Sex Chromosome Turnovers in Evolution

Abstract

Animals and plants display a remarkable diversity in the way they determine sex. This implies that changes in the mode of sex determination occur over evolutionary time. Changes that involve a modification of the identity of sex chromosomes are called sex chromosome turnovers, and are caused by the spread of a mutant gene with sex‐determining properties or the translocation of the ancestral sex determiner to a new genomic location. Through both empirical and theoretical studies, the mysteries surrounding the proximate and ultimate mechanisms responsible for turnovers, and their consequences on sex chromosome evolution, are gradually being unravelled. Nevertheless, many questions surrounding these evolutionary transitions remain unanswered: Why do turnover rates vary across taxa? What are the driving evolutionary forces? Why do certain types of transitions seem more common than others? Key Concepts In many species with separate sexes, sex is determined genetically by a single gene, located on the sex chromosomes. A sex chromosome turnover is a change in the identity of the sex chromosomes, resulting from a change in identity and/or location of the sex‐determining gene. The study of sex chromosome turnovers in evolution has been driven mainly by theoretical work, but empirical studies are gradually catching up. Different types of turnovers have been described, which have contrasting consequences for sex determination. Rates of transitions vary dramatically across taxa: they are rare in some taxa and very frequent in others. Many evolutionary mechanisms have been proposed as potential drivers of turnovers, but their relative implication and importance is still poorly understood. Certain types of transitions seem more frequent than others, and some lineages experiencing frequent turnovers show nonrandom transitions.

Sex chromosome turnover in African annual killifishes of the genus Nothobranchius

“…In Nothobranchius , the turnover rate may have been facilitated by their often small effective population sizes (Bartáková et al 2013; Cui et al 2019; van der Merwe et al 2021). This is consistent with the action of both genetic drift and mutation load model, (Blaser et al 2014; Saunders et al 2018) and also with the maintenance of male heterogamety (Jeffries et al 2018; Saunders 2019).…”

“…Several hypotheses on mechanisms and forces driving sex chromosome turnover and its fixation have been put forward (Saunders 2019; Vicoso 2019) and they may be applied also on the specific situation of sex chromosome-autosome fusions (Pennell et al 2015; Kitano et al 2024). One possible trigger may be selection on the newly created linkage disequillibrium between sex chromosome and autosomal addition, which might resolve sexual conflict (Charlesworth & Charlesworth 1980; van Doorn & Kirkpatrick 2007; Kitano et al 2009; Matsumoto & Kitano 2016).…”

“…The pace of differentiation and degeneration is not always well correlated with the evolutionary age of a given sex chromosome system (Zhou et al 2014; Charlesworth 2021; Kuhl et al 2021). One of the processes, which can restart sex chromosome differentiation, is sex chromosome turnover, i. e. replacement of ancestral sex chromosome system by a new one (Saunders 2019; Vicoso 2019; Meisel 2020).…”

Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges

“…This could be owing to the high plasticity of fish sex chromosomes and their frequent turnovers, which repeatedly reset the process of sex chromosome differentiation. This further facilitates the self-enforcing loop between low degeneration and successive turnovers [9,14,[21][22][23].…”

Homeology of sex chromosomes in Amazonian Harttia armored catfishes supports the X-fission hypothesis for the X1X2Y sex chromosome system origin

“…The majority of these systems show little genetic differentiation 8,11,12 and are therefore prone to frequent sex chromosome turnovers 7,[13][14][15] . These properties make teleost sex chromosomes a well-suited model for studying early phases of sex chromosome differentiation 16,17 and causes and consequences of sex chromosome turnovers (whereby the newly evolved system replaces the former one) 15,18,19 , and the bearing of sex chromosome evolution to the establishment of reproductive barriers between incipient species [20][21][22] .The study of sex chromosomes has undergone a remarkable transformation in recent years as genome sequencing, assembly and scaffolding techniques rapidly improved. Despite these advances, several unique biological features of sex chromosomes are still hardly tractable by computational tools, or their analysis requires multiple integrated methodologies and/or large number of individuals to be analyzed 18,23 .…”