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Parasites, Bright Males, and the Immunocompetence Handicap
Abstract
It has been argued that females should be able to choose parasite-resistant mates on the basis of the quality of male secondary sexual characters and that such signals must be costly handicaps in order to evolve. To a large extent, handicap hypotheses have relied on energetic explanations for these costs. Here, we have presented a phenomenological model, operating on an intraspecific level, which views the cost of secondary sexual development from an endocrinological perspective. The primary androgenic hormone, testosterone, has a dualistic effect; it stimulates development of characteristics used in sexual selection while reducing immunocompetence. This "double-edged sword" creates a physiological trade-off that influences and is influenced by parasite burden. We propose a negative-feedback loop between signal intensity and parasite burden by suggesting that testosterone-dependent signal intensity is a plastic response. This response is modified in accordance with the competing demands of the potential costs of parasite infection versus that of increased reproductive success afforded by exaggerated signals. We clarify how this trade-off is intimately involved in the evolution of secondary sexual characteristics and how it may explain some of the equivocal empirical results that have surfaced in attempts to quantify parasite's effect on sexual selection.
... However, increases in androgenic steroids can have negative effects on male fitness. First, testosterone is a known immunosuppressant and can increase an individual's susceptibility to pathogens, parasites, and disease (Hamilton and Zuk 1982;Folstad and Karter 1992). Second, testosterone can increase metabolic rate, which leads to a reduction in body condition via mass loss (Marler and Moore 1988;Marler et al. 1995;Oppliger et al. 2004). ...
... Although theoretical support for trade-offs between immune function and the quality of reproductive characteristics is strong (Hamilton and Zuk 1982;Folstad and Karter 1992;Rowe and Houle 1996), empirical support in the literature is mixed (e.g. Roberts et al. 2004;Simons et al. 2012). ...
The theoretical trade-off between immune and endocrine investment in mating animals has received mixed empirical support, particularly in reptiles. We investigated the relationship between male sexual characteristics, diet, and immune response to stress in an island population of tuatara (Sphenodon punctatus) across two mating seasons. Tuatara are promiscuous, with a highly skewed mating system where males face significant competition for access to mates and postcopulatory competition for fertilization success. We found that tuatara sperm viability and swim speed were negatively associated with male body condition and the ratio of heterophils to lymphocytes. Additionally, sperm swim speed was negatively associated with spine area, mite load, and the total number of circulating white blood cells, but was positively associated with tick number. This is likely a function of social dynamics in this system where larger male size predicts greater spatial overlap with potential rivals and increased tick load. Because the production of sexual characteristics may be costly, we also investigated the effect of diet on sperm quality. We did not identify an association between diet and sperm viability. However, sperm swim speed was negatively associated with carbon-13 and positively associated with nitrogen-15. We suspect that these results reflect the influence of seabird-based nutrients in this island ecosystem, particularly polyunsaturated fatty acid, and antioxidant damage on tuatara sperm. In total, these results provide evidence of a trade-off between pre- and post-copulatory sexual characteristics and the immune and endocrine systems in male tuatara.
... Since higher testosterone levels are associated with increased immunosuppression [67], our main findings are in line with the compensatory prophylaxis hypothesis [13], suggesting that disgust sensitivity should be elevated during immunosuppression. Moreover, previous studies have observed higher disgust sensitivity in women pregnant with male compared to female fetus [10,30], possibly reflecting mechanisms that lead to elevated testosterone levels in women pregnant with a male fetus [68]. ...
The emotion of disgust protects individuals against pathogens, and it has been found to be elevated during pregnancy. Physiological mechanisms discussed in relation to these changes include immune markers and progesterone levels. This study aimed to assess the association between steroids and disgust sensitivity in pregnancy. Using a prospective longitudinal design, we analyzed blood serum steroid concentrations and measured disgust sensitivity via text-based questionnaires in a sample of 179 pregnant women during their first and third trimesters. We found positive correlations between disgust sensitivity and the levels of C19 steroids (including testosterone) and its precursors in the Δ5 pathway (androstenediol, DHEA, and their sulfates) and the Δ4 pathway (androstenedione). Additionally, positive correlations were observed with 5α/β-reduced C19 steroid metabolites in both trimesters. In the first trimester, disgust sensitivity was positively associated with 17-hydroxypregnanolone and with some estrogens. In the third trimester, positive associations were observed with cortisol and immunoprotective Δ5 C19 7α/β-hydroxy-steroids. Our findings show that disgust sensitivity is positively correlated with immunomodulatory steroids, and in the third trimester, with steroids which may be related to potential maternal-anxiety-related symptoms. This study highlights the complex relationship between hormonal changes and disgust sensitivity during pregnancy.
... Shoulder-to-hip ratio is a sexually dimorphic trait in humans, where men on average have larger SHR compared to women. SHR is used as a metric of upper body mass and is considered an honest signal of immunocompetence, as only high-quality males would be able to withstand environmental pressures and be able to display a costly trait (Folstad & Karter, 1992;Zahavi & Zahavi, 1997). Muscularity may reflect underlying physiological quality (e.g., parasite and disease resistance) given the energetic demands of growing larger and fitter bodies (Sell et al., 2017). ...
Physical features in men, such as height and shoulder-to-hip ratio (SHR), have been shown to contribute to women’s mate preferences. The independent and interactive effects of height and SHR have been shown to be associated with attractiveness, masculinity, dominance, and fighting ability. It is suggested that these sexually dimorphic features are a reflection of men’s genetic quality, in addition to the ability to provide direct benefits (e.g., protection, resource provisioning). The current study investigated how ecological harshness may modulate women’s mate preferences to men displaying variations in height and SHR ratio. In a sample of predominately Hispanic women (N = 247), manipulating ecological harshness did not affect their ratings of men. Women considered taller men with larger SHRs as more attractive, masculine, dominant, and higher in fighting ability. Interestingly, these ratings were moderated by individual differences in women’s mate value but not sociosexuality. Women with higher mate value rated all men who were taller than the anchor woman (172 cm) in the presentation sequence as more attractive, masculine, dominant, and higher in fighting ability. The findings replicated previous research on the interactive effects of men’s height and SHR and showed that women calibrate their mating preferences as a function of their overall mate quality (i.e., mate value).
... Another explanation for SBP could be provided by androgenic hormones, such as testosterone, which are essential for the expression of male sexual characteristics and behaviour, but which on the other hand lead to immunodepressive side effects. This view is supported by Folstad and Karter (1992), who state that the empirical evidence from several vertebrate taxa clearly indicates that testosterone increases susceptibility and pathogenicity of parasitic infections and suppresses the immune system. The hypothesis of testosterone-parasite interplay has also been investigated in deer and supported by field results. ...
The existence of bronchopulmonary nematodes in German roe deer Capreolus capreolus is well documented, with two types of lung parasites that have been described previously: Dictyocaulus capreolus and Varestrongylus capreoli. However, little is known about the impact of these parasites on their host animal or which parameters influence outbreak and intensity of infection. The aim of this study was to obtain new information on the relevance of factors such as season, environmental conditions or age, sex, and body mass of the infected roe deer. To obtain our results, the respiratory tracts of 762 roe deer from south‐eastern Germany were examined.
In the sample, 42.5% of roe deer were infested with V. capreoli and 14.0% with D. capreolus, and 51.3% of animals were completely free of lung parasites. Testing for influencing variables, our regression models found both sex and age of the roe deer to statistically influence infestation, with male sex and younger age correlating with both stronger infestation and higher infestation rates. Accordingly, in male animals the infestation rates with V. capreoli and D. capreolus (45.1% and 20.1%, respectively) were higher than in females (39.4% and 8.0%, respectively).
The overall infestation rate of juvenile animals was remarkably higher (73%) than those of sub‐adults (38.3%) or adults (28.4%).
Across all age groups, infested animals showed lower body weights compared to non‐infested animals. According to our multiple linear regression model, roe deer infected with D. capreolus on average weighed 0.65 kg less than their healthy counterparts, and in the case of V. capreoli 0.72 kg less on average. While the burden on the well‐being of infested animals can only be assumed, these concrete figures (reduced body weight in infested compared to healthy animals) demonstrate the economic damage lung parasites cause to meat harvesting from bagged roe deer.
... We believe that this differentiation between the sexes, especially the predominance of male involvement, and the regression seen with choline chloride treatment is an important result. Considering that sex hormones, especially testosterone, modulate the dimorphism process of the normal brain during early development and the testosterone-immune deficiency handicap hypothesis (Folstad & Karter, 1992;Kissick et al., 2014;Xuan & Hampson, 2014), we suggest that this may be the possible reason why the endotoxic environment caused by prenatal LPS administration affects males more. ...
The neuroprotective effects of choline chloride, an essential nutrient, a precursor for the acetylcholine and synthesis of membrane phospholipids, have been associated with neurological and neurodegenerative diseases. Its contribution to autism spectrum disorder, a neurodevelopmental disorder, remains unknown. Thus, we aimed to evaluate the effects of choline chloride on social behaviours, and histopathological and biochemical changes in a rat autism model. The autism model was induced by administration of 100 μg/kg lipo-polysaccharide (LPS) on the 10th day of gestation. Choline chloride treatment (100 mg/kg/day) was commenced on PN5 and maintained until PN50. Social deficits were assessed by three-chamber sociability, open field, and passive avoidance learning tests. Tumour necrosis factor alpha (TNF-α), interleukin-2 (IL) and IL-17, nerve growth factor (NGF), and glutamate decarboxylase 67 (GAD67) levels were measured to assess neuroinflammatory responses. In addition, the number of hippocampal and cerebellar neurons and glial fibril-lary acidic protein (GFAP) expression were evaluated. Social novelty and passive avoidance learning tests revealed significant differences in choline chloride-treated male rats compared with saline-treated groups. TNF-α, IL-2, and IL-17 were significantly decreased after choline chloride treatment in both males and females. NGF and GAD67 levels were unchanged in females, while there were significant differences in males. Histologically, significant changes in terms of gliosis were detected in hippocampal CA1 and CA3 regions and cerebellum in choline chloride-treated groups. The presence of ameliorative effects of choline chloride treatment on social behaviour and neuroinflamma-tion through neuroinflammatory, neurotrophic, and neurotransmission pathways in a sex-dependent rat model of LPS-induced autism was demonstrated.
... Finally, our findings support the role of testosterone as a phenotypic integrator which may be central to territorial behavior (Hau et al., 2016;Ketterson and Nolan, 1992 Testosterone levels were correlated with phenotypic traits, territory size, and ecological characteristics of territory in both species, which differ in the mating system, parental care, and acoustic communication strategies. It is widely documented that testosterone levels increase during the breeding season (Wilczynski et al., 2005;Wingfield, 1984;Wingfield et al., 1990) and that maintaining high levels of testosterone for a prolonged period of time involves high costs for the animals (Hau, 2007), such as suppression of immune function (Olsson et al., 2000), reduction of parental care (Wingfield et al., 1990), increase of parasitic infections (Folstad and Karter, 2002;Salvador et al., 1996), and reduced survival (Sinervo et al., 2000). It would be interesting to monitor testosterone levels throughout the annual cycle, especially in species with prolonged reproduction and that defending territory for several years (i.e., O. lehmanni) in order to expand understanding of the role of circulating testosterone and territoriality at different lifecycle stages and the regulation of aggressive behaviors in anurans. ...
Vertebrates exhibit sexual dimorphism in response to infectious diseases and in morbidity and mortality rates to various pathogens. Females are generally more immunocompetent than males, despite their increased reproductive burden and the immunosuppressive effects of gestation. In addition, females generally have lower incidences of cancer compared to males; however, they have higher rates of autoimmune disorders. These sex differences may be a result of life history differences, sexual selection, genetics, and/or the physiological effects of hormones. As highly social mammals with complex life histories, primates offer a unique opportunity to investigate the evolution of enhanced female immunocompetence. This review aims to examine the evidence of this immunity gap, understand current hypotheses for its evolution, and explore the potential role of X chromosome specific genes and heterozygosity within this framework.
Given the limited availability of resources in nature, sexual attractiveness may trade off with immunocompetence, as the immunocompetence handicap hypothesis (ICHH) posits. In invertebrates, a direct link between trade‐offs through hormonal/molecular effectors in sexual signals and immunity has not been found so far. Here, we assessed how variation in sexual signals affected parasite infection in two sex pheromone selected lines of the moth Chloridea virescens : an attractive line with a low ratio of 16:Ald/Z11‐16:Ald and an unattractive line with a high ratio. When infecting these lines with an apicomplexan parasite, we found that the attractive Low line was significantly more susceptible to the parasite infection than the unattractive High line. Since the ratio difference between these two lines is determined by a delta‐11‐desturase, we hypothesized that this desaturase may have a dual role, i.e., in the quality of the sexual signal as well as an involvement in immune response, comparable to testosterone in vertebrates. However, when we used CRISPR/cas9 to knockout delta‐11‐desturase in the attractive Low line, we found that the pheromonal phenotype did change to that of the High line, but the infection susceptibility did not. Notably, when checking the genomic location of delta‐11‐desaturase in the C. virescens , we found that mucin is adjacent to delta‐11‐desaturase . When comparing the mucin sequences in both lines, we found four nonsynonymous SNPs in the coding sequence, as well as intronic variation between the two lines. These differences suggest that genetic hitchhiking may explain the variation in susceptibility to parasitic infection.
A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions. Furthermore, evidence from other vertebrate taxa suggests strongly that the model is applicable to other classes
1305 reindeer (Rangifer t. tarandus L.) of different age and sex have been examined with regard to infections of second and third instar Hypoderma tarandi (L.) larvae. Females and castrates revealed low larval abundance compared with males and calves, and females show, in general, a decreasing larval abundance with increasing age. Intact males have, in contrast to females and castrates, a positive correlation between dressed weight and number of parasites. These results are discussed with reference to sex and age group variation in immunocompetence and avoidance behaviour to ovipositing warble-flies. It is suggested that reindeer acquire immunity to recurrent infections. Intact males are assumed to reduce the ability to elicit an effective immune response due to high plasma-free corticosteroid concentrations from the joint action of rut stress and high plasma-free testosterone concentrations. This may explain the different dynamics in males and castrates, and contain an element of stabilizing selection.
The possibility that the evolution of mating preferences and secondary sex traits can be based on heritable differences in viability is examined with a three-locus model. Earlier genetic models suggested that viability-based processes alone cannot explain the evolution of mate choice and sex ornaments that reduce survival; a Fisherian mating advantage seemed necessary. The present model is based on a monogamous mating system that precludes such a mating advantage. A key assumption is that ornament development depends on the phenotypic condition and overall genotype of the possessor; there is evidence that secondary sex traits often mirror nutritional status and health, sometimes through hormonal mediation. Ornament and preference can then hitchhike slowly to high frequency with alleles that confer a slight survival advantage, provided that such alleles become available often enough. The evolution of mating preferences and secondary sex traits that reflect overall genotypic constitution therefore can be based solely on viability differences, no Fisherian mating advantage being required. In practice, these and several other mechanisms of sexual selection may occur together.
The morphology and parasite burdens of culled free-ranging zoo Gallus gallus were compared with those of captive roosters. Zoo roosters had 3 helminth gut parasites: Ascaridia galli, tapeworms, and Heterakis. Parasite distribution was generally over-dispersed, with most individuals having none or few worms. These levels were comparable to those artifically induced in test roosters. The appearance of the zoo birds was also similar to test roosters. Higher parasite burdens in zoo birds was negatively related to hackle feather redness, comb length, and especially testis volume. The latter finding is duscussed in light of information about the relationship between testosterone levels, sexual section, and the immune system. Females prefer a multivariate array of traits perceived as a continuous, rather than categorical, variable. -from Authors
The plumage colour of male pied flycatchers varies on a continuum from brownish and female-like to a conspicuous black-and-white. Males have a conspicuous plumage only during the breeding season, when the mortality rate was low and not correlated with plumage colour. Brownish males breed successfully, and breeding males had no lower annual rate of return than non-breeders. Experiments on male intrusion showed that possession of a cryptic, female-like plumage did not facilitate nest site settlement by such males. Dark males were on average older, arrived earlier, and defended more nestboxes than brown males. However, experiments showed that plumage colour was not a reliable indicator of the outcome of competitive combats between males. These facts argue against several existing hypotheses about variation in male plumage colour. A new explanation is proposed: a bright colour serves to signal presence and thereby reduces territory holding costs. The brownish males arrive only shortly before the females and thus will not benefit as much by being conspicuous as do the black-and-white males that arrive earlier in spring.
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The effects of gonadectomy and gonadal hormones on singly-established H. diminuta in rats on “complete” and “deficient” diets have been studied by means of estimations of the number of eggs eliminated by the parasite per 24-hour periods over varying intervals of time.A decline in the number of eggs of H. diminuta eliminated per 24 hours over a period of 3 months was observed in castrated male rats fed a “complete” diet which was comparable to the effects observed in normal male hosts on a “deficient” diet. Castrated males fed a “deficient” diet, however, exhibited a decline in the numbers of eggs of this cestode eliminated which was comparable to that observed in normal female hosts on a “deficient” diet.Testosterone and progesterone, administered at the rate of 1 mg per day, restored egg output to approximately normal levels in castrated male hosts. Testosterone was also similarly effective in normal female rats on “deficient” diet, but progesterone was ineffective.Chorionic gonadotropin raised the egg output of H. diminuta in normal male and female rats on “deficient” diet but not in gonadectomized hosts. A stimulation of testosterone production is postulated as a possible mechanism in the case of normal male rats and possibly the production of estrogen in the normal female hosts.Accidental concurrent infections with a few Moniliformis dubius had no evident effect on egg production of H. diminuta. These acanthocephalans were lost quickly from hosts on “deficient” diet.