Sexually-selected Traits Research Articles

Facial and genital color ornamentation, testosterone, and reproductive output in high-ranking male rhesus macaques

Males in many vertebrate species have colorful ornaments that evolved by sexual selection. The role of androgens in the genesis and maintenance of these signals is unclear. We studied 21 adult high-ranking male rhesus macaques from nine social groups in the free-ranging population on Cayo Santiago, Puerto Rico, and analyzed facial and genital skin luminance and redness, fecal androgens, rates of mating behaviors, and offspring sired. Facial and genital coloration varied in relation to age, mating behavior, reproductive success, and testosterone concentration. Our results indicate that skin coloration in high-ranking male rhesus macaques is a sexually-selected trait mediated by androgens. These results add to the growing literature on the proximate and ultimate causes of male sexual signals and highlight the need to examine how these characteristics change with age in other species.

Sexually-selected male weapon increases the risk of population extinction under environmental change: an experimental evidence.

Exaggerated sexually-selected traits, occurring more commonly in males, help individuals to increase reproductive success, but are costly to produce and maintain. These costs on the one hand may improve population fitness by intensifying selection against maladapted males, but on the other hand may increase the risk of extinction under environmental challenge. However, the impact of sexually selected traits on extinction risk have not been investigated experimentally. We used replicate populations of a male-dimorphic mite, Rhizoglyphus robini, to test if prevalence of a sexually-selected weapon affected the risk of extinction under temperature increase (2 0C per each of three consecutive generations). In two independent experiments that utilized either inbred lines or lines mass selected for or against the weapon to establish experimental replicate populations differing in the prevalence of the weapon, we found that populations with high weapon prevalence were more likely to go extinct. Extinctions occurred despite partial suppression of the weapon expression at increased temperature and were not explained by increased male mortality. Our results provide the first, to our knowledge, experimental evidence demonstrating dramatic effect of elaborated sexual traits on the risk of extinction under environmental challenge.

The Sexual Selection Landscape and Sexually-Selected Traits of the Crested Macaque (Macaca nigra)

The Sexual Selection Landscape and Sexually-Selected Traits of the Crested Macaque (Macaca nigra)

Evolution of sexually selected traits across animals

Sexual selection is thought to be a major driver of phenotypic diversity and diversification in animals, but large-scale evolutionary patterns in sexually selected (SS) traits remain largely unknown. Here, we survey and analyze the evolution of these traits across animal phylogeny. We find that female mate choice appears to be the most widespread mechanism of sexual selection, but male-male competition appears to be almost as frequent in chordates and male mate choice is also common in arthropods. Among sensory types, tactile traits appear to be most widespread whereas auditory traits are relatively uncommon. Rather than being ubiquitous or randomly distributed across animals, most of these different types of SS traits are confined to clades in arthropods and chordates, which form “hotspots” for the evolution of these diverse trait types. Thus, different sensory types show accelerated rates of evolution in these clades. Moreover, different types of SS traits are strongly correlated with each other in their evolution across animals. Finally, despite the intensive interest in the role of sexual selection in speciation, we find only limited support for the idea that SS traits drive large-scale patterns of diversification and species richness across all animals.

A comprehensive overview of the effects of urbanisation on sexual selection and sexual traits.

ABSTRACTUrbanisation can affect mating opportunities and thereby alter inter‐ and intra‐sexual selection pressures on sexual traits. Biotic and abiotic urban conditions can influence an individual's success in pre‐ and post‐copulatory mating, for example through impacts on mate attraction and mate preference, fertilisation success, resource competition or rival interactions. Divergent sexual selection pressures can lead to differences in behavioural, physiological, morphological or life‐history traits between urban and non‐urban populations, ultimately driving adaptation and speciation. Most studies on urban sexual selection and mating interactions report differences between urban and non‐urban populations or correlations between sexual traits and factors associated with increased urbanisation, such as pollution, food availability and risk of predation and parasitism. Here we review the literature on sexual selection and sexual traits in relation to urbanisation or urban‐associated conditions. We provide an extensive list of abiotic and biotic factors that can influence processes involved in mating interactions, such as signal production and transmission, mate choice and mating opportunities. We discuss all relevant data through the lens of two, non‐mutually exclusive theories on sexual selection, namely indicator and sensory models. Where possible, we indicate whether these models provide the same or different predictions regarding urban‐adapted sexual signals and describe different experimental designs that can be useful for the different models as well as to investigate the drivers of sexual selection. We argue that we lack a good understanding of: (i) the factors driving urban sexual selection; (ii) whether reported changes in traits result in adaptive benefits; and (iii) whether these changes reflect a short‐term ecological, or long‐term evolutionary response. We highlight that urbanisation provides a unique opportunity to study the process and outcomes of sexual selection, but that this requires a highly integrative approach combining experimental and observational work.

Decoupled Acoustic and Visual Components in the Multimodal Signals of the Common Cuckoo (Cuculus canorus)

Because of its parasitic habits, reproduction costs of the common cuckoo (Cuculus canorus) are mostly spent in pre-laying activities. Female costs are limited to searching host nests and laying eggs, whereas, males spend time in performing intense vocal displays, possibly with territorial purpose. This last aspect, together with a sexual plumage dimorphism, points to both intra- and inter-sexual selections operating within this species. One element triggering sexual selection is a differential fitness accrued by different phenotypes. Before analyzing possible sexual selection mechanisms operating in cuckoos, it is therefore necessary to verify whether there is a variability among male secondary characters by describing and quantifying them. Here we aimed to quantitatively characterize the main two potential candidates of sexual selection traits, i.e., calls and displays, shown by males at perches. During the 2019 breeding season, in a site within the Po Plain, we both audio and video recorded cuckoo males at five different perches. We analyzed acoustic variables as well as display sequences searching for potential correlations. We found a significant variation among calls that could be clustered into four vocal types. We also found that no visual displays were associated with vocal displays; cuckoo males were either vocal and motionless or soundless and active. We discuss our results under the perspective of the potential value of sexual selection in brood parasites and its role in its parasitic habit.

Antagonistic selection on body size and sword length in a wild population of the swordtail fish, Xiphophorus multilineatus: Potential for intralocus tactical conflict.

Alternative reproductive tactics (ARTs) have provided valuable insights into how sexual selection and life history trade‐offs can lead to variation within a sex. However, the possibility that tactics may constrain evolution through intralocus tactical conflict (IATC) is rarely considered. In addition, when IATC has been considered, the focus has often been on the genetic correlations between the ARTs, while evidence that the ARTs have different optima for associated traits and that at least one of the tactics is not at its optimum is often missing. Here, we investigate selection on three traits associated with the ARTs in the swordtail fish Xiphophorus multilineatus; body size, body shape, and the sexually selected trait for which these fishes were named, sword length (elongation of the caudal fin). All three traits are tactically dimorphic, with courter males being larger, deeper bodied and having longer swords, and the sneaker males being smaller, more fusiform and having shorter swords. Using measures of reproductive success in a wild population we calculated selection differentials, as well as linear and quadratic gradients. We demonstrated that the tactics have different optima and at least one of the tactics is not at its optimum for body size and sword length. Our results provide the first evidence of selection in the wild on the sword, an iconic trait for sexual selection. In addition, given the high probability that these traits are genetically correlated to some extent between the two tactics, our study suggests that IATC is constraining both body size and the sword from reaching their phenotypic optima. We discuss the importance of considering the role of IATC in the evolution of tactical dimorphism, how this conflict can be present despite tactical dimorphism, and how it is important to consider this conflict when explaining not only variation within a species but differences across species as well.

Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

Sexually selected traits are hypothesized to be honest signals of individual quality due to the costs associated with their maintenance, development, and/or production. Testosterone, a sex steroid associated with the development and/or production of sexually selected traits, has been proposed to enforce the honesty of sexually selected traits via its immunosuppressive effects (i.e., the Immunocompetence Handicap Hypothesis) and/or by influencing an individual’s exposure/susceptibility to oxidative stress (i.e., the Oxidation Handicap Hypothesis). Previous work testing these hypotheses has primarily focused on physiological measurements of immunity or oxidative stress, but little is known about the molecular pathways by which testosterone could influence immunity and/or oxidative stress pathways. To further understand the transcriptomic consequences of experimentally elevated testosterone in the context of handicap hypotheses, we used previously published RNA-seq data from studies that measured the transcriptome of individuals treated with either a testosterone-filled or an empty (i.e., control) implant. Two studies encompassing three species of bird and three tissue types fit our selection criteria and we reanalyzed the data using weighted gene co-expression network analysis. Testosterone-treated individuals exhibited signatures of immunosuppression and our results describe the molecular pathways underlying this effect. We also provide some evidence to suggest that the transcriptomic signature of immunosuppression is evolutionarily conserved between the three species. While our results provide no evidence to suggest testosterone mediates handicaps via pathways associated with oxidative stress, they do support the hypothesis that testosterone enforces the honesty of sexually-selected traits by influencing an individual’s immunocompetence. Overall, this study develops a framework for testing testosterone-mediated handicap hypotheses and provides guidelines for future integrative and comparative studies focused on the proximate mechanisms mediating sexually selected traits.

Defining an intrasexual male weapon polymorphism in a New Zealand harvestman (Opiliones: Neopilionidae) using traditional and geometric morphometrics

Abstract In many species, competition for mates has led to exaggerated male sexually-selected traits. Sexually-selected male weapons are used in male-male combat and include structures like horns, antlers and enlarged teeth. Weapons often vary intraspecifically in size, resulting in either a continuum of weapon sizes or in discrete male polymorphisms. More rarely, complex weapon polymorphisms can also include variation in weapon shape; however, these are difficult to quantify. Here we first use traditional linear morphometrics to describe a weapon trimorphism in the endemic New Zealand harvestman, Forsteropsalis pureoraTaylor, 2013. We identified three male morphs: a small-bodied gamma male with reduced chelicera, a large-bodied beta male with long, slender chelicerae, and a large-bodied alpha male with shorter, but very broad, robust chelicerae. Chelicera length alone failed to fully capture the variation in weapon investment. Using geometric morphometrics, we show that alpha males are different in weapon shape, whereas beta and gamma males have similar weapon shape, but vary in their body size and chelicera length. Additionally, we describe how the chelicerae function during male-male combat from observations of contests. This work demonstrates how combining linear and geometric morphometrics can help to elucidate complex polymorphism.

Polyphenism of visual and chemical secondary sexually-selected wing traits in the butterfly Bicyclus anynana: How different is the intermediate phenotype?

Polyphenism is a type of phenotypic plasticity supposedly adaptive to drastic and recurrent changes in the environment such as seasonal alternation in temperate and tropical regions. The butterfly Bicyclus anynana shows polyphenism with well-described wet and dry seasonal forms in sub-Saharan Africa, displaying striking morphological, physiological and behavioural differences in response to higher or lower developmental temperatures. During the seasonal transition in the wild, the intermediate phenotype co-occurs with wet and dry phenotypes. In this study, we aimed to characterize the secondary sexually-selected wing traits of the intermediate form to infer its potential fitness compared to wet and dry phenotypes. Among the previously described wing morphological traits, we first showed that the area of the fifth eyespot on the ventral hindwing is the most discriminant trait to identify wet, dry and intermediate phenotypes in both sexes. Second, we characterized the intermediate form for two secondary sexually-selected wing traits: the area and UV reflectance of the dorsal forewing pupil and the composition of the male sex pheromone. We showed that values of these two traits are often between those of the wet and dry phenotypes. Third, we observed increasing male sex pheromone production in ageing dry and wet phenotypes. Our results contrast with previous reports of values for sexually-selected traits in wet and dry seasonal forms, which might be explained by differences in rearing conditions or sample size effects among studies. Wet, dry and intermediate phenotypes display redundant sexually dimorphic traits, including sexually-selected traits that can inform about their developmental temperature in sexual interactions.

Female comparative mate choice influences strategic male nesting strategy in the peacock blenny Salaria pavo

Emerging evidence endorses the idea that comparative instead of rational choice is widespread among species and mating contexts. In a comparative scenario the attractiveness of a male is not absolute but depends on the attractiveness of the other males to whom he is compared by females. Therefore, a male may benefit from the ability to choose the appropriate context that enhances his attractiveness. Here we test for the occurrence of strategic male nesting strategies in the peacock blenny, Salaria pavo, a fish species in which females evaluate potential mates by comparing males. Our results show that the large majority of males choose the context that maximize their attractiveness by nesting close to less attractive neighbours. Overall, we suggest that, in the peacock blenny, comparative, non-directional female choice is associated to strategic male nesting strategies and this scenario may contribute to the maintenance of genetic variability of male sexually-selected traits.

Sexual selection in the Kinda baboon

Due to wide variation in the presence and degree of expression of a diverse suite of sexually-selected traits, the tribe Papionini represents an outstanding model for understanding how variation in sexual selection pressures and mechanisms leads to trait evolution. Here, we discuss the particular value of Papio as a model genus for studies of sexual selection, emphasizing the presence of multiple mating systems, and differences in the expression of sexually-selected traits among closely-related species. We draw particular attention to the Kinda baboon (Papio kindae), a comparatively less-studied baboon species, by providing a primer to Kinda baboon morphology, genetics, physiology, and behavior. Based on observations of large group sizes, combined with low degrees of sexual dimorphism and large relative testis size relative to other baboon species, we test the hypothesis that Kinda baboons have evolved under reduced direct, and increased indirect, male–male competition. We present the first long-term data on wild Kinda baboons in Zambia. Kinda baboon females show seasonal peaks in births and reproductive receptivity, and males exhibit a queing-rather than contest-based dominance acquisition with long alpha-male tenure lengths. We finish by making a number of explicit testable predictions about Kinda baboon sexual signals and behaviors, and suggest that Kinda baboons have potential to offer new insights into the selective environments that may have been experienced during homininization.

Why the Static Allometry of Sexually-Selected Traits Is So Variable: The Importance of Function.

Sexually-selected traits often show positive static allometry, with large individuals bearing disproportionately large structures. But many other sexually-selected traits show isometry or even negative allometry, with trait size varying relatively little with body size. We recently proposed that the functions of these traits (as aggressive signals, weapons, courtship signals, and contact courtship devices) determine their allometries. Positive allometry is generally favored for aggressive signals because aggressive signals are selected to emphasize body size (and thus fighting prowess). In contrast, the biomechanics of force application in weapons only sometimes select for positive allometry; the content of courtship signals is even less often related to body size; and contact courtship devices are selected to be relatively invariant across body sizes. Here we summarize the arguments in favor of this "functional allometry" hypothesis and expand a comparative test of its predictions. Our results indicate that sexual traits have the allometric slopes predicted by our hypothesis, regardless of which body part bears the structure.

The effect of predation risk on post-copulatory sexual selection in the Japanese pygmy squid

Conspicuous male sexual traits (e.g. weapons for male–male competition and displays for courting females) may attract predators. Under conditions of high predation risk, females typically become less choosy with respect to mates to reduce the time spent on mate selection. However, post-copulatory sexual traits, such as sperm ejaculation for sperm competition and sperm removal for cryptic female choice (CFC), may increase with predation risk because they are more inconspicuous to predators. To examine this hypothesis, we observed the reproductive behaviour in the Japanese pygmy squid, Idiosepius paradoxus, in which the male attaches ejaculated spermatangia to the female’s body and the female removes the spermatangia after copulation. Squid from two populations (Ohmura and Oki), with low and high predation levels, respectively, were copulated in tanks under controlled presence/absence of predator conditions. Among the Ohmura individuals, spermatangia removal was suppressed in the presence of a predator. Females may not be able to remove spermatangia effectively when facing a predator because they feel threatened by the predator; as a result, more spermatangia were retained during trials in which they were exposed to predators. In contrast, squid from the Oki (high predation) population, which is exposed to a higher predation risk, were not strongly affected by the predator presence. While the males ejaculated more spermatangia, the females removed more of them. The effect of sexual conflict may be greater than that of the predation risk in the pygmy squid. This suggests adaptive differences in post-copulatory sexual selection traits linked to predation. In general, the strength of pre-copulatory sexual selection decreases with increasing predation risk because the sexual traits attract predators. However, post-copulatory sexual traits which are often inconspicuous may not be influenced by predation risk. Post-copulatory behaviour of Japanese pygmy squid collected from two populations experiencing different predation levels were investigated under experimental predator presence/absence conditions. Among low predations, individual sperm rejection by females (a post-copulatory trait) was suppressed in the presence of a predator. In contrast, individuals from the high predation population reported no change in sperm rejection. As with pre-copulatory sexual selection, post-copulatory female choice was suppressed by predator presence among individuals from a low predation. However, post-copulatory female choice was not affected by predator presence among individuals from the high-predation population. This may indicate predation-driven adaptive differences and plastic responses in post-copulatory traits.

Relative costs and benefits of alternative reproductive phenotypes at different temperatures \u2013 genotype-by-environment interactions in a sexually selected trait

BackgroundThe maintenance of considerable genetic variation in sexually selected traits (SSTs) is puzzling given directional selection expected to act on these traits. A possible explanation is the existence of a genotype-by-environment (GxE) interaction for fitness, by which elaborate SSTs are favored in some environments but selected against in others. In the current study, we look for such interactions for fitness-related traits in the bulb mite, a male-dimorphic species with discontinuous expression of a heritable SST in the form of enlarged legs that are used as weapons.ResultsWe show that evolution at 18 °C resulted in populations with a higher prevalence of this SST compared to evolution at 24 °C. We further demonstrate that temperature modified male reproductive success in a way that was consistent with these changes. There was a genotype-by-environment interaction for reproductive success – at 18 °C the relative reproductive success of armored males competing with unarmored ones was higher than at the moderate temperature of 24 °C. However, male morph did not have interactive effects with temperature with respect to other life history traits (development time and longevity).ConclusionsA male genotype that is associated with the expression of a SST interacted with temperature in determining male reproductive success. This interaction caused an elaborate SST to evolve in different directions (more or less prevalent) depending on the thermal environment. The implication of this finding is that seasonal temperature fluctuations have the potential to maintain male polymorphism within populations. Furthermore, spatial heterogeneity in thermal conditions may cause differences among populations in SST selection. This could potentially cause selection against male immigrants from populations in different environments and thus strengthen barriers to gene flow.

The causes and evolutionary consequences of variation in female mate choice in insects: the effects of individual state, genotypes and environments.

Sexual selection generally involves males evolving secondary sexual characters that satisfy the mating preferences of females. Behavioral ecologists have spent considerable research effort on identifying how variation in sexually-selected traits in insects is maintained among males at the expense of investigating the proximate and ultimate causes of variation in female mating preferences for those male traits. The past decade has witnessed improved effort in redressing this bias in insects with researchers identifying a host of factors intrinsic and extrinsic to the female as mediating flexibility in female mating behavior. Evidence is mounting that a female's social environment, whether experienced during development or as an adult, is key to shaping her mating preferences. Others have extended these observations to show that the genetic identity of the conspecific individuals comprising the social environment can have profound effects on female mating preferences via indirect genetic effects (IGEs), or through interspecific indirect genetic effects (IIGEs) if the genotype of heterospecifics influences plasticity in mating preferences. Considerably more work is needed to not only expand our list of mediating intrinsic and extrinsic factors but also to identify how their interaction influences individual variation in male and female mating preferences.

The Fat-Dachsous signaling pathway regulates growth of horns in Trypoxylus dichotomus, but does not affect horn allometry

Males of the Asian rhinoceros beetle, Trypoxylus dichotomus, possess exaggerated head and thoracic horns that scale dramatically out of proportion to body size. While studies of insulin signaling suggest that this pathway regulates nutrition-dependent growth including exaggerated horns, what regulates disproportionate growth has yet to be identified. The Fat signaling pathway is a potential candidate for regulating disproportionate growth of sexually-selected traits, a hypothesis we advanced in a previous paper (Gotoh et al., 2015). To investigate the role of Fat signaling in the growth and scaling of the sexually dimorphic, condition-dependent traits of the in the Asian rhinoceros beetle T. dichotomus, we used RNA interference to knock down expression of fat and its co-receptor dachsous. Knockdown of fat, and to a lesser degree dachsous, caused shortening and widening of appendages, including the head and thoracic horns. However, scaling of horns to body size was not affected. Our results show that Fat signaling regulates horn growth in T. dichotomus as it does in appendage growth in other insects. However, we provide evidence that Fat signaling does not mediate the disproportionate, positive allometric growth of horns in T. dichotomus.

Evolutionary trade-off between naturally- and sexually-selected melanin-based colour traits in worldwide barn owls and allies

Natural selection typically constrains the evolution of sexually-selected characters. The evolution of naturally- and sexually-selected traits can be intertwined if they share part of their genetic machinery or if sex traits impair foraging success or increase the risk of depredation. The present study investigated phenotypic correlations between naturally- and sexually-selected plumage traits in the Tytonidae (barn owls, grass owls, and masked owls). Phenotypic correlations indicate the extent to which selection on one trait will indirectly influence the evolution of another trait. In this group of birds, the ventral body side varies from white to dark reddish, a naturally-selected pheomelanin-based colour trait with important roles in predator–prey interactions. Owls also exhibit eumelanin-based black spots, for which number and size signal different aspects of individual quality and are used in mate choice. These three plumage traits are strongly heritable and sexually dimorphic, with females being on average darker reddish and more spotted than males. Phenotypic correlations were measured between these three plumage traits in 3958 free-living barn owls in Switzerland and 10 670 skin specimens from 34 Tyto taxa preserved in museums. Across Tyto taxa, the sexually-selected plumage spottiness was positively correlated with the naturally-selected reddish coloration, with redder birds being more heavily spotted. This suggests that they are genetically constrained or that natural and sexual selection are not antagonistically exerted on plumage traits. In a large sample of Swiss nestlings and within 34 Tyto taxa, the three plumage traits were positively correlated. The production of melanin pigments for one plumage trait is therefore not traded off against the production of melanin pigments for another plumage trait. Only in the most heavily-spotted Tyto taxa do larger-spotted individuals display fewer spots. This indicates that, at some threshold value, the evolution of many spots constrains the evolution of large spots. These analyses raise the possibility that different combinations of melanin-based plumage traits may not be selectively equivalent.

Characterization of 16 novel microsatellite loci for Ephippiger diurnus (Orthoptera: Tettigoniidae) using pyrosequencing technology and cross-species amplification

A novel panel of 16 microsatellite markers, obtained by pyrosequencing of enriched genomic libraries, is reported for the fl ightless European bushcricket Ephippiger diurnus (Dufour) (Orthoptera: Tettigoniidae). Five multiplex and one simplex PCR protocols were optimized, and the polymorphism at the 16 loci was assessed in two natural populations from southern France. The mean allele number and (expected mean heterozygosity) were 8.94 (0.71) and 6.57 (0.70), respectively, in each population. Several loci were at Hardy-Weinberg disequilibrium (HWD), possibly due to the incidence of null alleles. The occurrence of null alleles has been previously reported for this species, and it is a common feature of microsatellite loci in Orthoptera. Cross-amplifi cation tests demonstrated the transferability of some of these loci to other ephippigerine species. The microsatellite loci reported here substantially increase the number of available loci for this species and will afford an accurate picture of E. diurnus phylogeography, the genetic structure of its populations, and an improved understanding of the evolution of male song and other sexually-selected traits in this highly variable species

Condition-dependent ejaculate production affects male mating behavior in the common bedbug Cimex lectularius.

Food availability in the environment is often low and variable, constraining organisms in their resource allocation to different life‐history traits. For example, variation in food availability is likely to induce condition‐dependent investment in reproduction. Further, diet has been shown to affect ejaculate size, composition and quality. How these effects translate into male reproductive success or change male mating behavior is still largely unknown. Here, we concentrated on the effect of meal size on ejaculate production, male reproductive success and mating behavior in the common bedbug Cimex lectularius. We analyzed the production of sperm and seminal fluid within three different feeding regimes in six different populations. Males receiving large meals produced significantly more sperm and seminal fluid than males receiving small meals or no meals at all. While such condition‐dependent ejaculate production did not affect the number of offspring produced after a single mating, food‐restricted males could perform significantly fewer matings than fully fed males. Therefore, in a multiple mating context food‐restricted males paid a fitness cost and might have to adjust their mating strategy according to the ejaculate available to them. Our results indicate that meal size has no direct effect on ejaculate quality, but food availability forces a condition‐dependent mating rate on males. Environmental variation translating into variation in male reproductive traits reveals that natural selection can interact with sexual selection and shape reproductive traits. As males can modulate their ejaculate size depending on the mating situation, future studies are needed to elucidate whether environmental variation affecting the amount of ejaculate available might induce different mating strategies.