Two transcriptionally distinct pathways drive female development in a reptile with both genetic and temperature dependent sex determination

Abstract

How temperature determines sex remains unknown. A recent hypothesis proposes that conserved cellular mechanisms (calcium and redox; CaRe status) sense temperature and identify genes and regulatory pathways likely to be involved in driving sexual development. We take advantage of the unique sex determining system of the model organism, Pogona vitticeps, to assess predictions of this hypothesis. P. vitticeps has ZZ male: ZW female sex chromosomes whose influence can be overridden in genetic males by high temperatures, causing male-to-female sex reversal. We compare a developmental transcriptome series of ZWf females and temperature sex reversed ZZf females. We demonstrate that early developmental cascades differ dramatically between genetically driven and thermally driven females, later converging to produce a common outcome (ovaries). We show that genes proposed as regulators of thermosensitive sex determination play a role in temperature sex reversal. Our study greatly advances the search for the mechanisms by which temperature determines sex.

Developmental dynamics of sex reprogramming by high incubation temperatures in a dragon lizard

“…GCA (grancalin) was also upregulated. Grancalin has previously been implicated in GSD female development in P. vitticeps , but the data here suggests a more generic role in reproduction that is not sex specific (8). The testes-like gonads displayed upregulation of a mix of both male and female related genes compared to the testes.…”

“…action of chromatin modifier genes) that influence the expression of sex genes (7). CaRe mechanisms have been implicated in the TSD cascades of several species (5), and most recently in the gene expression patterns associated with sex reversal in embryonic P. vitticeps (8). Four genes are consistently associated with sex reversal and TSD systems namely, JARID2, KDM6B, CIRBP and CLK4 (7–12).…”

Temperature-Induced Sex Reversal in Reptiles: Prevalence, Discovery, and Evolutionary Implications

“…How sex reversal occurs at a molecular level is currently not known, though it may involve temperature sensing through calcium and reactive oxygen species signalling in P. vitticeps [Weber and Capel, 2018;Castelli et al, 2020;Whiteley et al, 2021b]. While these ancient and ubiquitous environmental sensing mechanisms are very promising candidates for the transduction of an environmental signal to a sex determining signal, experimental demonstration is lacking [Castelli et al, 2020].…”

Epigenetic Regulation and Environmental Sex Determination in Cichlid Fishes

“…The study of sex reversal, whether artificially manipulated or natural, provides a valuable experimental system to address the role of sex-determining genes as well as molecular cascades in sex differentiation. While the temporal patterns of gene expression may differ dramatically between genetically and environmentally driven reversal, some of the specific genes and gene functions including epigenetic regulation are shared [e.g., bearded dragon: Whiteley et al, 2021]. A growing number of studies reveal epigenetic mechanisms by which environmental sex reversal can override the sexual fate determined by genetic factors [Ortega-Recalde et al, 2020].…”