host's immune response. Our results show that even though the host immune system is likely to ultimately evolve and adapt to the parasite infection, when sexual selection is part of this process, it can slow down this evolution on the host and give the parasite more time to get established.
... Parasite can in fact exert multiple selective pressures on host sexual traits and behaviour (David and Heeb 2009;Maan and Seehausen 2011). On the one side, parasites can affect host condition by altering (reducing) the expression of secondary sexual characters (Moller et al. 1999). ...
... Parasites can indeed have profound effects on life-histories of their hosts, as well as driving behavioural, physiological and morphological adaptations to prevail in the evolutionary arms race (Clayton and Moore 1997;Schmid-Hempel 2011). These effects can expand to affect host population dynamics, community structure, evolutionary trajectories and life-histories (Fitze et al. 2004b;Møller and Nielsen 2007;Lachish et al. 2011), including sexual selection processes (Hamilton and Zuk 1982;Møller et al. 1999). ...
Nest-dwelling ectoparasites are a major source of stress for growing nestling birds, as they can negatively impact on growth and physiology, with consequences on pre-fledging mortality. Ectoparasites are expected to also affect chromatic traits involved in parent-offspring communication, because their expression requires the same resources used by nestlings for parasites defence and/or it is linked to individual state. However, the effects of ectoparasites on growth, condition and expression of begging components are poorly known, especially in raptors. Here, we examined the effects of an experimental ectoparasites removal on growth (body mass and forearm length) and expression of begging traits (size and colour of flange, cere and gape) in lesser kestrel (Falco naumanni) nestlings. Our manipulation was very effective in removing ectoparasites and parasite load had several detrimental effects on early growth and expression of visual signals directed to parents. Deparasitized nestlings grew faster in terms of body mass and forearm length, as well as mouth width and cere length. In addition, the red chromaticity of cere decreased with age, with deparasitized nestlings showing a faster decrease concomitantly with the increase in body growth. Such negative effects disappeared in later nestling stages and ectoparasites did not affect pre-fledging survival. Our results showed that visual components of begging have the potential to reveal individual condition during early nestling stages, above and beyond ectoparasite infection. They are also consistent with previous evidence that ectoparasites weakly affect fitness in colonial and cavity-nesting avian hosts, which have evolved greater resistance due to prolonged host-parasite interactions.
Significance statement
Ectoparasites are considered a major stressor for nestling birds, as they can negatively affect their growth, survival but also traits involved in parent-offspring communication. We experimentally show that ectoparasite infection has only little and transient negative effects on the early growth of lesser kestrel nestlings. However, nestlings recover from such a slower growth without paying any cost in terms of final body size and pre-fledging survival. In addition, we reveal that mouth colour does not mirror the level of ectoparasite infestation, but it is a reliable signal of nestlings’ individual general condition. Therefore, ectoparasites only weakly affect fitness in this species, likely because of the intense host-parasite interaction, which is typical of colonial and cavity-nesting species.
... Spurfowl may breed within their first year, and gonad development can begin shortly after the first rains in spring (Jansen and Crowe 2005). The cost of testosterone production or developing secondary sex characteristics has been associated with reduced immune levels in males (Poulin 1996;Møller et al. 1999;Amundson et al. 2016). This, in addition to an as yet naïve immune system often seen in juvenile birds of both sexes (Biester and Schwarte 1959;Soulsby 1968;Cooper and Crites 1976), may lead to more helminth species successfully colonizing young males than young females. ...
Parasite ecology has recently focused on elucidating patterns and processes that shape helminth communities in avian hosts. However, helminths parasitizing gamebirds are still poorly understood. Here we describe the gastrointestinal nematode fauna of Swainson’s spurfowl, Pternistis swainsonii (Phasianidae) and helmeted guineafowl, Numida meleagris (Numididae), collected at three and four localities, respectively, in South Africa and analyze the prevalence, mean abundance and diversity of their helminth communities. Eleven nematode species were collected from spurfowl, which had a mean number of nematode species per host of 3.01 ± 0.18, whereas guineafowl harboured 15 nematode species, with a mean number of nematode species per host of 3.93 ± 0.12. Focusing on the most prevalent species, we also asked if host sex and/or age were associated with infracommunity structure with regard to nematode counts and species richness, as well as the species and taxonomic composition of infracommunities. While pooling data of nematode species masked the influence of host characteristics on helminth communities, analysis of individual nematode species revealed a number of patterns. In particular, adult female bias was seen in Tetrameres swainsonii in spurfowl and in Allodapa dentigera and Gongylonema congolense in guineafowl; Acuaria gruveli reached higher numbers in adult spurfowl than in juveniles, and helminth infracommunities in juvenile male guineafowl were more species rich than those in adult males. Combined, our results suggest that helminth communities of spurfowl and guineafowl are associated with a complex interplay of numerous factors, including host characteristics, parasite traits and environmental conditions.
... For example, in a variety of insect species, selection lines evolved under experimentally enforced monogamy have improved survival [30,[44][45][46] and increased immune function [47][48][49] relative to lines evolved under promiscuity. More broadly, mating system and reproductive investment are correlated with and known to causally affect longevity, survival and immune function [30,44,[50][51][52][53][54][55][56]. Through this mechanism of immune function, variation in sexual selection and reproductive investment is hypothesized to explain variation in the survival cost of parasitism [6]. ...
The extent to which parasites reduce host survival should depend upon how hosts balance trade-offs between reproduction and survival. For example, parasites are predicted to impose greater survival costs under polygynous or promiscuous mating systems in which competition for mates favours increased reproductive investment, particularly in males. We provide, to our knowledge, the first comparative test of the hypothesis that the mating system of the host is an important determinant of (i) the extent to which parasites reduce survival, and (ii) the extent to which males and females differ in the survival cost of parasitism. Using meta-analysis of 85 published estimates of the survival cost of parasitism from 72 studies of 64 species representing diverse animal lineages, we show that parasites impose a mean 3.5-fold increase in the odds of mortality on their hosts. Although this survival cost does not differ significantly across monogamous, polygynous and promiscuous mating systems, females incur a greater survival cost than males in monogamous species, whereas males incur a greater survival cost than females in polygynous and promiscuous species. Our results support the idea that mating systems shape the relative extent to which males and females invest in reproduction at the expense of defence against parasites.
... The sex bias is common in endoparasite and ectoparasite infestations. Different mating behaviors and different SSD (sexual size dimorphism) of male rats may affect their immunity that made them more vulnerable to parasites (Folstad & Karter, 1992;Moller et al., 1999). Male rats are more likely to be infested than female rats, because of larger size and wider range of activities (Peng et al., 2015). ...
Chigger mites is a group of arthropods and some of them are vectors of scrub typhus. As a common synanthropic rodent species, the Brown rat (Rattus norvegicus) often harbors lots of ectoparasites including chigger mites. According to some "data mining" strategies, the present study took the advantage of the abundant original data from a long-term field ecological investigation between 2001 and 2015 to make a detailed analysis of chigger mites on R. norvegicus in Yunnan Province, Southwest of China. From 18 of 33 investigated counties, only 1414 chigger mites were collected from 1113 Brown rats with relatively low infestations. The 1414 individual chigger mites were identified as comprising 61 species, 11 genera and 2 subfamilies of the family Trombiculidae with a high species diversity (S=61, H'=3.13). Of 61 mite species, there were four main species, Walchia ewingi, Ascoschoengastia indica, W. koi and A. rattinorvegici, which accounted for 44.41% of the total mites. All the chigger mites were of aggregated distribution among different individuals of R. norvegicus. The Brown rats in the outdoor habitats harbored much more individuals and species of chigger mites with a higher mean abundance (MA=1.46) and mean intensity (MI=12.53) than in the indoor habitats (P<0.05). The overall infestation of the rats was significantly higher in the mountainous landscapes than in the flatland landscapes (P<0.001). The species similarity (Css) of the mites on the male and female rats reached 64.44% with sex biased infestations. The male rats harbored more species and individuals of the mites than the female rats. The adult rats harbored more species and individuals of the mites than the juvenile rats. The species abundance distribution of the mites was successfully fitted by Preston's lognormal model with ŝ(R)=15e-[0.31(R-1)]2 (α=0.31, R2=0.95). On the basis of fitting the theoretical curve by Preston's model, the total mite species on R. norvegicus was estimated to be 86 species, and 25 rare mite species were missed in the sampling field investigation. The curve tendency of the species-plot relationship indicates that R. norvegicus have a great potential to harbor many species of chigger mites, and more species of the mites would be collected if more rats are sampled.
... Sex was associated with Haemoproteus infection in the Ruby-crowned Kinglet, White-crowned Sparrow, and Wilson's Warbler (Fig. 4). Sex-related differences in haemosporidian parasite prevalence are often observed in nature; however, sex bias in parasitism often varies between and within host-parasite systems [72]. Contrary to our prediction, our study demonstrated a strong malebiased parasite prevalence in the three species mentioned above, with the Ruby-crowned Kinglet having the largest difference between sexes (53% in males vs. 1% in females). ...
Background
The prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods
Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate the prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results
We estimated the prevalence and diversity of avian Haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open-cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species. Plasmodium prevalence was relatively low (5%), consistent with the idea that competent vectors may be rare at high altitudes.
Conclusions
Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host–parasite relationships of blood parasites and their avian hosts.
... For example, parasitic infection can abolish the attractiveness of male scent: female mice Mus musculus are more attracted to the odour of uninfected males than to that of males experimentally infected with parasitic protozoans or nematode worms (Kavaliers & Colwell 1993, 1995, Ehman & Scott 2002, Kavaliers et al. 2003, González-Quiñonez et al. 2011. Female birds can increase the resistance of their progeny to parasites and reduce their own risk of contracting contagious diseases or parasites only by avoiding infected males (Hamilton & Zuk 1982, Moller et al. 1999. Females of the long-nosed bat Leptonycteris curasoae are attracted to the odour of male dorsal patches (Muñoz-Romo et al. 2011b), and evidence indicates significant relationships between the presence of the patch and low ectoparasite loads (Muñoz-Romo & Kunz 2009) and between symmetry of patches and low ectoparasite loads (Muñoz-Romo et al. 2011a). ...
en
• Sexual dimorphism is the condition in which males and females of the same species are easily distinguished by specific traits (secondary sex characteristics), often related to body size, colour patterns, weapons, and ornaments. Males of many mammal species tend to be larger or more ornamented than females, and these characteristics tend to be more pronounced in polygynous, diurnal, and open‐habitat species.
• Bats have long been considered a largely non‐sexually dimorphic group due to lack of conspicuous differences in body size and other cranial and skeletal characters. However, bats, like many mammals, exhibit a diverse array of soft‐tissue integumentary glands and non‐glandular odour‐producing structures with intense odorous substances that have not been thoroughly investigated, although postulated functions include facilitating mate selection in their generally polygynous associations.
• To date, there has been no systematic assessment of the occurrence or expression of sexually dimorphic traits in bats, many of which show intriguing sexual dimorphism in soft tissue, and most of which involve intense odours. In this study, we review evidence of integumentary glands and non‐glandular odour‐producing structures known in bats, as a first step towards identifying future research pathways to study sexual dimorphism in bats.
• Highly variable glands and non‐glandular odour‐producing structures have been noticed in ten different regions of the body, but are most frequently found on the head and the ventral region of the neck. They have been described in nearly 9% of bat species and in 70% of 21 extant bat families.
• Our review, based on extremely scattered and unevenly detailed literature, unveils the extraordinary sexual dimorphism that has been observed in Chiroptera to date, identifying not only target body parts where sexually dimorphic traits are likely to be found, but also critical avenues for future investigation and discoveries, and stressing the importance of the timing of secondary sexual trait observations, behavioural studies, and chemical analyses.
RESUMEN EN ESPAÑOL
es
• El dimorfismo sexual es la condición en la que machos y hembras de la misma especie se distinguen fácilmente por rasgos específicos (características sexuales secundarias), a menudo relacionados con el tamaño corporal, patrones de color, elementos de defensa/competencia y ornamentos. Los machos de muchas especies de mamíferos tienden a ser más grandes o más ornamentados que las hembras, y estas características tienden a ser más pronunciadas en especies poligínicas, diurnas y de hábitat abiertos.
• Durante mucho tiempo se ha considerado a los murciélagos como un grupo en su mayoría sexualmente no dimórfico debido a la ausencia de diferencias notables en el tamaño corporal y otros caracteres craneales y esqueléticos. Sin embargo, los murciélagos, como muchos mamíferos, exhiben una gama diversa de glándulas tegumentarias (tejidos blandos) y estructuras no glandulares odoríferas con sustancias de olor intenso que no se han investigado a fondo, aunque las funciones postuladas incluyen facilitar la selección de pareja, en sus asociaciones generalmente poligínicas.
• Hasta la fecha no se ha realizado una evaluación sistemática de la aparición o expresión de rasgos sexualmente dimórficos en murciélagos, muchos de los cuales muestran un dimorfismo sexual intrigante en tejidos blandos, y la mayoría de los cuales involucran olores intensos. En este estudio, revisamos evidencia de glándulas tegumentarias y estructuras no glandulares odoríferas conocidas en murciélagos, como un primer paso hacia la identificación de futuras vías de investigación para estudiar el dimorfismo sexual en murciélagos.
• Se ha observado glándulas y estructuras no glandulares odoríferas muy variables en diez regiones corporales diferentes, pero se encuentran con mayor frecuencia en la cabeza y la región ventral del cuello. Estas han sido descritas en 9% de las especies y en 70% de las 21 familias de murciélagos existentes.
• Nuestra revisión, basada en literatura extremadamente dispersa y desigualmente detallada, revela el extraordinario dimorfismo sexual que se ha observado en Chiroptera hasta la fecha, identificando no sólo las partes del cuerpo clave donde es probable que se encuentren rasgos sexualmente dimórficos, sino también rumbos críticos para investigación y descubrimientos futuros, y enfatizando la importancia del instante de las observaciones de rasgos sexuales secundarios, de los estudios de comportamiento y de los análisis químicos.
... Sex was associated with Haemoproteus infection in the Ruby-crowned Kinglet, White-crowned Sparrow, and Wilson's Warbler (Figure 4). Sex-related differences in haemosporidian parasite prevalence are often observed in nature, however, sex-bias in parasitism often varies between and within host-parasite systems [72]. Contrary to our prediction, our study demonstrated a strong male-biased parasite prevalence in the three species mentioned above, with Ruby-crowned Kinglet having the largest difference between sexes (53% in males vs. 1% in females). ...
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
... Differences in parasite life history may also influence how infections are associated with signal expression. However, our view of this has been somewhat limited as the study of parasite-mediated sexual selection has largely focused on parasites that directly infect adult males (Beltran-Bech & Richard, 2014;Clayton, 1991;Møller, Christe, & Lux, 1999;Roberts et al., 2004). We propose expanding our view to also include parasites that infect other life history stages, such as offspring. ...
Associations between parasite loads and sexual signal expression have long been the focus of research. However, our understanding of how sexual selection operates in the context of multiple parasite infections within the same host is still quite limited. We examined the expression of plumage coloration, which is sexually selected in North American barn swallows, Hirundo rustica erythrogaster, and tail streamer length, which is sexually selected in other barn swallow subspecies, in the context of eight different parasite infections. We found that two parasites, nest mites and Plasmodium, were associated with colour expression, but in opposite directions. Attractive males were less likely to have mites in their nests, but more likely to be infected with Plasmodium. We found that different underlying mechanisms were generating the links between these different parasites and the same colour signal. Males that invested more in colour expression were less likely to survive when infected with Plasmodium, suggesting a physiological mechanism linking colour to Plasmodium infections. However, we found no clear cost to males when examining nest mites, which primarily infect offspring. Instead, using experimental mite manipulations, we provide evidence for a behavioural mechanism, where territorial behaviour and male–male competition likely drive the association between colour expression and nest mite infections. We did not find associations between parasites and streamer length in this subspecies, suggesting that the links between divergent sexual signals and parasites may be quite flexible. These results suggest that the evolution of a single sexual signal can be shaped by several, even opposing, links with different parasite infections.
... Sex was associated with Haemoproteus infection in the Ruby-crowned Kinglet, White-crowned Sparrow, and Wilson's Warbler (Figure 4). Sex-related differences in haemosporidian parasite prevalence are often observed in nature, however, sex-bias in parasitism often varies between and within host-parasite systems [72]. Contrary to our prediction, our study demonstrated a strong male-biased parasite prevalence in the three species mentioned above, with Ruby-crowned Kinglet having the largest difference between sexes (0.53 in males vs. 0.01 in females). ...
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species. Plasmodium prevalence was relatively low (5%), consistent with the idea that competent vectors may be rare at high altitudes.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
... Body condition is linked to immune responses in many invertebrate and vertebrate species (Møller and Saino 1994;Møller et al. 1999;Forsyth et al. 2005;Contreras-Garduño et al. 2006). The costs of maintaining the immune responses will be lower for individuals who are in good condition as they have more resources available to allocate. ...
The immune response can be costly. Studies in several arthropod species have indicated a trade-off between immunity and other life-history traits, including reproduction. In sexually dimorphic species in which females and males largely differ in their life history strategies and related energetic demands, we can expect to find sex differences in immune functions. Sex differences in immunity are well documented in vertebrates; however, we largely lack data from invertebrate systems. Lytic activity, the immune system's ability to lysate bacteria and viruses, has been widely used as a proxy for the strength of the immune response in several invertebrates. With this in mind, we used the burrowing wolf spider Allocosa senex to test differences in lytic activity between females and males. We also studied whether digging behavior affects the immune responses in this species. While females of A. senex construct simple refuges where they stay during the day, males construct deep burrows, which they donate to females after copulation. In accordance with our hypothesis, females showed higher lytic activity compared with males, and those males who dug showed higher levels of lytic activity than those that did not dig. Furthermore, male body condition and lytic activity did not correlate with burrow length, a trait under female choice in this species. Our results show sexual dimorphism in lytic activity responses, which are likely related to differences in life-history strategies and energetic requirements of each sex in A. senex spiders.
... The overall condition of an organism can be negatively affected by parasite load, and this in turn can affect mating success (Able 1996;Møller et al. 1999). For instance, field studies of red grouse (Lagopus lagopus) revealed that parasite load reduced body condition, which in turn resulted in reduced expression of secondary sexual characters (Vergara et al. 2012). ...
Sexual selection has been suggested to accelerate local adaptation and promote evolutionary rescue through several ecological and genetic mechanisms. Condition-dependent sexual selection has mainly been studied in laboratory settings, while data from natural populations are lacking. One ecological factor that can cause condition-dependent sexual selection is parasitism. Here, we quantified ectoparasite load (Arrenurus water mites) in a natural population of the common bluetail damselfly (Ischnura elegans) over 15 years. We quantified the strength of sexual selection against parasite load in both sexes and experimentally investigated the mechanisms behind such selection. Then we investigated how parasite resistance and tolerance changed over time to understand how they might influence population density. Parasites reduced mating success in both sexes, and sexual selection was stronger in males than in females. Experiments show that male-male competition is a strong force causing precopulatory sexual selection against parasite load. Although parasite resistance and male parasite tolerance increased over time, suggestive of increasing local adaptation against parasites, no signal of evolutionary rescue could be found. We suggest that condition-dependent sexual selection facilitates local adaptation against parasites and discuss its effects in evolutionary rescue.
... Although the adaptive function of NAbs are not well understood in reptiles, they are thought to be a key immune defence as NAbs are maintained or increased with age (Palacios et al. 2011 Ujvari and Madsen 2011;Zimmerman et al. 2017), may vary with environmental exposure (Palacios et al. 2011) and can offset investment in acquired antibody production after antigen exposure (Sandmeier et al. 2012). Parasite burden can be used as an indicator of individual health in wild animals (Moller et al. 1999). Both endo-and ectoparasites are frequently prevalent in reptiles (Jacobson 2007), and individuals with a high infestation of parasites are thought to be in general poor health. ...
The frequency and intensity of ecological perturbations affecting wild animal populations is expected to increase in the future with animals facing numerous global threats. Seahorse Key is a continental island off mainland Florida that has historically been a major rookery for several species of waterbirds. As a result of an unknown disturbance, the entire rookery abandoned Seahorse Key in April 2015 and shifted nesting activities to nearby Snake Key, resulting in an influx of food resources in the form of fish carrion to resident Florida cottonmouth snakes (Agkistrodon conanti), while snakes on Seahorse Key experienced a drastic reduction in food resources. Our objective was to assess plasma corticosterone concentrations, corticosterone negative feedback using dexamethasone, blood glucose, body condition, packed cell volume, natural antibody agglutination, white blood cell counts and ratios and erythrocyte sedimentation rate to characterize the long-term effects of differential resource availability in these two snake populations 3 years after this major ecological disturbance. We collected blood samples at three time points from cottonmouths on Seahorse Key (n = 6 individuals) and Snake Key (n = 13 individuals) in fall 2018. In due consideration of the small sample size, our study shows evidence that 3 years after the shift in waterbird nesting Seahorse Key cottonmouths exhibit a dampened acute stress response and presumptive impaired innate immune functions relative to cottonmouths on Snake Key. These results highlight the context-dependent nature of biomarkers and implicate the significant decrease in food resources on Seahorse Key in altering hormonal stress responses and innate immune functions, possibly leading to unknown long-term downstream effects. This study assessed the response of a wild population of pit viper to ecological disturbance in situ with the aim to improve our understanding of how animals cope with such perturbations and improve our capacity to make informed decisions for conservation.
... For instance, male-male contest competition for mates requires males to invest in muscle mass, large body size, and other expensive sexually selected traits and ornaments (Darwin 1871;Andersson 1994;Clutton-Brock 2007). These traits often correlate with parasite risk (Hamilton and Zuk 1982;Moller et al. 1999;Coulson et al. 2018). ...
Several factors are thought to shape male parasite risk in polygynous and polygynandrous mammals, including male-male competition, investment in potentially immunosuppressive hormones, and dispersal. Parasitism is also driven by processes occurring at larger scales, including host social groups and populations. To date, studies that test parasite-related costs of male behavior at all three scales—individual hosts, social groups, and the host population—remain rare. To fill this gap, we investigated multi-scale predictors of helminth parasitism in 97 male savanna baboons (Papio cynocephalus) living in the Amboseli ecosystem in Kenya over a 5-year span. Controlling for multi-scale processes, we found that many of the classic indicators of male mating effort—high dominance rank, testosterone, and glucocorticoids—did not predict helminth infection risk. However, we identified two parasite-related costs associated with male behavior: (i) socially connected males exhibited higher Trichuris trichiura egg counts and greater parasite species richness than socially isolated males and (ii) males with stable group residency exhibited higher parasite species richness than males who frequently dispersed to new social groups. At the population level, males harbored more parasites following periods of drought than rainfall. Lastly, parasites exhibited positive covariance suggesting that infection risk increases if a host already harbors one or more parasite taxa. These results indicate that multi-scale processes are important in driving male parasite risk and that some aspects of male behavior are costly. Together, our results provide an unusually holistic perspective on the drivers of parasite risk in the context of male behaviors and life histories.
Significance statement
Infection by gastrointestinal helminths can have major consequences for host fitness, especially in the context of male mating effort. Multi-scale processes—from the host to its social group and population—are important for understanding key drivers of parasitism. We leveraged long-term data from one of the longest running behavioral ecology studies of a wild primate population in the world, the well-studied Amboseli baboon population in Kenya. We found that traditional indicators of male mating effort (attaining high dominance rank, high testosterone and glucocorticoids) did not predict parasitism. However, male social connectedness to females, competitive group demography, and harsh weather were all associated with higher parasitism. Because socially connected males faced the highest parasite risk, males may face a tradeoff between male-female relationships and parasitism. Our results show how processes at multiple scales contribute to variation in male parasite risk.
... This meta-analysis demonstrated a strong negative relationship between parasite load and the expression of male secondary sexual characteristics. In total, the most extravagantly ornamented individuals are also the healthiest ones-and thus the most preferred as mates (Moller, Christie, & Lux, 1999). Of course in species in which there is substantial paternal investment (including humans), males will also be choosy about whom they mate with and will also select mates with indicators of high genetic fitness. ...
Evolutionary psychology is the application of the principles and knowledge of evolutionary biology to psychological theory and research. Its central assumption is that the human brain is comprised of a large number of specialized mechanisms that were shaped by natural selection over vast periods of time to solve the recurrent information-processing problems faced by our ancestors (Symons, 1995). These problems include such things as choosing which foods to eat, negotiating social hierarchies, dividing investment among offspring, and selecting mates. The field of evolutionary psychology focuses on identifying these information-processing problems, developing models of the brain-mind mechanisms that may have evolved to solve them, and testing these models in research (Buss, 1995; Tooby & Cosmides, 1992). The field of evolutionary psychology has emerged dramatically over the last 15 years, as indicated by exponential growth in the number of empirical and theoretical articles in the area (Table 1.1). These articles extend into all branches of psychology In this chapter we provide an introduction to the field of evolutionary psychology. We describe the methodology that evolutionary psychologists use to explain human cognition and behavior. This description begins at the broadest level with a review of the basic, guiding assumptions that are employed by evolutionary psychologists. We then show how evolutionary psychologists apply these assumptions to develop more specific theoretical models that are tested in research. We use examples of sex and mating to demonstrate how evolutionary psychological theories are developed and tested.
... Parasite load has detrimental consequences on fitness, reducing hosts' condition, which can often also affect mating success [35,36]. For instance, field studies on red grouse (Lagopus lagopus) revealed a negative effect of parasite load on body condition and resulted in condition-dependent expression of secondary sexual characters [37]. ...
Condition-dependent sexual selection has been suggested to reduce mutation load, and sexual selection might also accelerate local adaptation and promote evolutionary rescue through several ecological and genetic mechanisms. Research on condition-dependent sexual selection has mainly been performed in laboratory settings, while data from natural populations are lacking. One ecological factor that can cause condition-dependent sexual selection is parasitism. Here, we quantified ectoparasite load (Arrenurus water mites) in a natural population of the common bluetail damselfly (Ischnura elegans) over 15 years. We estimated parasite-mediated sexual selection in both sexes and investigated how parasite resistance and tolerance changed over time and influenced population density. Parasites reduced mating success in both sexes, but the effects were stronger in males than in females. The male fitness advantage of carrying fewer parasites was higher under experimental low-density conditions than under high-density field conditions, suggesting that male-male competition could reduce parasite-mediated sexual selection. We further show that population density declined during the study period, while parasite resistance and male fitness tolerance (fecundity) increased, suggestive of increasing local adaptation against parasites and ongoing evolutionary rescue. We suggest that condition-dependent sexual selection can facilitate population persistence and promote evolutionary rescue by increasing local adaptation against parasites.
Sexual selection has been a popular subject within evolutionary biology because of its central role in explaining odd and counterintuitive traits found in nature. Consequently, the literature associated with this field of study became vast, with meta-analytical studies attempting to draw inferences from it. These meta-analyses have now accumulated, varying in scope and quality, thus calling for a synthesis of these syntheses. Here, we conducted a systematic map with a report appraisal of meta-analyses on topics associated with sexual selection, aiming to comprehend the conceptual and methodological gaps in this secondary literature. To further understand these gaps and their potential origins, we also conducted bibliometric analyses that identify the gender and origin of researchers that generated these studies. We included 152 meta-analytical studies in our systematic map as a result of a systematic literature search. We found that most meta-analyses focused on males and on certain animal groups (e.g. birds), indicating severe sex and taxonomic biases. Moreover, the topics in these studies varied immensely, from proximate (e.g. relationship of ornaments with other traits) to ultimate questions (e.g. formal estimates of sexual selection strength), albeit the former were more common. We also observed several common issues in these studies, such as lack of detailed information regarding searches, screening, and analyses, which ultimately impairs the reliability of many of these meta-analyses. In addition, most of the meta-analyses’ authors were men affiliated to institutions from developed countries, pointing to both gender and geographical authorship biases. Many of our findings might simply reflect patterns in the current state of the primary literature and academia, suggesting that our study can serve as an indicator of the issues with the field of sexual selection at large. Still, we provide both conceptual and analytical recommendations to improve future studies in the field of sexual selection, such as to avoid including humans with other animals in meta-analyses, to clarify traits of interest instead of simply using loosely defined lingo, and to properly match studies’ questions and meta-analytical models.
Host-parasite relationships are important components of ecological systems that influence the evolution of both hosts and parasites. High levels of ectoparasitic infections can disrupt host homeostasis, causing adverse effects on health and performance. However, the effects of natural ectoparasitic levels on host physiology are less understood, with most research designs implementing experimental or hormonal manipulations of hosts. In this study, we examined the interplay between tick parasitism and host characteristics on body condition and locomotor performance in Eastern fence lizards in natural settings. We found a higher prevalence of tick infections in male lizards relative to females, with larger males being more likely to experience tick infection. Infected lizards appear to exhibit an energetic trade-off between increased immune function and reduced locomotor performance, which is consistent with the immunocompetence-handicap hypothesis. Higher prevalence of tick infections in adult male lizards may be explained by age as well as the immunosuppressive effects of testosterone. Tick infection did not appear to reduce overall body condition of lizard hosts. Our findings shed light on the interplay between ectoparasitic infection, host characteristics, and locomotor performance under natural conditions. Such insights are crucial for understanding host-parasite dynamics and determining the trade-offs for hosts within ecological contexts.
Fishes of the family Pomacentridae present a wide diversity of mating systems, ranging from polygyny to promiscuity and from individual territorial defense to the establishment of reproductive colonies of males. The damselfish species Abudefduf troschelii has a reproductive colony mating system, in which males temporarily aggregate in reproductive areas to court and attract females. Males defend an individual territory where they receive eggs and perform paternal care behaviors for their offspring. The present study evaluated the advantages of the colonial mating system in A. troschelii . During an entire reproductive period, in a breeding colony within a rocky reef, we located, marked, geo-referenced, and measured the distances between the territories of all males. We quantified the variance among males in their patterns of paternal care investment, eggs acquired, hatching success, reproductive success, body size, and changes in body coloration. We found that males spatially distributed their nests in groups or independently (i.e., solitary nests). Nesting groups are formed by larger males that show intense nuptial coloration during the entire receptivity period. They are located centrally to the colony and consist of three to six males whose territories overlap. In contrast, small solitary males that fail to acquire or maintain nuptial coloration during the receptivity period establish their nests peripherally to the colony, away from the territories of other males. Our results highlight that the reproductive benefits of colonial nesting are unequal for males, as the spatial distribution of nests within the colony determines the reproductive success of males. Group nesting confers the highest reproductive benefits to males regarding eggs obtained, hatching success, and relative fitness and also enables males to reduce their parental investment in brood care behaviors. The preference of females for oviposition could be associated with greater intrasexual competitiveness, defense ability, body condition, or experience of group-nesting males located at the center of the colony or because their progeny will have a lower probability of predation than they would in solitary nests males.
Choosing to mate with an infected partner has several potential fitness costs, including disease transmission and infection-induced reductions in fecundity and parental care. By instead choosing a mate with no, or few, parasites, animals avoid these costs and may also obtain resistance genes for offspring. Within a population, then, the quality of sexually selected ornaments on which mate choice is based should correlate negatively with the number of parasites with which a host is infected (‘parasite load’). However, the hundreds of tests of this prediction yield positive, negative, or no correlation between parasite load and ornament quality. Here, we use phylogenetically controlled meta-analysis of 424 correlations from 142 studies on a wide range of host and parasite taxa to evaluate explanations for this ambiguity. We found that ornament quality is weakly negatively correlated with parasite load overall, but the relationship is more strongly negative among ornaments that can dynamically change in quality, such as behavioral displays and skin pigmentation, and thus can accurately reflect current parasite load. The relationship was also more strongly negative among parasites that can transmit during sex. Thus, the direct benefit of avoiding parasite transmission may be a key driver of parasite mediated sexual selection. No other moderators, including methodological details and whether males exhibit parental care, explained the substantial heterogeneity in our dataset. We hope to stimulate research that more inclusively considers the many and varied ways in which parasites, sexual selection, and epidemiology intersect.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
The development of molecular tools has dramatically increased our knowledge of parasite diversity and the vectors that transmit them. From viruses and protists to arthropods and helminths, each branch of the Tree of Life offers an insight into significant, yet cryptic, biodiversity. Alongside this, the studies of host-parasite interactions and parasitism have influenced many scientific disciplines, such as biogeography and evolutionary ecology, by using comparative methods based on phylogenetic information to unravel shared evolutionary histories. Parasite Diversity and Diversification brings together two active fields of research, phylogenetics and evolutionary ecology, to reveal and explain the patterns of parasite diversity and the diversification of their hosts. This book will encourage students and researchers in the fields of ecology and evolution of parasitism, as well as animal and human health, to integrate phylogenetics into the investigation of parasitism in evolutionary ecology, health ecology, medicine and conservation.
El estudio de las “historias de vida” comprende el balance entre las demandas energéticas que requieren los organismos para nacer, crecer hasta la madurez, reproducirse y sobrevivir. La mayoría de los estudios sobre la historia de vida y biología reproductiva de las aves se han realizado en el Hemisferio Norte donde habitan menos del 25 % de las especies del planeta. El Jilguero Dorado es un Passeriforme relativamente abundante en Argentina y poco estudiado; son frecuentemente capturados como aves de jaula y los machos de esta especie presentan maduración tardía del plumaje (MTP). Los objetivos de esta Tesis fueron determinar si existen diferencias en los caracteres de historia de vida relativos a los nidos de machos blancos y amarillos y, además, determinar mediante una manipulación, si los adultos disminuyen el esfuerzo reproductivo presente resguardando su supervivencia, o si aumentan el esfuerzo parental a costa de su propia supervivencia en relación a la MTP. El estudio se llevó a cabo en un sistema de cajas nido ubicado en el IIB InTeCh, Chascomús, Pcia. de Buenos Aires, entre los años 2005 y 2010. Se encontró que las hembras apareadas con machos amarillos resultaron ser significativamente más pesadas que aquellas apareadas con machos blancos así como el peso de sus huevos; la vida media de los machos reproductivos amarillos de Jilguero Dorado fue de 3.2 años y la de los machos reproductivos blancos fue 5 meses menor; las hembras manipuladas apareadas con machos blancos disminuyeron su peso un 10% más que los controles así como fue menor la duración de sus visitas de alimentación a los pichones; los pichones pertenecientes a nidos de hembras manipuladas apareadas con machos blancos presentaron una menor tasa de
crecimiento y peso asintótico al abandonar el nido. Estos resultados apoyan la existencia de un apareamiento selectivo y en este caso, las hembras de menor calidad estarían obligadas a reproducirse con los machos blancos. Las respuestas encontradas en las variables analizadas de los machos blancos son idénticas a las de los machos amarillos en todos los aspectos analizados en este trabajo.
Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.
Background
Sexual signals produced by males play a central role in sexual selection, but the relationship between these traits and the quality of the bearer are often ambiguous. Secondary sexual traits may represent genetic quality of the bearer, resulting in positive relationships with physiological state, or may be costly to produce, showing trade-off with physiological state. A number of studies have explored the relationships between secondary sexual traits and other functional traits, but few have studied their fitness consequences. We studied the link between diverse physiological traits and both morphological and behavioural sexual traits and examined how their interplay influences offspring viability in the three-spined stickleback.
Results
Male sticklebacks showing nest building and courtship behaviour were smaller than those not investing in reproductive activities. There was no evidence that the expression of red nuptial colouration and the quality of courtship behaviour of males are positively related to their metabolic rates, swim ability, oxidative damage and mtDNA copy number. However, individuals showing larger red nuptial colour areas had higher levels of oxidative DNA damage in their sperm. Male courtship behaviour and aggressiveness, but not red colour area, were good predictors of offspring hatching and survival.
Conclusions
Our results suggest that, in our study population at the southern edge of the species’ distribution, sexual colouration of male sticklebacks was not a good indicator of their body state, but both courtship quality and aggressiveness during the courtship are reliable cues of their gamete quality, influencing the viability of their offspring. Thus, females that choose mates based on their courtship behaviour will have high fitness. In the study population, which represents a fast pace-of-life with high reproductive rate and short lifespan, sexual ornaments of males may not honestly signal their physiological and physical state because they invest at maximum in a single reproductive season despite high costs.
This chapter deals with a discussion of sexual selection followed by a definition of mating systems and their determinants. It describes male–male competition and its consequences, analyses female choice and the adaptive and nonadaptive bases for mate choice, and discusses evolutionary conflicts between the sexes and their consequences. The chapter investigates the cost of secondary sexual characters and its ecological and evolutionary consequences and examines the reasons for the presence of multiple secondary sexual characters and their significance. It explains the sex ratio theory and how it relates to sexual selection. Mating system is the label used for describing the way in which males and females are distributed in reproductive units, and the consequences of the distribution for reproductive behavior and parental care. Intrasexual selection is a very important force resulting in the evolution of armament and greater body size in one sex compared with the other. Sexual conflict may in fact be running sexual selection.
The traditional view of sex roles and sexual selection emphasizes the evolution of male ornaments as a result of female mate choice and male–male competition. Female ornaments are now receiving more attention, although their roles in mating decisions are still less well understood, especially considering cases in which colourful ornaments are expressed by both sexes. In this study, we analysed whether female skin coloration (luminance and redness of the face and hindquarters) influenced male mate choice and sexual behaviours in relation to intracycle (cycle phase), intercycle (number of consecutive cycles, conceptive nature of the cycle) and interindividual (age, social rank, weight and parity) variation in a captive social group of Japanese macaques, Macaca fuscata. Males did not preferentially choose darker/redder females. Moreover, males did not appear to use female skin coloration to apportion their mating efforts on the fertile phase of the menstrual cycle or during cycles that led to conception, or to discriminate between females. Collectively, our results suggest that female skin coloration may not have been sexually selected in this species and that males mated regardless of such variation across females. To our knowledge, our study is among the few to report a lack of male choice for female coloration in a species where both sexes display ornamentation. Our findings provide novel insights on the role and evolution of female coloration in sexual signalling and mating decisions.
The traditional view of sex roles and sexual selection emphasises the evolution of male ornaments as a result of female mate choice and male-male competition. Female ornaments are now receiving more attention, although their roles in mating decision are still less well understood, especially considering cases in which colourful ornaments are expressed by both sexes. In this study, we analysed whether female skin colouration (luminance and redness of the face and hindquarters) influenced male mate choice and sexual behaviours in relation to intra-cycle (cycle phase), inter-cycle (number of consecutive cycles, conceptive nature of the cycle), and inter-individual (age, social rank, weight, and parity) variation in a captive population of Japanese macaques ( Macaca fuscata ). Males did not preferentially choose darker/redder females. Moreover, males did not appear to use female skin colouration to apportion their mating efforts on the most fertile period of the menstrual cycle or during cycles that lead to conception, or to discriminate between females. To our knowledge, our study is among the few to report a lack of male choice for female colouration in a species where both sexes potentially display ornamentation. While female colouration appeared to contain information about intra-cycle, inter-cycle, and inter-individual variation in fecundity, this study further demonstrates that this trait may not have been sexually selected and that males mated regardless of such variation across females. This study adds to the growing research on the role and evolution of female colouration in the context of sexual signalling and mate attraction.
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
In order to investigate the highly debated immunocompetence handicap hypothesis (ICHH), this study examined secondary sexual signals, parasites and immune function in Red-winged Blackbirds (Agelaius phoeniceus). Secondary sexual signals investigated included body condition, physiological condition and epaulets. Parasites investigated included ectoparasites, endoparasites and blood parasites, and immune function tests included blood bacteria killing capacity, haemolysis and haemagglutination. Overall this study found that there were some significant intersexual differences in parasite infections, especially in endoparasites which occurred more often in males. In addition, there were no significant effects of parasites or immune function on signals related to either body condition or physiological condition. However, significant effects which show some support for the ICHH were found in the relationship between immune function, parasites and male epaulet areas. A similar relationship was also interestingly found in females, related to female epaulet scores. Overall, results seem to suggest that infection by ectoparasites has a significant effect on the expression of various secondary sexual signals. Further research, under controlled laboratory conditions are required for more significant conclusions relating to the ICHH.
Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass.
The process of sexual selection results from mating advantages gained when members of one sex, usually males, compete for access to the other sex, and when competitors in better condition or bearing more extravagant ornaments are selected by individuals of the opposite sex, usually females. These ideas, published in detail by Darwin in 1871, led to the foundation of modern theory describing animal breeding systems, and are still instigating numerous researchers in ongoing studies that seek to understand reproductive phenomena in animals. Sexual selection promotes adaptations in behavior, morphology, and physiology, and also is an agent of speciation. In the first part of this chapter, we present an overview of sexual selection theory and some of the major advances in the last few decades. We then present work that we have developed within the scope of sexual selection theory, using as a model a small Neotropical passerine, the blue-black grassquit (Volatinia jacarina). We describe general parameters of this species and why it is an ideal model to study sexual selection. We follow this with a summary of field and laboratory methods we have used, and then address conceptual topics subdivided into four major categories: (1) parasite-mediated sexual selection; (2) social and sexual mating systems; (3) female choice; and (4) the evolution of sexual ornamentation.
Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows (Hirundo rustica) by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.
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Cnemidophorus arubensis, an endemic teiid lizard of Aruba island, Netherlands Antilles, is parasitized by a haemogregarine protozoan. The proportion of animals infected (prevalence) was greater for males than females and for adults compared to juveniles. Brightly colored males were more likely to be infected than blandly colored males of the same body size. Percent of erythrocytes infected with parasite gametocytes, and parasite prevalence, were similar in both wet and dry seasons. Infected and noninfected lizards were similar for several hematological, physiological, anatomical, and behavioral measures of parasite virulence. The Aruban haemogregarine appears to have an avirulent effect on Cnemidophorus arubensis.
Secondary sexual characters may signal parasite resistance because the development of such traits can have costs to immune functioning. Here we show that expression of red coloration in the salmonid Arctic charr is a sexually dimorphic character that reveals information of potential importance in sexual selection. Intensity of the carotenoid dependent coloration is in both sexes negatively related to lymphocyte counts. A causal mechanism for this relationship could be reduced availability of carotenoids for immunological application created by increased carotenoid requirements for ornamental development. Alternatively, if more ornamented individuals also have lower intensities of infection, the observed relationship might be explained by healthy individuals being both bright and having low antigen stimulation of lymphocyte transformation and proliferation. Parasite intensities also show relationships with intensity of coloration, and this is used to evaluate the latter explanation.
Theories of sperm competition and die evolution of second- ary sexual characters may have a common denominator in a male trade-off between immune activity and ejaculate quality. Sperm cells are non-self to die male and therefore targets of immunological attacks in the reproductive tract Consequent- ly, sperm cells, and eventually ejaculate quality, are influenced by a male's ability to down-regulate immune responses during the production df ejaculates, a process potentially regulated by immunosuppressive gonadal hormones. The possibility for unconstrained immunosuppression during spermatogenesis will be decreased by parasitic infections, which thus can in- terfere with ejaculate quality. Males with genetic resistance against parasites will have a higher potential for elevated levels of immunosuppressive androgen hormones compared to non- resistant males. Therefore, parasite resistant males may be at an advantage during spermatogenesis and consequently have high-quality ejaculates. This logic suggesting that parasites may impose costs on sperm production has implications for both sperm competition theory and the current understand- ing of the evolution of sexually selected characters under an- drogen control (Folstad and Skarstein, 1995). We suggest that females may obtain heritable parasite resistance for their off-
spring by exploiting a male trade-off, evolutionary rooted in male need for germ line control.
Independent of age or geographic variation, males of many species of birds exhibit dramatic variation in the expression of elaborate secondary sexual characters. ''Good genes'' models of sexual selection propose that males with relatively low resistance to parasites suffer high parasite loads that inhibit their ability to express these characters fully. In turn, variation in such characters may reliably indicate male quality and may be used by females to choose males. This is the first study to monitor (via mark-recapture) the long-term effects of parasites on color and growth of plumage in individual birds. Specifically, we used house finches, Carpodacus mexicanus, a sexually dimorphic species in which females are known to prefer more brightly plumaged males for mating, to test the hypothesis that high parasite load in males is correlated with poor physiological condition and reduced development of male secondary sex characters. Our results clearly demonstrate that both ectoparasitic feather mite (Proctophyllodes sp.) infestations and endoparasitic avian pox viral infections during molt are correlated with poor physiological condition and reduced development of bright male plumage during the same molt period, thus supporting good genes models.
AN important problem in evolutionary biology since the time of Darwin has been to understand why females preferentially mate with males handicapped by secondary sexual ornaments1-3. One hypothesis of sexual selection theory is that these ornaments reliably reveal the male's condition4-6, which can be affected for example by parasites4,7-13. Here we show that in the three-spined stickleback (Gasterosteus aculeatus) the intensity of male red breeding coloration positively correlates with physical condition. Gravid females base their active mate choice on the intensity of the male's red coloration. Choice experiments under green light prevent the use of red colour cues by females, and males that were previously preferred are now chosen no more than randomly, although the courtship behaviour of the males remains unchanged. Parasitieation causes a deterioration in the males' condition and a decrease in the intensity of their red coloration. Tests under both lighting conditions reveal that the females recognize the formerly parasitized males by the lower intensity of their breeding coloration. Female sticklebacks possibly select a male with a good capacity for paternal care14 but if there is additive genetic variation for parasite resistance, then they might also select for resistance genes, as proposed by Hamilton and Zuk4.
Why do females prefer elaborate male mating displays in species where
they receive little more from males than their sperm? Here we review
three hypotheses for the evolution of mating preferences: direct
selection, the runaway process and the parasite mechanism. There is
growing support for direct selection, in which preferences evolve
because of their direct effects on female fitness rather than the
genetic effects on offspring resulting from mate choice.
Male secondary sexual characters may have evolved as intra-or intersexual signals of male phenotypic or genetic quality. In birds, singing performance may have the function to honestly reveal .health and vigor of individual males. Infectious diseases and poor body conditions would therefore be expected to negatively influence singing performance. Since bird pathogens are known to elicit both a humoral and a cell-mediated immune response, it can be predicted that a negative relationship exists between singing performance and activity of the immune system. This prediction was tested for the first time in this correlational study. The relationships between song rate and features and hematological variables (concentration of leukocytes in peripheral blood, ratio of gamma-globulins to total plasma proteins, Mood cell sedimentation ratej • hematocrit) and body condition were analyzed in a population of barn swallows (Hirundo rustica). Song rate was negatively correlated with lymphocyte concentration and with the ratio of gamma-globulins to plasma proteins. Spectrographic analysis showed that features of song were not significantly correlated with hematological variables or body condition. The level of circulating testosterone was not correlated with song rate nor hematological variables. Thii study is the first to show a correlation between a bird's singing performance and hematological profile and suggests that song rate of male barn swallows may reflect their health status. Song in this species might thus have evolved because it allows prospecting females to assess aspects of phenotypic and/or genetic quality of potential mates. Ecol 8:364-371 (1997)]
Hamilton and Zuk proposed that conspicuous male plumages of birds could be reliable signals of parasite resistance. We examined this prediction in a system involving blood trypanosomes in a passerine bird, the pied flycatcher (Ficedula hypoleuca). Trypanosome prevalence and intensity of infections were unrelated to male age and expression of a secondary sexual trait. However, trypanosome infections were absent or maintained at significantly lower levels in females expressing a male trait which females have been shown to prefer in males. This relationship held even after controlling for the significant effects that female age had on both the expression of the male trait and the rate of parasitism by trypanosomes. Given that the male trait is heritable and genetically correlated between the sexes, and there exists assortative mating based on white patch size and/or expression, a system of mutual mate choice may exist. In such a system, the benefits accrued to both males and females would be a higher chance of successful mating and the acquisition of genes for resistance to parasites to transmit to the offspring. These data thus support by an alternate route Hamilton and Zuk's hypothesis on parasite-driven sexual selection.
The effect of malarial parasitism on the ability of male western fence lizards, Sceloporus occidentalis, to compete for access to females was assessed experimentally. Pairs of male lizards, one infected with the malarial parasite, Plasmodium mexicanum, and the other not infected, were matched by size and color and placed in large seminatural outdoor enclosures along with an adult female lizard. Infected males displayed to females and to other males less often than did noninfected male lizards. Noninfected lizards were dominant in social interactions more often than malarious animals, based on duration and intensity of agonistic encounters toward the other male, and time spent with the female. Thus, malarial infection hinders the ability of male fence lizards to compete for mates.
The influence of parasites on mate selection and on a secondary sexual character was studied in guppies (Poecilia reticulata). In fish infected with Camallanus cotti or Gyrodactylus, females were found to prefer males with relatively few parasites, and this preference was associated with a higher display rate in less parasitised males.
Numerous mechanisms have been proposed to account for the evolution of cryptic and bright coloration in passerine birds. The Hamilton-Zuk revealing handicap model holds that cyclic interactions between hosts and parasites maintain additive genetic variance in secondary sexual traits and adaptive mate choice of resistant genotypes ensues (Hamilton and Zuk, 1982). Here I report no support for this model using various within-taxa techniques to test the functional relationship between the prevalence of hematozoan parasites and male brightness in many species of North American passerines. I establish that phylogeny and predation risk are most strongly associated with variation in male coloration. Ground-nesting passerines are considerably more cryptic than off-ground nesters, and there is evidence that ground-nesting passerines are under greater predation risk. Predation risk may limit the role of sexual selection in the development of bright coloration.
Fluctuating asymmetry (FA) in ornamental characters may reflect developmental stability in the translation from genotype
to phenotype. Antlers of reindeer show FA, are visually conspicuous ornaments and are important in intraspecific assessment.
We show that there is a negative relationship between size and asymmetry in visual antler characteristics (i.e., antler length
and number of tines) among free-ranging male reindeer in rut. This indicates that individuals that develop large ornaments
are better able to buffer developmental stress than individuals that develop small ornaments. There is no relationship between
asymmetry in antler length and asymmetry in jaw length, suggesting that symmetry in antlers does not reflect overall body
symmetry. This difference may be caused by trait-specific sensitivity to developmental stress. Such stress may partly be caused
by parasites, which show a positive association with asymmetry in antlers, but no relationship to asymmetry in jaws. Our results
indicate that antlers may be exposed to directional selection in a visual signaler-receiver system and that information about
parasite burden may be obtained from evaluation of asymmetry in antlers developed under exposure to a multitude of environmental
stresses.
Presents the results of an exploratory study into the correlations between Quiscalus quiscula phenotypes and morphology, and describes sources of natural variation in parasites and morphology within populations that may complicate interpretations of field data. Unequivocal support for the Hamilton-Zuk hypothesis did not emerge from preliminary study of haemotropic parasites in common grackles. The best test of Hamilton and Zuk's hypothesis is an examination of parasite-associated variation in epigamic characters, including behaviour, within an avian host species. -from Authors
Describes the relationship between bill colour and parasite load in Taeniopygia guttata castanotis studied in Northern Territory (Alice Springs and Top End) and Victoria, Australia. Some 80% of birds were infected by ectoparasites, largely by the mite Pellonyssus reedi (Acarina; Macronyssidae) and two undescribed Mallophaga (Brueelia sp. and Myrsidea sp.), though Ornithophila metallica (Diptera: Hippoboscidae) was also recovered. Contrary to predictions of the Hamilton-Zuk hypothesis, ectoparasite counts tended to correlate positively with bill colour in adults. Possible reasons are discussed. -P.J.Jarvis
Presents the results of a comparative study of haematozoa of tropical Central and South American birds and discusses the value of such studies for critically evaluating the Hamilton and Zuk hypothesis. The tropical data set allowed the study of a much larger sample (526 species) than had previously been examined, and one containing many of the gaudy birds found in tropical habitats. Use of tropical birds allowed comparison between migrant and resident species; because the Hamilton-Zuk hypothesis requires that parasites coevolve closely with their hosts, resident species should show the relationship between brightness and parasite level more strongly than migrant species, which are more likely to be exposed to different sets of haematozoa in wintering and breeding habitats. The confounding effect of phylogeny must be dealt with, ie certain groups of species may show the association between brightness and infection level merely because of shared ancestry. -from Author
In lek breeding sage grouse in E California, male mating success is strongly correlated with individual differences in lek attendance, and in the rate and acoustic quality of courtship display, suggesting that these provide cues by which females choose mates. Increased lek attendance and high display rates are also associated with elevated metabolic expenditure. This paper examines the hypothesis that the ability to commit energy to display is related to the incidence of blood parasites. A single hematozoan genus, Haemoproteus, was found in 37.5% of sage grouse. Parasitism varied across years and increased through the breeding season, but no measure of display performance or mating success was significantly correlated with decreased parasite load among adult males. Several additional lines of evidence, including numerically low infection intensities, absence of detectable effects of parasites on hematocrit and erythrocyte production, and seasonal distribution of parasite incidence all suggested that infections were unlikely to impact male courtship display. Alternative factors maintaining individual variation in male display performance in this population are evaluated. -Author
Provides empirical evidence to evaluate the Hamilton and Zuk hypothesis relating to coevolution of parasites and host as a mechanism for maintaining heritable variance in true fitness amongst males, ie that secondary sexual characteristics may allow females to select mates that are relatively resistant to the parasite genotypes exploiting the host population at that time. By mating with such males, females obtain resistance genes for their offspring. Female Centrocercus urophasianus do preferentially mate with males bearing low parasite loads. Sage grouse offer a good opportunity to study lek behaviour since large populations occur in relatively undisturbed habitats near Laramie, Wyoming, and they are easy to capture, mark, and observe. -from Authors
The functions of the little-studied avian spleen are reviewed and compared with those of its better known mammalian counterpart, which is generally larger in proportion to body size than in birds. A role in immunity similar to that in mammals is evident, but the organ's contribution to oxygen supply seems less extensive; splenic storage of erythrocytes, for example, is unrecorded for birds. The spleen is a principal organ of systemic immunity, and its importance in disease resistance is presumably accentuated by the scarcity of avian lymph nodes. The striking intraspecific variation in size partly reflects seasonal changes in spleen morphology and activity. Several explanations, principally based on changing oxygen demand, have been proposed previously for these periodical cycles. But seasonally small spleens could sometimes simply stem from a combination of (1) a cessation of active splenomegaly as seasonally patent infections recede, and (2) a seasonal lymphoid involution, occurring even if an individual has not recently responded to, and recovered from, an infection. Possible determinants for these and other processes are discussed from evolutionary and ecological perspectives. There is a pressing need for a thorough investigation of both hematological and immunological functions, using a phylogenetically and ecologically broad range of species, as well as modern histological and experimental techniques.
The Hamilton-Zuk hypothesis of sosigonic selection argues that intensity of mate choice and corresponding ornamentation is positively related to pressure from parasites that are competent to engender positive heritability of fitness. Research into this idea has been controversial, not least for the original group of species studied: nearctic passeriforms. These birds are examined yet again, addressing certain published reservations about previous results: (1) using phylogenetic regression to cater for similarity linked to shared ancestry, (2) investigating only independently scored brightness data, (3) excluding species represented by small samples of birds examined for parasites, as well as (4) those represented by zero haematozoa prevalences, and (5) controlling for sampling effort, body weight and ecological variables. For the data as a whole the association between total brightness and the number of birds parasitised by haematozoa relative to the number of individuals examined (haematozoa relative presence) was not consistently significant. Likewise when front and back brightnesses were considered separately nonsignificance resulted. On controlling for ecological variables, significant positive regressions were found more often with front brightness than with back brightness. Furthermore, brightness and mating system interact significantly with each other in their relations with the parasitism index. Following from this, omission of overt polygynists produced a robustly significant, positive, relationship between front brightness and relative parasite presence. This regression, involving 82 apparently monogamous species, explained only ca 10% of the total variation. The findings support parasite-mediated sexual selection, while at the same time emphasising additional factors in the determination of bird species' brightness and sexual selection intensity.
Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra-pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra-pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra-pair copulations and hence extra-pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra-pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra-pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.
Studies the effect of the parasitic haematophagous tropical fowl mite (Ornithonyssus bursa, Macronyssidae, Gamasida) on the reproduction of Hirundo rustica (Hirundinidae). Barn swallows regularly reuse old nests, but avoid old nests with mites. New nests are not primarily infected from old nests harboring large mite populations. Mite population density per nest after fledging was significantly positively related to mite population density on adult swallows upon arrival at the breeding site in early spring the same year. Mate choice may significantly affect levels of ectoparasitism, if parasite loads of nests originate from inoculates provided by adult barn swallows. Addition of mites to nests decreased reproductive success of the birds measured in terms of number of independent fledglings of 1st clutches and in terms of clutch size, brood size, and number of independent fledglings of 2nd clutches. Barn swallow nestlings in nests with mites had lower body mass but similar body size compared with nestlings in pyrethrin-sprayed nests. Incubation periods were longer and nestling periods shorter for nests with added mites. Interclutch intervals were significantly shorter in the group of sprayed nests, mainly because more such nests were reused for 2nd clutches and because adult swallows suffered less from mite infestations. Slightly fewer barn swallows had second clutches during the same breeding season if their nests held many mites. -from Author
We used data on the prevalence of blood parasites in approximately 5,000 individuals of 10 warbler (Parulinae) species captured in New Brunswick and Newfoundland to test the prediction that parasitism and plumage brightness should be positively correlated. We used independent subjective assessments of plumage brightness and two subjective and one objective estimate of plumage dimorphism. No significant correlations were found be- tween parasitism and any index of plumage. We found inconsistencies in our estimates of parasite prevalence for the same species sampled at two different sites and between males and females of the same species. These inconsistencies may be due to sampling error or to ecological differences between sites that produced different patterns of exposure of the birds to the parasites' vectors. Inability to quantify parasites accurately and consistently will make the testing of the Hamilton and Zuk hypothesis of sexual selection more difficult. Received 20 February 1990, accepted 21 August 1990.
The Hamilton & Zuk (1982) hypothesis of parasite-mediated sexual selection has been the subject of both inter- and intraspecific tests. Past reviews have used vote counting to determine whether this hypothesis is supported by empirical evidence. This study reanalysed 199 separate quantitative assessments of a central prediction of the Hamilton & Zuk hypothesis using meta-analytical techniques. Overall, our meta-analysis showed that there was a significant negative effect of parasites on male showiness as predicted. However the magnitude of this effect varied between host taxa and between endo and ectoparasitic taxa. As a whole intraspecific correlations between parasite load and male showiness provided very little support for the hypothesis with only the effect of parasites on fish morphology matching the Hamilton & Zuk prediction. There was more support for the hypothesis from interspecific studies especially those based upon the original Hamilton & Zuk (1982) data set, although other bird studies provided weaker support. The generality of the Hamilton & Zuk hypothesis in respect to parasite mediated sexual selection across taxa is thrown into doubt by these results. However, in some specific host-parasite systems the role of parasites appears important and future intraspecific tests of parasite-mediated sexual selection should perhaps focus on such systems.
In experiments using sets of 12 individually caged male field crickets (Gryllus veletis and G. pennsylvanicus) suspended above pitfall traps in an outdoor enclosure, each male attracted zero-nine females over a 4-day period in which 48–60 females were released. Male age was significantly positively correlated with the number of females attracted in both species, whereas male body size, time spent calling and level of infestation with gregarines (protozoan gut parasites) were unrelated to male attractiveness. Older male G. pennsylvanicus (at least 15 days past adult moult) also attracted significantly more females than did younger males (7–9 days after adult, moult) when pitfall traps and cages were set in the field, allowing naturally occurring females to fall into the traps. Because males were kept from contacting each other in the experiments examining correlates of attractiveness, females appeared to be actually choosing older males, rather than indirectly relying on the results of male-male competition.
The handicap hypothesis of honest signaling suggests that secondary sexual characters reliably reflect phenotypic or genotypic
quality of signalers. This hypothesis is based on the assumptions that signals are costly to produce and/or maintain and the
cost of a given level of signaling is higher for low quality than for high quality signalers. We tested these assumptions
in a field experiment in which the size of a secondary sexual character [tail length in male barn swallows (Hirundo rustica)] was experimentally manipulated. Males were randomly assigned to tail elongation, tail shortening, or two control treatments
(tail manipulation, or just capture, ringing, and handling). Male barn swallows were challenged with an injection of sheep
red blood cells, and blood was sampled on the day of first capture and after 3 to 4 weeks for determination of concentrations
of gamma-globulins. Tail-elongated males did not increase levels of gamma-globulins while males of the other three groups
demonstrated increases. Analyses of variation in gamma-globulins within treatment groups revealed a positive correlation between
gamma-globulins and original tail length among males with elongated tails. These results suggest that tail length imposes
an immu-nocompetence cost on males, and that males with naturally long tails are differentially better able to cope with this
cost.
Demonstrates for European and North American passerine birds that the proportion of individuals infected with blood parasites is significantly lower in polygynous than it is in monogamous species. One possibility is that polygynous species are, on average, more resistant to hematozoa infection. This could arise if there is heritable variation in resistance and if polygyny results in resistant males obtaining more mates. Females in polygynous species might settle with already-mated resistant males rather than unmated, less resistant males if they choose males resistant to parasites currently invading the population or if their decision to settle is influenced by the outcome of male-male competition, which might in part be affected by the health of the combatants. -from Author
We infected male guppies Poecilia reticulata with a naturally occurring monogenean parasite, Gyrodactylus turnbulli, in order to examine effects of parasitism on the expression of color patterns and on attractiveness to females. The color of carotenoid spots and ability to attract females were compared between experimentally infected fish and a control group of their fullsib brothers, which had identical color patterns and were treated identically except for actual exposure to parasites. The orange spots of males that had been infected for 9 days followed by treatment with medication to remove parasites became significandy paler and less saturated. Control males (also treated widi medication) showed no significant changes in their orange spots. Females in a divided aquarium choice-apparatus showed no preference between control and infection-treatment males initially, but showed significant discrimination after the infectiondisinfection treatment. Females spent less time near males that had been infected and responded to a smaller fraction of their courtship displays relative to control males. There were slight differences in courting rates of males between treatments. Parasitic infection appears to reduce the degree of expression of carotenoid colors in guppies, and females are able to discriminate against recently infected males, probably on the basis of the color change. By avoiding infected males, females may be able to avoid becoming infected themselves, or they may be able to identify mates based on "good genes" for parasite resistance diat can be passed on to their offspring.
Consistently with previous studies, female red jungle fowl (Gallus gallus) preferred to mate with males with longer, redder combs, but paid little attention to plumage characters. Individual variation in comb length was positively correlated with plasma testosterone level. Males with longer combs had fewer circulating lymphocytes, as would be expected if maintenance of secondary sexual characters is costly to the immune system.
One hypothesis assumes that sexual ornamentation has evolved to reveal an individual's health and vigour. Therefore, choosy mates may use ornamentation as an indicator of the presence and effectiveness of genes for resistance against parasites (Hamilton & Zuk (Science, Wash. 218, 384 (1982))). However, the connection between parasites and sexual ornamentation may be more direct: the different characters of the ornamentation could reveal the contribution of each sexual hormone to the whole hormone mix that induced the ornamentation. As androgens and oestrogens are known to weaken specifically parts of the immune system (Grossmann 1985), and several parasites require a specific aspect of the immune system to be countered effectively, the hormone mix may reveal the actual use of an animal's immune system which depends on the presence and burden of, or even susceptibility to, different parasites. Therefore detailed information about a host's parasites could be available by studying its sexual ornamentation. Breeding tubercles, the sexual ornamentation of many fish, are induced by several androgens and at least one oestrogen (Wiley & Colette 1970). I studied four characteristics of the ornamentation of male roach (Rutilus rutilus) and found that two of them could be used to discriminate between males that are infected with either Diplozoon or nematodes, the two most severe parasites found. Furthermore, the number of parasites of each group correlates negatively with the expression of one or both of the other ornamental characters. A female roach could potentially decode a male's ornamentation to gather a sort of clinical picture of him and use this information in her choice of mate.
Tested 3 conditions of the Hamilton and Zuk hypothesis (1982), which suggests that the extravagant male plumage of many bird species allows females to choose mates that are resistant to the parasites exploiting the host population at a given time: 1) whether parasites affect the fitness of their hosts; 2) whether there is heritable variation in parasite resistance, and 3) whether the expression of the sexual ornament varies with parasite burden. The haematophagous mite Ornithonyssus bursa (Macronyssidae, Gamasida) sucks blood from their barn swallow hosts. Parasite burdens and origin, but not rearing conditions, of nestlings, affected their adult tarsus length and maximum body weight shortly before fledging. Mite loads of adult barn swallows at spring arrival were more similar to mite loads of their own offspring, whether reared in their own or in foster nests inoculated with mites, than to loads of foster offspring. Parents with long tail ornaments had offspring with smaller mite loads in partial cross-fostering experiments. The amount of increase in male tail ornaments from one year to another was negatively related to experimentally manipulated mite loads of nests during the preceding breeding season. The assumptions of the hypothesis were thus supported. -from Author
HAMILTON and Zuk1 proposed that elaborate secondary sexual characters may have evolved because they act as cues in mate choice by revealing the health of a potential mate. From this theory, they derived the prediction that species which are more liable to parasitic infection should possess well-developed secondary sexual characters. They went on to demonstrate a positive association between prevalence of haematozoa and plumage brightness across species of North American passerine birds. Subsequent analyses by one of us2 on the same colour data confirmed that the relationship with male brightness existed even when the effects of phylogenetic associations were taken into account. The relationship was also found across European passerines when behavioural and ecological correlates of colour and phytogeny were accounted for2. Here, using independently derived plumage brightness scores, we question these conclusions.
Tested the following predictions in the barn swallow: (1) The expression of the secondary sexual characters is directly related to circulating levels of androgens. (2) Males with large secondary characteristics have few parasites. (3) High circulating levels of androgens do not lead to an increased abundance of parasites. Captured barn swallows were measured for morphological characters and checked for eco-parasites. Ss were observed at breeding sites throughout the breeding season; testosterone plasma levels were measured. Results suggest that the expression of the secondary sexual character was positively related to circulating levels of testosterone in the barn swallow. Evidence does not suggest that this relationship affects the ability of the swallows to cope with parasites, since sexually attractive, long-tailed males had fewer parasites than short-tailed males. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Darwin1 proposed that secondary sexual characters, such as
the long tails and bright plumage of many birds, evolved because females
use them as cues in male choice. The question of why females should
prefer males with such apparently deleterious characters is currently
the subject of vigorous debate2-7. Hamilton and
Zuk8 suggest that females use secondary sexual characters to
assess a male's ability to resist parasites. A prediction of this
hypothesis is that male brightness should correlate positively with
parasite load across species, and the only evidence advanced in support
of the model is Hamilton and Zuk's8 finding that such a
correlation exists across North American passerines. But interspecific
correlations of this sort can result from phylogenetic associations
through common descent or from independent associations with some
confounding variable, such as an aspect of behaviour or
ecology9-13. Here, I use data on European passerines and an
enlarged data set on North American passerines to demonstrate positive
relationships between male brightness and parasite prevalence which
remain when the effects of taxonomic, behavioural and ecological
variables are removed.
Through a series of replacement experiments with the bluehead wrasse, Thalassoma bifasciatum, we have identified male morphological characteristics that appear to be under phenotypic sexual selection. We were particularly interested in whether the various sources of sexual selection (male-male competition for unoccupied mating sites, defense of mating sites against small males, and female choice of males) were (1) independently associated with different phenotypic characteristics; (2) jointly affected the same characteristic in the same way; or (3) jointly affected the same characteristic in an antagonistic fashion. We replaced the resident large, brightly colored Terminal Phase (TP) males on a reef with the same number of TP males from other reefs. When transplanted, these males contest with each other to take over mating sites. The transplanted group of males were then scored for three components of fitness: (1) the quality of the site obtained through competition with other large males; (2) the male's ability to defend arriving females from small intruding males; and (3) changes in female visits to the site once the new male takes over. The first and second components are part of intrasexual selection; the third represents intersexual selection. We measured the opportunity for selection by partitioning variance in mating success, and measured the direct effects of sexual selection by estimating the covariance between morphology and fitness components. Opportunities for selection: Because females generally remain faithful to particular mating sites, most (54%) of the explainable variation in male mating success is due to the acquisition of a particular mating territory, which is the outcome of competition among TP males. There was less variation in mating success due to shifts in site use by females and defense of females against the intrusions of smaller males, but all components were significant. Effects of selection: Success in male-male competition among TP males, estimated by the quality of the territory acquired, was positively associated with body length and the relative length of the pectoral fin. Success in territorial defense against small males was primarily related to body length, with lesser contributions from body depth and the area of a white band on the flank. Contribution to fitness through female choice of males was positively associated with white band area. In the two instances where a character was associated with two fitness components, the direction of selection was the same. While body length was positively associated with winning intrasexual contests, it was not correlated to any behavioral measures of aggression. Similarly, the white band associated with attractiveness was not correlated with any aspect of courtship or aggression. Parasite load was uncorrelated with other morphological characters, and did not appear to affect any aspect of sexual selection. There was no evidence for stabilizing selection or significant additional contributions from second-order effects to the fitness surfaces. Fitness functions calculated using cubic splines were generally linear except for body length, which appeared sigmoid in its effect on site acquisition ability; this same feature tended to plateau in its effect on site defense. Analyses of the interactions of selection gradients with reef or experiment indicated that the effect of particular male characters on estimates of fitness was generally homogeneous in both time and space.
As predicted by the parasite burden-mate competition hypothesis (Howard and Minchella), significant relationships were observed between the prevalence and/or intensity of infection by the liver fluke, Fascioloides magna, and traits contributing to male reproductive success in white-tailed deer. Body size and total number of antler points were significantly reduced in heavily infected individuals, particularly for the younger age classes. Infected males lost significantly more weight than uninfected ones during the rut. Losses were more pronounced for males in older age classes. as might he expected if they expend the most energy during the breeding season.
1. An extensive post-mortem survey of grouse revealed that birds killed by predators in spring and summer had significantly greater burdens of the caecal nematode Trichostrongylus tenuis than grouse shot during the autumn. Furthermore, grouse that appeared to have died through the effects of parasites carried greater worm burdens than grouse killed by predators. 2. The proportion of grouse with high levels of parasite infection increased with the intensity of predator control as measured indirectly through keeper density. These two empirical observations suggest that predators selectively prey on heavily infected grouse. 3. The interactions between parasites and predators were examined experimentally by reducing the worm burdens of female grouse with an oral anthelmintic. Nests of treated and untreated females were subsequently located either by research workers flushing the incubating female or by dogs trained to locate birds by scent. The dogs found significantly fewer of the treated than control birds, suggesting that female grouse with large parasite burdens emit more scent and are more vulnerable to mammalian predation. 4. A modified mathematical model of the grouse-nematode system is described which incorporates the effects of both random and selective predation of heavily parasitized grouse. An analysis of the model illustrates the importance of interactions between grouse, parasites and predators in determining the relative densities of each. In particular, when predators selectively remove heavily parasitized individuals, then low levels of predation can lead to increases in the size of the host (or prey) population.
The American kestrel (Falco sparverius) — Trichinella pseudospiralis host-parasite association was used as a laboratory model to study the effect of a nematode infection on (1) mate choice of female kestrels and (2) competitive abilities of male kestrels during the breeding season. Females were given the opportunity to choose between infected and uninfected males. There was no significant difference in the proportion of females that chose uninfected (n = 18) over infected (n = 16) males. Eight of 11 competitions between infected and uninfected males exposed to a caged female and a nest box were dominated by uninfected males. Female kestrels seemed to base their choices on the intensity of display effort by the males; the experimental level of infection did not affect male courtship behaviour. Although T. pseudospiralis is known to debilitate American kestrels, parasitized males in mate-choice tests may have diverted energy from less important functions to court the females.
Hamilton and Zuk (1982) suggested that females could continuously base their choice of mates on heritable resistance to parasites, as generated in a process of coadaptational cycles of hosts and their parasites and advertized in terms of individual differences in plumage features or displays of the chosen sex. This hypothesis was based on three assumptions: (1) the full expression of secondary sexual traits of individual hosts is dependent on their overall health and vigour; (2) hosts are coevolving with their parasites, thereby continuously generating heritable resistance to parasites; and (3) parasites have negative effects on host viability. Given these assumptions one may then make the following intra- and interspecific predictions: (1) females will obtain mates with few or no parasites by choosing males with fully expressed sexual ornaments, (2) males with inferior ornaments will be less desirable partners and therefore take longer to become mated, (3) assortative mating occurs with respect to parasite loads, (4) females which mate with males with poorly developed secondary sexual characters will copulate outside their pair bond with males showing more fully expressed ornaments, and (5) in species especially vulnerable to parasite invasions, sexual selection will lead to more extreme development of health-certifying traits, allowing females to more accurately assess the parasite load of a male. Here I shall evaluate the empirical evidence for these assumptions and predictions and discuss alternative hypotheses advanced, in order to explain the importance of parasites for the sexual selection theory. An open question not yet studied satisfactorily is whether, and how often, coadaptational cycles exist, and, if they exist, how they should affect mate choice.
Hamilton and Zuk (1982) suggested that secondary sexual characters evolve because they allow females to assess a potential mate's ability to resist parasites. A prediction of this theory is that the degree of elaboration of secondary sexual characters should be positively correlated with parasite load across species. In support of their hypothesis, Hamilton and Zuk reported a correlation across North American passerine species between haematozoa prevalence and both brightness and song complexity and variety, scored on a subjective six point scale. Here we show that this relationship is confounded by phylogenetic associations. We use quantitative data on song duration, inter-song interval, song continuity, song rate, song versatility, and song and syllable repertoire size for 131 species of European and North American passerines to test the Hamilton-Zuk hypothesis. Across species, there are significant negative relationships between haematozoa prevalence and song continuity, contrary to the direction predicted by Hamilton and Zuk. In accordance with their prediction, there is a positive correlation with song versatility. However, these relationships come about through taxonomic associations: within taxa there are no consistent relationships between any of the song variables and haematozoa prevalence. None of the other song variables correlate with haematozoa prevalence. We conclude that there is no evidence of an association between song elaboration and parasites.
The number of a common parasite (Cuclotogaster sp.) on male satin bowerbirds was related to male mating success in a test of Hamilton and Zuk's (1982) bright male hypothesis. The data do not show the expected inverse correlation between female mating preferences and the level of parasitic infection of males predicted by that model. Nearly all matings are accomplished by bower-holding males (Borgia 1985a), but the vast majority of these males were uninfected. There were large differences in mating success among the uninfected bower holders, but this could not be explained by between male differences in the level of parasitic infection. From this I conclude that levels of parasitic infection are not now an important direct cause of intermale variation in mating success. The results are, however, consistent with a hypothesis that a low level of infection is indicative of the overall healthy condition of a male. If this is true, it supports the hypothesis that the ability to hold a bower may be an indicator of male condition to females.
Despite a tendency for males of polygynous bird species to show bright or elaborate plumage, comparative analyses have failed to show any consistent relationship between male brightness or plumage dimorphism and the form of breeding systems. Here we argue that this may be partly because the opportunity for sexual selection varies between species showing serial or seasonal monogamy and life-long monogamy. In waterfowl, both the brightness of male plumage and sexual dimorphism in colouration vary between these categories of monogamy. Other ecological factors related to male brightness or plumage dimorphism include male assistance in protecting young, latitude and an index of parasite sharing. The adaptive significance of these trends is discussed.
We examined associations among parasite infections, secondary sexual traits and testosterone in male red-winged blackbirds sampled at the start of the breeding season. Parasites quantified included ectoparasitic lice and mites and endoparasitic blood protozoans, nematodes, trematodes and cestodes. Secondary sexual traits that we quantified included body size, epaulet size and color, song repertoire size and song switching rate, and behavioral responses to male and female models. Overall we found few significant associations between parasites and secondary sexual traits, between secondary sexual traits and testosterone, or between parasites and testosterone. In addition, most parasite taxa appeared to infect birds independently, although the low prevalence (
Female mate preferences for extreme male ornaments may arise and be maintained because males signal their ability to raise
an immune defence against parasites by the size of their ornaments. The bursa of Fabricius is an organ involved in antibody
synthesis in young birds, but regresses before sexual maturity. The relationship between badge size, condition, and immune
defence was investigated in male house sparrows, Passer domesticus, which have a bib of black feathers under their beak, a secondary sexual character currently subject to a directional female
mate preference. The size of the bursa of Fabricius decreased during the first year of life in house sparrows. Males with
large secondary sexual characters had a smaller bursa than males with small badges. Individuals with a large directional asymmetry
in relative testis size had a larger bursa. The abundance of one parasite (a mallophagan) was positively related to bursa
size. There was a positive relationship between relative volume of bursa of Fabricius and the number of fault bars on feathers,
which is a measure of body condition. These results suggest that males with large badges have lower current levels of immune
response than males with small badges, and that males in good body condition, as evidenced from the absence of fault bars,
had a relatively small bursa of Fabricius.
We examined the hypothesis that trematode parasites played a role in the evolution of the red colour of male threespine sticklebacks (Gasterosteus aculeatus L.) and whether the parasites affected female fitness. Parasites (blackspot disease) played no role either in determining the outcome of male—male competition for breeding territories or in female mate choice. Among males with territories, mating success was highly variable. Some males obtained over 3000 eggs (approximately 10 matings) whereas others received none. In 1 year of the 2 year study, males with the greatest amount of red nuptial coloration had the greatest mating success. Although male colour may sometimes affect female choice in this system, this preference has probably not evolved because of the Hamilton—Zuk mechanism of sexual selection. The parasites had small, but statistically significant effects on female fitness. Females with high parasite loads were in poorer condition and produced fewer eggs than less parasitized fish.
Hamilton & Zuk (1982) predicted that there should be a relationship between a species' parasite load and its sexual showiness. The relationship between the number of parasite genera reported from a fish family and its sexual dichromatism was examined in British and Irish freshwater fish. Eleven other ecological and life history variables which may also cause sexual dichromatism were also examined. The changes in appearance that take place are always more marked in males and occur only during the breeding season. This strongly implicates sexual selection as an important selective determinant. There was a significant positive correlation between a fish family's sexual dichromatism and the number of parasite genera reported from it. This remained significant when the influences of near-significantly correlated ecological and life history variables were removed. Using more detailed published parasite data on six species, there was also a significant correlation between the mean number of parasite species per host individual and host sexual dichromatism. These results support Hamilton & Zuk's bright, parasiteresistant male and choosy female hypothesis.
Secondary sexual characters may have evolved because they allow females to assess the ability of conspecific males to resist parasites. In this study the prediction that the song output of swallow, Hirundo rustica, males will reflect their parasite load was tested. Male swallows sang more if they nested in colonies and were reproducing early during the season, and if their nests held few or no haematophagous tropical fowl mites, Ornithonyssus bursa. In one experiment the mite loads of swallow nests during the laying of the first clutch were manipulated and the song output of males during the fertile period of their mates prior to both the first and the second clutch was recorded. Song output did not differ between parasite treatments for first clutches (i.e. before treatment), but did so for second clutches, song output being inversely related to parasite abundance. In another experiment both mite loads of swallow nests and clutch sizes were manipulated simultaneously during the laying of the first clutch. There were no differences in song output between experimental groups for the first clutch, but mite load and the clutch size-mite load interaction affected song output during second clutches. It is likely that song output was reduced by the mites because, as a result of the anaemia they cause, they will reduce the working capacity of their hosts.