Condition‐dependent expression of pre‐ and postcopulatory sexual traits in guppies

Female choice can impose persistent directional selection on male sexually selected traits, yet such traits often exhibit high levels of phenotypic variation. One explanation for this paradox is that if sexually selected traits are costly, only the fittest males are able to acquire and allocate the resources required for their expression. Furthermore, because male condition is dependent on resource allocation, condition dependence in sexual traits is expected to underlie trade‐offs between reproduction and other life‐history functions. In this study we test these ideas by experimentally manipulating diet quality (carotenoid levels) and quantity in the guppy (Poecilia reticulata), a livebearing freshwater fish that is an important model for understanding relationships between pre‐ and post‐copulatory sexually selected traits. Specifically, we test for condition dependence in the expression of pre‐ and postcopulatory sexual traits (behavior, ornamentation, sperm traits) and determine whether diet manipulation mediates relationships among these traits. Consistent with prior work we found a significant effect of diet quantity on the expression of both pre‐ and postcopulatory male traits; diet‐restricted males performed fewer sexual behaviors and exhibited significant reductions in color ornamentation, sperm quality, sperm number, and sperm length than those fed ad libitum. However, contrary to our expectations, we found no significant effect of carotenoid manipulation on the expression of any of these traits, and no evidence for a trade‐off in resource allocation between pre‐ and postcopulatory episodes of sexual selection. Our results further underscore the sensitivity of behavioral, ornamental, and ejaculate traits to dietary stress, and highlight the important role of condition dependence in maintaining the high variability in male sexual traits.     

Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback

Despite recent progress, we still know relatively little about the genetic architecture that underlies adaptation to divergent environments. Determining whether the genetic architecture of phenotypic adaptation follows any predictable patterns requires data from a wide variety of species. However, in many organisms, genetic studies are hindered by the inability to perform genetic crosses in the laboratory or by long generation times. Admixture mapping is an approach that circumvents these issues by taking advantage of hybridization that occurs between populations or species in the wild. Here, we demonstrate the utility of admixture mapping in a naturally occurring hybrid population of threespine sticklebacks (Gasterosteus aculeatus) from Enos Lake, British Columbia. Until recently, this lake contained two species of sticklebacks adapted to divergent habitats within the lake. This benthic–limnetic species pair diverged in a number of phenotypes, including male nuptial coloration and body shape, which were previously shown to contribute to reproductive isolation between them. However, recent ecological disturbance has contributed to extensive hybridization between the species, and there is now a single, admixed population within Enos Lake. We collected over 500 males from Enos Lake and found that most had intermediate nuptial colour and body shape. By genotyping males with nuptial colour at the two extremes of the phenotypic distribution, we identified seven genomic regions on three chromosomes associated with divergence in male nuptial colour. These genomic regions are also associated with variation in body shape, suggesting that tight linkage and/or pleiotropy facilitated adaptation to divergent environments in benthic–limnetic species pairs.     

Divergent sexual selection via male competition: ecology is key

Sexual selection and ecological differences are important drivers of speciation. Much research has focused on female choice, yet the role of male competition in ecological speciation has been understudied. Here, we test how mating habitats impact sexual selection and speciation through male competition. Using limnetic and benthic species of threespine stickleback fish, we find that different mating habitats select differently on male traits through male competition. In mixed habitat with both vegetated and open areas, selection favours two trait combinations of male body size and nuptial colour: large with little colour and small with lots of colour. This matches what we see in reproductively isolated stickleback species, suggesting male competition could promote trait divergence and reproductive isolation. In contrast, when only open habitat exists, selection favours one trait combination, large with lots of colour, which would hinder trait divergence and reproductive isolation. Other behavioural mechanisms in male competition that might promote divergence, such as avoiding aggression with heterospecifics, are insufficient to maintain separate species. This work highlights the importance of mating habitats in male competition for both sexual selection and speciation.     

Environmental change mediates mate choice for an extended phenotype,but not for mate quality

Sexual cues, including extended phenotypes, are expected to be reliable indicators of male genetic quality and/or provide information on parental quality. However, the reliability of these cues may be dependent on stability of the environment, with heterogeneity affecting how selection acts on such traits. Here, we test how environmental change mediates mate choice for multiple sexual traits, including an extended phenotype–‐the structure of male‐built nests – in stickleback fish. First, we manipulated the dissolved oxygen (DO) content of water to create high or low DO environments in which male fish built nests. Then we recorded the mate choice of females encountering these males (and their nests), under either the same or reversed DO conditions. Males in high DO environments built more compact nests than those in low DO conditions and males adjusted their nest structure in response to changing conditions. Female mate choice for extended phenotype (male nests) was environmentally dependent (females chose more compact nests in high DO conditions), while female choice for male phenotype was not (females chose large, vigorous males regardless of DO level). Examining mate choice in this dynamic context suggests that females evaluate the reliability of multiple sexual cues, taking into account environmental heterogeneity.     

Heritability and heterochrony of polychromatism in a Lake Victoria Cichlid fish: Stepping stones for speciation?

In many haplochromine cichlid fish, male nuptial coloration is subject to female mate choice and plays a central role in the evolution of reproductive isolation between incipient species. Intraspecific variation in male coloration may serve as a target for diversifying sexual selection and provide a starting point for species divergence. Here, we investigated a polychromatism in Neochromis omnicaeruleus, a haplochromine from Lake Victoria, East-Africa. In this species, male coloration ranges from skyblue to yellow-red and females are grey-blue to yellow. We found that both genetic and environmental factors influence the expression of these colours during individual development. In a natural population, we found that male colour was associated with size and sexual maturity: yellow males were smaller than blue males and tended to be sexually immature. In females, size and maturity did not differ between colour types. Laboratory crosses revealed that there is a heritable component to the observed colour variation: yellow parents produced more yellow offspring than blue parents. Together with repeated aquarium observations of yellow individuals that gradually become blue, these data suggest that yellow males change to blue as they approach sexual maturity, and that the occurrence and timing of this transition is influenced by both environmental and genetic effects. The significance of this mechanism of colour expression as a possible target for divergent selection remains to be evaluated.     

Regulation of integumentary colour and plasma carotenoids in American Kestrels consistent with sexual selection theory

1. Sexually selected traits are expected to vary seasonally, with the maximal expression of the character being evident during mate choice; however, the mechanisms controlling or regulating such traits are generally poorly known.
2. Carotenoid pigments responsible for bright red or yellow coloration in the feathers, skin or other integumentary structures of birds are generally believed to vary seasonally because of diet.
3. Variation in carotenoid-dependent skin colour between winter and spring (mating season) was investigated, as was variation in plasma carotenoids across the breeding season in captive American Kestrels, Falco sparverius , fed a uniform diet.
4. Kestrels were more brightly coloured in the mating period than in winter, and plasma carotenoid concentrations declined from the time of mating to the rearing of young.
5. Although carotenoid levels were highly sexually dimorphic during mating and laying, males and both breeding and non-breeding females all had similar levels by the incubation period, and the pattern of variation over time suggests rheostatic regulation.
6. These results suggest kestrels may have the ability to regulate (rather than merely control) their colour physiologically, the variation in colour and carotenoids is consistent with that expected of a sexually selected trait, and the loss of colour after breeding may suggest a trade-off between the show and health functions of carotenoids.     

Hypoxia and life‐history traits in a eurytopic African cichlid

This study quantified variation in key life‐history traits of the widespread African mouth‐brooding cichlid Pseudocrenilabrus multicolor victoriae. Egg size, number, batch reproductive effort, size at maturity and brooding efficiency were compared among field populations across a wide range of dissolved oxygen (DO) concentrations from extreme hypoxia to normoxia. In the laboratory, a similar suite of characters was quantified in F1 of low‐ and high‐DO origin reared under low or high DO. In general, females from low‐DO habitats and females reared under low DO were characterized by a smaller size at maturity and no difference in batch reproductive effort when compared with females from high‐DO habitats or females reared under normoxia. A trade‐off between egg size and number was evident in the field and in the laboratory‐rearing experiment, but the direction of the trade‐off differed. Egg size was negatively correlated with egg number across field populations; females collected from low‐DO sites generally had more, smaller eggs relative to females from high‐DO sites. In the laboratory‐rearing experiment, F1 females of high‐DO origin produced larger, fewer eggs than F1 females of low‐DO origin, lending support to the field results and suggesting a heritable component to these traits. There was also an element of developmental plasticity, F1 females raised under low DO produced larger, fewer eggs compared with F1 females raised under high DO (regardless of population) suggesting that DO may interact with other variables to determine egg size in the field.     

Countergradient variation in carotenoid use between sympatric morphs of sockeye salmon (Oncorhynchus nerka) exposes nonanadromous hybrids in the wild by their mismatched spawning colour

Understanding the mechanisms that decrease gene flow between diverging populations is critical to understanding speciation. Anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific sockeye salmon Oncorhynchus nerka spawn sympatrically and interbreed, yet allele frequency differences at neutral loci indicate restricted gene flow. Disruptive natural selection associated with strong selective differences between anadromous and nonanadromous life histories is thought to maintain the genetic differentiation of the morphs. Recently, a putative third morph of O. nerka exhibiting green rather than red breeding colour has been found on the spawning grounds sympatric with sockeye and kokanee. We investigated the ancestry of these green fish in a 2‐year controlled breeding study by using previously documented heritable, countergradient variation in red breeding colour to distinguish pure and hybrid morphs. Stabilizing sexual selection for similar red breeding colour in sockeye and kokanee has led to adaptive differences in the efficiency of carotenoid uptake between the morphs given differences in carotenoid availability between marine and lacustrine habitats. On the same diet, offspring parented by the green fish were intermediate in colour and in the concentration of dietary carotenoid pigments in their flesh and skin to those parented by either sockeye or kokanee; they were most similar to those parented by known kokanee × sockeye hybrids. This countergradient variation in carotenoid use results in a genotype‐environment mismatch in nonanadromous hybrids that exposes them by their breeding colour on the spawning grounds. Given that red colour is important in mate choice, sexual selection will almost certainly reduce reproductive opportunities for these hybrids and promote sympatric divergence of these incipient species. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84 , 287–305.     

Sensory drive in cichlid speciation

The role of selection in speciation is a central yet poorly understood problem in evolutionary biology. The rapid radiations of extremely colorful cichlid fish in African lakes have fueled the hypothesis that sexual selection can drive species divergence without geographical isolation. Here we present experimental evidence for a mechanism by which sexual selection becomes divergent: in two sibling species from Lake Victoria, female mating preferences for red and blue male nuptial coloration coincide with their context-independent sensitivities to red and blue light, which in turn correspond to a difference in ambient light in the natural habitat of the species. These results suggest that natural selection on visual performance, favoring different visual properties in different spectral environments, may lead to divergent sexual selection on male nuptial coloration. This interplay of ecological and sexual selection along a light gradient may provide a mechanism of rapid speciation through divergent sensory drive.     

Recent speciation and secondary contact in endemic ants

Gene flow is the main force opposing divergent selection, and its effects are greater in populations in close proximity. Thus, complete reproductive isolation between parapatric populations is not expected, particularly in the absence of ecological adaptation and sharp environmental differences. Here, we explore the biogeographical patterns of an endemic ant species, Cataglyphis floricola, for which two colour morphs (black and bicolour) coexist in parapatry throughout continuous sandy habitat in southern Spain. Discriminant analyses of six biometric measurements of male genitalia and 27 cuticular hydrocarbons reveal high differentiation between morphs. Furthermore, the low number of shared alleles derived from nuclear markers (microsatellites) between the morphs at their contact zone suggests the absence of recent gene flow. Mitochondrial DNA (COI) phylogenetic analysis and median‐joining networks show that the black morph is basal to the bicolour morph, with unique haplotypes recovered for each morph. Mismatch distribution analysis and Bayesian skyline plots suggest that they are undergoing different demographic changes, with the bicolour and black morphs at demographic equilibrium and expansion, respectively. Thus, our results show complete reproductive isolation between the two colour morphs as evidenced from genetic, chemical and morphological data. We suggest that these divergence events could be explained by historical vicariance during the Pleistocene, in which reproductive traits experienced strong divergent selection between the morphs initiating or culminating speciation.     

Diet‐dependent female evolution influences male lifespan in a nuptial feeding insect

Theory predicts that lifespan will depend on the dietary intake of an individual, the allocation of resources towards reproduction and the costs imposed by the opposite sex. Although females typically bear the majority of the cost of offspring production, nuptial feeding invertebrates provide an ideal opportunity to examine the extent to which reproductive interactions through gift provisioning impose a cost on males. Here we use experimental evolution in an Australian ground cricket to assess how diet influences male lifespan and how the costs of mating evolve for males. Our findings show that males had significantly shorter lifespans in populations that adapted to a low‐quality diet and that this divergence is driven by evolutionary change in how females interact with males over reproduction. This suggests that the extent of sexual conflict over nuptial feeding may be under‐realized by focusing solely on the consequences of reproductive interactions from the female’s perspective.     

Is diversification in male reproductive traits driven by evolutionary trade-offs between weapons and nuptial gifts?

Many male animals have evolved exaggerated traits that they use in combat with rival males to gain access to females and secure their reproductive success. But some male animals invest in nuptial gifts that gains them access to females. Both these reproductive strategies are costly in that resources are needed to produce the weapon or nuptial gift. In closely related species where both weapons and nuptial gifts are present, little is known about the potential evolutionary trade-off faced by males that have these traits. In this study, we use dobsonflies (order Megaloptera, family Corydalidae, subfamily Corydalinae) to examine the presence and absence of enlarged male weapons versus nuptial gifts within and among species. Many dobsonfly species are sexually dimorphic, and males possess extremely enlarged mandibles that they use in battles, whereas in other species, males produce large nuptial gifts that increase female fecundity. In our study, we show that male accessory gland size strongly correlates with nuptial gift size and that when male weapons are large, nuptial gifts are small and vice versa. We mapped weapons and nuptial gifts onto a phylogeny we constructed of 57 species of dobsonflies. Our among-species comparison shows that large nuptial gift production evolved in many species of dobsonfly but is absent from those with exaggerated weapons. This pattern supports the potential explanation that the trade-off in resource allocation between weapons and nuptial gifts is important in driving the diversity of male mating strategies seen in the dobsonflies, whereas reduced male–male competition in the species producing large spermatophores could be an alternative explanation on their loss of male weapons. Our results shed new light on the evolutionary interplay of multiple sexually selected traits in animals.     

Genetic correlations and sex‐specific adaptation in changing environments

Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex‐specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long‐run patterns of sex‐specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.     

Genetic variance and phenotypic plasticity in a component of female mate choice in an ultrasonic moth

Abstract.— Female response to male advertisement signals in lesser waxmoths showed substantial genetic variation, phenotypic plasticity across rearing environments, and genotype-by-environment interactions resulting in crossing reaction norms. These results represent two previously underemphasized means by which genetic variation may be maintained in sexually selected traits: genetic variation in female response to male traits, and variation in the selection acting on both males and females. Genotype-by-environment interactions and reaction norms that cross indicate that divergent selection may act on male and female sexual traits if the level of environmental change is high. The processes that contribute to the maintenance of genetic variation may thus also contribute to population differentiation.     

Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fish Brachyrhaphis rhabdophora (Teleostei: Poeciliidae)

Predation can drive morphological divergence in prey populations, although examples of divergent selection are typically limited to nonreproductive individuals. In livebearing females, shape often changes drastically during pregnancy, reducing speed and mobility and enhancing susceptibility to predation. In the present study, we document morphological divergence among populations of nonreproductive female livebearing fish (Brachyrhaphis rhabdophora) in predator and nonpredator environments. We then test the hypothesis that shape differences among nonreproductive females are maintained among reproductive females between predator and nonpredator environments. Nonreproductive females in predator environments had larger caudal regions and more fusiform bodies than females in nonpredator environments; traits that are associated with burst speed in fish. Shape differences were maintained in reproductive females, although the magnitude of this difference declined relative to nonreproductive females, suggesting morphological convergence during pregnancy. Phenotypic change vector analysis revealed that females in predator environments became more similar to females in nonpredator environments in the transition from nonreproductive to reproductive. Furthermore, the level of reproductive allocation affected shape similarly between predator environments. These results suggest a life‐history constraint on morphology, in which predator‐driven morphological divergence among nonreproductive B. rhabdophora is not maintained at the same level during pregnancy. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 386–392.     

Interaction of rearing environment and reproductive tactic on gene expression profiles in Atlantic salmon

Organisms that share the same genotype can develop into divergent phenotypes, depending on environmental conditions. In Atlantic salmon, young males of the same age can be found either as sneakers or immature males that are future anadromous fish. Just as the organism-level phenotype varies between divergent male developmental trajectories, brain gene expression is expected to vary as well. We hypothesized that rearing environment can also have an important effect on gene expression in the brain and possibly interact with the reproductive tactic adopted. We tested this hypothesis by comparing brain gene expression profiles of the two male tactics in fish from the same population that were reared in either a natural stream or under laboratory conditions. We found that expression of certain genes was affected by rearing environment only, while others varied between male reproductive tactics independent of rearing environment. Finally, more than half of all genes that showed variable expression varied between the two male tactics only in one environment. Thus, in these fish, very different molecular pathways can give rise to similar macro-phenotypes depending on rearing environment. This result gives important insights into the molecular underpinnings of developmental plasticity in relationship to the environment.     

Innate and Learned Colour Preference in the Zebrafish, Danio rerio

Receiver biases towards specific sensory signals have been demonstrated in insects, birds and fish, both in the context of foraging and mate choice. In some cases, signals important in sexual selection appear to have evolved by exploiting a pre-existing bias in the sensory system. For instance, female preferences for male nuptial colouration may have arisen from selection on foraging practices. Using the zebrafish ( Danio rerio ), a species in which red is not a factor in mate choice, we tested for a foraging bias towards the colour red. We further investigated the plasticity of foraging biases by raising groups of fish on diets consisting solely of red, blue, green or white food. When we subsequently tested their colour preferences in a foraging context, each group responded most strongly to red, irrespective of the colour of food with which they had been conditioned. We also detected a significant effect of conditioning on colour preferences; fish responded more strongly to the colour that matched diet colour than to other colours. The observed receiver bias towards red may have evolved as an adaptive preference for carotenoid compounds in their diet. While the bias to red appears to be innate, our results indicate that learning is also important in shaping foraging biases.     

Condition dependence of sexually dimorphic colouration and longevity in the ambush bug Phymata americana

Sexually selected traits that are costly are predicted to be more condition dependent than nonsexually selected traits. Assuming resource limitation, increased allocation to a sexually selected trait may also come at a cost to other fitness components. To test these predictions, we varied adult food ration to manipulate condition in the colour dimorphic bug, Phymata americana. We compared the degree of condition dependence in a sexually selected trait expressed in males to a nonsexually selected trait expressed in males and females. We also evaluated the effects of condition on longevity of both sexes. We found that the expression of these colour pattern traits was strongly influenced by both diet and age. As expected, the strength of condition dependence was much more pronounced in the sexually selected, male-limited trait but the nonsexual trait also exhibited significant condition dependence in both sexes. The sexually selected male trait also exhibited a higher coefficient of phenotypic variation than the nonsexually selected trait in males and females. Diet had contrasting effects on male and female longevity; increased food availability had positive effects on female lifespan but these effects were not detected in males, suggesting that males allocated limited resources preferentially to sexually selected traits. These results are consistent with the expectation that optimal allocation to various fitness components differs between the sexes.     

Toxic hydrogen sulphide and dark caves: pronounced male life-history divergence among locally adapted Poecilia mexicana (Poeciliidae)

Chronic environmental stress is known to induce evolutionary change. Here, we assessed male life‐history trait divergence in the neotropical fish Poecilia mexicana from a system that has been described to undergo incipient ecological speciation in adjacent, but reproductively isolated toxic/nontoxic and surface/cave habitats. Examining both field‐caught and common garden–reared specimens, we investigated the extent of differentiation and plasticity of life‐history strategies employed by male P. mexicana. We found strong site‐specific life‐history divergence in traits such as fat content, standard length and gonadosomatic index. The majority of site‐specific life‐history differences were also expressed under common garden–rearing conditions. We propose that apparent conservatism of male life histories is the result of other (genetically based) changes in physiology and behaviour between populations. Together with the results from previous studies, this is strong evidence for local adaptation as a result of ecologically based divergent selection.     

Dietary carotenoid levels affect carotenoid and retinoid allocation in female Chinook salmon Oncorhynchus tshawytscha

This study examined the effect of dietary carotenoid availability on carotenoid and retinoid concentrations in the flesh, plasma, skin and eggs of female Chinook salmon Oncorhynchus tshawytscha. Carotenoid concentrations in all tissues were closely related to dietary availability. Early in the breeding season, carotenoids were stored primarily in the muscle, with a flesh carotenoid concentration of 9·9 µg g^?1 in fish fed a high carotenoid diet compared with 1·9 µg g^?1 in fish fed a low carotenoid diet. During the breeding season, carotenoid reserves were mobilized predominantly to the eggs and also to the skin. By the end of the breeding season, carotenoid concentrations in the eggs were 17·9 µg g^?1 in fish fed a high carotenoid diet and 3·9 µg g^?1 in fish fed a low carotenoid diet. Conversely, egg retinoid concentrations were only c. 20% lower in fish fed a low v. high carotenoid diet, which suggests that retinoid concentrations were not limited by the availability of carotenoid precursors. Egg carotenoid concentrations were not correlated with either skin carotenoid concentration or colouration, which suggests that female carotenoid displays are not a reliable signal that males can use to evaluate egg carotenoid resources.