Divergent sexual signals reflect costs of local parasites*

Many closely related populations are distinguished by variation in sexual signals and this variation is hypothesized to play an important role in reproductive isolation and speciation. Within populations, there is considerable evidence that sexual signals provide information about the incidence and severity of parasite infections, but it remains unclear if variation in parasite communities across space could play a role in initiating or maintaining sexual trait divergence. To test for variation in parasite-associated selection, we compared three barn swallow subspecies with divergent sexual signals. We found that parasite community structure and host tolerance to ecologically similar parasites varied between subspecies. Across subspecies we also found that different parasites were costly in terms of male survival and reproductive success. For each subspecies, the preferred sexual signal(s) were associated with the most costly local parasite(s), indicating that divergent signals are providing relevant information to females about local parasite communities. Across subspecies, the same traits were often associated with different parasites, indicating that parasite-sexual signal links are quite flexible and may evolve relatively quickly. This study provides evidence for (1) variation in parasite communities and (2) different parasite-sexual signal links among three closely related subspecies with divergent sexual signal traits, suggesting that parasites may play an important role in initiating and/or maintaining the divergence of sexual signals among these closely related, yet geographically isolated populations.     

Among‐population variation and correlations in sexually dimorphic traits of Silene latifolia

Abstract The degree of sexual dimorphism in a trait may be determined directly by disruptive selection, as well as by correlations with other traits under selection. We grew seeds from nine populations of the dioecious plant Silene latifolia in a common‐garden experiment to determine whether phenotypic variation and correlations existed for floral, leaf and resource allocation traits, and whether this variation had a genetic component. We also determined the traits which were sexually dimorphic, the degree of dimorphism, and whether it varied among populations. Seven traits exhibited among‐population variation and sexual dimorphism. Variation in the degree of dimorphism occurred only for two traits, suggesting that dimorphism may be evolving more slowly than trait means. Males had more, smaller flowers, shorter leaves, and allocated less of their total biomass to stems and more to leaves than females. Flower production was the most sexually dimorphic trait and was correlated with all measured traits. Most traits exhibited significant correlations between the sexes. The pattern of correlations and the degree of sexual dimorphism among traits lead us to suggest that intrasexual selection for an exaggerated floral display in males has indirectly led to sexual dimorphism in a host of other traits.     

Reproductive skew and female trait elaboration in a cooperatively breeding rail

Intrasexual competition for reproduction is thought to be an important factor in the evolution of ornaments and weapons in males. However, the evolution of morphologically similar traits in females is often explained through other mechanisms, and the role of intrasexual competition in female trait elaboration has received little attention. Here, we explore the factors associated with female trait elaboration in the cooperatively breeding Pukeko (the New Zealand race of the Purple Swamphen Porphyrio porphyrio melanotus) by comparing sexual dimorphism in an ornament across two populations. Importantly, the two populations considered differ in several social factors that could affect the degree of female–female competition, and could thereby produce differential selection on elaborate female traits. Recent studies have suggested that high reproductive skew (i.e. monopolization of reproduction by dominant individuals) could influence the intensity of intrasexual competition and select for female elaboration. However, we found that sexual dimorphism was diminished and Pukeko females had more elaborate ornaments under conditions of low reproductive skew. We discuss alternative factors that could influence the degree of female–female competition, and show that reproductive skew may not always provide an accurate estimate of the scope for intrasexual competition.     

Variations in life history traits and flight capacity among populations of the light brown apple moth Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae)

Abstract The empirical study of interpopulation variation in life history and other fitness traits has been an important approach to understanding the ecology and evolution of organisms and gaining insight into possible sources of variation. We report a quantitative analysis for variations of five life history traits (larval developmental time, adult body weight, adult lifespan, age at first reproduction, total fecundity) and flight capacity among populations of Epiphyas postvittana originating from four localities in Australia and one in New Zealand. These populations were compared at two temperatures (15° and 25°C) after being maintained under uniform laboratory conditions for 1.5 generations, so that the relative role of genetic divergence and phenotypic plasticity in determining interpopulation variation could be disentangled. Genetic differentiation between populations was shown in all measured traits, with the greatest divergence occurring in developmental time, fecundity and adult body size. However, these traits were highly sensitive to changes in environmental temperatures; and furthermore, significant interactions between population and temperature occurred in all traits except for flight capacity of female moths. Thus, phenotypic plasticity may be another cause of interpopulation variation. The interpopulation variation for some measured traits was apparently related to climatic differences found where the populations originated. Individuals of the populations from the warmer climates tended to develop more slowly at immature stages, producing smaller and less fecund moths but with stronger flight capacity, in comparison to those from the cooler regions. It seems, therefore, that natural populations of E. postvittana have evolved different strategies to cope with local environmental conditions.     

Sexual competition and N supply interactively affect the dimorphism and competiveness of opposite sexes in Populus cathayana

Several important dioecious species show sexual spatial segregation (SSS) along environmental gradients that have significant ecological effect on terrestrial ecosystem. However, little attention has been paid to understanding of how males and females respond to environmental gradients and sexual competition. We compared eco‐physiological parameters of males and females of Populus cathayana under different sexual competition patterns and nitrogen (N) supply levels. We found that males and females interacting with the same or opposite sex showed significant differences in biomass partition, photosynthetic capacity, carbon (C) and N metabolism, and leaf ultrastructure, and that the sexual differences to competition were importantly driven by N supply. The intersexual competition was enhanced under high N, while the intrasexual competition among females was amplified under low N. Under high N, the intersexual competition stimulated the growth of the females and negatively affected the males. In contrast, under low N, the males exposed to intrasexual competition had the highest tolerance, whereas females exposed to intrasexual competition showed the lowest adaptation among all competition patterns. Sexual competition patterns and N supply levels significantly affected the sexual dimorphism and competitiveness, which may play an important role in spatial segregation of P. cathayana populations.     

Physiological condition and wing pigmentation expression in a damselfly with seasonal polyphenism

Secondary sexual traits can be indicators of individual condition that may present seasonal polyphenism as a result of the differential costs of expression along the season. Wing spots in male damselflies of the Calopterygidae family are secondary sexual traits associated with intrasexual competition and mate choice. Hetaerina titia Drury is a calopterygid damselfly where males show red and black wing spots, contrasting with other species of the genus whose males only express a red wing spot. In the present study, we evaluate the seasonal variation of the expression of male's red and black wing spots and their allometric patterns. Additionally, we measure male condition in the form of proteins, lipids, soluble carbohydrates and glycogen in early and late seasons. Black wing spots present higher variation than red wing spots and males of the late season are more pigmented. Allometry is positive for wing red spot in the early season and for black spot in the late season. Males of the late season present a higher concentration of proteins, soluble carbohydrates and glycogen, although there is no variation in the lipid content. The results of the present study suggest that, in H. titia males, black pigmentation replaces the function of the red pigmentation to signal condition. Both traits, however, may be heavily affected by environmental situations (e.g. food availability).     

Variation of anal fin egg‐spots along an environmental gradient in a haplochromine cichlid fish

Male secondary sexual traits are targets of inter‐ and/or intrasexual selection, but can vary due to a correlation with life‐history traits or as by‐product of adaptation to distinct environments. Trade‐offs contributing to this variation may comprise conspicuousness toward conspecifics versus inconspicuousness toward predators, or between allocating resources into coloration versus the immune system. Here, we examine variation in expression of a carotenoid‐based visual signal, anal‐fin egg‐spots, along a replicate environmental gradient in the haplochromine cichlid fish Astatotilapia burtoni. We quantified egg‐spot number, area, and coloration; applied visual models to estimate the trait's conspicuousness when perceived against the surrounding tissue under natural conditions; and used the lymphocyte ratio as a measure for immune activity. We find that (1) males possess larger and more conspicuous egg‐spots than females, which is likely explained by their function in sexual selection; (2) riverine fish generally feature fewer but larger and/or more intensely colored egg‐spots, which is probably to maintain signal efficiency in intraspecific interactions in long wavelength shifted riverine light conditions; and (3) egg‐spot number and relative area correlate with immune defense, suggesting a trade‐off in the allocation of carotenoids. Taken together, haplochromine egg‐spots feature the potential to adapt to the respective underwater light environment, and are traded off with investment into the immune system.     

Host shifts and the beginning of signal divergence

Divergence between populations adapting to different environments may be facilitated when the populations differ in their sexual traits. We tested whether colonizing a novel environment may, through phenotypic plasticity, change sexual traits in a way that could alter the dynamics of sexual selection. This hypothesis has two components: changes in mean phenotypes across environments, and changes in the genetic background of the phenotypes that are produced -- or genotype x environment interaction (G x E). We simulated colonization of a novel environment and tested its effect on the mating signals of a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae), a clade that has diverged in a process involving host plant shifts and signal diversification. We found substantial genetic variation and G x E in most signal traits measured, with little or no change in mean signal phenotypes. We suggest that the expression of extant genetic variation across old and novel environments can initiate signal divergence.     

Wing pigmentation in Calopteryx damselflies: a role in thermoregulation?

Body melanization may show adaptive variation related to thermoregulation ability, and it is to be expected that the degree of melanization will change among populations or closely related species across environmental gradients of solar radiation and/or environmental temperature. Some melanized secondary sexual traits may also play a role in sexual selection, leading to interpopulation variation, which would not be predicted by thermoregulation pressures alone. We studied the relationships between the interpopulation variation in wing pigmentation level (i.e. melanized secondary sexual trait) of two closely related species of Calopteryx damselfly, and both solar radiation and maximum environmental temperature estimates. Wing pigmentation differs between these species, is gender specific and is used in species' discrimination. Only Calopteryx virgo meridionalis males showed a significant negative partial correlation between wing pigmentation degree and temperature. However, C. virgo meridionalis females showed a positive significant partial correlation between wing pigmentation degree and solar radiation. Wing pigmentation in Calopteryx xanthostoma males was not related to solar radiation or temperature. Thus, thermoregulation pressures poorly explained the observed variations in wing pigmentation between populations, although they might have an adaptive significance at the species' level. As wing pigmentation showed important latitudinal variation, several other selection pressures which might act on melanized traits are briefly discussed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 36–44.     

Sexual selection and population divergence I: The influence of socially flexible cuticular hydrocarbon expression in male field crickets (Teleogryllus oceanicus)

Debates about how coevolution of sexual traits and preferences might promote evolutionary diversification have permeated speciation research for over a century. Recent work demonstrates that the expression of such traits can be sensitive to variation in the social environment. Here, we examined social flexibility in a sexually selected male trait—cuticular hydrocarbon (CHC) profiles—in the field cricket Teleogryllus oceanicus and tested whether population genetic divergence predicts the extent or direction of social flexibility in allopatric populations. We manipulated male crickets’ social environments during rearing and then characterized CHC profiles. CHC signatures varied considerably across populations and also in response to the social environment, but our prediction that increased social flexibility would be selected in more recently founded populations exposed to fluctuating demographic environments was unsupported. Furthermore, models examining the influence of drift and selection failed to support a role of sexual selection in driving population divergence in CHC profiles. Variation in social environments might alter the dynamics of sexual selection, but our results align with theoretical predictions that the role social flexibility plays in modulating evolutionary divergence depends critically on whether responses to variation in the social environment are homogeneous across populations, or whether gene by social environment interactions occur.     

Old males reduce melanin‐pigmented traits and increase reproductive outcome under worse environmental conditions in common kestrels

Secondary sexual traits displayed by males and females may have evolved as a signal of individual quality. However, both individual quality and investment on producing or maintaining enhanced sexual traits change as individuals age. At the same time, the costs associated to produce sexual traits might be attenuated or increased if environmental conditions are benign or worse respectively. Accordingly, environmental conditions are expected to shape the association between the expression of sexual traits and their reproductive outcome as individuals age. Nonetheless, little is known about the environmental influence on the co‐variation between sexual traits and reproductive outcome throughout the life of individuals. We studied the age‐dependency of the number and size of back spots, a melanin‐based and sexual trait in adults of common kestrels (Falco tinnunculus). We analysed the age‐dependence of reproductive traits and the environmental influence, defined as vole abundance, using a 10‐year individual‐based dataset. We broke down age‐related changes of reproductive traits into within‐ and between‐individual variation to assess their contribution to population‐level patterns. Our results showed a within‐individual decrease in the number, but not the size, of back spots in males. The size of back spots was positively correlated with food availability in males. Reproductive performance of males increased as they aged, in agreement with the life‐history theory but depending of vole abundance. Remarkably, we found that having fewer back spots was positively associated with clutch size only for old individuals under low‐food conditions. We suggest that environmental variation may shape the association between the expression of a sexual signal and reproductive outcome. We speculate that the reliability of sexual traits is higher when environmental conditions are poor only for old individuals. Within an evolutionary context, we suggest that the expression of sexual traits might be constrained by environmental conditions at later stages of life.     

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.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

Warm developmental temperatures induce non-adaptive plasticity in the intrasexually selected colouration of a dragonfly

1. When the breeding environment fluctuates across generations, reproductive traits may evolve plasticity that optimises the balance between survival and mating success for the prevailing environment. 2. For sexually selected colouration, this balance can depend on environmental temperatures. Accordingly, breeding colouration often co-varies with temperature through space and time. However, whether such traits exhibit plasticity in response to environmental temperatures is poorly understood. 3. In the present study, a dragonfly (Pachydiplax longipennis) was reared under ambient or experimentally warmed conditions and tested for plasticity in its intrasexually selected wing colouration. Although wing colouration improves male territorial success, these advantages are smaller under warmer conditions than cooler conditions. It was therefore predicted that males reared under the ambient thermal conditions of the study site (Cleveland, Ohio) would develop more wing colouration than those reared under experimentally warmed conditions. 4. Contrary to this prediction, males reared in warm larval temperatures produced more wing colouration. Thus, although the secondary sexual colouration of this species displays some thermal plasticity, it does not appear to be adaptive relative to the known thermal variation of intrasexual selection in this population. 5. Given that the environment often determines the strength and direction of sexual selection, future studies should consider the potential for non-adaptive, and even maladaptive, developmental plasticity in the sexually selected traits of insects.     

Sexual conflict does not drive reproductive isolation in experimental populations of Drosophila pseudoobscura

Sexual conflict has been predicted to drive reproductive isolation by generating arbitrary but rapid coevolutionary changes in reproductive traits among allopatric populations. A testable prediction of this proposal is that allopatric populations experiencing different levels of sexual conflict should exhibit different levels of reproductive isolation. We tested this prediction using experimentally evolved populations of the promiscuous Drosophila pseudoobscura. We manipulated sexual conflict by enforcing either monogamy, maintaining natural levels of promiscuity, or elevating promiscuity. Within each treatment, we carried out sympatric and allopatric crosses using replicated populations and examined pre-zygotic (number of mating pairs, mating speed and copulation duration) and post-zygotic (hybrid inviability and sterility) indicators of reproductive isolation. After 50 generations of selection, none of the measures conformed to predictions of sexual conflict driving reproductive isolation. Our results cannot be explained by lack of genetic variation or weak selection and suggest that sexual conflict may not be a widespread engine of speciation.     

A role for ecology in the evolution of colour variation and sexual dimorphism in Hawaiian damselflies

Variation in traits that are sexually dimorphic is usually attributed to sexual selection, in part because the influence of ecological differences between sexes can be difficult to identify. Sex‐limited dimorphisms, however, provide an opportunity to test ecological selection disentangled from reproductive differences between the sexes. Here, we test the hypothesis that ecological differences play a role in the evolution of body colour variation within and between sexes in a radiation of endemic Hawaiian damselflies. We analysed 17 Megalagrion damselflies species in a phylogenetic linear regression, including three newly discovered cases of species with female‐limited dimorphism. We find that rapid colour evolution during the radiation has resulted in no phylogenetic signal for most colour and habitat traits. However, a single ecological variable, exposure to solar radiation (as measured by canopy cover) significantly predicts body colour variation within sexes (female‐limited dimorphism), between sexes (sexual dimorphism), and among populations and species. Surprisingly, the degree of sexual dimorphism in body colour is also positively correlated with the degree of habitat differences between sexes. Specifically, redder colouration is associated with more exposure to solar radiation, both within and between species. We discuss potential functions of the pigmentation, including antioxidant properties that would explain the association with light (specifically UV) exposure, and consider alternative mechanisms that may drive these patterns of sexual dimorphism and colour variation.     

Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals

A major challenge for studying the role of sexual selection in divergence and speciation is understanding the relative influence of different sexually selected signals on those processes in both intra‐ and interspecific contexts. Different signals may be more or less susceptible to co‐option for species identification depending on the balance of sexual and ecological selection acting upon them. To examine this, we tested three predictions to explain geographic variation in long‐ versus short‐range sexual signals across a 3,500 + km transect of two related Australian field cricket species (Teleogryllus spp.): (a) selection for species recognition, (b) environmental adaptation and (c) stochastic divergence. We measured male calling song and male and female cuticular hydrocarbons (CHCs) in offspring derived from wild populations, reared under common garden conditions. Song clearly differentiated the species, and no hybrids were observed suggesting that hybridization is rare or absent. Spatial variation in song was not predicted by geography, genetics or climatic factors in either species. In contrast, CHC divergence was strongly associated with an environmental gradient supporting the idea that the climatic environment selects more directly upon these chemical signals. In light of recently advocated models of diversification via ecological selection on secondary sexual traits, the different environmental associations we found for song and CHCs suggest that the impact of ecological selection on population divergence, and how that influences speciation, might be different for acoustic versus chemical signals.     

Contrasting patterns of sexually selected traits in Mediterranean and continental populations of European mouflon

The expression of sexually selected traits in highly dimorphic ungulates may be influenced by environmental quality. Variations in habitat conditions can impose different constraints on the allocation of energy resources to male life‐history traits, and possibly alter the female preferences for specific features. Here, we compared the horn growth patterns in male European mouflon Ovis aries musimon living in different habitats (Mediterranean vs. continental) but sharing a common genetic origin. We hypothesized that the expression of sexually selected traits such as horn development should be promoted in more favorable habitat conditions (i.e., Mediterranean). Using linear mixed models on data retrieved from individuals harvested under the same hunting regime, we found longer horns and greater individual variance in horn segment length in the Mediterranean population than in the continental one. Furthermore, Mediterranean rams showed no evidence of compensatory horn growth, as opposed to the continental rams. Unexpectedly, horn base circumference was greater in the continental habitat than in the Mediterranean one. The overall results suggest different patterns of investment in horns in the two populations, with seemingly stronger pressure and consequences of sexual selection on mouflon rams living in more favorable environments. Although the role of hunters' selectivity cannot be excluded a priori, our data suggest that the differences in the expression of sexually selected traits in our study populations may be influenced by environmental conditions. Because sexual selection can impose substantial fitness costs on individuals, further investigations on the trade‐offs between reproduction and survival would improve our understanding of the dynamics of mouflon populations living in different environmental conditions.