Introduction
Identifying organisms that are vulnerable to ongoing climate warming is
a challenging but critical task for ecologists and evolutionary
biologists. Ectothermic reptiles are highly dependent on environmental
temperature, and are thus extremely sensitive to climate warming (Hueyet al. 2012; Böhm et al. 2016). Squamate reptiles (lizards
and snakes) exhibit two reproductive modes: oviparity and viviparity.
Whether oviparous or viviparous species are more vulnerable to climate
warming is a long-standing puzzle. Explaining this puzzle is critical
for deriving conservation strategies (e.g. prioritizing species or zones
for conservation) as well as understanding how historical thermal
regimes have driven the transition between the two parity modes.
Although the evolutionary history and selective forces underlying the
two parity modes in squamate species have received extensive attention
(Shine 2014), few previous works have explored the sensitivity of
oviparous and viviparous species differ to climate warming (Sinervoet al. 2010; Jara et al. 2019). However, viviparous
species are thought to be more vulnerable to climate warming than
oviparous species for several reasons. First, viviparous species are
adaptively constrained to cold regions (high latitudes and elevations)
where climate warming is predicted to be more prominent (Tinkle &
Gibbons 1977; Pincheira-Donoso et al. 2013). Second, viviparous
species in cold regions have relatively low body temperatures and heat
tolerance, which constrains their activity as temperatures warm (Sinervoet al. 2010; Wang et al. 2017). This “cul-de-sac”
hypothesis gained supports from two studies that compared highland vs.
lowland lizards from Mexico and South America, because climate warming
shrinks the cold regions to which they have adapted and constrains their
activity more severely due to lower body temperatures (Sinervo et
al. 2010; Jara et al. 2019).
However, distributions of oviparous and viviparous squamates are
geographically widespread and often overlapping (Fig. 1). Specifically,
distributions of 90.7% of oviparous species (2146 in 2366 analyzed)
overlap with viviparous species, while distributions of 97.8%
viviparous species (541 in 553 analyzed) overlap with oviparous species
(see the methods). In addition, climate-driven range shifts may increase
overlap between the species with different parity modes, because
oviparous species’ suitable habitats shift to (currently) colder
regions, where viviparous species are occupying (Jara et al.2019). Obviously, a comparison between viviparous species from a cold
region and oviparous species from a warm region may not inform
warming-driven dynamics of the two modes where distributions overlap.
Moreover, understanding differential responses of sympatric oviparous
and viviparous species requires incorporating additional organismal
differences (e.g. on behavior, physiology and life history) that are
ecologically important (Kearney & Porter 2009). Oviparous and
viviparous squamates may be able to respond to warming in a similar
manner, including shifting thermoregulation behavior and body
temperature or by evolving shifted thermal performance curves (Yuanet al. 2016; Wang et al. 2017). Nonetheless, reproductive
life history (egg-laying vs. live-bearing), the only fundamental and
universal difference between the two parity modes, can respond to
climate warming differentially, and therefore should be the focus when
we compare differences between oviparous and viviparous species
(Blackburn 1993; Andrews 2000).
To answer how oviparous and viviparous species would differ in
responding to climate warming, we need an integrated consideration of
between-lineage differences in reproductive life history from maternal
investment to offspring survival. On one hand, oviparous mothers can
have more clutches per year than do viviparous mothers (Mesquitaet al. 2016), because they carry the embryos only for one third
of the embryonic development (Andrews & Mathies 2000). But on the other
hand, as viviparous mothers thermoregulate themselves, they actively
select developmental temperatures that differ from nest temperatures
(much longer than do oviparous mothers, which only hold the eggs for a
maximum of 1/3 of total embryonic development), substantially change
developmental time and increase embryonic survival (Shine 2004; Maet al. 2018). These differences in embryonic survival and the
time of hatching or birth, can furtherly lead to divergent number and
energy budgets of offspring, and therefore population growth between
species of the two parity modes (Buckley 2008; Levy et al.2016b). Moreover, the energetic costs of reproduction can also differ
between oviparous and viviparous females. In particular, oviparous
females spend relatively more energy on producing multiple clutches of
eggs (Landwer 1994), whereas viviparous females spend more energy during
prolonged gestation, because of large metabolic consumption when
carrying large embryos (Beuchat & Vleck 1990). These different
reproductive costs may shift differently under climate change,
influencing the total energy balance of a population, affecting energy
available for reproduction in the next year. In sum, climate warming may
have different effects on oviparous and viviparous squamates by
differentially affecting the reproductive timing, survival and energy
budgets of mothers as well as the survival and energy budgets of each
clutch/litter of offspring produced.
In this study, we used Sceloporus lizards in North America as a
model system to predict the impact of climate warming on oviparous and
viviparous squamates, because [1] this genus includes species of
both parity modes, [2] this region has the highest density of
sympatric squamates (including non-sceloporus species) of two
parity modes (Fig. 1), and [3] the physiology and life history
traits of these species are widely available (Table S1). We developed a
biophysical model that translates microclimates (hourly estimates for
1980-2000 versus 2080-2100) to operative temperatures, and simulates the
life history of lizards through thermoregulation, feeding (digestion),
reproduction and embryonic development. We used the model to estimate
yearly remaining energy after subtracting metabolic consumption and
energy content of all clutches/litters (of fresh eggs; only for
reproductive females) from energy intake of adults (termed “maternal
energy budget”) as well as total energy of surviving offspring (termed
“offspring survival”) under current and future climates (Fig. 2).
Because the energy budgets of individuals determine the survival and
reproductive potential in future (Iraeta et al. 2008), we
compared “maternal energy budget” and “offspring survival” between
oviparous and viviparous species to quantify the impact of climate
warming, and thereby assess whether these modes will be harmed by or
benefit from future warming.