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.