Sex chromosome evolution: The classical paradigm and so much beyond

TL;DR

This review explores the diversity and complexity of sex chromosome evolution, challenging traditional models by highlighting lineage-specific mechanisms, the non-inevitability of degeneration, and the uncertain role of sexually antagonistic selection.

Contribution

It provides a comprehensive overview of alternative pathways and mechanisms in sex chromosome evolution, emphasizing the diversity beyond the canonical model.

Findings

Many lineages experience sex chromosome turnovers.

Homomorphic sex chromosomes can persist over long periods.

Size expansion of sex chromosomes can occur without degeneration.

Abstract

Sex chromosomes have independently evolved in species with separate sexes in most lineages across the tree of life. However, the well-accepted canonical model of sex chromosome evolution is not universally supported. There is no single trajectory for sex chromosome formation and evolution across the tree of life, suggesting the underlying mechanisms and evolutionary forces are diverse and lineage specific. We review the diversity of sex chromosome systems, describe the canonical model of sex chromosome evolution, and summarize studies challenging various aspects of this model. They include evidence that many lineages experience frequent sex chromosome turnovers or maintain homomorphic sex chromosomes over long periods of time, suggesting sex chromosome degeneration is not inevitable. Sometimes the sex-limited Y/W chromosomes expand before they contract in size. Both transposable elements and gene gains could contribute to this size expansion, which further challenges gene loss being the hallmark of sex chromosome degeneration. Finally, empirical support for the role of sexually antagonistic selection as a driver of recombination suppression on sex chromosomes remains elusive. We summarize models that result in loss of recombination without invoking sexually antagonistic selection, which have not been empirically verified yet, and suggest future avenues for sex chromosome research.