Sex chromosome evolution: The remarkable diversity in the evolutionary rates and mechanisms

In this editorial letter, we summarize the current challenges in the field of sex chromosome evolution and introduce the 17 manuscripts which together provide insights into the diversity of sex chromosome evolutionary rates and mechanisms. Across the tree of life, many species with separate sexes have evolved sex chromosomes, on which (master) sexdetermining genes are located to determine the sex of an individual (Bachtrog et al., 2014; Beukeboom & Perrin, 2014). Sexlinked inheritance makes sex chromosomes a hotspot for sexspecific and sexual selection, and independently evolved sex chromosomes show convergent evolutionary and genomic characteristics (Ellison & Bachtrog, 2019; Furman et al., 2020; Hughes & Rozen, 2012; Ming et al., 2011). In different species across eukaryotes, sexlimited chromosomes (i.e. Y or W chromosomes) have evolved to exhibit a wide range of divergence from their homologous X or Z chromosomes (Ashman et al., 2014; Furman et al., 2020; Wright et al., 2016). The level of degeneration of sex chromosomes is highly lineagespecific. Mammals, most birds and insects, and several lineages of reptiles, amphibians and teleosts have highly degenerated Y or W chromosomes (i.e. a large proportion of gene loss, accumulation of repetitive sequences, enrichment of heterochromatin etc.). In contrast, sex chromosomes in many reptiles, fishes, amphibians and some dioecious angiosperm plants remain homomorphic (i.e. indistinguishable under the microscope) and little differentiated (i.e. both Z/X and W/Y chromosomes maintain a similar gene content), which is typically interpreted as representing early stages of sex chromosome evolution (Ashman et al., 2014; Bachtrog et al., 2014; Beukeboom & Perrin, 2014; Furman et al., 2020; Ma & Veltsos, 2021). Suppression of recombination can evolve to ensure that certain gene complexes are inherited together. The canonical model of sex chromosome evolution suggests that sexually antagonistic (SA) variants play an important role in recombination suppression and the following degeneration of sex chromosomes (Bachtrog, 2006; Bull, 1983; Charlesworth et al., 2005; Charlesworth & Crow, 1978; Fisher, 1931; Marais et al., 2005; Rice, 1987). Over time, the sexlimited chromosomes are predicted to lose many functional genes and degenerate substantially, due to a combination of evolutionary forces such as Muller's ratchet, genetic hitchhiking, reduced purifying selection and strong genetic drift (Charlesworth et al., 2005; Charlesworth & Crow, 1978; Rice, 1987). This model has been widely accepted and seems to imply a progressive degeneration of sex chromosomes with time (Furman et al., 2020; Graves, 2006; Griffin, 2012), and could account for the recombination suppression and degeneration of the highly differentiated sex chromosomes in mammals and most birds (Bachtrog, 2005; Cortez et al., 2014; Ohno, 2003; Zhou et al., 2014). In the past decade, studies of nonmodel organisms have begun to flourish due to the recent advances in genomewide sequencing methodologies, which have revealed a remarkable diversity in the rates of sex chromosome differentiation across the tree of life, as well as in the dynamics of birth and death of sex chromosomes (i.e. sex chromosome turnovers) in many fishes, amphibians and some reptiles (reviewed by Vicoso, 2019; Furman et al., 2020; Ma & Veltsos, 2021). Sequencing advancements have also made it possible to study sex chromosome evolution in wild populations, as well as in species with large genomes (i.e. >2G bp). The expansion of taxa with studied sex chromosomes has (perhaps unsurprisingly) provided results challenging the canonical model of sex chromosome evolution (see reviews from Ironside, 2010; Furman et al., 2020; Kratochvíl, Stöck, et al., 2021; Perrin, 2021), including: