Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Abstract

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

Keywords: evolution; sex chromosomes; sex determination; vertebrates.

Figure 1.

Canonical scenario of sex chromosome evolution. (1)—ancestral autosomes; (2)—emergence of a sex-determining gene (yellow); (3)—accumulation of sexually antagonistic/advantageous alleles (blue, pink) and/or deleterious recessive alleles (orange); (4)—cessation of recombination, depicted by a pericentromeric inversion changing the chromosome shape from metacentric to acrocentric as one potential example; (5)—degeneration of sex-specific (Y or W) chromosomes, i.e. accumulation of deleterious mutations, gene loss and accumulation of repeats and heterochromatin; (6)—loss of the entire sex-specific sex chromosome. For simplification, only the heterogametic sex is depicted.

Figure 2.

Overview of the steps in sex chromosome evolution with empirical support in vertebrates. This hypothetical network of evolutionary trajectories may branch off to potentially endless outcomes with a possibility to freeze for a long time and even reverse to certain states. Steps (1–6) are the same as in figure 1 but sexually antagonistic genes are not necessarily involved and can be replaced here by general sex-linked genes; (7)—switch to hermaphroditism or ESD, where no sex chromosomes are present; (8)—long-term evolution without emergence of sex chromosomes; (9)—long-term persistence of poorly differentiated sex chromosomes; (10)—reversal to stages with less differentiated sex chromosomes; (11)—expansion of repeats on sex-specific sex chromosome causing its change in size; (12)—accumulation of repeats on both sex chromosomes; (13)—fusion of the sex chromosomes with an autosome leading to expansion of the pseudoautosomal region; (14)—emergence of a new sex-determining locus on another chromosome; (15)—emergence of a new sex-determining locus within existing sex chromosomes; (16a,b)—two translocations of the same sex-determining locus to other chromosomes; (17)—origin of a new system of sex determination by involvement of B chromosome; (18)—emergence of sex-determining systems with three homologous sex chromosomes; (19)—fusion of sex chromosomes with an autosome leading to multiple neo-sex chromosomes; (20)—introgression of a sex-determining gene from a different population or species; (21)—allopolyploidization connected with emergence of a new sex-determining system in a genome of hybrid-origin. For simplification, only the heterogametic sex is depicted.