Thermal performance and the MF and FMF patterns
The Mighty Males hypothesis, if correct, stands to provide insight into
the evolution of thermal stress and thermal limits. This is because a
main prediction of the hypothesis is that parameters associated with TSD
(e.g., TPiv, the range of male-producing temperatures, etc) evolve so
that males are produced in thermal environments that impart relatively
high-quality phenotypes. Here, I summarize aspects of thermal
performance theory that are relevant to Mighty Males, as well as key
research on whether ecologically relevant incubation environments
regularly experience heat stress.
Thermal performance curves (TPCs) characterize the relationship between
performance and temperature (Huey & Stevenson 1979). Biochemical
constraints dictate that the shape of TPCs are typically Gaussian and
left skewed, and a key characteristic of TPCs is that they predict a
rapid decrease in performance at high temperature (Schoolfield et
al. 1981; Kingsolver 2009; Amarasekare & Johnson 2017). A consequences
of TPC asymmetry is that temperatures higher than the optimal
temperature for performance depress fitness more than an equivalent
temperature displacement below the optimal temperature (Martin & Huey
2008). Thermoregulatory behaviour should therefore evolve such that mean
body temperature is lower than the temperature that maximizes
performance, as organisms do not thermoregulate with perfect accuracy,
and overshooting the optimal temperature has relatively strong and
negative fitness consequences (Martin & Huey 2008). For reptiles with
TSD, capacity for embryonic thermoregulation exists (Ye et al.2019), but embryos cannot physically displace themselves, and so
thermoregulation is unlikely to result in widespread avoidance thermally
stressful environments (Telemeco et al. 2016). The key point here
is that avoidance of heat stress has a large influence on the evolution
of thermoregulation, such that avoidance of heat stress can be
considered evolutionarily important (Martin & Huey 2008). Given that
embryos cannot move, they are generally far more susceptible than adults
to the negative fitness consequences associated with heat stress.
There are many specific examples of how exposure to hot incubation
environments results in low-quality phenotypes, and through a variety of
pathways. For instance, exposure to extreme heat, but not extreme cold,
during natural incubation results in hatchling shell deformations in
wild Chyrsemys picta (‘extreme’ defined as ±2SD from grand mean
incubation temperature over two years), and the deformations themselves
seem to have negative fitness consequences (Telemeco et al.2013). Similarly, warm incubation temperatures supress the innate immune
response of hatchlings in two distantly related turtles species, whereas
cool temperatures enhance immune response (Freedberg et al. 2008;
Dang et al. 2015). It is also possible that elevated embryo
metabolism may not be matched by increased oxygen supply in reptiles
incubated at high temperatures (Hall & Warner 2019), such that negative
fitness consequences may arise in part through oxygen deprivation. As a
final example, high and constant incubation temperature is also
associated with small size at hatchling (Warner et al. in press; Packard
et al. 1987b , 1988; Janzen and Morjan 2002), likely because
temperature has stronger effect on development than on growth at all
life stages (Forster et al. 2011), and small size tends to be
associated with lower fitness in juveniles and adults (Rollinson & Rowe
2015; Armstrong et al. 2017). In sum, there are a variety of ways
in which hot environments can decrease phenotypic quality.
More generally, evidence of the stress imparted by high temperature
arises in the existence of heat-shock proteins (HSPs). HSPs are a
broadly conserved group of molecular chaperones designed to buffer the
impact of heat stress on phenotypes (Sørensen et al. 2003), for
which there is no known equivalent for cold stress (Sinclair & Roberts
2005). Both heat stress and/or the overexpression of heat-shock proteins
have subsequent deleterious and long-term effects on performance,
including development and survival, acting through a variety of
phenotypic pathways (Feder & Hofmann 1999; Kingsolver & Woods 2016).
Thus, one simple test of Mighty Males is to assess whether thermal
stress is more likely under female-producing conditions, by testing
whether the expression of heat shock proteins is positively associated
with female sex under environmentally relevant conditions. Critically,
testing this prediction should also be done in concert with exploring
the range of incubation temperatures in wild nests in order to estimate
environmentally-relevant temperatures. For instance, in some
populations, embryos of FMF populations rarely experiences temperatures
beyond the upper TPiv (e.g., Warner & Shine 2008a; Rollinson et
al. 2018); in other FMF populations, temperatures below the lower TPiv
are rare (Janzen 2008). Indeed, a broad spatial and temporal
characterization of incubation environments is necessary to estimate
environmentally relevant temperatures (e.g., Carter et al. 2018;
Francis et al. 2019).
Although heat stress is generally expected at high temperature,
embryonic thermal performance will ultimately adapt to the thermal
environment, such that ecological context is required understand thermal
stress and thermal limits. The Mighty Males hypothesis generates at
least two predictions will arise from local adaptations of embryos to
the thermal environment. The first deals specifically with FMF species.
The logic of the prediction arises from the theoretical expectation of a
trade-off between TPC height and breadth (Gilchrist 1995), such that in
seasonal environments, local adaptation of TPCs will result in
relatively platykurtotic TPCs centered on low mean temperatures (e.g.,
Fig. 4a,b). This reflects thermal adaptation to a relatively
unpredictable environment that features both seasonal variation in
thermal means, and pronounced diurnal thermal fluctuation of a magnitude
that varies seasonally (Amarasekare & Johnson 2017; Francis et
al. 2019). In other words, seasonality favours a form of TPC evolution
where individuals are relatively tolerant of, and adapted to, a wide
range of temperatures; hence “good” thermal environments for TSD
species feature a wide range of incubation temperatures. This prediction
is, therefore, that the range of male-producing temperatures will be
positively associated with the degree of temperature variation inherent
in the environment (Fig. 4a,b), or more specifically with the range of
incubation temperatures experienced by the average embryo. Indirect
support for this prediction is provided by Ewert et al. (2004), whose
data suggest that the range of male-producing temperatures was
positively associated with latitude in an FMF turtle across six
populations, as is generally expected under Mighty Males (Fig. 4c). A
quantitative test of this prediction is nevertheless warranted, as Ewert
et al. (2004) focus on latitude and not variance in the average
incubation environment. Unfortunately, it is not intuitive how thermal
adaption to seasonality would influence TSD parameters in MF species
under Mighty Males, precluding a similar prediction for MF species. In
any event, recent evidence suggests that TSD parameters are not strongly
related to latitude or longitude in at least one MF species (Carteret al. 2019a), although variance of incubation temperature was
not explored in this study.
The second prediction of Mighty Males under local adaptation to the
thermal environment is that females should suffer greater mortality than
males, especially at the egg and hatchling life stages. The logic is
that Mighty Males predicts TPiv to exhibit a correlated evolution with
thermal performance and thermal tolerance, specifically so that TPiv
marks the departure from favourable to unfavourable thermal environments
that impart low-quality phenotypes. The prediction may be difficult to
test at the adult stage, as viability selection on adults tends to be
relatively weak in nature in the first place (Kingsolver et al.2001, 2012), and females that are most strongly affected by thermal
stress will die either before hatching or shortly thereafter, leaving
females with relatively subtle phenotypic effects to survive until
adulthood. Indeed, the only study to my knowledge to examine survival
differences between the sexes of adult turtles found no difference
(Chaloupka & Limpus 2005). However, this prediction should be
straightforward to test at the egg and hatchling stage, where viability
selection tends to be stronger (Rollinson & Rowe 2015). The specific
expectation under constant incubation conditions is that fitness (e.g.,
embryonic survival) should depreciate relatively rapidly when embryos
are incubated above vs below (upper) TPiv. Under fluctuating thermal
conditions, a similar prediction for MF species is that fitness (e.g.,
survival or embryonic deformity rate) should be positively associated
with the extent of female-biased sex ratios. The recent publication of a
comprehensive database on phenotypic outcomes of reptilian incubation
will facilitate tests of this prediction (Noble et al. 2018b, a).