The evolutionary maintenance of ancient recombining sex chromosomes in the ostrich.

Sex chromosomes have evolved repeatedly across the tree of life and often exhibit extreme size dimorphism due to genetic degeneration of the sex-limited chromosome (e.g. the W chromosome of some birds and Y chromosome of mammals). However, in some lineages, ancient sex-limited chromosomes have escaped degeneration. Here, we study the evolutionary maintenance of sex chromosomes in the ostrich (Struthio camelus), where the W remains 65% the size of the Z chromosome, despite being more than 100 million years old. Using genome-wide resequencing data, we show that the population scaled recombination rate of the pseudoautosomal region (PAR) is higher than similar sized autosomes and is correlated with pedigree-based recombination rate in the heterogametic females, but not homogametic males. Genetic variation within the sex-linked region (SLR) (π = 0.001) was significantly lower than in the PAR, consistent with recombination cessation. Conversely, genetic variation across the PAR (π = 0.0016) was similar to that of autosomes and dependent on local recombination rates, GC content and to a lesser extent, gene density. In particular, the region close to the SLR was as genetically diverse as autosomes, likely due to high recombination rates around the PAR boundary restricting genetic linkage with the SLR to only ~50Kb. The potential for alleles with antagonistic fitness effects in males and females to drive chromosome degeneration is therefore limited. While some regions of the PAR had divergent male-female allele frequencies, suggestive of sexually antagonistic alleles, coalescent simulations showed this was broadly consistent with neutral genetic processes. Our results indicate that the degeneration of the large and ancient sex chromosomes of the ostrich may have been slowed by high recombination in the female PAR, reducing the scope for the accumulation of sexually antagonistic variation to generate selection for recombination cessation.

Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster.

Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 of 20 experimental populations (10 of which were individually significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. After 25 generations of experimental evolution these sexually antagonistic fitness effects appeared to be resolved. To formalize our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our model predictions support the conclusion that antagonistic coevolution between the sex chromosomes is plausible under the fitness effects observed in our experiments. Together, our results lend both empirical and theoretical support to the idea that cycles of antagonistic coevolution can occur between sex chromosomes and illustrate how this process, in combination with autosomal coadaptation, may drive genetic and phenotypic divergence between populations.

The Demographic Costs of Sexually Antagonistic Selection in Partially Selfing Populations.

AbstractWhen selection differs between the sexes, genes expressed by both males and females can experience sexually antagonistic (SA) selection, where beneficial alleles for one sex are deleterious for the other. Classic population genetics theory has been fundamental to understanding how and when SA genetic variation can be maintained by balancing selection, but these models have rarely considered the demographic consequences of coexisting alleles with deleterious fitness effects in each sex. In this article, we develop a stage-structured Mendelian matrix model and jointly analyze the evolutionary and demographic consequences of SA selection in obligately outcrossing (i.e., dioecious/gonochorous) and partially selfing hermaphrodite populations. We focus on identifying when SA polymorphisms are maintained by balancing selection and the population growth rate remains positive. Additionally, we analyze the effects of inbreeding depression manifesting at different life history stages and give an illustrative example of the potential for SA polymorphism in real populations using empirically estimated demographic rates for the hermaphroditic flowering plant Mimulus guttatus. Our results show that when population intrinsic growth rates approach 1, extinction occurs across large swathes of parameter space, favoring SA polymorphism or the fixation of male-beneficial alleles, and that inbreeding depression is a significant problem for maintaining SA polymorphism in partially selfing populations. Despite these demographic challenges, our example with M. guttatus appears to show that demographic rates observed in some real populations can sustain large regions of viable SA polymorphic space.

Natural selection and the distribution of chromosomal inversion lengths.

Chromosomal inversions contribute substantially to genome evolution, yet the processes governing their evolutionary dynamics remain poorly understood. Theory suggests that a readily measurable property of inversions-their length-can potentially affect their evolutionary fates. Emerging data on the lengths of polymorphic and fixed inversions may therefore provide clues to the evolutionary processes promoting inversion establishment. However, formal predictions for the distribution of inversion lengths remain incomplete, making empirical patterns difficult to interpret. We model the relation between inversion length and establishment probability for four inversion types: (1) neutral, (2) underdominant, (3) directly beneficial, and (4) indirectly beneficial, with selection favouring the latter because they capture locally adapted alleles at migration-selection balance and suppress recombination between them. We also consider how deleterious mutations affect the lengths of established inversions. We show that length distributions of common polymorphic and fixed inversions systematically differ among inversion types. Small rearrangements contribute the most to genome evolution under neutral and underdominant scenarios of selection, with the lengths of neutral inversion substitutions increasing, and those of underdominant substitutions decreasing, with effective population size. Among directly beneficial inversions, small rearrangements are preferentially fixed, whereas intermediate-to-large inversions are maintained as balanced polymorphisms via associative overdominance. Finally, inversions established under the local adaptation scenario are predominantly intermediate-to-large. Such inversions remain polymorphic or approach fixation within the local populations where they are favoured. Our models clarify how inversion length distributions relate to processes of inversion establishment, providing a platform for testing how natural selection shapes the evolution of genome structure.

Sexually Antagonistic Variation and the Evolution of Dimorphic Sexual Systems.

Multicellular Eukaryotes use a broad spectrum of sexual reproduction strategies, ranging from simultaneous hermaphroditism to complete dioecy (separate sexes). The evolutionary pathway from hermaphroditism to dioecy involves the spread of sterility alleles that eliminate female or male reproductive functions, producing unisexual individuals. Classical theory predicts that evolutionary transitions to dioecy are feasible when female and male sex functions genetically trade off with one another (allocation to sex functions is sexually antagonistic) and rates of self-fertilization and inbreeding depression are high within the ancestral hermaphrodite population. We show that genetic linkage between sterility alleles and loci under sexually antagonistic selection significantly alters these classical predictions. We identify three specific consequences of linkage for the evolution of dimorphic sexual systems. First, linkage broadens conditions for the invasion of unisexual sterility alleles, facilitating transitions to sexual systems that are intermediate between hermaphroditism and dioecy (androdioecy and gynodioecy). Second, linkage elevates the equilibrium frequencies of unisexual individuals within androdioecious and gynodioecious populations, which promotes subsequent transitions to full dioecy. Third, linkage dampens the role of inbreeding during transitions to androdioecy and gynodioecy, making these transitions feasible in outbred populations. We discuss implications of these results for the evolution of dimorphic reproductive systems and sex chromosomes.

Evolutionary Consequences of Sex-Specific Selection in Variable Environments: Four Simple Models Reveal Diverse Evolutionary Outcomes.

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes. Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time. This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of "sexually antagonistic" alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions. We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation. We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity. The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae).

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory-broadcast spawning males often release sperm slowly, with weak resource-dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter-intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal. Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae). We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per-gamete fertilization rate decreases precipitously with ejaculate size. Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

The Evolution of Reproductive Phenology in Broadcast Spawners and the Maintenance of Sexually Antagonistic Polymorphism.

Reproductive phenology is a crucial life-history trait that evolves in response to external environmental conditions and frequency- and density-dependent interactions within species. Broadcast spawners-which represent a large fraction of aquatic biodiversity-evolve phenologies that balance strong density-dependent fertilization success against abiotic environmental conditions that are required for successful reproduction. The overall balance between these processes may be particularly complex in dioecious species, where selection on reproductive timing potentially differs between the sexes. Here, we develop a population genetic model of reproductive phenology in a dioecious broadcast spawning species and show that environmental variability and density-dependent fertilization dynamics naturally give rise to profound sex differences in selection on gamete release strategies. The frequency-dependent nature of sperm competition generates sexually antagonistic selection on reproductive timing and facilitates the maintenance of genetic variation in phenological traits. Selection in females favors monomorphic spawning phenologies that maximize net fertilization success and offspring survival across environmental conditions, whereas selection in males often favors polymorphic phenologies that are primarily shaped by sperm competition. Our model helps explain several well-documented empirical observations in aquatic species, including high intraspecific variance of reproductive phenologies, sex-specific spawning phenologies, and spawning during environmentally suboptimal times.

Estimating monotonic rates from biological data using local linear regression.

Accessing many fundamental questions in biology begins with empirical estimation of simple monotonic rates of underlying biological processes. Across a variety of disciplines, ranging from physiology to biogeochemistry, these rates are routinely estimated from non-linear and noisy time series data using linear regression and ad hoc manual truncation of non-linearities. Here, we introduce the R package LoLinR, a flexible toolkit to implement local linear regression techniques to objectively and reproducibly estimate monotonic biological rates from non-linear time series data, and demonstrate possible applications using metabolic rate data. LoLinR provides methods to easily and reliably estimate monotonic rates from time series data in a way that is statistically robust, facilitates reproducible research and is applicable to a wide variety of research disciplines in the biological sciences.

Making sense of recent models of the "sheltering" hypothesis for recombination arrest between sex chromosomes.

In their most extreme form, sex chromosomes exhibit a complete lack of genetic recombination along much of their length in the heterogametic sex. Some recent models explain the evolution of such suppressed recombination by the "sheltering" of deleterious mutations by chromosomal inversions that prevent recombination around a polymorphic locus controlling sex. This sheltering hypothesis is based on the following reasoning. An inversion that is associated with the male-determining allele (with male heterogamety) is present only in the heterozygous state. If such an inversion carries a lower-than-average number of deleterious mutations, it will accrue a selective advantage, and will be sheltered from homozygosity for any mutations that it carries due to the enforced heterozygosity for the inversion itself. It can therefore become fixed among all carriers of the male-determining allele. Recent population genetics models of this process are discussed. It is shown that, except under the unlikely scenario of a high degree of recessivity of most deleterious mutations, inversions of this type that lack any other fitness effects will have at best a modest selective advantage; they will usually accumulate on proto-Y chromosomes at a rate close to, or less than, the neutral expectation. While the existence of deleterious mutations does not necessarily prevent the spread of Y-linked inversions, it is unlikely to provide a significant selective advantage to them.

Consequences of partially recessive deleterious genetic variation for the evolution of inversions suppressing recombination between sex chromosomes1.

The evolution of suppressed recombination between sex chromosomes is widely hypothesized to be driven by sexually antagonistic selection (SA), where tighter linkage between the sex-determining gene(s) and nearby SA loci is favored when it couples male-beneficial alleles to the proto-Y chromosome, and female-beneficial alleles to the proto-X. Although difficult to test empirically, the SA selection hypothesis overshadows several alternatives, including an incomplete but often-repeated "sheltering" hypothesis which suggests that expansion of the sex-linked region (SLR) reduces the homozygous expression of deleterious mutations at selected loci. Here, we use population genetic models to evaluate the consequences of partially recessive deleterious mutational variation for the evolution of otherwise neutral chromosomal inversions expanding the SLR on proto-Y chromosomes. Both autosomal and SLR-expanding inversions face a race against time: lightly-loaded inversions are initially beneficial, but eventually become deleterious as they accumulate new mutations, after which their chances of fixing become negligible. In contrast, initially unloaded inversions eventually become neutral as their deleterious load reaches the same equilibrium as non-inverted haplotypes. Despite the differences in inheritance and indirect selection, SLR-expanding inversions exhibit similar evolutionary dynamics to autosomal inversions over many biologically plausible parameter conditions. Differences emerge when the population average mutation load is quite high; in this case large autosomal inversions that are lucky enough to be mutation-free can rise to intermediate to high frequencies where selection in homozygotes becomes important (Y-linked inversions never appear as homozygous karyotypes); conditions requiring either high mutation rates, highly recessive deleterious mutations, weak selection, or a combination thereof.

The evolution of suppressed recombination between sex chromosomes and the lengths of evolutionary strata.

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.

Why is measuring and predicting fitness under genomic conflict so hard?

Genomic conflict between the sexes is caused by differences in the optimal male and female reproductive strategies, and is a major contributor to genetic, phenotypic, and life history variation. While early experimental work appeared to strongly support the sexual conflict paradigm, recent work has produced more ambiguous results. Recent advances in experimental evolution studies combined with theoretical arguments can shed light on why measuring fitness under a conflict is so challenging, including the incidental alteration of mating dynamics, demographic effects, and inherent complexity in what quantity selection maximizes. We stress that non-intuitive results do not necessarily mean the absence of conflict, and follow-up experiments to determine why a priori predictions failed can ultimately teach us more than if they had been confirmed.

Consequences of partially recessive deleterious genetic variation for the evolution of inversions suppressing recombination between sex chromosomes.

The evolution of suppressed recombination between sex chromosomes is widely hypothesized to be driven by sexually antagonistic selection (SA), where tighter linkage between the sex-determining gene(s) and nearby SA loci is favored when it couples male-beneficial alleles to the proto-Y chromosome, and female-beneficial alleles to the proto-X. Despite limited empirical evidence, the SA selection hypothesis overshadows several alternatives, including an incomplete but often-repeated "sheltering hypothesis" that suggests that expansion of the sex-linked region (SLR) reduces homozygous expression of partially recessive deleterious mutations at selected loci. Here, we use population genetic models to evaluate the consequences of deleterious mutational variation for the evolution of neutral chromosomal inversions expanding the SLR on proto-Y chromosomes. We find that SLR-expanding inversions face a race against time: lightly loaded inversions are initially beneficial, but eventually become deleterious as they accumulate new mutations, and must fix before this window of opportunity closes. The outcome of this race is strongly influenced by inversion size, the mutation rate, and the dominance coefficient of deleterious mutations. Yet, small inversions have elevated fixation probabilities relative to neutral expectations for biologically plausible parameter values. Our results demonstrate that deleterious genetic variation can plausibly drive recombination suppression in small steps and would be most consistent with empirical patterns of small evolutionary strata or gradual recombination arrest.

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics.

Sexually antagonistic (SA) genetic variation-in which alleles favored in one sex are disfavored in the other-is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research-including F ST and F IS statistics, genome-wide association studies, pedigree analyses, reciprocal transplant studies, and evolve-and-resequence experiments-to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex F ST and F IS, including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS, along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.

Long-term effects of predator arrival timing on prey community succession.

The stochastic arrival of competing species and their subsequent interactions have been highlighted as principal forces underlying biotic historical effects in community assembly. However, despite the widely recognized effect of predation on prey communities, the effects that the stochastic arrival of predators may have on assembling communities are poorly understood. We used a microbial microcosm experiment to investigate whether the timing of predator arrival to a prey community undergoing naturalistic succession affected species abundances and community diversity. Predator arrival timing affected the long-term abundance of a prey species that was persistent throughout succession in the absence of predators. Our data indicate that this timing effect occurred indirectly via transient interactions between early-successional prey species and predators. Specifically, we suggest that transient early-successional prey species served as a springboard for early-arriving (but not late-arriving) predators, allowing the exploiting predators to increase their abundances and subsequently alter long-term community dynamics. These results show that the history of predator arrival can have lasting consequences for community structure in ecological succession.

The interaction between sex-specific selection and local adaptation in species without separate sexes.

Local adaptation in hermaphrodite species can be based on a variety of fitness components, including survival, as well as both female and male sex-functions within individuals. When selection via female and male fitness components varies spatially (e.g. due to environmental heterogeneity), local adaptation will depend, in part, on variation in selection through each fitness component, and the extent to which genetic trade-offs between sex-functions maintain genetic variation necessary for adaptation. Local adaptation will also depend on the hermaphrodite mating system because self-fertilization alters several key factors influencing selection and the maintenance of genetic variance underlying trade-offs between the sex-functions (sexually antagonistic polymorphism). As a first step to guide intuition regarding sex-specific adaptation in hermaphrodites, we develop a simple theoretical model incorporating the essential features of hermaphrodite mating and adaptation in a spatially heterogeneous environment, and explore the interaction between sex-specific selection, self-fertilization and local adaptation. Our results suggest that opportunities for sex-specific local adaptation in hermaphrodites depend strongly on the extent of self-fertilization and inbreeding depression. Using our model as a conceptual framework, we provide a broad overview of the literature on sex-specific selection and local adaptation in hermaphroditic plants and animals, emphasizing promising future directions in light of our theoretical predictions.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Local adaptation and the evolution of inversions on sex chromosomes and autosomes.

Spatially varying selection with gene flow can favour the evolution of inversions that bind locally adapted alleles together, facilitate local adaptation and ultimately drive genomic divergence between species. Several studies have shown that the rates of spread and establishment of new inversions capturing locally adaptive alleles depend on a suite of evolutionary factors, including the strength of selection for local adaptation, rates of gene flow and recombination, and the deleterious mutation load carried by inversions. Because the balance of these factors is expected to differ between X (or Z) chromosomes and autosomes, opportunities for inversion evolution are likely to systematically differ between these genomic regions, though such scenarios have not been formally modelled. Here, we consider the evolutionary dynamics of X-linked and autosomal inversions in populations evolving at a balance between migration and local selection. We identify three factors that lead to asymmetric rates of X-linked and autosome inversion establishment: (1) sex-biased migration, (2) dominance of locally adapted alleles and (3) chromosome-specific deleterious mutation loads. This theory predicts an elevated rate of fixation, and depressed opportunities for polymorphism, for X-linked inversions. Our survey of data on the genomic distribution of polymorphic and fixed inversions supports both theoretical predictions.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Consequences of genetic linkage for the maintenance of sexually antagonistic polymorphism in hermaphrodites.

When selection differs between males and females, pleiotropic effects among genes expressed by both sexes can result in sexually antagonistic selection (SA), where beneficial alleles for one sex are deleterious for the other. For hermaphrodites, alleles with opposing fitness effects through each sex function represent analogous genetic constraints on fitness. Recent theory based on single-locus models predicts that the maintenance of SA genetic variation should be greatly reduced in partially selfing populations. However, selfing also reduces the effective rate of recombination, which should facilitate selection on linked allelic combinations and expand opportunities for balancing selection in a multilocus context. Here, I develop a two-locus model of SA selection for simultaneous hermaphrodites, and explore the joint influence of linkage, self-fertilization, and dominance on the maintainance of SA polymorphism. I find that the effective reduction in recombination caused by selfing significantly expands the parameter space where SA polymorphism can be maintained relative to single-locus models. In particular, linkage facilitates the invasion of male-beneficial alleles, partially compensating for the "female-bias" in the net direction of selection created by selfing. I discuss the implications of accounting for linkage among SA loci for the maintenance of SA genetic variation and mixed mating systems in hermaphrodites.