Developmental asynchrony and antagonism of sex determination pathways in a lizard with temperature-induced sex reversal

Abstract

Vertebrate sex differentiation follows a conserved suite of developmental events: the bipotential gonads differentiate and shortly thereafter sex specific traits become dimorphic. However, this may not apply to squamates, a diverse vertebrate lineage comprising of many species with thermosensitive sexual development. Of the three species with data on the relative timing of gonad differentiation and genital dimorphism, the females of two (Niveoscincus ocellatus and Barisia imbricata) exhibit a phase of temporary pseudohermaphroditism or TPH (gonads have differentiated well before genital dimorphism). We report a third example of TPH in Pogona vitticeps, an agamid with temperature-induced male to female sex reversal. These findings suggest that for female squamates, genital and gonad development may not be closely synchronised, so that TPH may be common. We further observed a high frequency of ovotestes, a usually rare gonadal phenotype characterised by a mix of male and female structures, exclusively associated with temperature-induced sex reversal. We propose that ovotestes are evidence of a period of antagonism between male and female sex-determining pathways during sex reversal. Female sexual development in squamates is considerably more complex than has been appreciated, providing numerous avenues for future exploration of the genetic and hormonal cues that govern sexual development.

Embryonic development of a parthenogenetic vertebrate, the mourning gecko (Lepidodactylus lugubris)

“…In the lizard Anolis carolinensis and Anguis fragilis , paired phalluses develop in both sexes; however, hemipenes are large in males and hemiclitores are small in females . However, other lizards, such as Pogona vitticeps and Barisia imbricata , have female embryos with large, hemipenis‐like organs that are equal in size and shape with males, that subsequently regress prior to and just after hatching, respectively . Our results, coupled with results from the recent literature, make it clear that many aspects of squamate sexual development warrant more detailed examination.…”

“…64,81,82 However, other lizards, such as Pogona vitticeps and Barisia imbricata, have female embryos with large, hemipenis-like organs that are equal in size and shape with males, that subsequently regress prior to and just after hatching, respectively. 65,83 Our results, coupled with results from the recent literature, make it clear that many aspects of squamate sexual development warrant more detailed examination. Further investigation of external genital development in L. lugubris will be discussed in-detail separately.…”

“…The hemiphallic bulges are more bulbous than the previous stage (Figure J). These bulges exhibit morphology more similar to developing hemipenes than hemiclitores in other squamates and will be henceforth be referred to as hemipenes …”

“…These bulges exhibit morphology more similar to developing hemipenes than hemiclitores in other squamates and will be henceforth be referred to as hemipenes. 64,65 Stage 35 ( Figure 4K,L) Mean SVL: 12.21 mm (sd = 0.69, n = 2). Neural: The areas of the brain adjacent to the optic tectum are relatively larger ( Figure 4K).…”

Identification of Y chromosome markers in the eastern three-lined skink (Bassiana duperreyi) using in-silico whole genome subtraction.

“…This suggests that, all populations retain the ancestral state and that our makers are likely to have broad applicability across the entire species range. The identification of sex-specific sequence has important practical value in many contexts, including ecological studies [62][63][64], conservation of threatened or endangered species [65][66][67][68], captive breeding [69], aquaculture [70,71], elimination of mortality as a possible explanation for sex ratio bias [32,72] sex forensics [73] and identifying genotypic sex [32,74,75] or in studies of early developmental processes where sex of the developing embryo is important [76,77].…”