Sex determination mode does not affect body or genital development of the central bearded dragon (Pogona vitticeps)

Abstract

BackgroundThe development of male- or female-specific phenotypes in squamates is typically controlled by either temperature-dependent sex determination (TSD) or chromosome-based genetic sex determination (GSD). However, while sex determination is a major switch in individual phenotypic development, it is unknownhow evolutionary transitions between GSD and TSD might impact on the evolution of squamate phenotypes, particularly the fast-evolving and diverse genitalia. Here, we take the unique opportunity of studying the impact of both sex determination mechanisms on the embryological development of the central bearded dragon (Pogona vitticeps). This is possible because of the transitional sex determination system of this species, in which genetically male individuals reverse sex at high incubation temperatures. This can trigger the evolutionary transition of GSD to TSD in a single generation, making P. vitticeps an ideal model organism for comparing the effects of both sex determination processes in the same species.ResultsWe conducted four incubation experiments on 265 P. vitticeps eggs, covering two temperature regimes (“normal” at 28 °C and “sex reversing” at 36 °C) and the two maternal sexual genotypes (concordant ZW females or sex-reversed ZZ females). From this, we provide the first detailed staging system for the species, with a focus on genital and limb development. This was augmented by a new sex chromosome identification methodology for P. vitticeps that is non-destructive to the embryo. We found a strong correlation between embryo age and embryo stage. Aside from faster growth in 36 °C treatments, body and external genital development was entirely unperturbed by temperature, sex reversal or maternal sexual genotype. Unexpectedly, all females developed hemipenes (the genital phenotype of adult male P. vitticeps), which regress close to hatching.ConclusionsThe tight correlation between embryo age and embryo stage allows the precise targeting of specific developmental periods in the emerging field of molecular research on P. vitticeps. The stability of genital development in all treatments suggests that the two sex-determining mechanisms have little impact on genital evolution, despite their known role in triggering genital development. Hemipenis retention in developing female P. vitticeps, together with frequent occurrences of hemipenis-like structures during development in other squamate species, raises the possibility of a bias towards hemipenis formation in the ancestral developmental programme for squamate genitalia.Electronic supplementary materialThe online version of this article (10.1186/s13227-017-0087-5) contains supplementary material, which is available to authorized users.

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

“…However, L. lugubris exhibit deviations from the other three gecko‐specific character states. Paired hemiphallic bulges of L. lugubris appear at stage 32, which is later than the gecko P. picta , the same timing as some pleurodonts, acrodonts, and gymnophthalmids, but earlier than anguimorphs, and later than other pleurodonts and lacertids . All three podial elements appear in the forelimbs at L. lugubris stage 32, which matches the timing of most geckos, gymnophthalmids, lacertids, some acrodonts, and anguimorphs, but is earlier than other acrodonts and pleurodonts, and later than other pleurodonts.…”

“…Paired hemiphallic bulges of L. lugubris appear at stage 32, which is later than the gecko P. picta, the same timing as some pleurodonts, acrodonts, and gymnophthalmids, but earlier than anguimorphs, and later than other pleurodonts and lacertids. 6,50,60,85,[87][88][89][90] All three podial elements appear in the forelimbs at L. lugubris stage 32, which matches the timing of most geckos, gymnophthalmids, lacertids, some acrodonts, and anguimorphs, but is earlier than other acrodonts and pleurodonts, and later than other pleurodonts. Finally, fusion of the facial primordia occurs at stage 33 which is the same timing as other geckos, some acrodonts, and anguimorphs, but earlier than lacertids, other acrodonts, and pleurodonts, and later than gymnophthalmids.…”

Reproductive phenotype predicts adult bite‐force performance in sex‐reversed dragons (Pogona vitticeps)

“…As adults, sex‐reversed ZZf individuals lay more eggs than their ZWf counterparts (Holleley et al, 2015). However, individuals of the two female groups can only be identified with certainty using genetic/chromosomal data (Whiteley et al, 2017). To date, potential differences in whole‐organism performance characteristics among sexual phenotypes have not been examined.…”

The effects of thermal stress on the early development of the lizard Anolis sagrei

“…Later stages, where embryonic growth is the primary process taking place, tend to be more robust to environmental perturbation. Strikingly, the homologous and critically important stages of morphogenesis occur when many lizard and snake eggs are laid and parental care ceases (Andrews & Mathies, ; Noro, Uejima, Abe, Manabe, & Tamura, ; Sanger, Losos, & Gibson‐Brown, ; Whiteley et al., ). This raises new concerns as to whether reptilian morphogenesis is as sensitive to thermal stress as observed in other vertebrate species.…”