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.