Limb morphology and natural selection
In proportion to SVL, we found Kozu lizards (n = 37) to have
significantly longer hind legs (0.44 ± 0.03, p < 0.001)
and hind foot lengths (0.21 ± 0.002, p < 0.001) than
Hachijo-Kojima lizards (0.41 ± 0.003 and 0.20 ± 0.002, respectively,n = 66). We found differences in estimated contributions of
morphological traits to relative sprint speed to be especially
pronounced for hind leg length and SVL (Table S5). We determined hind
leg length to have a 0.82 probability of positively affecting sprint
speed for Kozu lizards, and to have no effect on Hachijo-Kojima lizard
sprint speed (Fig. 4A). Regarding SVL (Fig. 4D), we found a 0.91
probability of it positively affecting Hachijo-Kojima lizard sprint
speed, and a 0.78 probability of it negatively affecting Kozu lizard
sprint speed. We did not detect any effect of hind foot length on sprint
speed for either island (Fig. 4B). Total tail length (Fig. 4C) had a
0.81 probability of positively affecting sprint speed for Kozu lizards,
but had no effect for Hachijo-Kojima.
For Kozu lizards (n = 113), the Bayesian 95% confidence interval
regarding the linear selection gradient β did not include 0,
but the non-linear selection gradient \(\gamma\) included 0 (Table S6).
Accordingly, the shape of the relationship between relative hind leg
length and relative tail break distance shows an upward and rising slope
(Fig. 5A), implying positive directional selection on hind leg length.
In contrast, for Miyake (n = 78) and Hachijo-Kojima (n =
59) lizards, the Bayesian 95% confidence interval for the linear
selection gradient β included 0 (Table S6), suggesting no
natural selection on hind leg length on these islands (Fig.5C-D).
Although for Mikura lizards (n = 38), the linear selection
gradient confidence interval only marginally includes 0, the shape of
the relationship between hind leg length and relative tail break
distance shows a rising slope (Fig. 5B) similar to that for Kozu
lizards.
DISCUSSION
We demonstrate that lizard foraging body temperatures are higher in the
presence of its snake predator (Fig. 1). In tandem with warmer-adapted
thermal performance and predation-induced selection for longer hind
legs, we show that these higher body temperatures are conducive to
optimal sprint speeds at temperatures suboptimal for the predator (Fig.
3; Table S4). We also found lizard body temperatures to have increased
throughout the study period, consistent with recent climatic warming
over the past few decades, regardless of snake predator presence or
absence (Fig. 2). This suggests a pathway through which predation in
ectotherm systems acts as a pivotal factor determining prey thermal
biology and thereby potentially regulating the degree of climate change
vulnerability. Given the functional importance of body temperature in
evasion by prey and success by predator, warming is also likely to
impact ectotherm predator-prey relationships, but in unpredictable ways.
Analyses and conclusions based on thermal performance curves are often
founded on many assumptions regarding their implications for fitness and
resulting climate change consequences (Sinclair et al. 2016). While a
significant body of work has consolidated the mechanisms through which
ectotherms are vulnerable to warming impacts according to their thermal
performance (Sinervo et al. 2010; Kearney 2013; Logan et al. 2013;
Sinclair et al. 2016) or exposure to predation (Schmitz and Barton 2014;
Sinclair et al. 2016; Laws 2017; Osmond et al. 2017), few studies have
explicitly linked predation and fitness within a thermal framework.
Elucidating the relationship between predation pressure and fitness, and
how this affects thermal physiology, contextualizes observable
differences in prey behaviour as a potentially decisive factor in
climate change vulnerability (Sinervo et al. 2010; Kearney 2013). Here
we show that predation-induced selection on morphology and thermal
performance results in warmer prey foraging body temperatures, where
further climatic warming could differentially affect these populations
relative to those free from the same predation type.
In mediating tradeoffs for survival, prey species can be pushed by
predation pressure to forage during hotter times of day (Tambling et al.
2015; Veldhuis et al. 2020). Yet a common expectation for lizard species
is for body temperatures to be lower under higher predation pressure due
to the heightened risks of behavioural thermoregulation (Huey and
Slatkin 1976; Salazar et al. 2019). In contrast, we provide evidence for
predation pressure by snakes to push lizard prey thermal biology towards
warmer temperatures. Main predation type is also likely to be an
important factor affecting prey thermal biology, seeing that P.
latiscutatus on snake-free islands are nonetheless hunted by birds
despite foraging at lower body temperatures than snake island
populations. Evasion strategies by prey lizards differ depending on
predator typee, where cryptic strategies are usually employed to avoid
predation by birds, and running for escaping terrestrial predators
(Samia et al. 2016). Accordingly, P. latiscutatus individuals on
snake-free islands tend to carry more cryptic dorsal patterns and
coloration (Brandley et al. 2014; Kuriyama et al. 2016), whereas those
under snake predation are better suited physiologically and
morphologically for escaping snake predation by running (Figs. 3 and 4).
Broadly, prey species are often exposed to a variety of predatory
strategies and densities, and understanding how these affect prey
behaviours, including thermal responses, are crucial in explaining their
current spatial distributions (Wirsing et al. 2010). This in turn could
be important for predicting future spatial distributions under climate
change as modeling tools are increasingly inclusive of interspecific
interactions (Singer et al. 2016).
Body temperatures in lizard species overall tend to follow temporal
environmental temperature patterns, such as within a day, or across
seasons or years (Clusella-Trullas and Chown 2014; Domínguez‐Guerrero et
al. 2020), yet the stability or steepness of this relationship can vary
depending on the number of predators or competitors present (Salazar et
al. 2019). In this regard, our observations suggest body temperatures
follow increases in environmental temperatures regardless of predation
exposure. Yet we demonstrate that predation does drive warmer body
temperatures, and with climatic warming likely to be ongoing in the near
future, could thereby impose changes in lizard activity restrictions
differently than for populations free from snake predation and which
depend on relatively lower body temperatures (Sinervo et al. 2010;
Kearney 2013). Accordingly, we provide evidence for thermal physiology
to be among the life history traits through which higher rates of
predation can improve prey persistence under environmental warming
(Osmond et al. 2017). Conversely, prey activity windows can also be more
restricted to the hottest times of day, and thus less flexible to
respond to warming because of predators hunting during cooler hours
(Veldhuis et al. 2020). Changes in the temporal and spatial occupancy of
thermal habitats by both prey and predator, and the ways in which they
compound and affect one another, thus need to be jointly considered in
order to adequately estimate climate change responses (Schmitz and
Barton 2014) for effective comparisons with systems free of predation.
Set within a natural laboratory system, our study provides valuable
empirical evidence on how predation shapes prey behaviour, morphology
and physiology, all of which are integral components of thermal
adaptation (Angilletta 2009). Such responses are instrumental in
mechanistically explaining prey intraspecific variability in habitat
suitability according to predation type, and, ultimately, persistence
under climatic warming (e.g. Landry Yuan et al. 2018). As in predation,
other biotic interactions can have either negative or positive effects
on environmental change vulnerability of species, as mediated by both
direct and indirect pathways (Singer et al. 2016; Engelhardt et al.
2020). Thus, the implementation of holistic approaches incorporating the
interplay between abiotic and biotic factors as well as life history
traits is essential in breaking down the processes through which species
affect one another, in order to understand biodiversity change in this
era of rapid anthropogenic change.
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ACKNOWLEDGEMENTS
This work was approved by the University of Hong Kong’s Committee of the
Use of Live Animals in Teaching & Research (4599-18), and financially
supported with funding awarded to M. Hasegawa (19H03307, 15H04426) by
the Japan Society for the Promotion of Science (JSPS). Fieldwork on Kozu
and Niijima was approved by local village governments in accordance with
their ordinances governing plant and animal protection, while no
specific permission is required for fieldwork on other Izu Islands. We
thank Yoji Kigasawa for allowing us to use his lizard body temperature
data taken on Miyake island in 1983. We also thank Dr. Yosuke Kojima and
Miki Hirose for their invaluable help in the field, as well as Dr. T.Y.
Hui for reviewing this manuscript and providing valuable comments. MH
expresses sincere thanks to the late Shouichi Sengoku and late Kazuyoshi
Miyashita for their mentorship during the early phase of fieldwork from
the late 1970’s to late 1980’s.