Sex reversal triggers the rapid transition from genetic to temperature-dependent sex

Abstract

Sex determination in animals is amazingly plastic. Vertebrates display contrasting strategies ranging from complete genetic control of sex (genotypic sex determination) to environmentally determined sex (for example, temperature-dependent sex determination). Phylogenetic analyses suggest frequent evolutionary transitions between genotypic and temperature-dependent sex determination in environmentally sensitive lineages, including reptiles. These transitions are thought to involve a genotypic system becoming sensitive to temperature, with sex determined by gene-environment interactions. Most mechanistic models of transitions invoke a role for sex reversal. Sex reversal has not yet been demonstrated in nature for any amniote, although it occurs in fish and rarely in amphibians. Here we make the first report of reptile sex reversal in the wild, in the Australian bearded dragon (Pogona vitticeps), and use sex-reversed animals to experimentally induce a rapid transition from genotypic to temperature-dependent sex determination. Controlled mating of normal males to sex-reversed females produces viable and fertile offspring whose phenotypic sex is determined solely by temperature (temperature-dependent sex determination). The W sex chromosome is eliminated from this lineage in the first generation. The instantaneous creation of a lineage of ZZ temperature-sensitive animals reveals a novel, climate-induced pathway for the rapid transition between genetic and temperature-dependent sex determination, and adds to concern about adaptation to rapid global climate change.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…There are phylogenies of closely related agamid lizards that reveal at least four flip‐flops through genetic sex determination (GSD) and temperature sex determination (TSD), generating novel sex chromosomes 27. Some reptile species have sex chromosome systems that can be overridden by temperature 28, 29; these dual systems are extremely labile, able to change rapidly to TSD systems and even between ZW and XY 30, 31. Similar GSD‐TSD transitions may be common in some fish and may also facilitate changes in sex determination 32, 33, 34.…”

Mammalian X homolog acts as sex chromosome in lacertid lizards

“…Some authors recently argued that it was likely to be ESD (Pokorná and Kratochvíl, 2009;Johnson Pokorná and Kratochvíl, 2016), and that GSD, and hence sex chromosomes, evolved multiple times within this clade and remained notably stable after their emergence (Pokorná and Kratochvíl, 2009;Johnson Pokorná and Kratochvíl, 2016;Gamble et al, 2015). However, evolutionary transitions from GSD to ESD are theoretically possible and have been experimentally induced in a reptile in the laboratory (Quinn et al, 2007;Holleley et al, 2015). In any case, more robust testing of the hypotheses of the ancestral sex determination and on the evolution of sex-determining mechanisms in amniotes is largely precluded by our very limited knowledge about the homology of sex chromosomes and sex-determining genes among particular groups.…”

Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome

“…Sex chromosomes are heterozygous in males in XY/XX systems (male heterogamety) and in females in ZW/ZZ systems (female heterogamety) (1)(2)(3)(4). Despite their involvement in a fundamental developmental process that might be expected to be highly conserved, sex determination systems are highly variable and generally show a poor fit to phylogeny (5)(6)(7)(8). The remarkable lability of sex determination systems implies a complex evolutionary history of transitions between systems and the recurrent evolution of new sex chromosomes.…”