Discussion
Oviparous and viviparous squamates are sympatric mainly in tropical and
subtropical regions. In these regions, climate warming should cause
maternal energy budgets of viviparous species to increase, but those of
oviparous species to decrease because of the increment of oviparous
reproductive frequency (Fig. 5). Although the offspring survival is
predicted to increase in both oviparous and viviparous species, the
anticipated increment in oviparous species is small in subtropical
regions (Fig. 6). Accordingly, climate warming will benefit viviparous
species, but likely lead to negative balance of energy in oviparous
species, suggesting oviparous squamates may be more vulnerable to
climate warming than viviparous species in the broad sympatric zone of
these species.
For oviparous species in most subtropical regions (except for east
coast), climate warming enhances reproductive output by increasing
clutch numbers (Fig. 3b), but decreases embryonic developmental success
(Fig. 4a, b), and leave little time for late-hatching offspring to grow
before hibernation (Fig. S1). More specifically, under climate warming,
oviparous females in most subtropical regions produce additional
clutches because they keep producing new clutches late in the year
(around July) (Fig. 6e, f). However, these females fail to provide
developmental temperatures that are high enough to ensure developmental
success in late reproductive season (Ma et al. 2018). In
addition, those late hatchlings may not have enough time before
hibernation for energy accumulation to survive the severe winter, and
therefore have low survivorship (Sun et al. 2018). These negative
impacts on embryos and hatchings will undoubtedly decrease offspring
survival, which reduce the reproductive efficiency of oviparous
squamates in the subtropical region (i.e. they reproduce more but have
fewer surviving offspring).
The reduction of maternal energy budgets for oviparous species under the
scenario of climate warming largely results from the increased number of
clutches per year (Fig. 5e). Longer activity seasons under warming
enable oviparous mothers to produce more clutches, which is in
accordance with the facts that nearly half of oviparous species produce
multiple clutches per year (see our analysis in the methods) (Mesquitaet al. 2016), and experimental warming can increase clutch
numbers in oviparous squamates (Du et al. 2005; Lu et al.2018). It is noteworthy that our analysis assumes that food availability
is unlimited for females. If females face food constraints under
warming, the negative balance of energy would be even more severe
(Raymond B. Huey & Joel G. Kingsolver 2019). Of course, this negative
balance can be partly offset by maternal decision on energy allocation,
if females select to allocate a constant fraction of assimilated energy
to reproduction (Meiri et al. 2012), or dynamically allocate
resources to reproduction according to environmental conditions and
individual state (Senner et al. 2015). Accordingly, the oviparous
species may be able to enhance their own fitness by reducing
reproductive frequency and therefore reproductive investment.
Previous studies predict that species in cold regions are more
vulnerable to climate warming than oviparous species in warm regions.
This “cul-de-sac” hypothesis states progressively warming climates are
driving viviparous reptile extinction (Sinervo et al. 2010; Jaraet al. 2019). This prediction is based on the cold climate
hypothesis of viviparity evolution, which suggests that the evolution of
viviparity has facilitated the radiation of reptiles into cold climates
(Shine & Bull 1979). Thus warming climates will favor oviparous
species. Extending this previous understanding, our study suggests that
oviparous species are more vulnerable than viviparous species in the
tropics and subtropics, where both modes are sympatric. The
vulnerability of oviparous species is not only due to negative balance
of maternal energy budget, but also due to their increment in maternal
reproductive investment that does not yield a corresponding increment in
offspring survival. Even at high elevations in tropical and subtropical
zones (e.g. Mexican Plateau and Colorado Plateau), maternal energy
budgets increase for oviparous and viviparous species (Fig. 5b, d), but
offspring survival increases only for viviparous species (not for
oviparous species) (Fig. 6b, d). These results are contrary to the
“cul-de-sac” hypothesis (Pincheira-Donoso et al. 2013).
Instead, our results are consistent with the maternal manipulation
hypothesis of viviparity evolution (Shine 1995), which suggests that the
evolution of viviparity has improved the fitness of reptiles not only in
cold regions but also in other conditions where gravid females are able
to maintain body temperatures different from those available in external
nests (e.g. hot regions and fluctuating environments). Accordingly, we
may expect that viviparity enables species to tolerate climate warming
(with higher and more variable temperatures) and outcompete oviparous
reproduction. This explanation fits well with the observation that
viviparity has been a successful strategy among reptiles in warm
climates (Packard et al. 1977).
Our analysis focused on the energy budget of mothers and offspring, but
did not consider the role of the phenotypic plasticity and evolutionary
adaptation of physiological and life-history traits that could occur
among species and populations across latitudes and elevations (Sundayet al. 2019). In addition, our study did not take species
interactions into account, which may also affect the vulnerability of
species to climate warming. For example, the competition between
sympatric oviparous and viviparous squamates and/or the food web of
squamate-insect-plant may be affected by climate warming, and in turn
determine species vulnerability. Unfortunately, those above-mentioned
physiological, ecological and evolutionary parameters are currently
unavailable for the majority of species, which hampers their inclusion
in mechanistic models. Despite these caveats, both our models –
biophysical and life-history models – are the first to reveal that
oviparous squamates are more vulnerable to climate warming than are
oviparous species where both modes are sympatric. This finding suggests
that enhanced conservation effort should be directed to oviparous
squamates in tropical and subtropical zones. Our results may be relevant
to other taxa (e.g., insects, amphibians) that have both viviparous and
oviparous modes.