As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug-of-war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex-specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex-specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole-genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra- and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex-specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a “conflict over shared genes.”
The evolution of sexual dimorphism is constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location, and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identify approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D . melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D . melanogaster distribution range and in their sister species D . simulans , indicating widespread and evolutionarily persistent (about 1 million years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.
Evolutionary conflict between the sexes can induce arms races in which males evolve traits that are detrimental to the fitness of their female partners, and vice versa. This interlocus sexual conflict (IRSC) has been proposed as a cause of perpetual intersexual antagonistic coevolution with wide-ranging evolutionary consequences. However, theory suggests that the scope for perpetual coevolution is limited, if traits involved in IRSC are subject to pleiotropic constraints. Here, we consider a biologically plausible form of pleiotropy that has hitherto been ignored in treatments of IRSC and arrive at drastically different conclusions. Our analysis is based on a quantitative genetic model of sexual conflict, in which genes controlling IRSC traits have side effects in the other sex, due to incompletely sex-limited gene expression. As a result, the genes are exposed to intralocus sexual conflict (IASC), a tug-of-war between opposing male-and female-specific selection pressures. We find that the interaction between the two forms of sexual conflict has contrasting effects on antagonistic coevolution: Pleiotropic constraints stabilize the dynamics of arms races if the mating traits are close to evolutionary equilibrium but can prevent populations from ever reaching such a state. Instead, the sexes are drawn into a continuous cycle of arms races, causing the buildup of IASC, alternated by phases of IASC resolution that trigger the next arms race. These results encourage an integrative perspective on the biology of sexual conflict and generally caution against relying exclusively on equilibrium stability analysis.sexual conflict | arms race | intersexual additive genetic correlation | sex-differential expression | pleiotropy
The breeding and non-breeding ‘castes’ of eusocial insects provide a striking example of role-specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long-lived egg-layers, while workers are short-lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter-caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this ‘intralocus caste antagonism’ should be the maintenance of genetic variation for fitness and maladaptation within castes (termed ‘caste load’), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three-way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.
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