Sex chromosome turnovers and genetic drift: a simulation study

Abstract

The recent advances of new genomic technologies have enabled the identification and characterization of sex chromosomes in an increasing number of nonmodel species, revealing that many plants and animals undergo frequent sex chromosome turnovers. What evolutionary forces drive these turnovers remains poorly understood, but it was recently proposed that drift might play a more important role than generally assumed. We analysed the dynamics of different types of turnovers using individual-based simulations and show that when mediated by genetic drift, turnovers are usually easier to achieve than substitutions at neutral markers, but that their dynamics and relative likelihoods vary with the type of the resident and emergent sex chromosome system (XY and/or ZW) and the dominance relationships among the sex-determining factors. Focusing on turnovers driven by epistatically dominant mutations, we find that drift-mediated turnovers that preserve the heterogamety pattern are 2-4× more likely than those along which the heterogametic sex changes. This ratio nevertheless decreases along with effective population size and can even reverse in case of extreme polygyny. This can be attributed to a 'drift-induced' selective force, known to influence transitions between male and female heterogamety, but which according to our study does not affect turnovers that preserve the heterogametic sex.

How to identify sex chromosomes and their turnover

“…Indeed, several studies have recently provided important insight into the dynamics and drivers of turnover (Blackmon & Demuth, ; Jeffries et al, ; Kitano & Peichel, ). A large body of theoretical work outlines predictions for when and why sex chromosome transitions occur (Bachtrog et al, ; Beukeboom & Perrin, ), under the hypotheses of genetic drift (Bull & Charnov, ; Saunders et al, ), accumulation of deleterious mutation on the sex‐limited chromosomes (Blaser et al, , ), selection on sex ratio (Jaenike, ; Werren & Beukeboom, ) and sexually antagonistic selection (van Doorn & Kirkpatrick, , ). Here, we highlight key predictions for each of the hypotheses to motivate future sex chromosome research.…”

“…First, drift‐induced sex chromosome transitions that maintain patterns of heterogamety are predicted to be 2–4 times more likely than those which reverse heterogamety when the invading sex determining locus is dominant; however, this ratio is influenced by effective population size and mating system. This is because transitions that preserve heterogamety involve fixation of the ancestral X or Z chromosome, which have a higher frequency in the population, while transitions reversing heterogamety require fixation of the ancestral Y or W (Saunders et al, ). Comparative studies across independently evolved sex chromosomes offer the potential to test this directly, provided that the sampling resolution is sufficient and the identity of sex chromosome pairs is known.…”

“…Despite the growing awareness that sex chromosomes have evolved independently many times throughout eukaryotes, our understanding of the processes driving the formation and turnover of new sex chromosome systems is limited and many unanswered questions remain. A large body of theoretical work outlines predictions for when and why sex chromosome transitions occur (Beukeboom & Perrin, ), including genetic drift (Bull & Charnov, ; Saunders, Neuenschwander, & Perrin, ), mutation load on the sex‐limited chromosomes (Blaser, Grossen, Neuenschwander, & Perrin, ; Blaser, Neuenschwander, & Perrin, ), selection on sex ratio (Jaenike, ; Werren & Beukeboom, ) and sexually antagonistic selection (van Doorn & Kirkpatrick, , ), yet attempts to empirically test these have been restricted to a few clades (Blackmon & Demuth, ; Jeffries et al, ; Kitano & Peichel, ; Wright et al, ). Identifying the evolutionary and genomic mechanisms predicted to drive sex chromosome turnover is a major priority, which in turn will shed light on why sex determination is labile in some taxa and not in others.…”

A rapid rate of sex-chromosome turnover and non-random transitions in true frogs

“…A turnover can occur if the existing sex-locus is translocated to an autosome 22 , 23 , or if a new gene acquires the sex-determining role via mutation 24 , 25 . The subsequent fixation of the new sex chromosome is thought to be mediated by one (or a combination) of four main evolutionary forces 26 , namely (i) genetic drift 27 – 29 ; (ii) sex-ratio selection, induced by sex biases arising, e.g., from meiotic-drive elements or endoparasites 30 – 32 ; (iii) sexually antagonistic selection on a gene linked to the new sex determiner 24 , 33 ; and (iv) deleterious mutation load accumulating on the non-recombining Y or W chromosome 34 , 35 .…”

Impact of deleterious mutations, sexually antagonistic selection and mode of recombination suppression on transitions between male and female heterogamety

“…Nevertheless, neutral turnovers that maintain the system of heterogamety ( e . g ., XY to a new XY system) are 2-4 times more likely to occur than the former (except under extremely low N e ; Saunders et al 2018). One reason is that an XY to XY turnover requires the fixation of the ancestral X chromosome as an autosome, while an XY to ZW turnover requires the fixation of the ancestral Y.…”