Environmental sex reversal or selection for sex chromosome lability?
Sex determination in fishes appears to be regulated along a continuum of genetic and environmental factors (Heule, Salzburger, & Böhne, 2014) and experiments involving hormone treatments or temperature shock can induce sex-reversal in some species (Devlin & Nagahama, 2002). Thus, environmental factors stimulating production of steroid hormones could influence genetic sex (Nakamura, 2010). Hatchery data for some percichthyids suggest a possibility of temperature- and/or hormone-driven sex-ratio biases (Ingram et al., 2012; Lyon et al., 2012). Our data support sex-reversal in Macquarie perch: a homozygous YY genotype for the XY-gametologous region in one male (male 2 on Fig. 1) suggests the existence of XY females, also supported by phenotypic females with Y-alleles and putatively lower fertilization rates. In addition, the XX genotype in another male for the sexing region, but not the other XY-gametologous SNP (male 19 on Fig. 1) could be explained by recombination between X and Y chromosomes in a XY female ancestor (simultaneous reverse mutation at seven loci being unlikely). Environmental variation overriding genetic sex can promote sex chromosome turnover (Baroiller et al., 2009) and induce shifts between XY and ZW systems (Holleley et al., 2015). Indeed, the prevalence in golden perch of SNPs with female-specific alleles, despite XY sex determination inferred from karyology (Shams et al., 2019), suggests ancestral transitions between ZW and XY systems, or even possible co-existence of XY and ZW systems in this species, as inferred for other fishes (Nguyen et al., 2021).
Alternatively, intraspecific polymorphism for sex-determining loci could be present in Macquarie perch, as observed in some tilapia species (Tao et al., 2021). Unstable environments, where one sex can become locally extinct by drift or maladaptation, can promote sex-chromosome turnover. Different sex-determination systems can evolve rapidly in populations of the same species in response to loss of sex chromosomes by drift. For example, natural populations of zebrafish have a monogenic ZW sex-determination system, whereas polygenic sex-determination systems of different laboratory strains have been inferred (Anderson et al., 2012; Bradley et al., 2011; Liew et al., 2012), thought to have evolved de novo after loss of W-alleles by unmasking latent pre-existing environmental sex-determination mechanisms or polygenic sex-determination (Wilson et al., 2014). In Macquarie perch, which breeds in shallow running waters and may experience extreme conditions during prolonged droughts or after catastrophic fires, frequent sex-chromosome turnover could prevent local extinctions. Weaker selection on sex chromosome lability in the golden perch and Murray cod, which occur in more stable and connected lowland river systems, can partially explain the apparently older age of the sex chromosomes of these percichthyids.