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.