Sex determination, longevity, and the birth and death of reptilian species

Abstract

Vertebrate sex‐determining mechanisms (SDMs) are triggered by the genotype (GSD), by temperature (TSD), or occasionally, by both. The causes and consequences of SDM diversity remain enigmatic. Theory predicts SDM effects on species diversification, and life‐span effects on SDM evolutionary turnover. Yet, evidence is conflicting in clades with labile SDMs, such as reptiles. Here, we investigate whether SDM is associated with diversification in turtles and lizards, and whether alterative factors, such as lifespan's effect on transition rates, could explain the relative prevalence of SDMs in turtles and lizards (including and excluding snakes). We assembled a comprehensive dataset of SDM states for squamates and turtles and leveraged large phylogenies for these two groups. We found no evidence that SDMs affect turtle, squamate, or lizard diversification. However, SDM transition rates differ between groups. In lizards TSD‐to‐GSD surpass GSD‐to‐TSD transitions, explaining the predominance of GSD lizards in nature. SDM transitions are fewer in turtles and the rates are similar to each other (TSD‐to‐GSD equals GSD‐to‐TSD), which, coupled with TSD ancestry, could explain TSD's predominance in turtles. These contrasting patterns can be explained by differences in life history. Namely, our data support the notion that in general, shorter lizard lifespan renders TSD detrimental favoring GSD evolution in squamates, whereas turtle longevity permits TSD retention. Thus, based on the macro‐evolutionary evidence we uncovered, we hypothesize that turtles and lizards followed different evolutionary trajectories with respect to SDM, likely mediated by differences in lifespan. Combined, our findings revealed a complex evolutionary interplay between SDMs and life histories that warrants further research that should make use of expanded datasets on unexamined taxa to enable more conclusive analyses.

Transitions in sex determination and sex chromosomes across vertebrate species

“…Consistent with the hypothesis that species with ESD might have unequal sex ratios and therefore be prone to invasions by GSD to restore balanced sex ratios (Fisher, ), we find that transitions from ESD to GSD occur at higher rates than the reverse in both fish and squamates. Our results are also consistent with previous studies in squamates, which have also found that transitions from ESD to GSD are more common than the reverse (Gamble et al., ; Pokorná & Kratochvíl, ; Sabath, Itescu, et al., ). However, there is no difference in transition rates between ESD and GSD in turtles, possibly due to the longer lifespan of turtles (Sabath, Itescu, et al., ).…”

“…However, these results were equivocal as net diversification intervals in birds, which have heteromorphic sex chromosomes, are similar to those in turtles and crocodylians (Philips & Edmands, ). Indeed, other analyses have found no association between diversification rates and the presence of ESD or GSD in turtles, squamates or birds (Organ & Janes, ; Sabath, Itescu, et al., ). Thus, there is not strong evidence that the presence of heteromorphic sex chromosomes influences speciation rates in vertebrates.…”

“…As a result, we might expect a bias towards GSD systems. A recent analysis found mixed support for this hypothesis, with no differences in transition rates between GSD and ESD in turtles, but a higher rate of transition from ESD to GSD in squamate reptiles (Gamble et al., ; Pokorná & Kratochvíl, ; Sabath, Itescu, et al., ). However, the rates of transitions between GSD and ESD have not been tested in other suitable groups, such as fish.…”

Chromosomal Rearrangements during Turtle Evolution Altered the Synteny of Genes Involved in Vertebrate Sex Determination

“…Most turtles exhibit the ancestral TSD from which GSD evolved independently multiple times, sometimes as male-heterogametic (XX/XY) and other times as femaleheterogametic (ZZ/ZW) sex chromosome systems [Valenzuela and Adams, 2011;Bachtrog et al, 2014;Sabath et al, 2016]. Phylogenetic analyses vary in their estimate of the number of evolutionary transitions among sex-determining modes that are reconstructed in turtles [Valenzuela and Adams, 2011;Sabath et al, 2016].…”

“…Phylogenetic analyses vary in their estimate of the number of evolutionary transitions among sex-determining modes that are reconstructed in turtles [Valenzuela and Adams, 2011;Sabath et al, 2016]. Recent molecular evidence supports the scenario that 5 transitions from TSD to GSD and 2 reversals back to TSD from GSD occurred during turtle evolution [Valenzuela and Adams, 2011].…”