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Relationship between male standard length and courtship exhibited by male three-spine sticklebacks (Gasterosteus aculeatus) under high and low dissolved oxygen (DO) levels. Male courtship is the first principal component of seven common stickleback courtship behaviors (see text). Loadings of these behaviors on PC1 are given in Table S1.
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Sexual cues, including extended phenotypes, are expected to be reliable indicators of male genetic quality and/or provide information on parental quality. However, the reliability of these cues may be dependent on stability of the environment, with heterogeneity affecting how selection acts on such traits. Here we test how environmental change medi...
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Citations
... In fifteen-spined sticklebacks, Spinachia spinachia, females prefer to spawn in nests built high up in algae, and such nests are safer from egg predation [69]. In three-spined sticklebacks, males build looser nests in low compared to high dissolved oxygen, and females prefer to spawn in nest-designs that match the local environment [70]. Males in high condition build nests faster and more neatly [71], and males with higher cognitive abilities build more elaborate nests [72]. ...
Among ray-finned fishes that provide parental care, many spawn in constructed nests, ranging from bowls, burrows and ridges to nests made of algae or bubbles. Because a nest by definition is a construction that enhances the nest-builder's fitness by helping it meet the needs of the developing offspring, nest-building behaviour is naturally selected, as is a preference for spawning with mates that provide well-built nests. However, nest-building behaviour can also be sexually selected, when nest traits increase mating success, protect against sperm competition or nest take-overs by conspecifics. Here, we offer a systematic review, with examples of how competition for sites and location of fish nests relates to sexual selection. We examine direct and indirect benefits of mate choice linked to nest traits, and different types of nests, from a sexual selection perspective. Nest-related behaviours are often under both natural and sexual selection, and we disentangle examples where that is the case, with special attention to females. We highlight some taxa in which nest building is likely to be sexually selected, but lack of research has left them uninvestigated. Some of them are established aquarium species, making them particularly amenable for future research. Finally, we compare with arthropods, amphibians and birds.
This article is part of the theme issue ‘The evolutionary ecology of nests: a cross-taxon approach’.
... Here, we aimed to determine whether the ability of male three-spined sticklebacks (Gasterosteus aculeatus) to adjust their nest building behaviour in response to variation in water flow depends on their evolutionary history with still or flowing water environments. In sticklebacks, males are the sole contributor to nest-building, and their nests serve both as incubators for eggs as well as a signal to attract females [48,54,60]. After establishing a territory, male sticklebacks construct nests by transporting nest material (e.g. ...
... For instance, smaller males are often more sensitive to environmental cues and exhibit greater plasticity of reproductive traits, such as nest defence [110] and sneaky mating [111], because of fewer opportunities to mate [112], lower dominance [113] and higher risk of depleting energy reserves [45,114]. In sticklebacks, larger males are often preferred by females [54,60], are better at protecting young [115], and tend to build larger nests [71,77]. Consistent with this, our experiment revealed that larger males, regardless of the water flow conditions they built their nest in, or the habitat they originated from, incorporated more material into their nests than smaller males, probably improving the stability and protective value of the nest (e.g. ...
The primary function of animal nests is to protect developing offspring from hostile and fluctuating environments. Animal builders have been shown to adjust nest construction in response to changes in their environment. However, the extent of this plasticity, and its dependence on an evolutionary history of environmental variability, is not well understood. To test whether an evolutionary history with flowing water impacts male ability to adjust nests in response to flow regime, we collected three-spined sticklebacks (Gasterosteus aculeatus) from three lakes and three rivers, and brought them into reproductive condition in controlled laboratory aquaria. Males were then allowed to nest under both flowing and static conditions. Nest building behaviour, nest structure and nest composition were all recorded. In comparison to males building nests under static conditions, males building in flowing water took longer to construct their nests and invested more in nesting behaviour. Moreover, nests built in flowing water contained less material, were smaller, more compact, neater and more elongated than nests built under static conditions. Whether males came from rivers or lakes had little impact on nesting activities, or male capacity to adjust behaviours in response to flow treatment. Our findings suggest that aquatic animals which have experienced a stable environment over a long period of time retain plasticity in nest-building behaviours that allow them to adjust nests to ambient flow conditions. This ability may prove crucial in coping with the increasingly unpredictable flow regimes found in anthropogenically altered waterways and those resulting from global climate change.
This article is part of the theme issue ‘The evolutionary ecology of nests: a cross-taxon approach’.
... Behavioural ecology; Biodiversity ecology; Evolutionary ecology; Theorectical ecology Rankin, 2006), and parental investment (Fromhage & Jennions, 2016;Kokko & Jennions, 2008;Székely et al., 2000). In addition, resource availability can have strong effects on sexual selection in relation to mate monopolization (Emlen & Oring, 1977), mate signaling and attraction (Borgia et al., 1987;Dawkins, 1982;Enquist, 1985;Grafen, 1990;Head et al., 2017;Johnstone et al., 2009;Pärssinen et al., 2019;Penn & Számadó, 2019;Rowe & Houle, 1996;Schaedelin & Taborsky, 2009;Zahavi, 1975Zahavi, , 1977, and the benefits of mate choice (Andersson, 1994;Miller & Svensson, 2014). Furthermore, resource availability affects sexual selection by determining which individuals and traits enter the mating pool, where the mating pool consists of the individuals that are currently prepared to mate at a current time and location (Ahnesjö et al., 2001;Shuker & Kvarnemo, 2021). ...
A bstract
Sexual selection influences the evolution of phenotypic traits and contributes to patterns of biodiversity. In many animals, mating involves sequential steps. Often, individuals must secure resources that are essential for mating (nests, territories, food), and then after securing a resource, individuals engage in competition for access to limited opposite sex mates and gametes. A large body of empirical research and some verbal models have illustrated that resource acquisition can influence sexual selection. In general, though, we lack a priori predictions of when and how resource acquisition will influence sexual selection. Here, we use a mathematical framework to explore the link between resource acquisition and sexual selection on an advantageous mate‐acquisition trait across biologically relevant trade‐off scenarios. Our findings provide a set of testable predictions of how resource acquisition can influence sexual selection on mating traits. In general, selection on mate‐acquisition traits is expected to be heavily influenced by: (1) the episode of selection considered, and in particular, whether one considers selection associated with the mating pool only or selection associated with both the mating pool and pre‐mating pool; (2) whether resource‐acquisition and mate‐acquisition traits are positively associated or whether they trade off; and (3) the proportion of males with the resource‐ and mate‐acquisition traits.
... We furthermore measured male courtship activity. Studies on free-ranging male three-spined stickleback often use the number or duration of zig-zag courtship dances to measure male sexual activity (e.g., Kraak and Bakker 1998;McGhee et al. 2015;Head et al. 2017). However, these dances are performed over considerable distances. ...
Phenotypic plasticity is widespread in animals. Still, how plastic responses to predator presence affect traits under sexual selection and influence mating preferences is not well understood. Here, we examined how simulated chronic predator presence during development and acute predator presence during mate choice affect the expression of male secondary sexual traits and female mating preference in the three-spined stickleback, Gasterosteus aculeatus. Males reared under chronic predator presence developed less intense red breeding coloration but showed higher courtship activity than males that grew up in a predator-free environment. Acute predator presence during mate choice trials did not influence male behavior or ornamentation. Predator presence experienced during development did not affect female mating preferences, whereas acute predator presence altered preferences for male courtship activity. Male body size and eye coloration influenced the intensity of female mating preferences, while the trait changing most in response to predator presence during development (red coloration) had no significant impact. The observed interplay between developmental plasticity in male ornamental traits and environment-dependent female mating preferences may lead to dynamic processes altering the strength and direction of sexual selection depending on both the chronic and acute risk of predation. These processes may contribute to the maintenance of within-and among-population variation in secondary sexual traits, and may, ultimately, facilitate speciation.
... In these cases, the authors either did not provide citations for statements describing a trait as sexually selected or provided indirect evidence (e.g., the trait is sexually dimorphic, linked with territory quality, or more common among dominant individuals). About half of the papers did cite evidence of the trait being linked with mate choice and/or reproductive success (99/203 traits or 49%), and a few exceptional papers directly tested the link with mate choice and/or reproductive success, as well as trait plasticity (17/203 or 8%; see Head et al., 2017;Martín & López, 2006 for good examples). ...
Many sexually selected traits exhibit phenotypic plasticity. Despite a growing appreciation for the ecological context in which sexual selection occurs, and for the role of plasticity in shaping traits associated with local adaptation and divergence, there is an important gap in knowledge about the onset and duration of plasticity in sexual trait expression. Integrating this temporal dimension of plasticity into models of sexual selection informs our understanding of the information conveyed by sexual traits and our predictions related to trait evolution, and is critical in this time of unprecedented and rapid environmental change. We conducted a systematic review of 869 studies to ask how trait modalities (e.g., visual and chemical) relate to the onset and duration of plasticity in vertebrate sexual signals. We show that this literature is dominated by studies of coloration in birds and fish, and most studies take place during the breeding season. Where possible, we integrate results across studies to link physiology of specific trait modalities with the life stage (e.g., juvenile, breeding, or nonbreeding) during which plasticity occurs in well-studied traits. Limitations of our review included a lack of replication in our dataset, which precluded formal analysis. We argue that the timing of trait plasticity, in addition to environmental context, is critical for determining whether and how various communication signals are associated with ecological context, because plasticity may be ongoing or occur at only one point in an individual's lifetime, and determining a fixed trajectory of trait expression. We advocate for careful consideration of the onset and duration of plasticity when analyzing how environmental variation affects sexual trait expression and associated evolutionary outcomes.
... In addition, male courtship behaviours may potentially indicate its cognitive abilities (but see Minter et al. 2017). In this species, males build a complex nest with filamentous algae and kidney secretion not only to protect eggs (Wootton 1976) but also to attract mates (Barber et al. 2001;Östlund-Nilsson and Holmlund 2003;Head et al. 2017). The quality of a nest may reveal information about the builder's skills (Rushbrook et al. 2008) and cognitive performances (Schaedelin and Taborsky 2009). ...
Cognitive abilities may be crucial for individuals to respond appropriately to their social and natural environment, thereby increasing fitness. However, the role of cognitive traits in sexual selection has received relatively little attention. Here, we studied 1) whether male secondary sexual traits (colour, courtship, and nest) reflect their cognitive ability, 2) whether females choose mates based on males' and their own cognitive abilities, and 3) how the interplay between secondary sexual traits and cognitive ability determines male attractiveness in the three-spined stickleback (Gasterosteus aculetaus). For this, we first evaluated the cognitive ability of sexually mature males and females in a detour-reaching task. Then, female preference was repeatedly assessed in a dichotomous-choice test, where the female was exposed to two males with contrasting performances (relatively good and bad) in the detour-reaching task. Female preference for better performing males was affected by the female's own cognitive ability. Females with relatively medium-low cognitive ability preferred males with high ability, whereas females with high ability showed no preference. We also found that males with higher cognitive abilities built more elaborated nests, but showed weaker red nuptial colouration. To our knowledge, this is among the first results that illustrate how cognitive traits of both sexes influence female mate preference, which has implications for the strength and direction of sexual selection.
... Indeed, females have been shown to rely on different cues when environmental conditions vary (Chaine & Lyon, 2008;de Jong, Amorim, Fonseca, & Heubel, 2018). Similarly, the relevance of (more indirect) nest cues versus (more direct) male phenotype cues has varied between studies (Head, Fox, & Barber, 2017;Heubel, 2018). Many earlier studies investigating the role of alternative cues in mate choice face the challenge to clearly isolate the preference for nest quality from preference for male phenotypes, and none has independently controlled multiple nest traits when studying female choice (but see Bose et al., 2018). ...
... Indeed, nest entrance width has previously been recorded as constantly changing (Svensson & Kvarnemo, 2005) and less repeatable than cover building (Japoshvili et al., 2012) in sand goby males. Stickleback females prefer compact nests only at high oxygen levels while preferring males in good condition irrespective of oxygen level (Head et al., 2017) and common goby females might behave similarly. ...
Nests play a critical role for offspring development across the animal kingdom. Nest quality may contribute to the builder's extended phenotype and serve as an ornament during mate choice. We examined male and female nest choice in the common goby (Pomatoschistus microps), a benthic fish with male‐only parental care where females deposit eggs in male‐built nests. Using prebuilt nest models, we independently manipulated two candidate nest quality traits: (a) nest entrance width with a role in oxygen ventilation, and (b) extent of sand cover with a role in camouflage. In simultaneous choice trials, male gobies exhibited no preference for any nest model type. This suggests that initial characteristics of a nesting substrate have minor importance for males, which usually remodel the nest. Females were given a choice between two males occupying either entrance‐ or cover‐manipulated nests. The same pair of males was then exposed to a second female but now with alternated nest types assigned. Most females were consistent in choosing the same, typically the heavier male of the two regardless of nest properties. However, the females that chose the same nest regardless of the male preferred low over high sand coverage and narrow over wide nest entrance. Our results indicate that females base their mating decision on a combination of male phenotype and nest traits. While we found no indication that females are attracted to highly decorated nests, our study is the first in fishes to disentangle a preference for narrow (and thus more protective) nest entrances independent of nest coverage. Using model nests, we manipulated nest traits and studied male and female preferences for different nest types. Females preferred protected nests with narrow entrances and low cover. This preference may incur a male cost and thus lead to a potential sexual conflict. This conflict of interest may explain why males constantly re‐build and adjust nests to current environmental conditions.
... Hughes and Aung 2017;Kruger and Kruger 2018), but it currently lacks a coherent theoretical framework to organize a range of disparate traits. Following theory from evolutionary biology, the current review conceptualizes this category as extended phenotypic traits (Dawkins 1982;Head et al. 2017;Schaedelin and Taborsky 2009). ...
... Extended phenotype is a concept that is relatively widely used in sexual selection research in nonhuman animals (Bailey 2012;Head et al. 2017;Jordan et al. 2016;Schaedelin and Taborsky 2009). An organism's construction behaviors, for example, may sometimes modify the environment in fitness-enhancing (or fitness-damaging) ways. ...
... Another analytical dimension recognizes that extended phenotypes can impact an organism's fitness either through viability selection (by improving survival, thus indirectly enhancing reproductive fitness) (Blamires et al. 2017(Blamires et al. , 2018Hoover et al. 2011) and/or through sexual selection (Rubalcaba et al. 2016;Head et al. 2017;Miller 2001;Schaedelin and Taborsky 2009). It is important to recognize viability selection and sexual selection as different processes that generate different selection pressures on organisms to invest in extended phenotypes ( Fig. 1) (cf. ...
[Target Article.] Objectives: Sexual selection typically centers on bodily and psychological traits. Non-bodily traits ranging from housing and vehicles through art to social media can, however, influence sexual selection even in absence of the phenotype proper. The theoretical framework of human sexual selection is updated in this article by unifying four theoretical approaches and conceptualizing non-bodily traits as extended phenotypic traits.
Methods:
Existing research is synthesized with extended phenotype theory, life history theory, and behavioral ecology. To test population-level hypotheses arising from the review, ecological and demographic data on 122 countries are analyzed with multiple linear regression modelling.
Results:
A four-factor model of intelligence, adolescent fertility, population density, and atmospheric cold demands predicts 64% of global variation in economic complexity in 1995 and 72% of the variation in 2016.
Conclusions:
The evolutionary pathways of extended phenotypes frequently undergo a categorical broadening from providing functional benefits to carrying signalling value. Extended phenotypes require investments in skills and bioenergetic resources, but they can improve survival in high latitudes, facilitate the extraction of resources from the environment, and substantially influence sexual selection outcomes. Bioenergetic investments in extended phenotypes create individual- and population-level tradeoffs with competing life history processes, exemplified here as a global tradeoff between adolescent fertility and economic complexity. The merits of the present model include a more systematic classification of sexual traits, a clearer articulation of their evolutionary-developmental hierarchy, and an analysis of ecological, genetic, and psychological mechanisms that modulate the flow of energy into extended phenotypes and cultural innovations.
... Mate choice is expected to select for traits that reliably indicate mate quality and/or compatibility [14], but environments change in space and time, and cues that are indicative of mate quality in one environment may represent suboptimal or maladaptive cues under changed conditions. In fast-changing environments, mate quality may be highly environment-dependent, and individuals might choose based on unreliable cues unless multiple cues or alternative signals are involved in choice [21,22]. For instance, increased water turbidity due to eutrophication reduced reliance on visual cues for mate quality in several fish species, leading to a greater investment in courtship and reliance on other (e.g. ...
Plasticity, both within and across generations, can shape sexual traits involved in mate choice and reproductive success, and thus direct measures of fitness. Especially, transgenerational plasticity (TGP), where parental environment influences offspring plasticity in future environments, could compensate for otherwise negative effects of environmental change on offspring sexual traits. We conducted a mate choice experiment using stickleback ( Gasterosteus aculeatus ) with different thermal histories (ambient 17°C or elevated 21°C) within and across generations under simulated ocean warming using outdoor mesocosms. Parentage analysis of egg clutches revealed that maternal developmental temperature and reproductive (mesocosm) environment affected egg size, with females that developed at 17°C laying smaller eggs in 21°C mesocosms, likely owing to metabolic costs at elevated temperature. Paternal developmental temperature interacted with the reproductive environment to influence mating success, particularly under simulated ocean warming, with males that developed at 21°C showing lower overall mating success compared with 17°C males, but higher mating success in 21°C mesocosms. Furthermore, mating success of males was influenced by the interaction between F1 developmental temperature and F0 parent acclimation temperature, demonstrating the potential role of both TGP and within-generation plasticity in shaping traits involved in sexual selection and mate choice, potentially facilitating rapid responses to environmental change.
This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.
... Adult three-spined sticklebacks were collected from Carsington Reservoir, U.K. (53°3 0 30″N 1°37 0 50″W), and held in aquarium facilities at the University of Leicester. Full-sibling clutches of fertilized eggs were produced via in vitro fertilization of these wild-caught adults and resulting fry were reared to reproductive condition in the laboratory under light and temperature regimes that mimicked those in their natural habitat (described in Head et al., 2017). On reaching reproductive maturity (determined by the presence of breeding colouration), fish were separated by sex and maintained in recirculating aquaria in single-sex groups. ...
... Males were checked daily for the presence of a nest and after 4 days of nest construction, any unused threads were removed from the tank and males were presented with a free-swimming gravid female of known mass, who had been acclimated to the respective DO treatment for a 2-6-h period. Prior to introduction of the female, half of the experimental males experienced a reversal in DO conditions and period of acclimation to the new conditions (from high to low DO, or from low to high DO) as part of a separate experiment (see Head et al., 2017 for details). However, for each male, courtship, mating, paternal care and associated embryo development all occurred under the same DO treatment level and previous DO conditions experienced were not considered in the analyses presented here due to lack of clear predictions and a desire not to overfit models. ...
... Courtship behaviour was recorded to confirm that spawning had taken place (results presented in Head et al., 2017). Four males did not spawn, resulting in sample sizes of 28 males in each of the DO treatments. ...
For species exhibiting parental care, the way in which parents adjust care behaviour to compensate for environmental change potentially influences offspring survival and, ultimately, population viability. Using the three‐spined stickleback (Gasterosteus aculeatus) – a species in which males provide parental care by building and tending a nest and fanning the eggs – we examined how low dissolved oxygen (DO) levels affect paternal care, embryo development and survival. While levels of nest tending were unaffected by DO level, we found that larger males fanned their embryos more under low oxygen conditions. This resulted in faster rates of embryo development within the clutches of these larger males, but reduced embryo survival at 7d post‐fertilisation compared to clutches of smaller males. Our results suggest that although parents may attempt to compensate for environmental change via alterations to care behaviour, their ability to do so can be dependent on parental phenotype. This sets up the potential for oxygen levels to act on the strength and direction of selection within populations. We discuss possible explanations for the surprising result that supposedly adaptive changes in care behaviour by large males (i.e. increased fanning) led to reduced embryo survival at 7d post‐fertilisation, and whether, as a consequence, acute environmental conditions may have the potential to overwhelm selection on sexual traits.
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