Target Of Sexual Selection Research Articles

Effects of female-specific selection for reproductive investment on male fertility traits.

Despite sharing an autosomal genome, the often divergent reproductive strategies of males and females cause the selection to act in a sex-specific manner. Selection acting on one sex can have negative, positive, or neutral fitness consequences on the opposite sex. Here, we test how female-limited selection on reproductive investment in Japanese quail (Coturnix japonica) affects male fertility-related traits. Despite there being no difference in the size of males' testes from lines selected for high female reproductive investment (H-line) or low female reproductive investment (L-line), in both lines, the left testis had a greater volume of sperm-producing tissue. Since H-line females have a larger left-side restricted oviduct, this suggests a positive genetic correlation between male and female gonad function and that internal testis structure is a target of sexual selection. However, despite H-line males having previously been found to have greater fertilization success in a competitive scenario, we found little evidence of a difference between the lines in sperm number, motility, velocity, length, or the number of sperm that reached the ova. Precopulatory cues and/or the role of seminal fluid in sperm motility may thus be more likely to contribute to the H-line male fertilization advantage in this species.

Bare parts in the Galliformes: the evolution of a multifunctional structure.

A morphological trait can have multiple functions shaped by varying selective forces. Bare parts in birds, such as wattles, casques and combs, are known to function in both signalling and thermoregulation. Studies have demonstrated such structures are targets of sexual selection via female choice in several species of Galliformes (junglefowl, turkeys and grouse), though other studies have shown some role in thermoregulation (guineafowl). Here, we tested fundamental hypotheses regarding the evolution and maintenance of bare parts in Galliformes. Using a phylogeny that included nearly 90% of species in the order, we evaluated the role of both sexual and natural selection in shaping the function of bare parts across different clades. We found a combination of both environmental and putative sexually selected traits strongly predicted the variation of bare parts for both males and females across Galliformes. When the analysis is restricted to the largest family, Phasianidae (pheasants, junglefowl and allies), sexually selected traits were the primary predictors of bare parts. Our results suggest that bare parts are important for both thermoregulation and sexual signalling across Galliformes but are primarily under strong sexual selection within the Phasianidae.

Convergent rates of protein evolution identify novel targets of sexual selection in primates.

Sexual selection is the differential reproductive success of individuals, resulting from competition for mates, mate choice, or success in fertilization. In primates, this selective pressure often leads to the development of exaggerated traits which play a role in sexual competition and successful reproduction. In order to gain insight into the mechanisms driving the development of sexually selected traits, we used an unbiased genome-wide approach across 21 primate species to correlate individual rates of protein evolution to relative testes size and sexual dimorphism in body size, 2 anatomical hallmarks of sexual selection in mammals. Among species with presumed high levels of sperm competition, we detected strong conservation of testes-specific proteins responsible for spermatogenesis and ciliary form and function. In contrast, we identified accelerated evolution of female reproductive proteins expressed in the vagina, cervix, and fallopian tubes in these same species. Additionally, we found accelerated protein evolution in lymphoid tissue, indicating that adaptive immune functions may also be influenced by sexual selection. This study demonstrates the distinct complexity of sexual selection in primates revealing contrasting patterns of protein evolution between male and female reproductive tissues.

Sexual Selection and Proteinaceous Diversity in the Femoral Gland Secretions of Lacertid Lizards

Sexual selection contributes to the diversity of chemical signals in various animal groups. Lizards are good model species to study how sexual selection shapes signal diversity, as they are a chemically oriented taxonomic group with different levels of social interactions. Many lizard species bear epidermal glands secreting a waxy mixture of lipids and proteins, which are used in intraspecific communication. Previous among-species comparative analyses failed to find a relationship between the strength of sexual selection with the composition of the lipid blend in lizards. Here, we extend the investigation to the proteinaceous fraction. By using a phylogenetically informed approach, we correlated the average electrophoretic profiles of the protein from the femoral glands of 36 lacertid lizard species with the level of sexual dimorphism in size and shape, which are proxies for the strength of sexual selection. We found that as sexual size dimorphism advances, five distinct molecular weight regions in the protein profile increased their expression. Using tandem mass spectrometry, we successfully identified one of these five proteins: a carbonic anhydrase—an enzyme catalyzing the reversible hydration of carbon dioxide. Our findings suggest that proteins may be the target of sexual selection, as an active semiochemicals or as a dynamic support to other molecules: sexual selection may act indirectly on semiochemicals (namely lipids) by modifying the matrix (namely proteins).

Thermal Plasticity in Behavioral Traits Mediates Mating and Reproductive Dynamics in an Ectotherm.

AbstractEnvironmental temperatures potentially influence reproductive performance and sexual selection by restricting opportunities for activity. However, explicit tests of the behavioral mechanisms linking thermal variation to mating and reproductive performance are rare. We address this gap in a temperate lizard by combining social network analysis with molecular pedigree reconstruction in a large-scale thermal manipulation experiment. Populations exposed to cool thermal regimes presented fewer high-activity days compared with populations exposed to a warmer regime. While plasticity in thermal activity responses in males masked overall differences in activity levels, prolonged restriction nevertheless affected the timing and consistency of male-female interactions. Females were less capable than males of compensating for lost activity time under cold stress, and less active females in this group were significantly less likely to reproduce. While sex-biased activity suppression appeared to limit male mating rates, this did not correspond to a heightened intensity of sexual selection or shifts in the targets of sexual selection. In many populations facing thermal activity restriction, sexual selection on males may play a limited role relative to other thermal performance traits in facilitating adaptation.

Proposing a neural framework for the evolution of elaborate courtship displays

In many vertebrates, courtship occurs through the performance of elaborate behavioral displays that are as spectacular as they are complex. The question of how sexual selection acts upon these animals’ neuromuscular systems to transform a repertoire of pre-existing movements into such remarkable (if not unusual) display routines has received relatively little research attention. This is a surprising gap in knowledge, given that unraveling this extraordinary process is central to understanding the evolution of behavioral diversity and its neural control. In many vertebrates, courtship displays often push the limits of neuromuscular performance, and often in a ritualized manner. These displays can range from songs that require rapid switching between two independently controlled ‘voice boxes’ to precisely choreographed acrobatics. Here, we propose a framework for thinking about how the brain might not only control these displays, but also shape their evolution. Our framework focuses specifically on a major midbrain area, which we view as a likely important node in the orchestration of the complex neural control of behavior used in the courtship process. This area is the periaqueductal grey (PAG), as studies suggest that it is both necessary and sufficient for the production of many instinctive survival behaviors, including courtship vocalizations. Thus, we speculate about why the PAG, as well as its key inputs, might serve as targets of sexual selection for display behavior. In doing so, we attempt to combine core ideas about the neural control of behavior with principles of display evolution. Our intent is to spur research in this area and bring together neurobiologists and behavioral ecologists to more fully understand the role that the brain might play in behavioral innovation and diversification.

Environmental Correlates of Sexual Signaling in the Heteroptera: A Prospective Study.

Simple SummarySexual selection influences a broad range of morphological, behavioral, and physiological characteristics, helping to drive the divergence of populations, up to and including the formation of new species. However, we are still limited in our ability to predict what traits sexual selection may favor and under what circumstances. We addressed sexual selection in the Hemiptera, also known as true bugs, identifying four main forms of sexual communication used by the sub-order Heteroptera (chemical signals, acoustic signaling via stridulation, abdominal vibration, and tactile signaling via antennation). We compared how these modes of sexual communication occur within three broad habitat types in which they are found (leaf-litter, plant-based, and semi-aquatic habitats), reviewing each mode of communication, their environmental context, and providing a wide range of examples of their occurrence within the Heteroptera. We argue that looking for associations between mechanisms of sexual selection and particular ecologies will help us move towards a more predictive theory of sexual selection. In our rapidly changing world, these kinds of studies may also be important in understanding the role sexual selection will play in determining species persistence.Sexual selection is a major evolutionary process, shaping organisms in terms of success in competition for access to mates and their gametes. The study of sexual selection has provided rich empirical and theoretical literature addressing the ecological and evolutionary causes and consequences of competition for gametes. However, there remains a bias towards individual, species-specific studies, whilst broader, cross-species comparisons looking for wider-ranging patterns in sexual selection remain uncommon. For instance, we are still some ways from understanding why particular kinds of traits tend to evolve under sexual selection, and under what circumstances. Here we consider sexual selection in the Heteroptera, a sub-order of the Hemiptera, or true bugs. The latter is the largest of the hemimetabolous insect orders, whilst the Heteroptera itself comprises some 40,000-plus described species. We focus on four key sexual signaling modes found in the Heteroptera: chemical signals, acoustic signaling via stridulation, vibrational (substrate) signaling, and finally tactile signaling (antennation). We compare how these modes vary across broad habitat types and provide a review of each type of signal. We ask how we might move towards a more predictive theory of sexual selection, that links mechanisms and targets of sexual selection to various ecologies.

What Determines Paternity in Wild Lizards? A Spatiotemporal Analysis of Behavior and Morphology.

Mating behavior in animals can be understood as a sequence of events that begins with individuals encountering one another and ends with the production of offspring. Behavioral descriptions of animal interactions characterize early elements of this sequence, and genetic descriptions use offspring parentage to characterize the final outcome, with behavioral and physiological assessments of mates and mechanisms of copulation and fertilization comprising intermediate steps. However, behavioral and genetic descriptions of mating systems are often inconsistent with one another, complicating expectations for crucial aspects of mating biology, such as the presence of multiple mating. Here, we use behavioral and genetic data from a wild population of the lizard Anolis cristatellus to characterize female multiple mating and the potential for sexual selection through female mate choice in this species. We find that 48% of sampled females bore offspring sired by multiple males. Moreover, spatiotemporal proximity between males and females was associated with whether a male sired a female's offspring, and if yes, how many offspring he sired. Additionally, male body size, but not display behavior, was associated with reproductive outcomes for male-female pairs. While much remains to be learned about the mechanisms of mating and targets of sexual selection in A. cristatellus, it is clear that female multiple mating is a substantial component of this species' mating system in nature.

Flexibility of nuptial colouration in a unique ecotype of threespine stickleback (Gasterosteus aculeatus)

Nuptial colouration in animals may serve as a signal of competitor and (or) mate quality during breeding. In many temperate fishes, nuptial colouration develops during discrete breeding seasons and is a target of sexual selection. We examine nuptial colouration and behaviour of a unique ecotype of threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758), wherein males turn from dull brown-grey to pearlescent white during the breeding season. The main goal of this work was to determine the relative role of white colouration in intersexual competition and mate choice. In a combination of field and laboratory work, we found that males are brightest white when engaging in courtship activities in the presence of a female; this indicates that white colouration may be primarily related to enhancing signalling during mate attraction. White colouration intensity increased as the breeding season progressed and may be related to an influx of conspecifics. Colour change from cryptic grey to bright white occurred rapidly (<90 s) and may be deployed to enhance behavioural signals. We conclude that bright white colouration in the white ecotype is a potential signal of mate quality and may have evolved from a previously existing capacity for colour plasticity in common threespine stickleback.

Drosophila female reproductive tract gene expression reveals coordinated mating responses and rapidly evolving tissue-specific genes.

Sexual reproduction in internally fertilizing species requires complex coordination between female and male reproductive systems and among the diverse tissues of the female reproductive tract (FRT). Here, we report a comprehensive, tissue-specific investigation of Drosophila melanogaster FRT gene expression before and after mating. We identified expression profiles that distinguished each tissue, including major differences between tissues with glandular or primarily nonglandular epithelium. All tissues were enriched for distinct sets of genes possessing secretion signals that exhibited accelerated evolution, as might be expected for genes participating in molecular interactions between the sexes within the FRT extracellular environment. Despite robust transcriptional differences between tissues, postmating responses were dominated by coordinated transient changes indicative of an integrated systems-level functional response. This comprehensive characterization of gene expression throughout the FRT identifies putative female contributions to postcopulatory events critical to reproduction and potentially reproductive isolation, as well as the putative targets of sexual selection and conflict.

Sexual selection on performance traits in an Australian lizard with alternative reproductive tactics.

Sexual selection shapes the adaptive landscape in complex ways that lead to trait integration. Much of our understanding of selection comes from studies of morphological traits. However, few studies attempt to quantify the form and direction of selection on performance even though it is predicted to be a more direct target of selection in nature. We measured sexual selection on performance traits (bite force, sprint speed and endurance) in an Australian lizard, the Eastern water skink (Eulamprus quoyii). We first staged 123 contests between size-matched males to investigate whether performance traits were important in determining contest outcome. In a second experiment, we established six breeding populations in large replicate semi-natural enclosures to estimate whether performance traits predicted reproductive success. Our results show that none of the performance measures were important in predicting contest outcome and were not generally strong predictors of reproductive success. However, our analyses suggest a complex fitness landscape driven by males adopting different alternative reproductive tactics (ARTs). We provide a rare test of the role performance plays in sexual selection and highlight the need to test common assumptions regarding the link between maximal performance and fitness. Our results suggest that performance traits may not necessarily be direct targets of sexual selection, but rather indirect targets through their integration with morphological and/or behavioural traits, highlighting a need for more explicit tests of the predicted links between performance and fitness.

No evidence of male-biased sexual selection in a snake with conventional Darwinian sex roles.

Decades of research on sexual selection have demonstrated that ‘conventional’ Darwinian sex roles are common in species with anisogamous gametes, with those species often exhibiting male-biased sexual selection. Yet, mating system characteristics such as long-term sperm storage and polyandry have the capacity to disrupt this pattern. Here, these ideas were explored by quantifying sexual selection metrics for the western diamond-backed rattlesnake (Crotalus atrox). A significant standardized sexual selection gradient was not found for males (βSS = 0.588, p = 0.199) or females (βSS = 0.151, p = 0.664), and opportunities for sexual selection (Is) and selection (I) did not differ between males (Is = 0.069, I = 0.360) and females (Is = 0.284, I = 0.424; both p > 0.05). Furthermore, the sexes did not differ in the maximum intensity of precopulatory sexual selection (males: s′max = 0.155, females: s′max = 0.080; p > 0.05). Finally, there was no evidence that male snout–vent length, a trait associated with mating advantage, is a target of sexual selection (p > 0.05). These results suggest a lack of male-biased sexual selection in this population. Mating system characteristics that could erode male-biased sexual selection, despite the presence of conventional Darwinian sex roles, are discussed.

Male body size does not affect the refractory period of females in the West Indian sweet potato weevil Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) and the seed bug Togo hemipterus (Scott) (Heteroptera: Lygaeidae)

Multiple mating by females increases both the risk and intensity of sperm competition for males. The ability to temporarily or permanently inhibit female receptivity to further mating represents a highly adaptive strategy to reduce the risk of sperm competition. Males of the West Indian sweet potato weevil Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae) and the seed bug Togo hemipterus (Scott) (Heteroptera: Lygaeidae) use accessory gland substances to inhibit remating in females. It is known that there is variance in the length of the female refractory period (i.e., the effectiveness of male ejaculate substances that inhibit female remating) within a species. However, it is unclear what types of male traits affect the length of the female refractory period. The mechanism of the female refractory period is not sufficiently revealed. We focused on male body size, which is often a target of sexual selection, and investigated the relationship between male body size and both the refractory period of females and mating duration. Contrary to our thought, male body size did not significantly influence the refractory period of females or mating duration in either species. Smaller male body size was not particularly favored by post-copulatory sexual selection in either species.

Digit identity matters: origin and evolution of sexual dimorphism in the digit lengths of tropidurid lizards

AbstractSexual dimorphism in digit lengths reflects phenotypic evolution mediated by developmental steroids. Differences in the identity of the sexually-dimorphic digit may evolve if the concentrations of sex-steroid receptors in the digit are easily modified and the initial changes have low impact on fitness. Accordingly, sexual dimorphism in digit lengths might initially originate under neutral selective regimes, being subsequently co-opted by embryonic hormonal effects on sensitive traits that are more likely to be targeted by selection. Correlated variation among sexually-dimorphic traits might therefore reflect pleiotropic hormonal modulation during development. Moreover, the identity and trend of the sexually-dimorphic digit might be evolutionarily labile even among closely-related species. We evaluated this model by assessing the identity of sexually-dimorphic digits among 11 Tropiduridae lizard species and inferring evolutionary patterns of sexual dimorphism. Assuming that digit lengths can be used as a proxy for hormonal modulation of steroid-sensitive traits during development, we tested for evolutionary associations among sexual dimorphism of digit lengths, body size and other traits that may be direct targets of sexual selection in the Tropiduridae. Sexual dimorphism in digit lengths is evolutionarily labile in the Tropiduridae, and diversity, instead of conservatism, seems to rule developmental mechanisms underlying the evolution of sexual dimorphism in digit ratios.

Selection on multiple sexual signals in two Central and Eastern European populations of the barn swallow.

Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations, although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Central and East European barn swallow (Hirundo rustica rustica) populations from Czech Republic and Romania over multiple years. We then related these differences in selection to variation in sexual characters among barn swallow populations. Our results show that tail length and ventral coloration vary between populations, sexes, and age classes (first‐time breeders vs. experienced birds). We found that selection on tail length was stronger in first‐time breeders than in experienced birds and in males than in females in the Romanian population, while these differences between age groups and sexes were weak in Czech birds. We suggest that the populational difference in selection on tail length might be related to the differences in breeding conditions. Our results show that ventral coloration is darker (i.e., has lower brightness) in the Romanian than in the Czech population, and in experienced birds and males compared with first‐time breeders and females, respectively. The sexual difference in ventral coloration may suggest sexual selection on this trait, which is supported by the significant directional selection of ventral coloration in first‐time breeding males on laying date. However, after controlling for the confounding effect of wing length and tarsus length, the partial directional selection gradient on this trait turned nonsignificant, suggesting that the advantage of dark ventral coloration in early breeding birds is determined by the correlated traits of body size. These findings show that ventral coloration may be advantageous over the breeding season, but the underlying mechanism of this relationship is not clarified.

Sexual selection and the evolution of sperm morphology in sharks.

Post-copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post-copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter- and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.

Ventral colour, not tail streamer length, is associated with seasonal reproductive performance in a Chinese population of Barn Swallows (Hirundo rustica gutturalis)

Phenotypic differentiation is common among populations that have large geographic distributions. One proposed mechanism driving phenotype divergence is sexual selection, which predicts that trait differences among closely related populations are underlain by variation in reproductive performance. Here, we examined a population of Asian Barn Swallows (Hirundo rustica gutturalis) in northeastern China. We ask whether traits shown to be under divergent sexual selection in other Barn Swallow populations are under sexual selection in this north Asian population by determining whether two features of phenotype variation, tail streamer length and ventral plumage colouration (including both throat and belly regions), are sexually dimorphic, associated with patterns of assortative mating and predictive of reproductive success. In this population, the length of tail streamers did not correlate with ventral plumage colouration in either males or females. The length of tail streamers was sexually dimorphic, but we did not find assortative mating by tail streamer length. By contrast, we found no sexual dichromatism but we did find assortative mating by throat colouration. Our correlational results indicated that the breeding performance of male Barn Swallows was associated with differences in their ventral plumage colouration, suggesting that ventral plumage colouration is likely a target of sexual selection in this population. Our finding that tail streamer length is unlikely to be under sexual selection is consistent with studies of other H. rustica gutturalis populations. The result that ventral plumage colour is likely to be under sexual selection is partially consistent with previous studies on Japanese H. rustica gutturalis, in which male throat but not belly plumage colour is the sexually selected trait.

Within-individual variation in signal production limits female choice in noisy treefrog choruses

In acoustically communicating animals such as anurans and orthopterans, individual signalers can display remarkable variation in signal traits, even within a single bout of calling. This within-individual variation has the potential to “mask” the between-individual variation that is the target of sexual selection. Thus, receivers may not always be able to discriminate among males based on properties of their acoustic signals, even when female choice is well documented in the lab. The effect of within-individual variation may be compounded by noise generated by breeding choruses of conspecifics, which can prevent signal detection or discrimination. We manipulated within-individual variation in two signal traits (call rate and pulse rate) that are critically important for mate choice in Hyla chrysoscelis, Cope’s gray treefrog. We replicated our design at three realistic levels of chorus noise. Within-individual variation in signal traits reduced the strength of sexual selection on one of two traits, and receivers were less likely to discriminate against lower-quality signals under conditions of realistic chorus noise. Our results suggest that preference functions generated using stimuli that lack within-individual variation, under ideal listening conditions, may chronically over-estimate the strength of sexual selection on signal traits in natural populations.

Evolutionary allometry reveals a shift in selection pressure on male horn size.

How selection pressures acting within species interact with developmental constraints to shape macro-evolutionary patterns of species divergence is still poorly understood. In particular, whether or not sexual selection affects evolutionary allometry, the increase in trait size with body size across species, of secondary sexual characters, remains largely unknown. In this context, bovid horn size is an especially relevant trait to study because horns are present in both sexes, but the intensity of sexual selection acting on them is expected to vary both among species and between sexes. Using a unique data set of sex-specific horn size and body mass including 91 species of bovids, we compared the evolutionary allometry between horn size and body mass between sexes while accounting for both the intensity of sexual selection and phylogenetic relationship among species. We found a nonlinear evolutionary allometry where the allometric slope decreased with increasing species body mass. This pattern, much more pronounced in males than in females, suggests either that horn size is limited by some constraints in the largest bovids or is no longer the direct target of sexual selection in very large species.

Evolution of male copulatory organs in box crabs (Decapoda: Eubrachyura: Calappidae De Haan, 1833)

Male genitalia are extraordinarily diverse, and this diversity makes them valuable taxonomic and phylogenetic markers. Genitalia of true crabs (Brachyura) consist of two pairs of modified appendages, or gonopods. The first pair is tubular, and holds the second pair during copulation. Whether the second pair is shorter or longer than the first pair has important implications for copulation. Its length is often similar in closely related species, e.g. within genera and families, but is highly variable in the Brachyura at large. The genus Calappa Weber, 1795 contains species with long, short, and intermediate-length second gonopods, representing an unusually variable pattern. We investigated the evolution of the second gonopods in Calappa and other members of Calappidae. We assembled a molecular multi-locus phylogeny (mitochondrial marker: COI and 16S, nuclear marker: Enolase, H3 and 28S). Based on this phylogeny, long second gonopods are the ancestral state for Calappa as well as Calappidae in general. Short second gonopods evolved once, while intermediate-length second gonopods evolved independently at least four times. Scanning electron microscopic images of second gonopods of 22 species of Calappidae reveal that shortening of the second gonopod is always achieved by a shortening of the terminal segment. Congruently, taxon-specific structures at the tip of the terminal segment of the second gonopod, such as spines and pistil-like protrusions, are limited to long second gonopods. Based on current knowledge, a shortening of the second gonopod should be accompanied by extensive changes in the copulatory mechanism of males and females, including changes to the copulatory mechanism, mechanism of species recognition, targets of sexual selection, and the potential for sperm removal. Calappa therefore provides a vital example for the study of changes in copulatory mechanisms.