Selfish X chromosomes and speciation

Abstract

In two papers published at about the same time almost thirty years ago, Frank (Evolution, 45, 1991a, 262) and Hurst and Pomiankowski (Genetics, 128, 1991, 841) independently suggested that divergence of meiotic drive systems-comprising genes that cheat meiosis and genes that suppress this cheating-might provide a general explanation for Haldane's rule and the large X-effect in interspecific hybrids. Although at the time, the idea was met with skepticism and a conspicuous absence of empirical support, the tide has since turned. Some of the clearest mechanistic explanations we have for hybrid male sterility involve meiotic drive systems, and several other cases of hybrid sterility are suggestive of a role for meiotic drive. In this article, I review these ideas and their descendants and catalog the current evidence for the meiotic drive model of speciation. In addition, I suggest that meiotic drive is not the only intragenomic conflict to involve the X chromosome and contribute to hybrid incompatibility. Sexually and parentally antagonistic selection pressures can also pit the X chromosome and autosomes against each other. The resulting intragenomic conflicts should lead to co-evolution within populations and divergence between them, thus increasing the likelihood of incompatibilities in hybrids. I provide a sketch of these ideas and interpret some empirical patterns in the light of these additional X-autosome conflicts.

Introduction: Sex chromosomes and speciation

“…Selfish genetic elements that compete for transmission provide an alternative explanation for the role of sex chromosomes in reproductive isolation. Patten () reviews the history of a model focused on meiotic drive (postsegregational bias, strictly speaking) that was initially dismissed but has recently gained traction. Because X and Y chromosomes do not recombine with one another, they are susceptible to the evolution of multilocus drive systems—involving, for example, separate drive, target and modifier loci—which can in turn trigger evolutionary arms races.…”

“…The resulting co‐evolutionary arms race can lead to the build‐up of otherwise cryptic (suppressed) drive systems within species that become unmasked in hybrids, where incompatible combinations of alleles reduce fertility. Patten () summarizes the growing empirical evidence for this model (including discoveries of cryptic X‐linked drivers that also cause incompatibility in hybrids) while emphasizing the contribution of the X to speciation via other forms of intragenomic conflict (including sexual and parental antagonism). Building on this theme, O'Neill and O'Neill () discuss the myriad ways selfish evolution of the sex chromosomes compromises genomic stability.…”

“…Selfish genetic elements that compete for transmission provide an alternative explanation for the role of sex chromosomes in reproductive isolation. Patten (2018) reviews the history of a model focused on meiotic drive (postsegregational bias, strictly speaking) that was initially dismissed but has recently gained traction.…”

Sexual antagonism leads to a mosaic of X‐autosome conflict

“…Mosaic sex bias along the X is interesting because X‐autosome conflict potentially plays a role in disease (Frank and Crespi ), in speciation (Crespi and Nosil ), and in genomic evolution (Patten ). With regard to the specific genetic assumptions, X‐autosome conflict depends in interesting ways on the variability among loci in dominance and the relation between ploidy level and the contribution of each allele to phenotypic value.…”

Editorial 2019

“…A personal essay from Jerry Coyne (Coyne, 2018) in this issue gives an historical sketch of his seminal contribution to the field as well as some insightful discussion on the leading hypotheses to explain the pattern. The rest of the issue is a healthy mix of theory (e.g., Charlesworth, Campos, & Jackson, 2018;Ghenu, Blanckaert, Butlin, Kulmuni, & Bank, 2018;Patten, 2018), review (Cutter, 2018;Irwin, 2018;O'Neill & O'Neill, 2018;Presgraves, 2018), methods development (Steinrücken, Spence, Kamm, Wieczorek, & Song, 2018) and empirical papers, some focusing on comparing patterns of differentiation and gene flow between incipient species at autosomes and sex chromosomes (Van Belleghem et al, 2018;Moran et al, 2018;Steinrücken et al, 2018), others looking at sequence and expression evolution of sex-linked genes (Filatov, 2018;Llopart, 2018), some mapping the genomic architecture of reproductive isolation (Liu & Karrenberg, 2018) or even using comparative phylogenetic approaches (Pennell, Mank, & Peichel, 2018). Of significance, the issue included systems that have not been studied very commonly in this context such as plants (Filatov, 2018;Liu & Karrenberg, 2018) and worms (Cutter, 2018).…”