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Data from: How populations differentiate despite gene flow: sexual and natural selection drive phenotypic divergence within a land fish, the Pacific leaping blenny

Background: Divergence between populations in reproductively important features is often vital for speciation. Many studies attempt to identify the cause of population differentiation in phenotype through the study of a specific selection pressure. Holistic studies that consider the interaction of several contrasting forms of selection are more rare. Most studies also fail to consider the history of connectivity among populations and the potential for genetic drift or gene flow to facilitate or limit phenotypic divergence. We examined the interacting effects of natural selection, sexual selection and the history of connectivity on phenotypic differentiation among five populations of the Pacific leaping blenny (Alticus arnoldorum), a land fish endemic to the island of Guam. Results: We found key differences among populations in two male ornaments—the size of a prominent head crest and conspicuousness of a coloured dorsal fin—that reflected a trade-off between the intensity of sexual selection (male biased sex ratios) and natural selection (exposure to predators). This differentiation in ornamentation has occurred despite evidence suggesting extensive gene flow among populations, which implies that the change in ornament expression has been recent (and potentially plastic). Conclusions: Our study provides an early snapshot of divergence in reproductively important features that, regardless of whether it reflects genetic or plastic changes in phenotype, could ultimately form a reproductive barrier among populations.

opencc-zeroDec 2011View details →

Data from: MHC variation is related to a sexually selected ornament, survival and parasite resistance in common yellowthroats

Hamilton and Zuk (1982) proposed that females choose mates based on ornaments whose expression is dependent on their genetically based resistance to parasites. The Major Histocompatibility Complex (MHC) plays an important role in pathogen recognition and is a good candidate for testing the relationships between immune genes and both ornament expression and parasite resistance. We tested the hypothesis that female common yellowthroats prefer to mate with more ornamented males, because it is a signal of their MHC-based resistance to parasites and likelihood of survival. In this species, females prefer males that have larger black facial masks as extra-pair mates. Using pyrosequencing, we found that mask size was positively related to the number of different MHC class II alleles, as predicted if greater variation at the MHC allows for the recognition of a greater variety of pathogens. Furthermore, males with more MHC class II alleles had greater apparent survival, and resistance to malaria infection was associated with the presence of a particular MHC class II allele. Thus, extra-pair mating may provide female warblers with immunity genes that are related to parasite resistance, survival and the expression of a male ornament, consistent with good genes models of sexual selection.

opencc-zeroJul 2019View details →

Data from: Contemporary sexual selection does not explain variation in male display traits among populations

Sexual selection is widely hypothesized to facilitate the evolution of reproductive isolation through divergence in sexual traits and sexual trait preferences. However, direct evidence of divergent sexual selection causing intraspecific trait divergence remains limited. Using the wolf spider Schizocosa crassipes, we characterized patterns of female mate choice within and among geographic locations and related those patterns to geographic variation in male display traits to test whether divergent sexual selection caused by mate choice explains intraspecific trait variation. We found evidence of phenotypic selection on male behavior arising from female mate choice, but no evidence that selection varied among locations. Only those suites of morphological and behavioral traits that did not influence mate choice varied geographically. These results are inconsistent with ongoing divergent sexual selection underlying the observed intraspecific divergence in male display traits. These findings align with theory on the potentially restrictive conditions under which divergent sexual selection may persist, and suggest that long-term studies capable of detecting periodic or transient divergent sexual selection will be critical to rigorously assess the relative importance of divergent sexual selection in intraspecific trait divergence.

opencc-zeroDec 2014View details →

Data from: Paternity analyses in wild-caught and lab-reared Caribbean cricket females reveal the influence of mating environment on post-copulatory sexual selection

Polyandry is ubiquitous in insects and provides the conditions necessary for male- and female-driven forms of post-copulatory sexual selection to arise. Populations of Amphiacusta sanctaecrucis exhibit significant divergence in portions of the male genitalia that are inserted directly into the female reproductive tract, suggesting that males may exercise some post-copulatory control over fertilization success. We examine the potential for male-male and male-female post-copulatory interactions to influence paternity in wild-caught females of A. sanctaecrucis and contrast our findings with those obtained from females reared in a high-density laboratory environment. We find that female A. sanctaecrucis exercise control by mating multiple times (females mount males), but that male-male post-copulatory interactions may influence paternity success. Moreover, post-copulatory interactions that affect reproductive success of males are not independent of mating environment: clutches of wild-caught females exhibit higher sire diversity and lower paternity skew than clutches of lab-reared females. There was no strong evidence for last-male precedence in either case. Most attempts at disentangling the contributions of male-male and male-female interactions toward post-copulatory sexual selection have been undertaken in a laboratory setting and may not capture the full context in which they take place —such as the relationship between pre-mating and post-mating interactions. Our results reinforce the importance of designing studies that can capture the multifaceted nature of sexual selection for elucidating the role of post-copulatory sexual selection in driving the evolution of male and female reproductive traits, especially when different components (e.g., pre-copulatory and post-copulatory interactions) do not exert independent effects on reproductive outcomes.

Data from: Genome size variation affects song attractiveness in grasshoppers: evidence for sexual selection against large genomes

Genome size is largely uncorrelated to organismal complexity and adaptive scenarios. Genetic drift as well as intragenomic conflict have been put forward to explain this observation. We here study the impact of genome size on sexual attractiveness in the bow-winged grasshopper Chorthippus biguttulus. Grasshoppers show particularly large variation in genome size due to the high prevalence of supernumerary chromosomes that are considered (mildly) selfish, as evidenced by non-Mendelian inheritance and fitness costs if present in high numbers. We ranked male grasshoppers by song characteristics that are known to affect female preferences in this species and scored genome sizes of attractive and unattractive individuals from the extremes of this distribution. We find that attractive singers have significantly smaller genomes, demonstrating that genome size is reflected in male courtship songs and that females prefer songs of males with small genomes. Such a genome size dependent mate preference effectively selects against selfish genetic elements that tend to increase genome size. The data therefore provide a novel example of how sexual selection can reinforce natural selection and can act as an agent in an intragenomic arms race. Furthermore, our findings indicate an underappreciated route of how choosy females could gain indirect benefits.

opencc-zeroDec 2018View details →

Data from: How sexual and natural selection shape sexual size dimorphism: evidence from multiple evolutionary scales

1. Sexual size dimorphism (SSD) is pervasive across taxa and reflects differences in the effects of sexual and natural selection on body size between the sexes. However, disentangling the complex eco-evolutionary interactions between these two mechanisms remains a major challenge for biologists. 2. Here, we combine macro-evolutionary (between-species), local evolutionary (between-population) and fine-scale evolutionary (within-population) patterns of SSD to explore how sexual and natural selection interact and shape the evolution of SSD in Australian agamid lizards. Australian agamid lizards show substantial variation in SSD, ecological traits and species density making them an ideal study system to address this question. 3. At the between-species level, population density, ecological generalism and mean species size significantly predict SSD variation, however, only ecological generalism was found to significantly explain variation in larger than average male-biased SSD. At the population level, density positively correlated with SSD in native habitats, but not city park habitats. Last, agonistic behaviour acted as the primary driver of SSD at the within-population level. 4. Our results indicate how sexual and natural selection can interact at different evolutionary scales, and show the importance of considering both selective mechanisms when investigating patterns of SSD.

opencc-zeroMar 2020View details →

The intensity of sexual selection, body size and reproductive success in a mating system with male-male combat: Is bigger better?

Body size is a key selected trait in many animal systems: larger size is sexually selected for in males because it confers a reproductive advantage during contest competition for access to females, and larger females are naturally selected for fecundity. Herein, we used radio-telemetry to gather a large dataset of male-female interactions and DNA paternity analyses to characterize the intensity of sexual selection and the link between two body size metrics (body length and condition, the latter manipulated experimentally for males) and reproductive success in a population of puff adders (Bitis arietans). Our multiple estimates of the intensity of sexual selection generally indicated that males experienced stronger sexual selection than females. However, the Bateman gradients did not differ by sex, despite the fact that males increased reproductive success by mating with multiple females while females did not. We also found no strong evidence that females experienced indirect fitness benefits through multiple matings. Body size was not a key predictor of male reproductive success, and for females, body condition—but not body length—was the critical fecundity trait. Altogether, a combination of factors suggests that post–copulatory mechanisms of sexual selection (e.g., sperm competition, cryptic female choice) may play critical roles in this mating system and perhaps that of other snakes. We interpret our findings in the context of sexual conflict—a ubiquitous and potent driver of mating strategy evolution—to propose a scenario for the evolution of female promiscuity that is applicable to many other animal systems where males roam widely to locate females at high costs.

opencc-zeroDec 2012View details →

Data from: Neutral and selection-driven decay of sexual traits in asexual stick insects

Environmental shifts and lifestyle changes may result in formerly adaptive traits becoming non-functional or maladaptive. The subsequent decay of such traits highlights the importance of natural selection for adaptations, yet its causes have rarely been investigated. To study the fate of formerly adaptive traits after lifestyle changes, we evaluated sexual traits in five independently derived asexual lineages, including traits that are specific to males and therefore not exposed to selection. At least four of the asexual lineages retained the capacity to produce males that display normal courtship behaviours and are able to fertilize eggs of females from related sexual species. The maintenance of male traits may stem from pleiotropy, or from these traits only regressing via drift, which may require millions of years to generate phenotypic effects. By contrast, we found parallel decay of sexual traits in females. Asexual females produced altered airborne and contact signals, had modified sperm storage organs, and lost the ability to fertilize their eggs, impeding reversals to sexual reproduction. Female sexual traits were decayed even in recently derived asexuals, suggesting that trait changes following the evolution of asexuality, when they occur, proceed rapidly and are driven by selective processes rather than drift.

Data from: Identifying signatures of sexual selection using genomewide selection components analysis

Sexual selection must affect the genome for it to have an evolutionary impact, yet signatures of selection remain elusive. Here we use an individual-based model to investigate the utility of genome-wide selection components analysis, which compares allele frequencies of individuals at different life history stages within a single population to detect selection without requiring a priori knowledge of traits under selection. We modeled a diploid, sexually reproducing population and introduced strong mate choice on a quantitative trait to simulate sexual selection. Genome-wide allele frequencies in adults and offspring were compared using weighted FST values. The average number of outlier peaks (i.e., those with significantly large FST values) with a quantitative trait locus in close proximity ("real" peaks) represented correct diagnoses of loci under selection, whereas peaks above the FST significance threshold without a quantitative trait locus reflected spurious peaks. We found that, even with moderate sample sizes, signatures of strong sexual selection were detectable, but larger sample sizes improved detection rates. The model was better able to detect selection with more neutral markers, and when quantitative trait loci and neutral markers were distributed across multiple chromosomes. Although environmental variation decreased detection rates, the identification of real peaks nevertheless remained feasible. We also found that detection rates can be improved by sampling multiple populations experiencing similar selection regimes. In short, genome-wide selection components analysis is a challenging but feasible approach for the identification of regions of the genome under selection.

Data from: Demographic drivers of age-dependent sexual selection

Sexual selection has a critical role in evolution, and it is fundamental to identify what ecological factors drive its variation. Disentangling the ecological correlates of sexual selection over the long term, however, is challenging and has rarely been done in nature. We sought to assess how demographic changes influenced the intensity, direction and form of sexual selection and whether selective pressures varied with age. We tested whether breeder sex ratio, number of competitors and age structure influenced selection differentials on horn length of wild bighorn rams (Ovis canadensis) of different age classes on Ram Mountain, Alberta. We used 21 years of data including a detailed pedigree, demographic parameters and repeated morphological measurements. Sexual selection on horn length of males of all ages was directional and positive. Selection intensity increased with the number of competitors, reflecting male–male encounter rate during the rut, but was independent of breeder sex ratio or age structure. This result can also be linked to changes in population size because the number of competitors was highly correlated to total number of sheep. This demographic effect likely arises from age-dependent mating tactics. Males aged 2–4 years are weakly competitive and experienced stronger sexual selection as they accounted for a greater proportion of all males. Selection experienced by mature males appeared independent of demography. Our study provides a rare description of the demographic determinants of sexual selection in nature.

opencc-zeroDec 2014View details →

Data from: Signal architecture: temporal variability and individual consistency of multiple sexually selected signals

1. Multiple signals should be favoured when the benefit of additional signals outweigh their costs. Despite increased attention on multiple-signalling systems, few studies have focused on signal architecture to understand the potential information content of multiple signals. 2. To understand the patterns of signal plasticity and consistency over the lifetime of individuals we conducted a longitudinal study of multiple signals known to be under sexual selection in male lark buntings, Calamospiza melanocorys. 3. Within years, we found extensive among-individual variation in all four plumage ornaments we measured. Surprisingly, there were few correlations among these signals, suggesting that individuals contain a mosaic of signals. Signals were only moderately repeatable across years, which indicates some signal plasticity or age related change. In some years, the direction of change in particular signals relative to the previous year was consistent for most individuals in the population, suggesting that broad scale ecological factors affected the ornament phenotype. Different ornaments were affected by different ecological or social factors because the population-wide shift in a given signal was independent of change in other signals. 4. Our combined results suggest that different signals—including different components of the same color patch in some cases—provide diverse and independent information about the individual to signal receivers in the context of sexual selection.

Data from: Rapid diversification of sexual signals in Hawaiian Nesosydne planthoppers (Hemiptera: Delphacidae): the relative role of neutral and selective forces

Changes in sexual signals have the potential to promote rapid divergence and reproductive isolation among populations of animals. Thus, identifying processes contributing to variation in signals is key to understanding the drivers of speciation. However, it is difficult to identify the processes initiating changes in signals in empirical systems because (1) the demographic history of populations under study is usually unclear, and (2) there is no unified hypothesis-testing framework for evaluating the simultaneous contribution of multiple processes. A unique system for study in the Hawaiian Islands, the planthopper species Nesosydne chambersi, offers a clear demographic context to disentangle these factors. By measuring variation in male vibratory sexual signals across different genetic populations on the island of Hawaii, we found that that multiple signal traits varied significantly between populations. We developed a mixed modelling framework to simultaneously test competing hypotheses about which processes contribute to changes in signal traits: genetic drift, sensory drive or reproductive character displacement. Our findings suggest that signal divergence proceeds along different axes for different signal traits under the influence of both neutral and selective processes. They are the first, to our knowledge, to document the relative importance of multiple processes on divergence in sexual signals.

Data from: Sexual selection targets cetacean pelvic bones

Male genitalia evolve rapidly, probably as a result of sexual selection. Whether this pattern extends to the internal infrastructure that influences genital movements remains unknown. Cetaceans (whales and dolphins) offer a unique opportunity to test this hypothesis: since evolving from land-dwelling ancestors, they lost external hind limbs and evolved a highly reduced pelvis which seems to serve no other function except to anchor muscles that maneuver the penis. Here we create a novel morphometric pipeline to analyze the size and shape evolution of pelvic bones from 130 individuals (29 species) in the context of inferred mating system. We present two main findings: 1) males from species with relatively intense sexual selection (inferred by relative testes size) have evolved relatively large penises and pelvic bones compared to their body size, and 2) pelvic bone shape diverges more quickly in species pairs that have diverged in inferred mating system. Neither pattern was observed in the anterior-most pair of vertebral ribs, which served as a negative control. This study provides evidence that sexual selection can affect internal anatomy that controls male genitalia. These important functions may explain why cetacean pelvic bones have not been lost through evolutionary time.

opencc-zeroDec 2016View details →

Data from: Male genital titillators and the intensity of post-copulatory sexual selection across bushcrickets

Animal genitalia are diverse and a growing body of evidence suggests that they evolve rapidly under post-copulatory sexual selection. This process is predicted to be more intense in polyandrous species, although there have been very few comparative studies of the relationship between the complexity of genital structures in males and measures of the degree of polyandry. In some bushcricket families, males possess sclerotized copulatory structures known as titillators, which are inserted into the female's genital chamber and moved rhythmically. Like other genital structures, bushcricket titillators are widely used as important taxonomic characters and show considerable variation across species in structure, shape, and the extent to which they are spined. Here, we examine relationships between the presence/absence of titillators, titillator complexity, and both mating frequency and the degree of polyandry in bushcrickets, using phylogenetic comparative analyses. Using published sources combined with original observations, data were obtained for the mean level of polyandry, the duration of the male and female sexual refractory periods, and the level of complexity of titillators. To analyze data, we fitted phylogenetic generalized least squares models. No significant relationships were found between titillator presence or complexity and either the level of polyandry, duration of the male's sexual refractory period, or the ratio of the female and male sexual refractory periods. The duration of the female's refractory period, however, was positively associated with titillator presence and negatively associated with titillator complexity. The data therefore partially support the hypothesis that post-copulatory sexual selection drives genital evolution in this taxon.

Data from: Are sexually selected traits affected by a poor environment early in life?

Background: Challenging conditions experienced early in life, such as a restricted diet, can detrimentally affect key life-history traits. Individuals can reduce these costs by delaying their sexual maturation, albeit at the price of the later onset of breeding, to eventually reach the same adult size as individuals that grow up in a benevolent environment. Delayed maturation can, however, still lead to other detrimental morphological and physiological changes that become apparent later in adulthood (e.g. shorter lifespan, faster senescence). In general, research focuses on the naturally selected costs of a poor early diet. In mosquitofish (Gambusia holbrooki), males with limited food intake early in life delay maturation to reach a similar adult body size to their well-fed counterparts ('catch-up growth'). Here we tested whether a poor early diet is costly due to the reduced expression of sexually selected male characters, namely genital size and ejaculate traits. Results: We found that a male's diet early in life significantly influenced his sperm reserves and sperm replenishment rate. Shortly after maturation males with a restricted early diet had significantly lower sperm reserves and slower replenishment rates than control diet males, but this dietary difference was no longer detectable in older males. Conclusions: Although delaying maturation to reach the same body size as well fed juveniles can ameliorate some costs of a poor start in life, our findings suggest that costs might still arise because of sexual selection against these males. It should be noted, however, that the observed effects are modest (Hedges' g = 0.20–0.36), and the assumption that lower sperm production translates into a decline in fitness under sperm competition remains unconfirmed.

opencc-zeroDec 2012View details →

Data from: Reconstructing paternal genotypes to infer patterns of sperm storage and sexual selection in the hawksbill turtle

Postcopulatory sperm storage can serve a range of functions, including ensuring fertility, allowing delayed fertilization and facilitating sexual selection. Sperm storage is likely to be particularly important in wide-ranging animals with low population densities, but its prevalence and importance in such taxa, and its role in promoting sexual selection, are poorly known. Here, we use a powerful microsatellite array and paternal genotype reconstruction to assess the prevalence of sperm storage and test sexual selection hypotheses of genetic biases to paternity in one such species, the critically endangered hawksbill turtle, Eretmochelys imbricata. In the majority of females (90.7%, N = 43), all offspring were sired by a single male. In the few cases of multiple paternity (9.3%), two males fertilized each female. Importantly, the identity and proportional fertilization success of males were consistent across all sequential nests laid by individual females over the breeding season (up to five nests over 75 days). No males were identified as having fertilized more than one female, suggesting that a large number of males are available to females. No evidence for biases to paternity based on heterozygosity or relatedness was found. These results indicate that female hawksbill turtles are predominantly monogamous within a season, store sperm for the duration of the nesting season and do not re-mate between nests. Furthermore, females do not appear to be using sperm storage to facilitate sexual selection. Consequently, the primary value of storing sperm in marine turtles may be to uncouple mating and fertilization in time and avoid costly re-mating.

opencc-zeroDec 2018View details →

Data from: The causal relationship between sexual selection and sexual size dimorphism in marine gastropods

Sexual size dimorphism is widespread among dioecious species but its underlying driving forces are often complex. A review of sexual size dimorphism in marine gastropods revealed two common patterns: firstly, sexual size dimorphism, with females being larger than males, and secondly females being larger than males in mating pairs; both of which suggest sexual selection as being causally related with sexual size dimorphism. To test this hypothesis, we initially investigated mechanisms driving sexual selection on size in three congeneric marine gastropods with different degrees of sexual size dimorphism, and, secondly, the correlation between male/female sexual selection and sexual size dimorphism across several marine gastropod species. Male mate choice via mucus trail following (as evidence of sexual selection) was found during the mating process in all three congeneric species, despite the fact that not all species showed sexual size dimorphism. There was also a significant and strong negative correlation between female sexual selection and sexual size dimorphism across 16 cases from seven marine gastropod species. These results suggest that sexual selection does not drive sexual size dimorphism. There was, however, evidence of males utilizing a similar mechanism to choose mates (i.e. selecting a female slightly larger than own size) which may be widespread among gastropods, and in tandem with present variability in sexual size dimorphism among species, provide a plausible explanation of the observed mating patterns in marine gastropods.

Data from: Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations

Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and Eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signaling axes, despite very low-level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely-related wild populations.

Data from: Sexually antagonistic association between paternal phenotype and offspring viability reinforces total selection on a sexually selected trait

The evolution of conspicuous sexually selected traits, such as horns or antlers, has fascinated biologists for more than a century. Elaborate traits can only evolve if they substantially increase reproduction, because they probably incur survival costs to the bearer. Total selection on these traits, however, includes sexual selection on sires and viability selection on offspring and can be influenced by changes in each of these components. Non-random associations between paternal phenotype and offspring viability may thus affect total selection on sexually selected traits. Long-term data on wild bighorn sheep (Ovis canadensis) provide the first evidence in nature that association between paternal phenotype and lamb viability strengthens total selection on horn size of adult rams, a sexually selected trait. The association of paternal horn length and offspring viability was sexually antagonistic: long-horned males sired sons with high viability but daughters of low viability. These results shed new light on the evolutionary dynamics of an iconic sexually selected trait and have important implications for sustainable wildlife management.