Protein deprivation facilitates the independent evolution of behavior and morphology.

Ecological conditions such as nutrition can change genetic covariances between traits and accelerate or slow down trait evolution. As adaptive trait correlations can become maladaptive following rapid environmental change, poor or stressful environments are expected to weaken genetic covariances, thereby increasing the opportunity for independent evolution of traits. Here, we demonstrate the differences in genetic covariance among multiple behavioral and morphological traits (exploration, aggression, and body weight) between southern field crickets (Gryllus bimaculatus) raised in favorable (free-choice) versus stressful (protein-deprived) nutritional environments. We also quantify the extent to which differences in genetic covariance structures contribute to the potential for the independent evolution of these traits. We demonstrate that protein-deprived environments tend to increase the potential for traits to evolve independently, which is caused by genetic covariances that are significantly weaker for crickets raised on protein-deprived versus free-choice diets. The weakening effects of stressful environments on genetic covariances tended to be stronger in males than in females. The weakening of the genetic covariance between traits under stressful nutritional environments was expected to facilitate the opportunity for adaptive evolution across generations. Therefore, the multivariate gene-by-environment interactions revealed here may facilitate behavioral and morphological adaptations to rapid environmental change.

Artificial selection reveals sex differences in the genetic basis of sexual attractiveness.

Mutual mate choice occurs when males and females base mating decisions on shared traits. Despite increased awareness, the extent to which mutual choice drives phenotypic change remains poorly understood. When preferences in both sexes target the same traits, it is unclear how evolution will proceed and whether responses to sexual selection from male choice will match or oppose responses to female choice. Answering this question is challenging, as it requires understanding, genetic relationships between the traits targeted by choice, mating success, and, ultimately, fitness for both sexes. Addressing this, we applied artificial selection to the cuticular hydrocarbons of the fly Drosophila serrata that are targeted by mutual choice and tracked evolutionary changes in males and females alongside changes in mating success. After 10 generations, significant trait evolution occurred in both sexes, but intriguingly there were major sex differences in the associated fitness consequences. Sexually selected trait evolution in males led to a genetically based increase in male mating success. By contrast, although trait evolution also occurred in females, there was no change in mating success. Our results suggest that phenotypic sexual selection on females from male choice is environmentally, rather than genetically, generated. Thus, compared with female choice, male choice is at best a weak driver of signal trait evolution in this species. Instead, the evolution of apparent female ornamentation seems more likely due to a correlated response to sexual selection on males and possibly other forms of natural selection.

Evolutionary time-series analysis reveals the signature of frequency-dependent selection on a female mating polymorphism.

A major challenge in evolutionary biology is understanding how stochastic and deterministic factors interact and influence macroevolutionary dynamics in natural populations. One classical approach is to record frequency changes of heritable and visible genetic polymorphisms over multiple generations. Here, we combined this approach with a maximum likelihood-based population-genetic model with the aim of understanding and quantifying the evolutionary processes operating on a female mating polymorphism in the blue-tailed damselfly Ischnura elegans. Previous studies on this color-polymorphic species have suggested that males form a search image for females, which leads to excessive mating harassment of common female morphs. We analyzed a large temporally and spatially replicated data set of between-generation morph frequency changes in I. elegans. Morph frequencies were more stable than expected from genetic drift alone, suggesting the presence of selection toward a stable equilibrium that prevents local loss or fixation of morphs. This can be interpreted as the signature of negative frequency-dependent selection maintaining the phenotypic stasis and genetic diversity in these populations. Our novel analytical approach allows the estimation of the strength of frequency-dependent selection from the morph frequency fluctuations around their inferred long-term equilibria. This approach can be extended and applied to other polymorphic organisms for which time-series data across multiple generations are available.

Asymmetric isolating barriers between different microclimatic environments caused by low immigrant survival.

Spatially variable selection has the potential to result in local adaptation unless counteracted by gene flow. Therefore, barriers to gene flow will help facilitate divergence between populations that differ in local selection pressures. We performed spatially and temporally replicated reciprocal field transplant experiments between inland and coastal habitats using males of the common blue damselfly (Enallagma cyathigerum) as our study organism. Males from coastal populations had lower local survival rates than resident males at inland sites, whereas we detected no differences between immigrant and resident males at coastal sites, suggesting asymmetric local adaptation in a source-sink system. There were no intrinsic differences in longevity between males from the different environments suggesting that the observed differences in male survival are environment-dependent and probably caused by local adaptation. Furthermore, the coastal environment was found to be warmer and drier than the inland environment, further suggesting local adaptation to microclimatic factors has lead to differential survival of resident and immigrant males. Our results suggest that low survival of immigrant males mediates isolation between closely located populations inhabiting different microclimatic environments.

The evolutionary stability of cross-sex, cross-trait genetic covariances.

Although knowledge of the selective agents behind the evolution of sexual dimorphism has advanced considerably in recent years, we still lack a clear understanding of the evolutionary durability of cross-sex genetic covariances that often constrain its evolution. We tested the relative stability of cross-sex genetic covariances for a suite of homologous contact pheromones of the fruit fly Drosophila serrata, along a latitudinal gradient where these traits have diverged in mean. Using a Bayesian framework, which allowed us to account for uncertainty in all parameter estimates, we compared divergence in the total amount and orientation of genetic variance across populations, finding divergence in orientation but not total variance. We then statistically compared orientation divergence of within-sex (G) to cross-sex (B) covariance matrices. In line with a previous theoretical prediction, we find that the cross-sex covariance matrix, B, is more variable than either within-sex G matrix. Decomposition of B matrices into their symmetrical and nonsymmetrical components revealed that instability is linked to the degree of asymmetry. We also find that the degree of asymmetry correlates with latitude suggesting a role for spatially varying natural selection in shaping genetic constraints on the evolution of sexual dimorphism.

Sex-specific fitness consequences of nutrient intake and the evolvability of diet preferences.

The acquisition of nutrients is fundamental for the maintenance of bodily functions, growth, and reproduction in animals. As a result, fitness can be maximized only when animals are able to direct their attention to foods that reflect their current nutritional needs. Despite significant literature documenting the fitness consequences of nutrient composition and preference, less is known about the underlying genetic architecture of the dietary preferences themselves, specifically, the degree to which they can respond to selection. We addressed this by integrating evolutionary quantitative genetics and nutritional geometry to examine the shape of the sex-specific fitness surfaces and the availability of genetic variance for macronutrient preferences in the fruit fly Drosophila melanogaster. Combining these analyses, we found that the microevolutionary potential of carbohydrate and protein preference was above average in this population, because the expected direction of selection was relatively well aligned with the major axis of the genetic variance-covariance matrix, G. We also found that potential exists for sexually antagonistic genetic constraint in this system; macronutrient blends maximizing fitness differed between the sexes, and cross-sex genetic correlations for their consumption were positive. However, both sexes were displaced from their feeding optima, generating similar directional selection on males and females, with the combined effect being that minimal sex-specific genetic constraints currently affect dietary preferences in this population.

The B-matrix harbors significant and sex-specific constraints on the evolution of multicharacter sexual dimorphism.

The extent to which sexual dimorphism can evolve within a population depends on an interaction between sexually divergent selection and constraints imposed by a genetic architecture that is shared between males and females. The degree of constraint within a population is normally inferred from the intersexual genetic correlation, r(mf) . However, such bivariate correlations ignore the potential constraining effect of genetic covariances between other sexually coexpressed traits. Using the fruit fly Drosophila serrata, a species that exhibits mutual mate preference for blends of homologous contact pheromones, we tested the impact of between-sex between-trait genetic covariances using an extended version of the genetic variance-covariance matrix, G, that includes Lande's (1980) between-sex covariance matrix, B. We find that including B greatly reduces the degree to which male and female traits are predicted to diverge in the face of divergent phenotypic selection. However, the degree to which B alters the response to selection differs between the sexes. The overall rate of male trait evolution is predicted to decline, but its direction remains relatively unchanged, whereas the opposite is found for females. We emphasize the importance of considering the B-matrix in microevolutionary studies of constraint on the evolution of sexual dimorphism.

Density-dependent male mating harassment, female resistance, and male mimicry.

Genetic variation in female resistance and tolerance to male mating harassment can affect the outcome of sexually antagonistic mating interactions. We investigated female mating rates and male mating harassment in natural populations of a damselfly (Ischnura elegans). This damselfly species has a heritable sex-limited polymorphism in females, where one of the morphs is a male mimic (androchrome females). The three female morphs differ in mating rates, and these differences are stable across populations and years. However, the degree of premating resistance toward male mating attempts varied across generations and populations. Male mating harassment of the female morphs changed in a density-dependent fashion, suggesting that male mate preferences are plastic and vary with the different morph densities. We quantified morph differences in male mating harassment and female fecundity, using path analysis and structural equation modeling. We found variation between the morphs in the fitness consequences of mating, with the fecundity of one of the nonmimetic morphs declining with increasing male mating harassment. However, androchrome females had lower overall fecundity, presumably reflecting a cost of male mimicry. Density-dependent male mating harassment on the morphs and fecundity costs of male mimicry are thus likely to contribute to the maintenance of this female polymorphism.

Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females.

Costs of sperm production may lead to prudence in male sperm allocation and also to male mate choice. Here, we develop a life history-based mutual mate choice model that takes into account the lost-opportunity costs for males from time out in sperm recovery and lets mate competition be determined by the prevailing mate choice strategies. We assume that high mating rate may potentially lead to sperm depletion in males, and that as a result, female reproduction may be limited by the availability of sperm. Increasing variation in male quality leads, in general, to increased selective mate choice by females, and vice versa. Lower-quality males may, however, gain access to more fecund higher-quality females by lowering their courting rate, thus increasing their sperm reserves. When faced with strong male competition for mates, low-quality males become less choosy, which leads to assortative mating for quality and an increased mating rate across all males. With assortative mating, the frequency of antagonistic interactions (sexual conflict) is reduced, allowing males to lower the time spent replenishing sperm reserves in order to increase mating rate. This in turn leads to lower sperm levels at mating and therefore could lead to negative effects on female fitness via sperm limitation.

Spatial and temporal dynamics in a sexual selection mosaic.

Selective regimes and phenotypic optima could either change smoothly and in a clinal fashion or be spatially organized in a more unpredictable mosaic pattern over the geographic landscape. When natural or sexual selection is driven by intra- or interspecific biotic interactions, fine-grained spatial variation in selective regimes could result in selection mosaics rather than clinal variation in selection. We investigated temporal variation and spatial organization in sexual selection on male body size along an ecological coastal-inland gradient of a polymorphic damselfly Ischnura elegans. Body size increased in a clinal fashion along this gradient: animals were smaller in size at the coast, but became larger in the inland areas. In contrast, the sexual selection regimes on male body size showed evidence of more fine-grained spatial organization with no evidence for a clinal pattern and low spatial autocorrelations between populations. These spatially fine-grained sexual selection regimes varied in sign and magnitude and were driven by a combination of the densities of heritable female color morphs and local female body sizes. We suggest that the spatial organization of the selective regimes can be interpreted as a sexual selection mosaic that is influenced by highly localized density- and frequency-dependent social interactions.

Female sexual polymorphism and fecundity consequences of male mating harassment in the wild.

Genetic and phenotypic variation in female response towards male mating attempts has been found in several laboratory studies, demonstrating sexually antagonistic co-evolution driven by mating costs on female fitness. Theoretical models suggest that the type and degree of genetic variation in female resistance could affect the evolutionary outcome of sexually antagonistic mating interactions, resulting in either rapid development of reproductive isolation and speciation or genetic clustering and female sexual polymorphisms. However, evidence for genetic variation of this kind in natural populations of non-model organisms is very limited. Likewise, we lack knowledge on female fecundity-consequences of matings and the degree of male mating harassment in natural settings. Here we present such data from natural populations of a colour polymorphic damselfly. Using a novel experimental technique of colour dusting males in the field, we show that heritable female colour morphs differ in their propensity to accept male mating attempts. These morphs also differ in their degree of resistance towards male mating attempts, the number of realized matings and in their fecundity-tolerance to matings and mating attempts. These results show that there may be genetic variation in both resistance and tolerance to male mating attempts (fitness consequences of matings) in natural populations, similar to the situation in plant-pathogen resistance systems. Male mating harassment could promote the maintenance of a sexual mating polymorphism in females, one of few empirical examples of sympatric genetic clusters maintained by sexual conflict.