Explaining sex beyond TSD
If Mighty Males is correct, then sex determination occurs because of the effect of the environment on phenotypic quality. Temperature just happens to be a pervasive agent in the environment that has a profound influence on phenotype. But if sex determination occurs because of environmental effects on phenotypic quality, then it seems possible that environmental factors other than temperature should affect sex in TSD species. Or, other environmental factors might at least modify how temperature affects sex, ultimately ensuring that high-quality phenotypes are linked to male production. In fact, there is good evidence that factors other than temperature affect sex ratios in “TSD” species. A strength of Mighty Males is that it can explain multiple forms of ESD operating within a “TSD” group or population.
In two TSD species of turtle (Trachemys and Graptemys ), incubation of turtle eggs under low O2 and/or high CO2 concentrations simultaneously increases mortality (suggesting negative phenotypic effects) and results in a dramatic overproduction of females (Etchberger et al. 2002). This suggests multiple ESD mechanisms in the same species, and the finding is ecologically relevant as elevated CO2 and depressed O2 concentrations can occur naturally in turtle nests through embryonic and microbial respiration, coupled with low gas exchange with the surface e.g., under wet conditions (Ackerman 1980; Ackerman & Lott 2004). If we accept that Mighty Males acts through phenotypic quality and not necessarily temperature alone, then the overproduction of females in low O2 environments is not surprising, given the low phenotypic quality of individuals that likely arise from stressful and oxygen deprived environments. As another example, moisture in wild reptile nests affects fitness-related traits, with moist nests tending to produce larger and more robust offspring (reviewed by Packard 1999). Experimental addition of water to turtle embryos during the thermosensitive period results in male-biased sex ratios (LeBlanc & Wibbels 2009; Lolavar & Wyneken 2017), suggesting that moisture affects both phenotype and sex in some turtle species, but not all turtle species (Paukstis et al. 1984; Packard et al. 1989), in the direction predicted by Mighty Males. More generally, a multiplicity of ESD mechanisms is not unexpected under Mighty Males, and the possibility of multiple ESD mechanisms under TSD should be investigated more broadly (Warner et al. 2017).
Finally, in addition to accommodating multiple forms of ESD operating within ‘TSD” species, Mighty Males can also explain forms of TSD that are sensitive to the maternal environment. For example, Maternal effects on TPiv occur in at least two MF species of freshwater turtle, where embryos incubated at the population TPiv are more likely to develop into females when eggs are laid late in the season, compared to eggs laid early in the season. Thus a decline in TPiv across the season is inferred, which is observed under constant conditions in the lab, and this decline affects the sex ratio under fluctuating temperatures in the field (Bowden et al. 2000; Carter et al. 2017). Hormonal differences provide a proximate reason for the greater propensity of embryos to become female as the season progresses, but no ultimate reason has been proposed (Bowden et al. 2000). Life-history theory and a variety of data suggest that individuals in low condition nest later in reproductive season (Rowe et al. 1994), laying fewer eggs that are relatively poorly provisioned (Harms et al.2005). In turtles, for instance, relatively young females nest late in the season, and their offspring have lower survival than offspring of the same size that are produced by older females (Paitz et al.2007; Rollinson & Brooks 2008). Female quality may be the ultimate driver of changes TPiv across the reproductive season, with an overproduction of females reflecting the low-quality offspring produced by mothers in relatively poor condition (Trivers & Willard 1973). Notably, this would not be the first example of maternal effects modifying the extent of TSD in a reptile (Radder et al. 2009), but it is one that involves modification of intraspecific TSD patterns by maternal effects in a manner potentially consistent with Mighty Males.