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The idea that sex differences in selection drive the evolution of suppressed recombination between sex chromosomes is well developed in population genetics. Yet, despite a now classic body of theory, empirical evidence that sexually antagonistic selection drives the evolution of recombination arrest remains equivocal and alternative hypotheses underdeveloped. Here, we investigate whether the length of “evolutionary strata” formed by chromosomal inversions (or other large-effect recombination modifiers) expanding the non-recombining sex-linked region (SLR) on sex chromosomes can be informative of how selection influenced their fixation. We develop population genetic models to show how the length of an SLR-expanding inversion, and the presence of partially recessive deleterious mutational variation, affect the fixation probability of three different classes of inversions: (1) intrinsically neutral, (2) directly beneficial (i.e., due to breakpoint or positional effects), and (3) those capturing sexually antagonistic (SA) loci. Our models indicate that neutral inversions, and those capturing an SA locus in linkage disequilibrium with the ancestral SLR, will exhibit a strong fixation bias toward small inversions; while unconditionally beneficial inversions, and those capturing a genetically unlinked SA locus, will favor fixation of larger inversions. The footprint of evolutionary stratum size left behind by different selection regimes is strongly influenced by parameters affecting the deleterious mutation load, the physical position of the ancestral SLR, and the distribution of new inversion lengths.

Alternative reproductive tactics (ARTs) often exhibit more than one mating behavior depending on social context (i.e., behavioral plasticity). It has been hypothesized that by constraining an ART from reaching optimal morphological states, intralocus tactical conflict could promote the maintenance of behavioral plasticity in ARTs, rather than the use of a fixed mating behavior to match an optimal morphological state. For selection on either behavior or morphology to influence one another, there would need to be genetic integration between these traits within the behaviorally plastic males. To examine this possibility, we compared the relationship between body shape, body size and propensity to use sneak-chase behavior across experienced wild-caught males and inexperienced lab reared males from the behaviorally plastic ART (sneaker males) of the swordtail fish Xiphophorus multilineatus. The smaller, more narrow-bodied sneaker males use both force copulatory sneak-chases and courtship behavior to access females, while the larger, deeper-bodied courter males are fixed in their use of courtship behavior. We detected similar relationships between body size and the propensity to use sneak-chase behavior within the sneaker males when they were alone with a female (no competitor present) for both experienced and inexperienced males, suggesting genetic integration between behavior and body size. Body shape, on the other hand, was more complex and suggested both genetic integration (more fusiform males from both groups were more likely to use sneak-chase), as well as learning depending on subtle differences in body shape. We discuss how intralocus tactical conflict on morphological traits that are genetically integrated with behaviors has the potential to maintain behavioral plasticity in the X. multilineatus sneaker males and influence the evolution of ARTs in general.

Abstract Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment. Significance statement Sexual conflict occurs between the two sexes over numerous life history traits, and it is complex to disentangle how these traits interact and affect each other. Here we use a long-term evolution experiment to investigate sexual dimorphism in somatic maintenance. We found no effect of feminising the X chromosome on female immune defence. However, we did find that increased female control over mating rate resulted in longer female lifespan, but reduced male lifespan, and that these effects were dependent on social context (isolated or in mixed-sex groups). Unlike previous studies on the effect of sexual conflict on longevity, our experiment did not manipulate environmental conditions nor the adult sex ratio, which is likely to reduce both pre- and post-copulatory sexual selection.

The sexes may have different optima in cognitive traits due to differences in life history strategies and the expense of investing in metabolically costly brain tissue. However, given genetic correlations, each sex could be constrained from reaching its cognitive optimum due to intralocus sexual conflict. We compared learning performance of two male alternative reproductive tactics and females from known genotypes (both sire and dam) in the livebearing fish Xiphophorus multilineatus. We predicted that females' learning performance would align with the learning performance of their sire's genotype due to genetic correlation of cognitive traits. Using a classical conditioning assessment (associating a flashing light with a food reward), we detected mating tactic dimorphism in learning performance, with the behaviourally plastic sneaker males outperforming the behaviourally fixed courter males. Unexpectedly, females sired by the faster-learning sneaker males performed significantly worse than sneaker males. We also detected an influence of brain size on female learning performance. Previous studies have found that females invest more in offspring sired by courter males, and we therefore hypothesize that maternal effects could potentially mitigate the influence of sexual conflict on a cognitive trait.

Alternative reproductive tactics (ARTs) have improved our understanding of the evolution of adaptive variation; for instance, their study has led us to understand that the best phenotype (e.g. large and flashy) for a tactic that uses one mating behavior (e.g. court females) is often not the best phenotype (e.g. small and inconspicuous) for a tactic that uses a different mating behavior (e.g. chase and force-copulate females). However, genetic correlations of shared traits across ARTs can constrain ARTs from reaching their optimal states, resulting in intralocus tactical conflict (IATC). While constraints on evolution in general have been well-established and studied, there are some important implications of constraints due to intralocus tactical conflict on ARTs that have not been incorporated into the field of evolutionary ecology. Here we describe how an appreciation of IATC, including how to detect it and when to expect it, can change our perspectives in three areas: 1) adaptive states for traits associated with ARTs (e.g. growth rates, behavioural plasticity); 2) how selection due to ecological variation across populations can produce patterns of divergence between ARTS; 3) and the evolutionary stability of polymorphisms (e.g. how IATC can explain losses of one ART, and why this can lead to rapid speciation).

There is growing evidence across taxa for a mortality-growth rate tradeoff, however the extent to which individuals experience selection both for and against growing faster in the wild can be difficult to assess. We used otoliths to assess growth rates in the wild for Xiphophorus multilineatus, a species of swordtail fish with genetically influenced male alternative reproductive tactics. The ARTs are thought to be maintained due to a trade-off between a higher probability of reaching sexual maturity (smaller sneaker males) and maturing later as a large male with higher mating success (larger courter males). We show that the early juvenile growth rates of the subadult courter males were faster as compared to the other juveniles, potentially suggesting selection for growing faster to increase the probability of reaching sexual maturity. However, variance in the early juvenile growth rates of adult courter males was reduced (truncating high values) as compared to the subadult courter males and overall growth rates were faster in the subadult courter males than the adult courter males. These results support a cost of growing faster as juveniles: reduced longevity as an adult. We also detected a negative relationship between the early growth rates of females and their age, further supporting a longevity cost to growing faster. While both male ARTs are likely to experience stabilizing selection on growth rates, the differences between the morphs in how they optimize this tradeoff in relation to overall fitness (courters optimize growing faster to increase probability of reaching sexual maturity, sneakers optimize longevity as adults) has the potential to lead to disruptive selection between the ARTs on growth rates. We show that the data collected here is consistent with the “growth-mortality optimization” hypothesis and highlight some of the challenges that stabilizing selection presents for examining adaptive variation of growth rates in a natural environment.

Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last years. A major challenge is the integration of disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequencies using either a heuristic (PoolSNP) or a probabilistic variant caller (SNAPE-pooled). We use this pipeline to generate the largest data repository of genomic data available for D. melanogaster to date, encompassing 271 previously published and unpublished population samples from over 100 locations in > 20 countries on four continents. Several of these locations have been sampled at different seasons across multiple years. This dataset, which we call Drosophila Evolution over Space and Time (DEST), is coupled with sampling and environmental meta-data. A web-based genome browser and web portal provide easy access to the SNP dataset. We further provide guidelines on how to use Pool-Seq data for model-based demographic inference. Our aim is to provide this scalable platform as a community resource which can be easily extended via future efforts for an even more extensive cosmopolitan dataset. Our resource will enable population geneticists to analyze spatio-temporal genetic patterns and evolutionary dynamics of D. melanogaster populations in unprecedented detail., DrosEU is funded by a Special Topic Networks (STN) grant from the European Society for Evolutionary Biology (ESEB). MK (M. Kapun) was supported by the Austrian Science Foundation (grant no. FWF P32275); JG by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (H2020-ERC-2014-CoG-647900) and by the Spanish Ministry of Science and Innovation (BFU-2011-24397); TF by the Swiss National Science Foundation (SNSF grants PP00P3_133641, PP00P3_165836, and 31003A_182262) and a Mercator Fellowship from the German Research Foundation (DFG), held as a EvoPAD Visiting Professor at the Institute for Evolution and Biodiversity, University of Münster; AOB by the National Institutes of Health (R35 GM119686); MK (M. Kankare) by Academy of Finland grant 322980; VL by Danish Natural Science Research Council (FNU) grant 4002-00113B; FS Deutsche Forschungsgemeinschaft (DFG) grant STA1154/4-1, Project 408908608; JP by the Deutsche Forschungsgemeinschaft Projects 274388701 and 347368302; AU by FPI fellowship (BES-2012-052999); ET Israel Science Foundation (ISF) grant 1737/17; MSV, MSR and MJ by a grant from the Ministry of Education, Science and Technological Development of the Republic of Serbia (451-03-68/2020-14/200178); AP, KE and MT by a grant from the Ministry of Education, Science and Technological Development of the Republic of Serbia (451-03-68/2020-14/200007); and TM NSERC grant RGPIN-2018-05551.

Using basic ecological concepts, we introduce sperm ecology as a framework to study sperm cells. First, we describe environmental effects on sperm and conclude that evolutionary and ecological research should not neglect the overwhelming evidence presented here (both in external and internal fertilizers and in terrestrial and aquatic habitats) that sperm function is altered by many environments, including the male environment. Second, we determine that the evidence for sperm phenotypic plasticity is overwhelming. Third, we find that genotype-by-environment interaction effects on sperm function exist, but their general adaptive significance (e.g., local adaptation) awaits further research. It remains unresolved whether sperm diversification occurs by natural selection acting on sperm function or by selection on male and female microenvironments that enable optimal plastic performance of sperm (sperm niches). Environmental effects reduce fitness predictability under sperm competition, predict species distributions under global change, explain adaptive behavior, and highlight the role of natural selection in behavioral ecology and reproductive medicine.

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here, we explore how self-fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, as inbreeding reduces the frequency of heterozygotes and speeds fixation. This expectation was supported, but although previous results suggest that the more an allele that is deleterious to one sex is dominant in that sex, the smaller the region of parameter space that will admit polymorphism, we found that this effect is weakened by self-fertilization. However, the effect of inbreeding is not strong enough to completely cancel out the effect of dominance: For a given frequency of inbreeding, it will still be the case that the more dominant the alleles are in their deleterious context, the smaller the region of parameter space in which they can exist at polymorphism.

Colour polymorphic species with extensive ranges often exhibit large-scale geographic patterns of morph frequency variation. Because colour polymorphism is associated with correlated differences in multiple traits, such as thermal performance, a likely proximate explanation for such patterns is morph-specific responses to temperature variation. The colour polymorphic Blue-tailed damselfly Ischnura elegans exhibits large-scale geographic variation in morph frequencies, but the possibility that temperature is a proximate explanation for the latitudinal cline in morph frequencies has only ever been tested within a single developmental stage (egg survival and hatching time), where no difference between the morphs was found. I therefore carried out a temperature manipulation on larvae of I. elegans which I raised to maturity in the laboratory. I found that individuals exhibited incomplete compensatory growth after being exposed to cold temperatures, and that individuals which did not emerge successfully and those that experienced cold temperatures had more juvenile morphology in the last instar. In addition, there were sex-specific and morph-specific effects of temperature on adult morphology, such that sexual size dimorphism was increased when individuals experienced warm temperatures throughout the larval stage, and that cold temperatures tended to result in larger size of androchromes and their offspring compared to the other morphs. These results are generally consistent with the large-scale geographic variation in morph frequencies found in this species.

Intralocus sexual conflict occurs when opposing selection pressures operate on loci expressed in both sexes, constraining the evolution of sexual dimorphism and displacing one or both sexes from their optimum. We eliminated intralocus conflict in Drosophila melanogaster by limiting transmission of all major chromosomes to males, thereby allowing them to win the intersexual tug-of-war. Here, we show that this male-limited (ML) evolution treatment led to the evolution (in both sexes) of masculinized wing morphology, body size, growth rate, wing loading, and allometry. In addition to more male-like size and shape, ML evolution resulted in an increase in developmental stability for males. However, females expressing ML chromosomes were less developmentally stable, suggesting that being ontogenetically more male-like was disruptive to development. We suggest that sexual selection over size and shape of the imago may therefore explain the persistence of substantial genetic variation in these characters and the ontogenetic processes underlying them.

Conspicuous heritable polymorphisms are useful to address the question if morph frequencies are stable or whether they fluctuate between generations. Ecological geneticists have studied colour polymorphisms in the past, but there are few long-term studies of genetic dynamics across multiple generations. We studied morph-frequency dynamics and female fecundity in the trimorphic blue-tailed damselfly (Ischnura elegans). The morphs include a male-coloured (androchrome) type of female, which is thought to be maintained by frequency-dependent sexual conflict. Morph frequencies changed significantly between years across all populations. There was evidence for directional frequency change since androchrome females increased in 9 of 10 populations across a 4-year period. There was heterogeneity between populations in their evolutionary trajectories, partly caused by population age: androchrome frequencies were initially high in young populations but gradually decreased and approached the level of old populations. We discuss the possible causes of morph-frequency fluctuations, and the role of morph-specific fecundity, dispersal and other forces influencing evolutionary dynamics in this system.

Although colour polymorphisms in adult organisms of many taxa are often adaptive in the context of sexual selection or predation, genetic correlations between colour and other phenotypic traits expressed early in ontogeny could also play an important role in polymorphic systems. We studied phenotypic and genetic variation in development time among female colour morphs in the polymorphic damselfly Ischnura elegans in the field and by raising larvae in a common laboratory environment. In the field, the three different female morphs emerged at different times. Among laboratory-raised families, we found evidence of a significant correlation between maternal morph and larval development time in both sexes. This suggests that the phenotypic correlation between morph and emergence time in the field has a parallel in a genetic correlation between maternal colour and offspring development time. Maternal colour morph frequencies could thus potentially change as correlated responses to selection on larval emergence dates. The similar genetic correlation in male offspring suggests that sex-limitation in this system is incomplete, which may lead to an ontogenetic sexual conflict between selection for early male emergence (protandry) and emergence times associated with maternal morph.

Hemiclones are naturally occurring or artificially produced individuals that share a single specific genetic haplotype. Natural hemiclones are produced via hybridization between two closely related species, whereas hemiclonal analysis in Drosophila is carried out in the laboratory via crosses with artificially created ‘clone-generator’ females with a specific genetic make-up. Hemiclonal analysis in Drosophila has been applied successfully to date to obtain measures of standing genetic variation for numerous traits. Here, we review the current hemiclonal literature and suggest future directions for hemiclonal research, including its application in molecular and genomic studies, and the adaptation of natural hemiclonal systems to carry out Drosophila-type studies of standing genetic variation.

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.

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 F(ST) 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 [F(ST )(selected) > F(ST )(neutral)], or if negative frequency-dependent selection maintains genetic polymorphisms and pulls populations towards a common stable equilibrium [F(ST) (selected) < F(ST) (neutral)]. Here, we compared F(ST) 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 F(ST) 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.

In this study we investigated the developmental basis of adult phenotypes in a non-model organism, a polymorphic damselfly (Ischnura elegans) with three female colour morphs. This polymorphic species presents an ideal opportunity to study intraspecific variation in growth trajectories, morphological variation in size and shape during the course of ontogeny, and to relate these juvenile differences to the phenotypic differences of the discrete adult phenotypes; the two sexes and the three female morphs. We raised larvae of different families in individual enclosures in the laboratory, and traced morphological changes during the course of ontogeny. We used principal components analysis to examine the effects of Sex, Maternal morph, and Own morph on body size and body shape. We also investigated the larval fitness consequences of variation in size and shape by relating these factors to emergence success. Females grew faster than males and were larger as adults, and there was sexual dimorphism in body shape in both larval and adult stages. There were also significant effects of both maternal morph and own morph on growth rate and body shape in the larval stage. There were significant differences in body shape, but not body size, between the adult female morphs, indicating phenotypic integration between colour, melanin patterning, and body shape. Individuals that emerged successfully grew faster and had different body shape in the larval stage, indicating internal (non-ecological) selection on larval morphology. Overall, morphological differences between individuals at the larval stage carried over to the adult stage. Thus, selection in the larval stage can potentially result in correlated responses in adult phenotypes and vice versa.

Rapid evolutionary change over a few generations has been documented in natural populations. Such changes are observed as organisms invade new environments, and they are often triggered by changed interspecific interactions, such as differences in predation regimes. However, in spite of increased recognition of antagonistic male-female mating interactions, there is very limited evidence that such intraspecific interactions could cause rapid evolutionary dynamics in nature. This is because ecological and longitudinal data from natural populations have been lacking. Here we show that in a color-polymorphic damselfly species, male-female mating interactions lead to rapid evolutionary change in morph frequencies between generations. Field data and computer simulations indicate that these changes are driven by sexual conflict, in which morph fecundities are negatively affected by frequency- and density-dependent male mating harassment. These frequency- dependent processes prevent population divergence by maintaining a female polymorphism in most populations. Although these results contrast with the traditional view of how sexual conflict enhances the rate of population divergence, they are consistent with a recent theoretical model of how females may form discrete genetic clusters in response to male mating harassment.

A handful of studies have investigated sexually antagonistic constraints on achieving sex-specific fitness optima, although exclusively through male-genome-limited evolution experiments. In this article, we established a female-limited X chromosome evolution experiment, where we used an X chromosome balancer to enforce the inheritance of the X through the matriline, thus removing exposure to male selective constraints. This approach eliminates the effects of sexually antagonistic selection on the X chromosome, permitting evolution toward a single sex-specific optimum. After multiple generations of selection, we found strong evidence that body size and development time had moved toward a female-specific optimum, whereas reproductive fitness and locomotion activity remained unchanged. The changes in body size and development time are consistent with previous results, and suggest that the X chromosome is enriched for sexually antagonistic genetic variation controlling these particular traits. The lack of change in reproductive fitness and locomotion activity could be due to a number of mutually nonexclusive explanations, including a lack of sexually antagonistic variance on the X chromosome for those traits or confounding effects of the use of the balancer chromosome. This study is the first to employ female-genome-limited selection and adds to the understanding of the complexity of sexually antagonistic genetic variation.

Most studies on eco-evolutionary feedbacks concern the influence of abiotic factors, or predator–prey and host–parasite interactions, while studies involving sexual interactions are lagging behind. This is at odds with the potential of these interactions to engage in such processes. Indeed, there is now ample evidence that sexual selection is affected by ecological change and that sexually selected traits can evolve rapidly, which may modify the ecological context of populations, and thus the selection pressures they will be exposed to. Here we review evidence for such eco-evolutionary processes. We discuss examples of eco-evolutionary change in an attempt to understand the challenges related with identifying and characterizing such processes. In particular, we focus on the challenges associated with accurately identifying the components of the feedback as well as their causal relation. Finally, we evaluate scenarios where understanding eco-evolutionary feedbacks of sexual selection may help us appreciate the effects of sexual selection in shaping evolutionary processes. (Less)

The evolution of separate sexes from hermaphroditism is thought to have occurred independently many times, and is linked to the evolution of sex chromosomes. Even though we have a good understanding of the theoretical steps in the evolution of sex chromosomes from a hermaphrodite ancestor, the initial stages are still hard to study because many sex chromosome systems are old. We addressed this problem by experimentally selecting a hermaphrodite via sex-limited experimental evolution for several generations, simulating the early stages in the evolution of a sex chromosome. More specifically, we used a GFP (green fluorescent protein) marker as a proxy for a sex-determining locus, and selected replicate populations of the simultaneously hermaphroditic flatworm Macrostomum lignano for fitness via the male sex role, female sex role, or both (i.e. a control). After 14 generations, a fitness assay revealed clear evidence for incipient sex role specialization, presumably reflecting the release from constraints usually imposed by selection on the other sex role. Importantly, however, this was not simply explained by differential sex allocation in the different selection regimes - insofar as morphological traits reflect the underlying trade-off over resource allocation to the male and female sex functions - because testis and ovary sizes did not diverge among treatments. Our study shows that sex role specialization can occur rapidly as a result of sex-limited selection, which is consistent with genetic constraints between sex-roles, and in line with the first predicted steps towards the evolution of a new sex chromosome system.