Multiple capacitors for natural genetic variation in Drosophila melanogaster

Cryptic genetic variation (CGV) or a standing genetic variation that is not ordinarily expressed as a phenotype is released when the robustness of organisms is impaired under environmental or genetic perturbations. Evolutionary capacitors modulate the amount of genetic variation exposed to natural selection and hidden cryptically; they have a fundamental effect on the evolvability of traits on evolutionary timescales. In this study, I have demonstrated the effects of multiple genomic regions of Drosophila melanogaster on CGV in wing shape. I examined the effects of 61 genomic deficiencies on quantitative and qualitative natural genetic variation in the wing shape of D. melanogaster. I have identified 10 genomic deficiencies that do not encompass a known candidate evolutionary capacitor, Hsp90, exposing natural CGV differently depending on the location of the deficiencies in the genome. Furthermore, five genomic deficiencies uncovered qualitative CGV in wing morphology. These findings suggest that CGV in wing shape of wild‐type D. melanogaster is regulated by multiple capacitors with divergent functions. Future analysis of genes encompassed by these genomic regions would help elucidate novel capacitor genes and better understand the general features of capacitors regarding natural genetic variation.     

Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids

Sexual selection contributes strongly to the evolution of sexual dimorphism among animal taxa. However, recent comparative analyses have shown that evolution of sexual dimorphism can be influenced by extrinsic factors like mating system and environment, and also that different types of sexual dimorphism may present distinct evolutionary pathways. Investigating the co-variation among different types of sexual dimorphism and their association with environmental factors can therefore provide important information about the mechanisms generating variation in sexual dimorphism among contemporary species. Using phylogenetic comparative analyses comparing 49 species of Tanganyikan cichlid fishes, we first investigated the pairwise relationship between three types of sexual dimorphism [size dimorphism (SSD), colour dimorphism (COD) and shape dimorphism (SHD)] and how they were related to the strength of pre- and post-copulatory sexual selection. We then investigated the influence of ecological features on sexual dimorphism. Our results showed that although SSD was associated with the overall strength of sexual selection it was not related to other types of sexual dimorphism. Also, SSD co-varied with female size and spawning habitat, suggesting a role for female adaptations to spawn in small crevices and shells influencing SSD in this group. Further, COD and SHD were positively associated and both show positive relationships with the strength of sexual selection. Finally, the level of COD and SHD was related to habitat complexity. Our results thus highlight distinct evolutionary pathways for different types of sexual dimorphism and further that ecological factors have influenced the evolution of sexual dimorphism in Tanganyikan cichlid fishes.     

Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host''s ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.     

Sex and tissue‐specific evolution of developmental plasticity in Drosophila melanogaster

Developmental plasticity influences the size of adult tissues in insects. Tissues can have unique responses to environmental perturbation during development; however, the prevalence of within species evolution of tissue‐specific developmental plasticity remains unclear. To address this, we studied the effects of temperature and nutrition on wing and femur size in D. melanogaster populations from a temperate and tropical region. Wings were more sensitive to temperature, while wings and femurs were equally responsive to nutrition in both populations and sexes. The temperate population was larger under all conditions, except for femurs of starved females. In line with this, we observed greater femur size plasticity in response to starvation in temperate females, leading to differences in sexual dimorphism between populations such that the slope of the reaction norm of sexual dimorphism in the tropical population was double that of the temperate population. Lastly, we observed a significant trend for steeper slopes of reaction norms in temperate than in tropical females, but not in males. These findings highlight that plasticity divergence between populations can evolve heterogeneously across sexes and tissues and that nutritional plasticity can alter sexual dimorphism in D. melanogaster.     

Sexual size dimorphism in island plants: the niche variation hypothesis and insular size changes

The niche variation hypothesis predicts insular populations exhibit increased sexual size dimorphism (SSD), to minimize intraspecific competition. Although many animal taxa conform to this prediction, insular patterns of SSD have yet to be investigated in plants. Here, we tested for differences in SSD of dioecious plants that colonised four island groups (Kermadec, Three Kings, Chatham and Auckland Islands) from New Zealand. Using herbarium collections, we quantified leaf and stem sizes of 263 individuals from 28 dioecious taxa. We developed a novel analytical technique to explore changes in the direction of SSD on islands. Lastly, we tested for evolutionary size changes of male and female plants on islands. The degree of SSD did not vary predictably between insular and mainland taxa, contrary to predictions of the niche variation hypothesis. Furthermore, the direction of SSD was not predictable on islands, while it was consistently female biased on the mainland. Our results suggest that selection favours increased size of both sexes on islands and that SSD is unpredictable for insular plants.     

Sexual dimorphism in cranial shape and size in geomyoid rodents: multivariate and evolutionary perspectives

Geomyoid rodents provide a great study system for the analysis of sexual dimorphism. They are polygynic and many inhabit harsh arid environments thought to promote sexual dimorphism. In fact, there has been extensive work published on the sexual size dimorphism of individual populations and species within this rodent clade. However, little work has been undertaken to assess the evolutionary patterns and processes associated with this sexual dimorphism. We use multivariate analyses of cranial measurements in a phylogenetic framework to determine the distribution of size and shape dimorphism among geomyoids and test for Rensch’s rule. Our results suggest that sexual dimorphism is more common in geomyids than heteromyids, but it is not in fact universal. There is evidence for variation in sexual dimorphism across populations. Additionally, in many taxa, geographic variation appears to overwhelm existing sexual dimorphism. We find support for the repeated independent evolution of shape and size dimorphism across geomyoid taxa, but we do not find support for an association between size and shape dimorphism. There is no evidence for Rensch’s rule in geomyoids, whether at the superfamily or family level. Together, our findings suggest that there is no single explanation for the evolution of sexual dimorphism in geomyoids and that, instead, it is the product of numerous evolutionary events. Future studies incorporating phylogenetic relationships will be necessary to paint a more complete picture of the evolution of sexual dimorphism in geomyoids.     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Sexual selection on male size drives the evolution of male‐biased sexual size dimorphism via the prolongation of male development

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro‐ and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra‐ and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female‐biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.     

A Genetic Test of Sexual Size Dimorphism in Pre-Emergent Chinook Salmon

Sex differences in early development may play an important role in the expression of sexual size dimorphism at the adult stage. To test whether sexual size dimorphism is present in pre-emergent chinook salmon (Oncorhynchus tshawytscha), alevins were reared at two temperatures (10 °C and 15 °C) and sexed using the OtY1 marker on the Y-chromosome. Linear mixed models were used to test for sex differences in alevin size within families while controlling for the random effects of sire and dam nested within sire. Males and females did not differ in weight at 10 °C but males were heavier than females at 15 °C. Sex accounted for 2% of the within-family variance in weight. In addition, at 15°C, the relationship between weight and sex was greater in families with larger eggs. Whereas male-biased sexual size dimorphism was present at the juvenile stage, female-biased sexual size dimorphism was present at sexual maturity. Males were also younger than females at sexual maturity. A head start on growth by males may underlie their earlier maturation at a smaller size, thus leading to female-biased SSD at the adult stage.     

Sexual size dimorphism decreases with temperature in a blowfly,Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae)

1. There is wide intra‐specific variation in sexual size dimorphism (SSD). Much of this variation is probably as a result of sexual differences in the selective pressure on body size. However, environmental variables could affect males and females differently, causing variation in SSD. 2. We examined the effects of two temperatures (20 and 30 °C) on SSD in six populations of the blowfly, Chrysomya megacephala. 3. We found that body size increased with temperature in all the populations studied, and the sexes differed in phenotypic plasticity of body size in response to rearing temperature. This created substantial temperature‐induced variation in SSD (i.e. sex × temperature interaction). Males were often smaller than females, but the degree of dimorphism was smaller at the higher temperature (30 °C) and larger at the lower temperature (20 °C). This change in SSD was not because of a gender difference in the effect of temperature on development time. Further studies should address whether this variation can be produced by adaptive canalisation of one sex against variation in temperature, or whether it may be a consequence of non‐adaptive developmental differences between the sexes. 4. Although most studies assume that the magnitude of SSD is fixed within a species, the present study demonstrates that rearing temperature can generate considerable intra‐specific variation in the degree of SSD.     

Genetic variability of sexual size dimorphism in a natural population of<Emphasis Type="Italic">Drosophila melanogaster</Emphasis>: An isofemale-line approach

Most animal species exhibit sexual size dimorphism (SSD). SSD is a trait difficult to quantify for genetical purposes since it must be simultaneously measured on two kinds of individuals, and it is generally expressed either as a difference or as a ratio between sexes. Here we ask two related questions: What is the best way to describe SSD, and is it possible to conveniently demonstrate its genetic variability in a natural population? We show that a simple experimental design, the isofemale-line technique (full-sib families), may provide an estimate of genetic variability, using the coefficient of intraclass correlation. We consider two SSD indices, the female-male difference and the female/male ratio. For two size-related traits, wing and thorax length, we found that both SSD indices were normally distributed. Within each family, the variability of SSD was estimated by considering individual values in one sex (the female) with respect to the mean value in the other sex (the male). In a homogeneous sample of 30 lines ofDrosophila melanogaster, both indices provided similar intraclass correlations, on average 0.21, significantly greater than zero but lower than those for the traits themselves: 0.50 and 0.36 for wing and thorax length respectively. Wing and thorax length were strongly positively correlated within each sex. SSD indices of wing and thorax length were also positively correlated, but to a lesser degree than for the traits themselves. For comparative evolutionary studies, the ratio between sexes seems a better index of SSD since it avoids scaling effects among populations or species, permits comparisons between different traits, and has an unambiguous biological significance. In the case ofD. melanogaster grown at 25?C, the average female/male ratios are very similar for the wing (1.16) and the thorax (1.15), and indicate that, on average, these size traits are 15–16% longer in females.     

Independent evolution of the sexes promotes amphibian diversification

Classic ecological theory predicts that the evolution of sexual dimorphism constrains diversification by limiting morphospace available for speciation. Alternatively, sexual selection may lead to the evolution of reproductive isolation and increased diversification. We test contrasting predictions of these hypotheses by examining the relationship between sexual dimorphism and diversification in amphibians. Our analysis shows that the evolution of sexual size dimorphism (SSD) is associated with increased diversification and speciation, contrary to the ecological theory. Further, this result is unlikely to be explained by traditional sexual selection models because variation in amphibian SSD is unlikely to be driven entirely by sexual selection. We suggest that relaxing a central assumption of classic ecological models—that the sexes share a common adaptive landscape—leads to the alternative hypothesis that independent evolution of the sexes may promote diversification. Once the constraints of sexual conflict are relaxed, the sexes can explore morphospace that would otherwise be inaccessible. Consistent with this novel hypothesis, the evolution of SSD in amphibians is associated with reduced current extinction threat status, and an historical reduction in extinction rate. Our work reconciles conflicting predictions from ecological and evolutionary theory and illustrates that the ability of the sexes to evolve independently is associated with a spectacular vertebrate radiation.     

A Test of Rensch’s Rule in Greater Horseshoe Bat (Rhinolophus ferrumequinum) with Female-Biased Sexual Size Dimorphism

Sexual size dimorphism (SSD) is widespread within the animal kingdom. Rensch’s rule describes a relationship between SSD and body size: SSD increases with body size when males are the larger sex, and decreases with body size when females are the larger sex. Rensch’s rule is well supported for taxa that exhibit male-biased SSD but patterns of allometry among taxa with female-biased size dimorphism are mixed, there is evidence both for and against the rule. Furthermore, most studies have investigated Rensch’s rule across a variety of taxa; but among-population studies supporting Rensch’s rule are lacking, especially in taxa that display only slight SSD. Here, we tested whether patterns of intraspecific variation in SSD in greater horseshoe bats conform to Rensch’s rule, and evaluated the contribution of latitude to Rensch’s rule. Our results showed SSD was consistently female-biased in greater horseshoe bats, although female body size was only slightly larger than male body size. The slope of major axis regression of log₁₀ (male) on log₁₀ (female) was significantly different from 1. Forearm length for both sexes of greater horseshoe bats was significantly negatively correlated with latitude, and males displayed a slightly but nonsignificant steeper latitudinal cline in body size than females. We suggest that variation in patterns of SSD among greater horseshoe bat populations is consistent with Rensch’s rule indicating that males were the more variable sex. Males did not have a steeper body size–latitude relationship than females suggesting that sex-specific latitudinal variation in body size may not be an important contributing factor to Rensch’s rule. Future research on greater horseshoe bats might best focus on more comprehensive mechanisms driving the pattern of female-biased SSD variation.     

Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard

To elucidate the developmental aspects of the evolution of sexual size dimorphism (SSD), an understanding of the sex-specific ontogeny of body size is critical. Here, we evaluate the relative importance of genetic and environmental determinants of SSD in juvenile common lizards (Lacerta vivipara). We examined the prenatal and post-natal effects of population density and habitat humidity on SSD, as well as the maternal effects of food availability, corticosterone level, humidity and heat regime during gestation. Analyses indicated strong prenatal and post-natal plasticity in body size per se and yielded three main results with respect to SSD. First, SSD in juvenile common lizards matches qualitatively the SSD observed in adults. Secondly, SSD was influenced by none of the prenatal factors investigated here, suggesting poor sex-biased maternal effects on offspring size. Thirdly, SSD was sensitive to post-natal habitat humidity, which positively affected growth rate more strongly in females than in males. Thus, natural variation in SSD in juvenile common lizards appears to be primarily determined by a combination of sex-biased genetic factors and post-natal conditions. We discuss the possibility that viviparity may constrain the evolution of sex-biased maternal effects on offspring size.     

Life-history variation and allometry for sexual size dimorphism in Pacific salmon and trout

Allometry for sexual size dimorphism (SSD) is common in animals, but how different evolutionary processes interact to determine allometry remains unclear. Among related species SSD (male : female) typically increases with average body size, resulting in slopes of less than 1 when female size is regressed on male size: an allometric relationship formalized as 'Rensch's rule' . Empirical studies show that taxa with male-biased SSD are more likely to satisfy Rensch's rule and that a taxon's mean SSD is negatively correlated with allometric slope, implicating sexual selection on male size as an important mechanism promoting allometry for SSD. I use body length (and life-history) data from 628 (259) populations of seven species of anadromous Pacific salmon and trout (Oncorhynchus spp.) to show that in this genus life-history variation appears to regulate patterns of allometry both within and between species. Although all seven species have intraspecific allometric slopes of less than 1, contrary to expectation slope is unrelated to species' mean SSD, but is instead negatively correlated with two life-history variables: the species' mean marine age and variation in marine age. Second, because differences in marine age among species render SSD and body size uncorrelated, the interspecific slope is isometric. Together, these results provide an example of how evolutionary divergence in life history among related species can affect patterns of allometry for SSD across taxonomic scales.     

Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism

Sexual size dimorphism (SSD) describes divergent body sizes of adult males and females. While SSD has traditionally been explained by sexual and fecundity selection, recent advances in physiology and developmental biology emphasize that SSD would occur proximately because of sexual differences in ontogenetic growth trajectories (i.e., growth rate and duration). Notably, these ontogenetic traits are subject to energetic or time constraints and thus traded off with fitness components (e.g., survival and reproduction). To elucidate the importance of such ontogenetic trade‐offs in the evolution of SSD, we developed a new theoretical framework by extending quantitative genetic models for the evolution of sexual dimorphism in which we reinterpret the trait as body size and reformulate sex‐specific fitness in size‐dependent manners. More specifically, we assume that higher growth rate or longer growth duration leads to larger body size and higher reproductive success but incurs the cost of lower survivorship or shorter reproduction period. We illustrate how two sexes would optimize ontogenetic growth trajectories in sex‐specific ways and exhibit divergent body sizes. The present framework provides new insights into the evolutionary theory of SSD and predictions for empirical testing.     

The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny

Differences among taxa in sexual size dimorphism of adults can be produced by changes in distinct developmental processes and thus may reflect different evolutionary histories. Here we examine whether divergence in sexual dimorphism of adults between recently established Montana and Alabama populations of the house finch (Carpodacus mexicanus) can be attributed to population differences in growth of males and females. In both populations, males and females were similar at hatching, but as a result of sex-specific growth attained sexual size dimorphism by the time of independence. Timing and extent of growth varied between the sexes: Females maintained maximum rates of growth for a longer time than males, whereas males had higher initial growth rates and achieved maximum growth earlier and at smaller sizes than females. Ontogeny of sexual dimorphism differed between populations, but in each population, sexual dimorphism in growth parameters and sexual dimorphism at the time of nest leaving were similar to sexual dimorphism of adults. Variation in growth of females contributed more to population divergence than did growth of males. In each population, we found close correspondence between patterns of sexual dimorphism in growth and population divergence in morphology of adults: Traits that were the most sexually dimorphic in growth in each population contributed the most to population divergence in both sexes. We suggest that sex-specific expression of phenotypic and genetic variation throughout the ontogeny of house finches can result in different responses to selection between males and females of the same age, and thus produce fast population divergence in the sexual size dimorphism.     

Natural allelic variations of xenobiotic-metabolizing enzymes affect sexual dimorphism in Oryzias latipes

Sexual dimorphisms, which are phenotypic differences between males and females, are driven by sexual selection. Interestingly, sexually selected traits show geographical variations within species despite strong directional selective pressures. This paradox has eluded many evolutionary biologists for some time, and several models have been proposed (e.g. ‘indicator model’ and ‘trade-off model’). However, disentangling which of these theories explains empirical patterns remains difficult, because genetic polymorphisms that cause variation in sexual differences are still unknown. In this study, we show that polymorphisms in cytochrome P450 (CYP) 1B1, which encodes a xenobiotic-metabolizing enzyme, are associated with geographical differences in sexual dimorphism in the anal fin morphology of medaka fish (Oryzias latipes). Biochemical assays and genetic cross experiments show that high- and low-activity CYP1B1 alleles enhanced and declined sex differences in anal fin shapes, respectively. Behavioural and phylogenetic analyses suggest maintenance of the high-activity allele by sexual selection, whereas the low-activity allele possibly has experienced positive selection due to by-product effects of CYP1B1 in inferred ancestral populations. The present data can elucidate evolutionary mechanisms behind genetic variations in sexual dimorphism and indicate trade-off interactions between two distinct mechanisms acting on the two alleles with pleiotropic effects of xenobiotic-metabolizing enzymes.     

Two sexes respond equally to food restriction in a sexually dimorphic but not body mass dimorphic jumping spider

Natural selection favors animals that evolve developmental and behavioral responses that buffer the negative effects of food restrictions. These buffering responses vary both between species and within species. Many studies have shown sex‐specific responses to environmental changes, usually in species with sexual size dimorphism (SSD), less found in species with weak or no SSD, which suggests that sizes of different sexes are experiencing different selections. However, previous studies usually investigated development and behavior separately, and the balanced situation where males and females of sexually dimorphic species respond in the same way to food restriction remains little known. Here, we investigated this in Phintelloides versicolor (Salticidae) that presents sexual dimorphism in color and shape but weak SSD. We examined whether food restriction induced the same responses in males and females in development duration, adult body size and weight, daily time allocated to foraging, and hunting. We found food restriction induced similar responses in both sexes: both exhibited longer development duration, smaller adult body size and weight, higher probability of staying outside nests and noticing prey immediately, and higher hunting success. However, there were sexual differences regardless of food condition: females showed faster development, smaller adult body size, higher probability of staying outside of nests, and higher hunting success. These indicated the differential selection on male and female sizes of P. versicolor could be under a balanced situation, where males and females show equal developmental and behavioral plasticity to environmental constraints.     

A test of genetic models for the evolutionary maintenance of same-sex sexual behaviour

The evolutionary maintenance of same-sex sexual behaviour (SSB) has received increasing attention because it is perceived to be an evolutionary paradox. The genetic basis of SSB is almost wholly unknown in non-human animals, though this is key to understanding its persistence. Recent theoretical work has yielded broadly applicable predictions centred on two genetic models for SSB: overdominance and sexual antagonism. Using Drosophila melanogaster, we assayed natural genetic variation for male SSB and empirically tested predictions about the mode of inheritance and fitness consequences of alleles influencing its expression. We screened 50 inbred lines derived from a wild population for male–male courtship and copulation behaviour, and examined crosses between the lines for evidence of overdominance and antagonistic fecundity selection. Consistent variation among lines revealed heritable genetic variation for SSB, but the nature of the genetic variation was complex. Phenotypic and fitness variation was consistent with expectations under overdominance, although predictions of the sexual antagonism model were also supported. We found an unexpected and strong paternal effect on the expression of SSB, suggesting possible Y-linkage of the trait. Our results inform evolutionary genetic mechanisms that might maintain low but persistently observed levels of male SSB in D. melanogaster, but highlight a need for broader taxonomic representation in studies of its evolutionary causes.