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Data from: Aging asexual lineages and the evolutionary maintenance of sex
Ho, Eddie Ka Ho; Agrawal, Aneil F. — 2017-05-08 Finite populations of asexual and highly selfing species suffer from a reduced efficacy of selection. Such populations are thought to decline in fitness over time due to accumulating slightly deleterious mutations or failing to adapt to changing conditions. These within-population processes that lead non-recombining species to extinction may help maintain sex and outcrossing through species level selection. Although inefficient selection is proposed to elevate extinction rates over time, previous models of species selection for sex assumed constant diversification rates. For sex to persist, classic models require that asexual species diversify at rates lower than sexual species; the validity of this requirement is questionable, both conceptually and empirically. We extend past models by allowing asexual lineages to decline in diversification rates as they age, i.e., non-recombining lineages “senesce” in diversification rates. At equilibrium, senescing diversification rates maintain sex even when asexual lineages, at young ages, diversify faster than their sexual progenitors. In such cases, the age distribution of asexual lineages contains a peak at intermediate values rather than showing the exponential decline predicted by the classic model. Coexistence requires only that the average rate of diversification in asexuals be lower than that of sexuals.
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Data from: Remating and sperm competition in replicate populations of Drosophila melanogaster adapted to alternative environments
Arbuthnott, Devin; Agrawal, Aneil F.; Rundle, Howard D. — 2015-01-31 The prevalence of sexual conflict in nature, as well as the supposedly arbitrary direction of the resulting coevolutionary trajectories, suggests that it may be an important driver of phenotypic divergence even in a constant environment. However, natural selection has long been central to the operation of sexual conflict within populations and may therefore constrain or otherwise direct divergence among populations. Ecological context may therefore matter with respect to the diversification of traits involved in sexual conflict, and if natural selection is sufficiently strong, such traits may evolve in correlation with environment, generating a pattern of ecologically-dependent parallel evolution. In this study we assess among-population divergence both within and between environments for several traits involved in sexual conflict. Using eight replicate populations of Drosophila melanogaster from a long-term evolution experiment, we measured remating rates and subsequent offspring production of females when housed with two separate males in sequence. We found no evidence of any variation in male reproductive traits (offense or defense). However, the propensity of females to remate diverged significantly among the eight populations with no evidence of any environmental effect, consistent with sexual conflict promoting diversification even in the absence of ecological differences. On the other hand, females adapted to one environment (ethanol) tended to produce a higher proportion of offspring sired by their first mate as compared to those adapted to the other (cadmium) environment, suggesting ecologically-based divergence of this conflict phenotype. Because we find evidence for both stochastic population divergence operating outside of an ecological context and environment-dependent divergence of traits under sexual conflict, the interaction of these two processes is an important topic for future work.
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Data from: Sensitivity of the distribution of mutational fitness effects to environment, genetic background, and adaptedness: a case study with Drosophila
Wang, Alethea D.; Sharp, Nathaniel Philip; Agrawal, Aneil F. — 2013-10-28 Heterogeneity in the fitness effects of individual mutations has been found across different environmental and genetic contexts. Going beyond effects on individual mutations, how is the distribution of selective effects, f(s), altered by changes in genetic and environmental context? In this study, we examined changes in the major features of f(s) by estimating viability selection on 36 individual mutations in Drosophila melanogaster across two different environments in two different genetic backgrounds that were either adapted or nonadapted to the two test environments. Both environment and genetic background affected selection on individual mutations. However, the overall distribution f(s) appeared robust to changes in genetic background but both the mean, E(s), and the variance, V(s) were dependent on the environment. Between these two properties, V(s) was more sensitive to environmental change. Contrary to predictions of fitness landscape theory, the match between genetic background and assay environment (i.e., adaptedness) had little effect on f(s).
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On male harm: How it is measured and how it evolves in different environments
Rundle, Howard D.; Yun, Li; Agrawal, Aneil F. — 2021-04-29 <p>Males can harm the females they interact with, but populations/species vary widely 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 <em>Drosophila melanogaster</em> 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.</p>
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Data from: An experimental test of the mutation-selection balance model for the maintenance of genetic variance in fitness components
Sharp, Nathaniel P.; Agrawal, Aneil F. — 2018-10-18 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 and whether fitness components differ in this respect. In theory, the level of standing variance in fitness due to mutation-selection balance 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 mutation-selection balance 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 mutation-selection balance (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 mutation-selection balance model. https://creativecommons.org/publicdomain/zero/1.0/
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Data from: Ecological specialization in populations adapted to constant versus heterogeneous environments
Wang, Ao; Singh, Amardeep; Huang, Yuheng; Agrawal, Aneil F. — 2019-02-28 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: (i) a salt-enriched environment, (ii) a cadmium-enriched environment, (iii) a temporally varying environment, and (iv) 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.
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Data from: Environmental complexity and the purging of deleterious alleles
Singh, Amardeep; Agrawal, Aneil F.; Rundle, Howard D. — 2017-07-31 Sexual interactions among adults can generate selection on both males and females with genome-wide consequences. Sexual selection through males is one component of this selection that has been argued to play an important role in purging deleterious alleles. A common technique to assess the influence of sexual selection is by a comparison of experimental evolution under enforced monogamy vs. polygamy. Mixed results from past studies may be due to the use of highly simplified lab conditions that alter the nature of sexual interactions. Here we examine the rate of purging of 22 gene disruption mutations in experimental polygamous populations of Drosophila melanogaster in each of two mating environments: a simple, high density environment (i.e., typical fly vials) and a lower density, more spatially complex environment. Based on past work, we expect sexual interactions in the latter environment to result in stronger selection in both sexes. Consistent with this, we find that mutations tend to be purged more quickly in populations evolving in complex environments. We discuss possible mechanisms by which environmental complexity might modulate the rate at which deleterious alleles are purged and putatively ascribe a role for sexual interactions in explaining the treatment differences in our experiment.
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Data from: Quantitative genetic variance in experimental fly populations evolving with or without environmental heterogeneity
Huang, Yuheng; Stinchcombe, John R.; Agrawal, Aneil F. — 2015-09-07 Heterogeneous environments are typically expected to maintain more genetic variation in fitness within populations than homogeneous environments. However, the accuracy of this claim depends on the form of heterogeneity as well as the genetic basis of fitness traits and how similar the assay environment is to the environment of past selection. Here we measure quantitative genetic variance for three traits important for fitness using replicated experimental populations of Drosophila melanogaster evolving under four selective regimes: constant salt-enriched medium (Salt), constant cadmium-enriched medium (Cad), and two heterogeneous regimes that vary either temporally (Temp) or spatially (Spatial). As theory predicts, we found that Spatial populations tend to harbor more genetic variation than Temp populations or those maintained in a constant environment that is the same as the assay environment. Contrary to expectation, Salt populations tend to have more genetic variation than Cad populations in both assay environments. We discuss the patterns for quantitative genetic (QG) variances across regimes in relation to previously reported data on genome-wide sequence diversity. For some traits, the QG patterns are similar to the diversity patterns of ecological selected SNPs whereas the QG patterns for some other traits resembled that of neutral SNPs.
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Data from: The condition dependency of fitness in males and females: the fitness consequences of juvenile diet assessed in environments differing in key adult resources
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Zikovitz, Andrea E.; Agrawal, Aneil F. — 2013-05-13 Variation in environmental or genetic quality leads to phenotypic variation in condition, but how much variation in fitness is created by this variation in condition? Using Drosophila melanogaster, we manipulated condition via alternative larval diets and then tested several key factors predicted to influence how much variation in fitness results from differences in condition. Specifically, we were interested in whether male and female fitness are affected equally by condition and whether the strength of selection on condition depends on the abundance of key resources limiting the reproductive output of each sex. We measured selection on condition in alternative assay contexts that varied in the abundance of adult food (a key resource for females) or in the abundance of females (a key resource for males). Overall, selection tended to be stronger on males than females. However, selection on males was weakened when the abundance of their key resource (females) was elevated. Increasing the abundance of the key resource for females (live yeast) elevated their reproductive output as expected but did not change the strength of selection in this sex. Instead, this manipulation increased selection on males, suggesting that this environmental factor indirectly affects selection on males via their interaction with females.
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Data from: Mutation accumulation in selfing populations under fluctuating selection
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Ho, Eddie Ka Ho; Agrawal, Aneil F. — 2018-07-05 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 N¬e. 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.
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Data from: Competition for mates and the improvement of nonsexual fitness
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Yun, Li; Chen, Patrick J.; Kwok, Kevin E.; Angell, Christopher S.; Rundle, Howard D.; Agrawal, Aneil F. — 2019-05-25 Competition for mates can be a major source of selection, not just on secondary sexual traits but across the genome. Mate competition strengthens selection on males via sexual selection, which typically favours healthy, vigorous individuals and, thus, all genetic variants that increase overall quality. However, recent studies suggest another major effect of mate competition that could influence genome-wide selection: sexual harassment by males can drastically weaken selection on quality in females. Because of these conflicting effects, the net effect of mate competition is uncertain, though perhaps not entirely unpredictable. We propose that the environment in which mate competition occurs mediates the importance of sexual selection relative to sexual conflict, and hence the net effect of mate competition on nonsexual fitness. To test this, we performed experimental evolution with 63 fruit fly populations adapting to novel larval conditions where each population was maintained with or without mate competition. In half the populations with mate competition, adults interacted in simple, high-density environments. In the remainder, adults interacted in more spatially complex environments in which male-induced harm is reduced. Populations evolving with mate competition in the complex environment adapted faster to novel larval environments than did populations evolving without mate competition or with mate competition in the simple environment. Moreover, mate competition in the complex environment caused a substantial reduction in inbreeding depression in egg-to-adult viability relative to the other two mating treatments. These results demonstrate that the mating environment has a substantial and predictable effect on nonsexual fitness through adaptation and purging.
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Data from: Male-biased fitness effects of spontaneous mutations in Drosophila melanogaster
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Sharp, Nathaniel Philip; Agrawal, Aneil F. — 2012-10-12 In populations with males and females, sexual selection may often represent a major component of overall selection. Sexual selection could act to eliminate deleterious alleles in concert with other forms of selection, thereby improving the fitness of sexual populations. Alternatively, the divergent reproductive strategies of the sexes could promote the maintenance of sexually-antagonistic variation, causing sexual populations to be less fit. The net impact of sexual selection on fitness is not well understood, due in part to limited data on the sex-specific effects of spontaneous mutations on total fitness. Using a set of mutation accumulation lines of Drosophila melanogaster, we found that mutations were deleterious in both sexes and had larger effects on fitness in males than in females. This pattern is expected to reduce the mutation load of sexual females and promote the maintenance of sexual reproduction.
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Data from: The effects of competition on the strength and softness of selection
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Ho, Eddie K. H.; Agrawal, Aneil F. — 2012-08-22 Deleterious alleles are constantly introduced into populations due to mutation. In subdivided populations, the impact of these mutations depends on the strength of selection as well as the softness of selection, i.e., the extent to which fitness is governed by local rather than global competition. It is widely appreciated that the intensity and type of competition will affect selection on deleterious mutations but most empirical work has focused solely on the effects of competition on selection strength. However, competition has rarely been studied in the context of selection ‘softness’ even though competition is at the conceptual root of soft selection. All other things being equal, theory predicts that inter- and intraspecific competition have opposing effects on the softness of selection. Using Drosophila melanogaster, we estimated the strength and softness of selection in a “baseline” competitive environment as well as two additional competitive environments characterized by either additional intra- or interspecific competitors. We found that competitive environment had little effect on the average strength of selection. While the softness of selection was affected by the type of competition, the direction of change varied across tests of different genes, contrary to expectation. Though the “hard/soft” selection paradigm implicitly assumes that all individuals are equally sensitive to the local competitive environment, we found this not to be the case. Wild-type individuals were more sensitive to changes in the genetic quality of their local competitors than mutant individuals.
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Data from: The physical environment mediates male harm and its effect on selection in females
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Yun, Li; Chen, Patrick J.; Singh, Amardeep; Agrawal, Aneil F.; Rundle, Howard D. — 2017-06-01 Recent experiments indicate that male preferential harassment of high-quality females reduces the variance in female fitness, thereby weakening natural selection through females and hampering adaptation and purging. We propose that this phenomenon, which results from a combination of male choice and male-induced harm, should be mediated by the physical environment in which intersexual interactions occur. Using Drosophila melanogaster, we examined intersexual interactions in small and simple (standard fly vials) versus slightly more realistic (small cages with spatial structure) environments. We show that in these more realistic environments, sexual interactions are less frequent, are no longer biased towards high-quality females, and that overall male harm is reduced. Next, we examine the selective advantage of high- over low-quality females while manipulating the opportunity for male choice. Male choice weakens the viability advantage of high-quality females in the simple environment, consistent with previous work, but strengthens selection on females in the more realistic environment. Laboratory studies in simple environments have strongly shaped our understanding of sexual conflict but may provide biased insight. Our results suggest that the physical environment plays a key role in the evolutionary consequences of sexual interactions and ultimately the alignment of natural and sexual selection.
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Data from: Variation in the strength of inbreeding depression across environments: effects of stress and density dependence
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Yun, Li; Agrawal, Aneil F. — 2014-09-05 In what types of environments should we expect to find strong inbreeding depression? Previous studies indicate that inbreeding depression, δ, is positively correlated with the stressfulness of the environment in which it is measured. However, it remains unclear why stress, per se, should increase δ. To our knowledge, only “competitive stress” has a logical connection to δ. Through competition for resources, better quality (outbred) individuals make the environment worse for lower quality (inbred) individuals, accentuating the differences between them. For this reason, we expect inbreeding depression to be stronger in environments where the fitness of individuals is more sensitive to the presence of conspecifics (i.e., where fitness is more density dependent). Indeed, some studies suggest a role for competition within environments but this idea has not been tested in the context of understanding variation in δ across environments. Using Drosophila melanogaster, we estimated δ for viability in 22 different environments. These environments were simultaneously characterized for (i) stressfulness and (ii) density dependence. Though stress and density dependence are moderately correlated with each other, inbreeding depression is much more strongly correlated with density dependence. These results suggest that mean selection across the genome is stronger in environments where competition is intense, rather than in environments that are stressful for other reasons.

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(Author: Agrawal, Aneil F.)

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