Sex chromosome evolution: historical insights and future perspectives

Abstract

Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology in sex chromosome evolution and new multilocus models of sex chromosome divergence.

The microevolutionary response to male-limited X-chromosome evolution inDrosophila melanogasterreflects macroevolutionary patterns

“…Sex chromosomes have long been of interest to researchers in evolution and genetics, due to their special mode of inheritance and association with sex determination (Abbott et al 2017). In XY systems, the X chromosome is expected to be feminized (enriched in female-biased genes compared to the autosomes) and/or demasculinized (impoverished for male-biased genes compared to the autosomes) because it spends two thirds of its time in females, compared to only half for autosomes.…”

“…Ellegren 2009, Wright et al 2015), due to the difficulty in constructing experimental tests of macroevolutionary patterns (although there are some exceptions; Dean et al 2012). Manipulative experiments testing predictions about sex chromosome evolution are therefore particularly valuable, since they make it possible to disentangle causal effects from stochastic effects (Kawecki et al 2012, Abbott et al 2017. We carried out a male-limited X chromosome evolution experiment in Drosophila melanogaster designed to integrate predictions from both sexual antagonism and sex chromosome evolution, where X chromosomes were passed from father to son for >40 generations, and never expressed in females.…”

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

“…Therefore, our results apply equally to cases of X‐to‐X or Z‐to‐Z hybrid incompatibilities (Lohse & Ross, ). Although haplodiploid systems do not include all of the unique evolutionary phenomena exhibited by sex chromosomes (Abbott et al., ), our results for haplodiploids are relevant for sex chromosomes. Our model predicts the long‐term evolution of a population under the simultaneous influence of heterozygote advantage and hybrid incompatibility and indicates the signatures that this type of fitness landscape could leave depending on whether it finds itself on an X chromosome or an autosome.…”

Multiple evidences suggest sox2 as the main driver of a young and complex sex determining ZW/ZZ system in turbot (Scophthalmus maximus)

“…We got a comprehensive picture of the complex mechanism underlying SD in this species and framed this information within teleost SD evolution. In particular, our work represents a contribution to the knowledge of the origin and evolution of "young sex chromosome pairs" (Charlesworth, 2019), still very unknown unlike the most studied mammalian, avian and Drosophila systems, which represent "old sex chromosomes" with specific genetic features: size heteromorphism, specialized gene content, reduced recombination and degeneration (Abbott et al, 2017).…”