Polygenic response of sex chromosomes to sexual antagonism.

Sexual antagonism occurs when males and females differ in their phenotypic fitness optima but are constrained in their evolution to these optima because of their shared genome. The sex chromosomes, which have distinct evolutionary "interests" relative to the autosomes, are theorized to play an important role in sexually antagonistic conflict. However, the evolutionary responses of sex chromosomes and autosomes have usually been considered independently, that is, via contrasting the response of a gene located on either an X chromosome or an autosome. Here, we study the coevolutionary response of the X chromosome and autosomes to sexually antagonistic selection acting on a polygenic phenotype. We model a phenotype initially under stabilizing selection around a single optimum, followed by a sudden divergence of the male and female optima. We find that, in the absence of dosage compensation, the X chromosome promotes evolution toward the female optimum, inducing coevolutionary male-biased responses on the autosomes. Dosage compensation obscures the female-biased interests of the X, causing it to contribute equally to male and female phenotypic change. We further demonstrate that fluctuations in an adaptive landscape can generate prolonged intragenomic conflict and accentuate the differential responses of the X and autosomes to this conflict.

Recombination and selection against introgressed DNA.

Introgressed DNA is often deleterious at many loci in the recipient species' genome, and is therefore purged by selection. Here, we use mathematical modeling and whole-genome simulations to study the influence of recombination on this process. We find that aggregate recombination controls the genome-wide rate of purging in the early generations after admixture, when purging is most rapid. Aggregate recombination is influenced by the number of chromosomes and heterogeneity in their size, and by the number of crossovers and their locations along chromosomes. A comparative prediction is that species with fewer chromosomes should purge introgressed ancestry more profoundly, and should therefore exhibit weaker genomic signals of historical introgression. Turning to within-genome patterns, we show that, in species with autosomal recombination in both sexes, more purging is expected on sex chromosomes than autosomes, all else equal. The opposite prediction holds for species without autosomal recombination in the heterogametic sex. Finally, positive correlations between recombination rate and introgressed ancestry have recently been observed within the genomes of several species. We show that these correlations are likely driven not by recombination's effect in unlinking neutral from deleterious introgressed alleles, but by recombination's effect on the rate of purging of deleterious introgressed alleles themselves.

Assortative mating enhances postzygotic barriers to gene flow via ancestry bundling.

Hybridization and subsequent genetic introgression are now known to be common features of the histories of many species, including our own. Following hybridization, selection often purges introgressed DNA genome-wide. While assortative mating can limit hybridization in the first place, it is also known to play an important role in postzygotic selection against hybrids and, thus, the purging of introgressed DNA. However, this role is usually thought of as a direct one: a tendency for mates to be conspecific reduces the sexual fitness of hybrids, reducing the transmission of introgressed ancestry. Here, we explore a second, indirect role of assortative mating as a postzygotic barrier to gene flow. Under assortative mating, parents covary in their ancestry, causing ancestry to be "bundled" in their offspring and later generations. This bundling effect increases ancestry variance in the population, enhancing the efficiency with which postzygotic selection purges introgressed DNA. Using whole-genome simulations, we show that the bundling effect can comprise a substantial portion of mate choice's overall effect as a postzygotic barrier to gene flow. We then derive a simple method for estimating the impact of the bundling effect from standard metrics of assortative mating. Applying this method to data from a diverse set of hybrid zones, we find that the bundling effect increases the purging of introgressed DNA by between 1.2-fold (in a baboon system with weak assortative mating) and 14-fold (in a swordtail system with strong assortative mating). Thus, assortative mating's bundling effect contributes substantially to the genetic isolation of species.

A new model of sex chromosome evolution.

A new model, based on the evolution of gene regulation, challenges the classical theory.

Dominance shifts increase the likelihood of soft selective sweeps.

Genetic models of adaptation to a new environment have typically assumed that the alleles involved maintain a constant fitness dominance across the old and new environments. However, theories of dominance suggest that this should often not be the case. Instead, the alleles involved should frequently shift from recessive deleterious in the old environment to dominant beneficial in the new environment. Here, we study the consequences of these expected dominance shifts for the genetics of adaptation to a new environment. We find that dominance shifts increase the likelihood that adaptation occurs from standing variation, and that multiple alleles from the standing variation are involved (a soft selective sweep). Furthermore, we find that expected dominance shifts increase the haplotypic diversity of selective sweeps, rendering soft sweeps more detectable in small genomic samples. In cases where an environmental change threatens the viability of the population, we show that expected dominance shifts of newly beneficial alleles increase the likelihood of evolutionary rescue and the number of alleles involved. Finally, we apply our results to a well-studied case of adaptation to a new environment: the evolution of pesticide resistance at the Ace locus in Drosophila melanogaster. We show that, under reasonable demographic assumptions, the expected dominance shift of resistant alleles causes soft sweeps to be the most frequent outcome in this case, with the primary source of these soft sweeps being the standing variation at the onset of pesticide use, rather than recurrent mutation thereafter.

Changes in selection pressure can facilitate hybridization during biological invasion in a Cuban lizard.

Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.

Variation in Genetic Relatedness Is Determined by the Aggregate Recombination Process.

The genomic proportion that two relatives share identically by descent-their genetic relatedness-can vary depending on the history of recombination and segregation in their pedigree. Previous calculations of the variance of genetic relatedness have defined genetic relatedness as the proportion of total genetic map length (cM) shared by relatives, and have neglected crossover interference and sex differences in recombination. Here, we consider genetic relatedness as the proportion of the total physical genome (bp) shared by relatives, and calculate its variance for general pedigree relationships, making no assumptions about the recombination process. For the relationships of grandparent-grandoffspring and siblings, the variance of genetic relatedness is a simple decreasing function of [Formula: see text], the average proportion of locus pairs that recombine in meiosis. For general pedigree relationships, the variance of genetic relatedness is a function of metrics analogous to [Formula: see text] Therefore, features of the aggregate recombination process that affect [Formula: see text] and analogs also affect variance in genetic relatedness. Such features include the number of chromosomes and heterogeneity in their size, the number of crossovers and their spatial organization along chromosomes, and sex differences in recombination. Our calculations help to explain several recent observations about variance in genetic relatedness, including that it is reduced by crossover interference (which is known to increase [Formula: see text]). Our methods further allow us to calculate the neutral variance of ancestry among F2s in a hybrid cross, enabling precise statistical inference in F2-based tests for various kinds of selection.

Unexpected reproductive fidelity in a polygynous frog.

Polygynous mating systems with group fidelity are a common animal organization, typically consisting of multiple females in a mated group with a single male for an extended period (sometimes referred to as harem polygyny). Single-male polygyny with reproductive fidelity occurs in invertebrates, bony fishes, and some tetrapods, such as lizards, mammals, and birds. In amphibians, reproductive fidelity in polygynous groups is not fully demonstrated. Combining data on larval development, molecular paternity assignment, and in situ behavioral observations, we reveal high fidelity during a prolonged breeding season in a Neotropical polygynous frog. Males dominate scarce breeding sites, guarding offspring, and mating exclusively with multiple females that exhibit dominance rank. This system likely evolved in response to intense competition for breeding sites and intrasexual competition for mates.

On the logic of Fisherian sexual selection.

In Fisher's model of sexual selection, a female preference for a male trait spreads together with the trait because their genetic bases become correlated. This can be interpreted as a "greenbeard" system: a preference gene, by inducing a female to mate with a trait-bearing male, favors itself because the male is disproportionately likely also to carry the preference gene. Here, we use this logic to argue that Fisherian sexual selection in diploids proceeds via two channels: (i) trait-bearing males are disproportionately the product of matings between preference-bearing mothers and trait-bearing fathers, and thus trait and preference genes are correlated "in trans"; (ii) trait and preference genes come into gametic phase disequilibrium, and thus are correlated "in cis." Gametic phase disequilibrium is generated by three distinct mechanisms that we identify. The trans channel does not operate when sexual selection is restricted to the haploid phase, and therefore represents a fundamental difference between haploid and diploid models of sexual selection. We show that the cis and trans channels contribute equally to the spread of the preference when recombination between the preference and trait loci is free, but that the trans channel is substantially more important when linkage is tight.

Mating preferences of selfish sex chromosomes.

The evolution of female mating preferences for harmful male traits is a central paradox of sexual selection1-9. Two dominant explanations for this paradox8,10 are Fisher's runaway process, which is based on genetic correlations between preference and trait1,3,4, and Zahavi's handicap principle, in which the trait is an honest costly signal of male quality2,6,8,11. However, both of these explanations require the exogenous initial spread of female preferences before harmful male traits can evolve1-4,6,8,11. Here I present a mechanism for the evolution of female mating preferences for harmful male traits that is based on the selfish evolutionary interests of sex chromosomes. I demonstrate that female-biased genetic elements-such as the W and X sex chromosomes-will evolve mating preferences for males who display traits that reduce their fitness and/or that of their male offspring, but increase fitness in female offspring. In particular, W-linked preferences can cause nearly lethal male traits to sweep to fixation. Sex-linked preferences can drive the evolution of traits such as ornamental handicaps and male parental care, and can explain variation in ornamentation and behaviour across taxa with divergent sex-determining mechanisms.

Sexual antagonism and the instability of environmental sex determination.

The sex of an organism can be determined by its genetics or its early environment. Across the animal kingdom, genetic sex determination (GSD) is far more common than environmental sex determination (ESD). Here, we propose an explanation for this pattern: the coupling of genes that bias offspring sex ratios towards one sex with genes that are beneficial in that sex but costly in the other. Gradual strengthening of the sex-specific tendency of this association eventuates in a neo-sex chromosome; that is, GSD. Our model predicts to which system of heterogamety ESD will evolve when nesting behaviour is an important determinant of brood sex ratios. It explains the puzzling observation in some GSD species of sex reversal induced by extreme environments. The model also suggests an approach to discovering sex-determining genes in ESD species.

Drift-Induced Selection Between Male and Female Heterogamety.

Evolutionary transitions between male and female heterogamety are common in both vertebrates and invertebrates. Theoretical studies of these transitions have found that, when all genotypes are equally fit, continuous paths of intermediate equilibria link the two sex chromosome systems. This observation has led to a belief that neutral evolution along these paths can drive transitions, and that arbitrarily small fitness differences among sex chromosome genotypes can determine the system to which evolution leads. Here, we study stochastic evolutionary dynamics along these equilibrium paths. We find non-neutrality, both in transitions retaining the ancestral pair of sex chromosomes, and in those creating a new pair. In fact, substitution rates are biased in favor of dominant sex determining chromosomes, which fix with higher probabilities than mutations of no effect. Using diffusion approximations, we show that this non-neutrality is a result of "drift-induced selection" operating at every point along the equilibrium paths: stochastic jumps off the paths return with, on average, a directional bias in favor of the dominant segregating sex chromosome. Our results offer a novel explanation for the observed preponderance of dominant sex determining genes, and hint that drift-induced selection may be a common force in standard population genetic systems.