Abstract
Despite decades of cytogenetic and genomic research of dynamic sex chromosome evolution in teleost fishes, multiple sex chromosomes have been largely neglected. In this review, we compiled available data on teleost multiple sex chromosomes, identified major trends in their evolution and suggest further trajectories in their investigation. In a compiled dataset of 440 verified records of fish sex chromosomes, we counted 75 multiple sex chromosome systems with 60 estimated independent origins. We showed that male-heterogametic systems created by Y-autosome fusion predominate and that multiple sex chromosomes are over-represented in the order Perciformes. We documented a striking difference in patterns of differentiation of sex chromosomes between male and female heterogamety and hypothesize that faster W sex chromosome differentiation may constrain sex chromosome turnover in female-heterogametic systems. We also found no significant association between the mechanism of multiple sex chromosome formation and percentage of uni-armed chromosomes in teleost karyotypes. Last but not least, we hypothesized that interaction between fish populations, which differ in their sex chromosomes, can drive the evolution of multiple sex chromosomes in fishes. This underlines the importance of broader inter-population sampling in studies of fish sex chromosomes.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)’.
Highlights
The classical model of sex chromosome evolution posits that they evolved from a pair of autosomes that acquired a sex-determining factor
We showed that male-heterogametic systems created by Y-autosome fusion predominate and that multiple sex chromosomes are over-represented in the order Perciformes
In our dataset with teleost species, abundance of multiple sex chromosome systems originated by rearrangements of Y chromosomes (50 out of 54 of independent origins; electronic supplementary material, Appendix S1– Appendix figure 1 and table S7), which is never involved in female meiosis, and scarcity of X–A (n = 2) and Z–A (n = 1) fusions makes any formal analysis of the effect of meiotic drive on fish multiple sex chromosome formation impossible
Summary
The classical model of sex chromosome evolution posits that they evolved from a pair of autosomes that acquired a sex-determining factor. In lineages with old and highly degenerate sex chromosomes e.g. mammals and some birds [4,42,43], little can be learned about the factors and mechanisms behind suppressed recombination and sequence divergence between the sex chromosomes, the investigation of younger autosomal additions to sex chromosomes is vital for this type of study [44,45] In fishes, both standard and multiple sex chromosomes often display a low degree of differentiation [8,9]. Multiple sex chromosomes can be detected by light microscopy as they usually result in different chromosome numbers between sexes [35] and one sex chromosome often notably differs in size and/or morphology This facilitates more thorough sex chromosome investigations in particular teleost groups, as is the case with sticklebacks (Gasterosteidae), which represent the most comprehensively studied teleost taxon concerning the evolution and differentiation of multiple sex chromosomes. This has been largely untapped with the exception of two recent reviews compiling information on multiple sex chromosomes in fishes [29,41]
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