Sex chromosome repeats tip the balance towards speciation

Abstract

Because sex chromosomes, by definition, carry genes that determine sex, mutations that alter their structural and functional stability can have immediate consequences for the individual by reducing fertility, but also for a species by altering the sex ratio. Moreover, the sex-specific segregation patterns of heteromorphic sex chromosomes make them havens for selfish genetic elements that not only create suboptimal sex ratios but can also foster sexual antagonism. Compensatory mutations to mitigate antagonism or return sex ratios to a Fisherian optimum can create hybrid incompatibility and establish reproductive barriers leading to species divergence. The destabilizing influence of these selfish elements is often manifest within populations as copy number variants (CNVs) in satellite repeats and transposable elements (TE) or as CNVs involving sex-determining genes, or genes essential to fertility and sex chromosome dosage compensation. This review catalogs several examples of well-studied sex chromosome CNVs in Drosophilids and mammals that underlie instances of meiotic drive, hybrid incompatibility and disruptions to sex differentiation and sex chromosome dosage compensation. While it is difficult to pinpoint a direct cause/effect relationship between these sex chromosome CNVs and speciation, it is easy to see how their effects in creating imbalances between the sexes, and the compensatory mutations to restore balance, can lead to lineage splitting and species formation.

Consequence of Paradigm Shift with Repeat Landscapes in Reptiles: Powerful Facilitators of Chromosomal Rearrangements for Diversity and Evolution

“…The ancient tuatara, all crocodilians, a majority of turtles, and some lizards show TSD [8,180,181], whereas most snakes, many lizards, and some turtles exhibit GSD, and a continuum of differentiation between homomorphic and heteromorphic sex chromosomes within taxa is observed [14,182]. Heteromorphic sex chromosomes show accumulation of satellites and amplification of microsatellites or telomeric repeats on Y or W sex chromosomes in many reptilian species and other amniotes [20,45,[183][184][185]. In some reptiles the sex chromosome contains no significant enrichment of repeats [185], whereas minimally differentiated XY chromosomes are observed in three cryptodiran turtles (Staurotypus crassicollis, S. triporcatus, and S. salvinii), in which the Y chromosomes are smaller than the X chromosomes owing to a difference in the copy number of 18S-28S rRNA genes [26,118].…”

Introduction: Sex chromosomes and speciation

“…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. Focusing on mammals, the authors describe several examples of rapidly diversifying copy number variants in repetitive DNAs on the sex chromosomes that could contribute to reproductive isolation.…”

What is Speciation Genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species

“…The effects of CNVs on speciation can also be indirect. Recently a study of several genera found that CNVs on sex chromosomes were responsible for rapid changes to the sex ratio (O'Neill & O'Neill, 2018). These changes happen very quickly, making them responsible for the development of hybrid incompatibilities if two populations are in allopatry, ultimately leading to speciation.…”