Mating environments mediate the evolution of behavioral isolation during ecological speciation.

The evolution of behavioral isolation is often the first step toward speciation. While past studies show that behavioral isolation will sometimes evolve as a by-product of divergent ecological selection, we lack a more nuanced understanding of factors that may promote or hamper its evolution. The environment in which mating occurs may be important in mediating whether behavioral isolation evolves for two reasons. Ecological speciation could occur as a direct outcome of different sexual interactions being favored in different mating environments. Alternatively, mating environments may vary in the constraint they impose on traits underlying mating interactions, such that populations evolving in a "constraining" mating environment would be less likely to evolve behavioral isolation than populations evolving in a less constraining mating environment. In the latter, mating environment is not the direct cause of behavioral isolation but rather permits its evolution only if other drivers are present. We test these ideas with a set of 28 experimental fly populations, each of which evolved under one of two mating environments and one of two larval environments. Counter to the prediction of ecological speciation by mating environment, behavioral isolation was not maximal between populations evolved in different mating environments. Nonetheless, mating environment was an important factor as behavioral isolation evolved among populations from one mating environment but not among populations from the other. Though one mating environment was conducive to the evolution of behavioral isolation, it was not sufficient: assortative mating only evolved between populations adapting to different-larval environments within that mating environment, indicating a role for ecological speciation. Intriguingly, the mating environment that promoted behavioral isolation is characterized by less sexual conflict compared to the other mating environment. Our results suggest that mating environments play a key role in mediating ecological speciation via other axes of divergent selection.

The evolution of sexual dimorphism in gene expression in response to a manipulation of mate competition.

Many genes are differentially expressed between males and females and patterns of sex-biased gene expression (SBGE) vary among species. Some of this variation is thought to have evolved in response to differences in mate competition among species that cause varying patterns of sex-specific selection. We used experimental evolution to test this by quantifying SBGE and sex-specific splicing in 15 Drosophila melanogaster populations that evolved for 104 generations in mating treatments that removed mate competition via enforced monogamy, or allowed mate competition in either small, simple, or larger, structurally more complex mating environments. Consistent with sex-specific selection affecting SBGE, initially sex-biased genes diverged in expression more among treatments than unbiased genes, and there was greater expression divergence for male- than female-biased genes. It has been suggested the transcriptome should be "feminized" under monogamy because of the removal of sexual selection on males; we did not observe this, likely because selection differs in additional ways between monogamy vs. polygamy. Significant divergence in average expression dimorphism between treatments was observed and, in some treatment comparisons, the direction of the divergence differed across different sex-bias categories. There was not a generalized reduction in expression dimorphism under enforced monogamy.

Population Genomics of the Facultatively Sexual Liverwort Marchantia polymorpha.

The population genomics of facultatively sexual organisms are understudied compared with their abundance across the tree of life. We explore patterns of genetic diversity in two subspecies of the facultatively sexual liverwort Marchantia polymorpha using samples from across Southern Ontario, Canada. Despite the ease with which M. polymorpha should be able to propagate asexually, we find no evidence of strictly clonal descent among our samples and little to no signal of isolation by distance. Patterns of identity-by-descent tract sharing further showed evidence of recent recombination and close relatedness between geographically distant isolates, suggesting long distance gene flow and at least a modest frequency of sexual reproduction. However, the M. polymorpha genome contains overall very low levels of nucleotide diversity and signs of inefficient selection evidenced by a relatively high fraction of segregating deleterious variants. We interpret these patterns as possible evidence of the action of linked selection and a small effective population size due to past generations of asexual propagation. Overall, the M. polymorpha genome harbors signals of a complex history of both sexual and asexual reproduction.

An investigation of the sex-specific genetic architecture of fitness in Drosophila melanogaster.

In dioecious populations, the sexes employ divergent reproductive strategies to maximize fitness and, as a result, genetic variants can affect fitness differently in males and females. Moreover, recent studies have highlighted an important role of the mating environment in shaping the strength and direction of sex-specific selection. Here, we measure adult fitness for each sex of 357 lines from the Drosophila Synthetic Population Resource in two different mating environments. We analyze the data using three different approaches to gain insight into the sex-specific genetic architecture for fitness: classical quantitative genetics, genomic associations, and a mutational burden approach. The quantitative genetics analysis finds that on average segregating genetic variation in this population has concordant fitness effects both across the sexes and across mating environments. We do not find specific genomic regions with strong associations with either sexually antagonistic (SA) or sexually concordant (SC) fitness effects, yet there is modest evidence of an excess of genomic regions with weak associations, with both SA and SC fitness effects. Our examination of mutational burden indicates stronger selection against indels and loss-of-function variants in females than in males.

Two Forms of Sexual Dimorphism in Gene Expression in Drosophila melanogaster: Their Coincidence and Evolutionary Genetics.

Phenotypic sexual dimorphism can be mediated by sex differences in gene expression. We examine two forms of sexual dimorphism in gene expression in Drosophila melanogaster: 1) sex-biased gene expression (SBGE) in which the sexes differ in the amount a gene is expressed and 2) sexual dimorphism in isoform usage, that is, sex-specific splicing (SSS). In whole body (but not the head) expression, we find a negative association between SBGE and SSS, possibly suggesting that these are alternate routes to resolving sexual antagonistic selection. Next, we evaluate whether expression dimorphism contributes to the heterogeneity among genes in rmf, the intersexual genetic correlation in body expression that constrains the extent to which a gene's expression can evolve independently between the sexes. We find lower rmf values for genes with than without SSS. We find higher rmf values for male- than female-biased genes (except genes with extreme male bias), even though male-biased genes are known to have greater evolutionary divergence in expression. Finally, we examine population genetic patterns in relation to SBGE and SSS because genes with expression dimorphism have likely experienced a history of sex differences in selection. SSS is associated with reduced values of Tajima's D and elevated direction of selection (DoS) values, suggestive of higher rates of adaptive evolution. Though DoS is highly elevated for genes with extreme male bias, DoS otherwise tends to decline from female-biased to unbiased to male-biased genes. Collectively, the results indicate that SBGE and SSS are differentially distributed across the genome and are associated with different forms of selection.

Sex-Specific Variance in Fitness and the Efficacy of Selection.

AbstractVariance in fitness is thought to be greater in males than in females in many species. If this is so, there are two potentially contradictory consequences on the efficacy of selection (Nes): greater variance in fitness may allow stronger selection (i.e., increased s), but it will also cause stronger genetic drift (i.e., reduced Ne). We develop a simple model to ask how the stronger condition dependency of fitness in males than in females affects selection and fitness variance in each sex to examine the net effect on the efficacy of selection. We measured the phenotypic variance in fitness for each sex in Drosophila melanogaster in different environmental and mating contexts. Variance in fitness was only approximately one and a half to two times higher in males than in females; juvenile mortality likely dampens the difference in variation between the sexes. Combining these results with previous studies of sex-specific selection on mutations, we infer that the increased drift due to males counterbalances the stronger selection on males in this species, leaving Nes similar to what would be expected if both sexes were "female-like" with respect to selection and variance in fitness. Reasons why this could differ in other species are discussed.

Quantifying male harm and its divergence.

Male harm arises when traits that increase reproductive success in competition with other males also harm females as a side effect. The extent of harm depends on male and female phenotypes, both of which can diverge between populations. Within a population, harm is inferred when increased exposure to males reduces female fitness, but studies of the divergence of male harm rarely manipulate male exposure. Here, we quantify male harm and compare its magnitude between two lab populations of Drosophila serrata that were derived from a common ancestor 7 years earlier and subsequently held under conditions that minimized environmental differences. We manipulated female exposure to males in a factorial design involving all four combinations of males and females from these populations, providing insight into divergence in both sexes. Our results reveal substantial harm to females and provide stronger evidence of divergence in males than in females. Using these and other published data, we discuss conceptual issues surrounding the quantification and comparison of harm that arise because it involves a comparison of multiple quantities (e.g., female fitness under varying male exposure), and we demonstrate the increased insight that is gained by manipulating male exposure to quantify these quantities.

Species richness and identity both determine the biomass of global reef fish communities.

Changing biodiversity alters ecosystem functioning in nature, but the degree to which this relationship depends on the taxonomic identities rather than the number of species remains untested at broad scales. Here, we partition the effects of declining species richness and changing community composition on fish community biomass across >3000 coral and rocky reef sites globally. We find that high biodiversity is 5.7x more important in maximizing biomass than the remaining influence of other ecological and environmental factors. Differences in fish community biomass across space are equally driven by both reductions in the total number of species and the disproportionate loss of larger-than-average species, which is exacerbated at sites impacted by humans. Our results confirm that sustaining biomass and associated ecosystem functions requires protecting diversity, most importantly of multiple large-bodied species in areas subject to strong human influences.

On Male Harm: How It Is Measured and How It Evolves in Different Environments.

AbstractMales can harm the females that they interact with, but populations and species widely vary in the occurrence and extent of harm. We consider the merits and limitations of two common approaches to investigating male harm and apply these to an experimental study of divergence in harm. Different physical environments can affect how the sexes interact, causing plastic and/or evolved changes in harm. If harmful male phenotypes are less likely to evolve in situations where females have more control over sexual interactions, populations evolving in environments in which females have greater control should have less harmful males. We test this idea using experimental populations of Drosophila melanogaster that have evolved in either of two environments that vary in the extent to which females can avoid males or in a third environment without mate competition (i.e., enforced monogamy). We demonstrate an evolved reduction in harm in the absence of mate competition and also in a mate competition environment in which females have greater control. We also show a plastic effect in that otherwise harmful males are no longer so when tested in the environment in which females have greater control. Our results reveal the different perspectives provided by the two methods of studying harm.

Patterns and Causes of Signed Linkage Disequilibria in Flies and Plants.

Most empirical studies of linkage disequilibrium (LD) study its magnitude, ignoring its sign. Here, we examine patterns of signed LD in two population genomic data sets, one from Capsella grandiflora and one from Drosophila melanogaster. We consider how processes such as drift, admixture, Hill-Robertson interference, and epistasis may contribute to these patterns. We report that most types of mutations exhibit positive LD, particularly, if they are predicted to be less deleterious. We show with simulations that this pattern arises easily in a model of admixture or distance-biased mating, and that genome-wide differences across site types are generally expected due to differences in the strength of purifying selection even in the absence of epistasis. We further explore how signed LD decays on a finer scale, showing that loss of function mutations exhibit particularly positive LD across short distances, a pattern consistent with intragenic antagonistic epistasis. Controlling for genomic distance, signed LD in C. grandiflora decays faster within genes, compared with between genes, likely a by-product of frequent recombination in gene promoters known to occur in plant genomes. Finally, we use information from published biological networks to explore whether there is evidence for negative synergistic epistasis between interacting radical missense mutations. In D. melanogaster networks, we find a modest but significant enrichment of negative LD, consistent with the possibility of intranetwork negative synergistic epistasis.

Estimation of the SNP Mutation Rate in Two Vegetatively Propagating Species of Duckweed.

Mutation rate estimates for vegetatively reproducing organisms are rare, despite their frequent occurrence across the tree of life. Here we report mutation rate estimates in two vegetatively reproducing duckweed species, Lemna minor and Spirodela polyrhiza We use a modified approach to estimating mutation rates by taking into account the reduction in mutation detection power that occurs when new individuals are produced from multiple cell lineages. We estimate an extremely low per generation mutation rate in both species of duckweed and note that allelic coverage at de novo mutation sites is very skewed. We also find no substantial difference in mutation rate between mutation accumulation lines propagated under benign conditions and those grown under salt stress. Finally, we discuss the implications of interpreting mutation rate estimates in vegetatively propagating organisms.

Population genomics of the facultatively asexual duckweed Spirodela polyrhiza.

Clonal propagation allows some plant species to achieve massive population sizes quickly but also reduces the evolutionary independence of different sites in the genome. We examine genome-wide genetic diversity in Spirodela polyrhiza, a duckweed that reproduces primarily asexually. We find that this geographically widespread and numerically abundant species has very low levels of genetic diversity. Diversity at nonsynonymous sites relative to synonymous sites is high, suggesting that purifying selection is weak. A potential explanation for this observation is that a very low frequency of sex renders selection ineffective. However, there is a pronounced decay in linkage disequilibrium over 40 kb, suggesting that though sex may be rare at the individual level it is not too infrequent at the population level. In addition, neutral diversity is affected by the physical proximity of selected sites, which would be unexpected if sex was exceedingly rare at the population level. The amount of genetic mixing as assessed by the decay in linkage disequilibrium is not dissimilar from selfing species such as Arabidopsis thaliana, yet selection appears to be much less effective in duckweed. We discuss alternative explanations for the signature of weak purifying selection.

Testing for local adaptation in adult male and female fitness among populations evolved under different mate competition regimes.

Mating/fertilization success and fecundity are influenced by sexual interactions among individuals, the nature and frequency of which can vary among different environments. The extent of local adaptation for such adult fitness components is poorly understood. We allowed 63 populations of Drosophila melanogaster to independently evolve in one of three mating environments that alter sexual interactions: one involved enforced monogamy, while the other two permitted polygamy in either structurally simple standard fly vials or in larger "cages" with added complexity. Adult male and female reproductive fitness were measured after 16 and 28 generations, respectively, via full reciprocal transplants. In males, reciprocal local adaptation was observed between the monogamy and simple polygamy treatments, consistent with the evolution of reproductively competitive males under polygamy that perform poorly under monogamy because they harm their only mate. However, males evolved in the complex polygamy treatment performed similarly or better than all other males in all mating environments, consistent with previous results showing higher genetic quality in this treatment. Differences in female fitness were more muted, suggesting selection on females was less divergent across the mating treatments and echoing a common pattern of greater phenotypic and expression divergence in males than females.

Ecological specialization in populations adapted to constant versus heterogeneous environments.

Populations vary in their degree of ecological specialization. An intuitive, but often untested, hypothesis is that populations evolving under greater environmental heterogeneity will evolve to be less specialized. How important is environmental heterogeneity in explaining among-population variation in specialization? We assessed juvenile viability of 20 Drosophila melanogaster populations evolving under one of four regimes: (1) a salt-enriched environment, (2) a cadmium-enriched environment, (3) a temporally varying environment, and (4) a spatially varying environment. Juvenile viability was tested in both the original selective environments and a set of novel environments. In both the original and novel environments, populations from the constant cadmium regime had the lowest average viability and the highest variance in viability across environments but populations from the other three regimes were similar. Our results suggest that variation in specialization among these populations is most simply explained as a pleiotropic by-product of adaptation to specific environments rather than resulting from a history of exposure to environmental heterogeneity.

Sexual Conflict and Sexually Transmitted Infections (STIs): Coevolution of Sexually Antagonistic Host Traits with an STI.

In many taxa, there is a conflict between the sexes over mating rate. The outcome of sexually antagonistic coevolution depends on the costs of mating and natural selection against sexually antagonistic traits. A sexually transmitted infection (STI) changes the relative strength of these costs. We study the three-way evolutionary interaction among male persistence, female resistance, and STI virulence for two types of STIs: a viability-reducing STI and a reproduction-reducing STI. A viability-reducing STI escalates conflict between the sexes. This leads to increased STI virulence (i.e., full coevolution) if the costs of sexually antagonistic traits occur through viability but not through reproduction. In contrast, a reproduction-reducing STI de-escalates the sexual conflict, but STI virulence does not coevolve in response. We also investigated the establishment probability of STIs under different combinations of evolvability. Successful invasion by a viability-reducing STI becomes less likely if hosts (but not parasites) are evolvable, especially if only the female trait can evolve. A reproduction-reducing STI can almost always invade because it does not kill its host. We discuss how the evolution of host and parasite traits in a system with sexual conflict differs from a system with female mate choice.

An experimental test of the mutation-selection balance model for the maintenance of genetic variance in fitness components.

Despite decades of research, the factors that maintain genetic variation for fitness are poorly understood. It is unclear what fraction of the variance in a typical fitness component can be explained by mutation-selection balance (MSB) and whether fitness components differ in this respect. In theory, the level of standing variance in fitness due to MSB can be predicted using the rate of fitness decline under mutation accumulation, and this prediction can be directly compared to the standing variance observed. This approach allows for controlled statistical tests of the sufficiency of the MSB model, and could be used to identify traits or populations where genetic variance is maintained by other factors. For example, some traits may be influenced by sexually antagonistic balancing selection, resulting in an excess of standing variance beyond that generated by deleterious mutations. We describe the underlying theory and use it to test the MSB model for three traits in Drosophila melanogaster We find evidence for differences among traits, with MSB being sufficient to explain genetic variance in larval viability but not male mating success or female fecundity. Our results are consistent with balancing selection on sexual fitness components, and demonstrate the feasibility of rigorous statistical tests of the MSB model.

Coalescence and Linkage Disequilibrium in Facultatively Sexual Diploids.

Under neutrality, linkage disequilibrium results from physically linked sites having nonindependent coalescent histories. In obligately sexual organisms, meiotic recombination is the dominant force separating linked variants from one another, and thus in determining the decay of linkage disequilibrium with physical distance. In facultatively sexual diploid organisms that principally reproduce clonally, mechanisms of mitotic exchange are expected to become relatively more important in shaping linkage disequilibrium. Here we outline mathematical and computational models of a facultative-sex coalescent process that includes meiotic and mitotic recombination, via both crossovers and gene conversion, to determine how linkage disequilibrium is affected with facultative sex. We demonstrate that the degree to which linkage disequilibrium is broken down by meiotic recombination simply scales with the probability of sex if it is sufficiently high (much greater than [Formula: see text] for population size N). However, with very rare sex (occurring with frequency on the order of [Formula: see text]), mitotic gene conversion plays a particularly important and complicated role because it both breaks down associations between sites and removes within-individual diversity. Strong population structure under rare sex leads to lower average linkage disequilibrium values than in panmictic populations, due to the influence of low-frequency polymorphisms created by allelic sequence divergence acting in individual subpopulations. These analyses provide information on how to interpret observed linkage disequilibrium patterns in facultative sexuals and to determine what genomic forces are likely to shape them.

The effects of male harm vary with female quality and environmental complexity in Drosophila melanogaster.

Mate competition provides the opportunity for sexual selection which often acts strongly on males, but also the opportunity for sexual conflict that can alter natural selection on females. Recent attention has focused on the potential of sexual conflict to weaken selection on females if male sexual attention, and hence harm, is disproportionately directed towards high- over low-quality females, thereby reducing the fitness difference between these females. However, sexual conflict could instead strengthen selection on females if low-quality females are more sensitive to male harm than high-quality females, thereby magnifying fitness differences between them. We quantify the effects of male exposure on low- versus high-quality females in Drosophila melanogaster in each of two environments ('simple' and 'complex') that are known to alter behavioural interactions. We show that the effects of male harm are greater for low- compared to high-quality females in the complex but not the simple environment, consistent with mate competition strengthening selection on females in the former but not in the latter environment.

Mutation accumulation in selfing populations under fluctuating selection.

Selfing species are prone to extinction, possibly because highly selfing populations can suffer from a continuous accumulation of deleterious mutations, a process analogous to Muller's ratchet in asexual populations. However, current theory provides little insight into which types of genes are most likely to accumulate deleterious alleles and what environmental circumstances may accelerate genomic degradation. Here, we investigate temporal changes in the environment that cause fluctuations in the strength of purifying selection. We simulate selfing populations with genomes containing a mixture of loci experiencing constant selection and loci experiencing selection that fluctuates in strength (but not direction). Even when both types of loci experience the same average strength of selection, loci under fluctuating selection contribute disproportionately more to deleterious mutation accumulation. Moreover, the presence of loci experiencing fluctuating selection in the genome increases the deleterious fixation rate at loci under constant selection; under most realistic scenarios, this effect of linked selection can be attributed to a reduction in Ne . Fluctuating selection is particularly injurious when selective environments are strongly autocorrelated over time and when selection is concentrated into rare bouts of strong selection. These results imply that loci under fluctuating selection are likely important drivers of extinction in selfing species.