The FM and FMF patterns in squamates and the tuatara
Several elegant studies have shown that squamates can exhibit intraspecific differences in sex determining mechanisms, specifically in GSD vs TSD (Pen et al. 2010; Holleley et al. 2015). The ecology and evolution of TSD may therefore be more complex in squamates than in turtles and crocodilians, but I nevertheless believe that Mighty Males can provide insight in to TSD in squamate reptiles. The biggest challenge is to reconcile Mighty Males with the occurrence of the FM pattern in squamates and the tuatara. This is because FM is inconsistent with the assumption that warm temperatures produce low-quality phenotypes.
There are several reasons that the MF does not undermine the Mighty Males hypothesis. The first reason is that the FM pattern is extremely rare (Mitchell et al. 2006), and arguably, FM may not even exist. A majority of TSD species originally described as FM have subsequently been recategorized as FMF when a wider range of incubation temperatures were tested (Lang & Andrews 1994; Godfrey et al. 2003). The recategorization is extensive, and may even include Agama agama(Steele et al. 2018), the species that gave rise to the study of TSD in the first place. In fact, I am only aware of one species, the tuatara, where evidence of FM has been recently defended (Mitchellet al. 2006); unfortunately, the conservation status of the tuatara makes further investigation difficult. Future investigation of FM in squamates may therefore uncover evidence of FMF, such that the Mighty Males hypothesis its various predictions can be explored.
Assuming the FM pattern is real but very rare, then the adaptive explanation for TSD in the tuatara and squamates may be different than in turtles and crocodilians. In other words, Mighty Males (FMF, and MF) would apply to turtles, crocodilians, and other explanations for TSD would apply to FM squamates and the tuatara. Existing explanations for TSD in short-lived FM squamates and short-lived FM fish rely on the timing of reproduction, where females are produced under cool temperatures early in the growing season so that growth and hence fecundity is maximized during a short life cycle (e.g., Conover 1984; Warner & Shine 2005; Pen et al. 2010). Such a mechanism is very unlikely in turtles or crocodilians because of late age at maturity and incredible variation in growth rates (Armstrong et al. 2017; Congdon et al. 2018). Divergent adaptive explanations for TSD could arise if TSD evolved independently in different reptile lineages. Notably, the tuatara and squamates are sister groups (Rest et al.2003), whereas turtles and Archosaurs, which includes crocodilians, comprise a different sister group (Crawford et al. 2012). An intriguing possibility, therefore, is that the ancestor of turtles and crocodilians exhibited TSD, whereas the ancestor of squamates exhibited GSD, such that TSD evolved only recently in the tuatara and a few squamate lineages. Different adaptive explanations for TSD might then become likely in these different groups. One study supports the notion of divergent ancestral sex-determining mechanisms in major reptile clades (Janzen & Krenz 2004), but more recent evidence suggests that TSD is ancestral in all reptile groups, and that GSD is derived (Pokorná & Kratochvíl 2009; Gamble et al. 2015; Sabath et al.2016). This second explanation for the FM pattern, then, seems to depend on transitions to GSD followed by reversions to TSD in squamates; there is currently no evidence for this (see also Holleley et al.2015), but we know that sex determining mechanism are, at least, highly labile in some reptiles (Gamble et al. 2015). Alternatively, millions of years of independent evolution of TSD in turtles and crocodilians vs squamates and the tuatara may have plausibly resulted in differences in the adaptive function of TSD, even if TSD is ancestral to both groups.
I emphasize that it is only the rare FM pattern that is difficult to reconcile with Mighty Males, whereas the FMF pattern observed in most lizards can and should be explored under the lens of Mighty Males. For instance, the leopard gecko (Eublepharis macularius ) features an FMF pattern, although males and females are produced over a broader range of temperature than in many other species, allowing temperature and sex to be decoupled without hormonal manipulation. Females have a determinate clutch size of two eggs, and female fitness is not very sensitive to temperature. Males experience high intra-sex aggression, presumably allowing them to secure mating opportunities, and consistent with Mighty Males, males produced at intermediate incubation temperature win significantly more aggressive encounters (reviewed by Rhen & Crews 2001). Similarly, lifetime reproductive success for an FMF lizard,A. muricatus , was greatest for males produced at intermediate temperatures, as opposed to sex-reversed males produced under high and low temperatures, whereas performance of naturally-produced females was inconsistent across years (Warner & Shine 2008b). This provides some evidence that male-producing temperatures provide the greatest lifetime reproductive success, at least for males. In sum, in both of these FMF squamate examples, fitness interacts with temperature and sex in a manner that is broadly consistent with Mighty Males, underlining that the explanatory scope of Mighty Males is not necessarily limited to turtles and crocodilians.