Thomas P. Gosden

Spatial and temporal dynamics in a sexual selection mosaic

Abstract 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 polymorphisms, sexual conflict and limits to speciation processes in animals

Heritable and visually detectable polymorphisms, such as trophic polymorphisms, ecotypes, or colour morphs, have become classical model systems among ecological geneticists and evolutionary biologists. The relatively simple genetic basis of many polymorphisms (one or a few loci) makes such species well-suited to study evolutionary processes in natural settings. More recently, polymorphic systems have become popular when studying the early stages of the speciation process and mechanisms facilitating or constraining the evolution of reproductive isolation. Although colour polymorphisms have been studied extensively in the past, we argue that they have been underutilized as model systems of constraints on speciation processes. Colouration traits may function as signalling characters in sexual selection contexts, and the maintenance of colour polymorphisms is often due to frequency-dependent selection. One important issue is why there are so few described cases of female polymorphisms. Here we present a synthetic overview of female sexual polymorphisms, drawing from our previous work on female colour polymorphisms in lizards and damselflies. We argue that female sexual polymorphisms have probably been overlooked in the past, since workers have mainly focused on male-male competition over mates and have not realized the ecological sources of genetic variation in female fitness. Recent experimental evolution studies on fruit flies (Drosophila melanogaster) have demonstrated significant heritable variation among female genotypes in the fitness costs of resistance or tolerance to male mating harassment. In addition, female-female competition over resources could also generate genetic variation in female fitness and promote the maintenance of female sexual polymorphisms. Female sexual polymorphisms could subsequently either be maintained as intrapopulational polymorphisms or provide the raw material for the formation of new species.

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.

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.

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.

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, rmf. 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 Landes (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.

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.

On the evolution of heightened condition dependence of male sexual displays

The maintenance of genetic variation in male sexual display traits in the face of strong directional sexual selection from female preferences is an ongoing evolutionary conundrum. Condition dependence and the genic capture hypothesis are often cited as theoretical resolutions to this problem, yet little is known about the ability of condition dependence itself to evolve. We set out to test how a suite of cuticular hydrocarbons (CHCs) used in sexual displays are affected by adult diet and the potential for any condition‐dependent response to evolve in a laboratory‐adapted population of the Australian fruit fly Drosophila serrata. We performed a dietary manipulation within a half‐sib breeding design, raising adult males either with or without access to live yeast, a manipulation that had previously shown strong effects on female fitness. Diet had strong phenotypic effects, with males from the different diets producing different CHC blends. The blend of CHCs under sexual selection showed a degree of elevated condition dependence. Regardless of the heightened sensitivity of favoured CHC blends to diet and the presence of genetic variance for the traits, we were unable to detect any genetic variance in the reaction norms for the male dietary response. Our results suggest that there is limited opportunity for males to evolve further condition dependence in response to yeast availability in this population.

Patterns of differentiation in a colour polymorphism and in neutral markers reveal rapid genetic changes in natural damselfly populations

The existence and mode of selection operating on heritable adaptive traits can be inferred by comparing population differentiation in neutral genetic variation between populations (often using FST values) with the corresponding estimates for adaptive traits. Such comparisons indicate if selection acts in a diversifying way between populations, in which case differentiation in selected traits is expected to exceed differentiation in neutral markers [FST (selected) > FST (neutral)], or if negative frequency‐dependent selection maintains genetic polymorphisms and pulls populations towards a common stable equilibrium [FST (selected) < FST (neutral)]. Here, we compared FST values for putatively neutral data (obtained using amplified fragment length polymorphism) with estimates of differentiation in morph frequencies in the colour‐polymorphic damselfly Ischnura elegans. We found that in the first year (2000), population differentiation in morph frequencies was significantly greater than differentiation in neutral loci, while in 2002 (only 2 years and 2 generations later), population differentiation in morph frequencies had decreased to a level significantly lower than differentiation in neutral loci. Genetic drift as an explanation for population differentiation in morph frequencies could thus be rejected in both years. These results indicate that the type and/or strength of selection on morph frequencies in this system can change substantially between years. We suggest that an approach to a common equilibrium morph frequency across all populations, driven by negative frequency‐dependent selection, is the cause of these temporal changes. We conclude that inferences about selection obtained by comparing FST values from neutral and adaptive genetic variation are most useful when spatial and temporal data are available from several populations and time points and when such information is combined with other ecological sources of data.

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.