Abstract
The evolution of body size, both within and between species, has been long predicted to be influenced by multifarious environmental factors. However, the specific drivers of body size variation have remained difficult to understand because of the wide range of proximate factors that consistently covary with ectotherm body sizes across populations with varying local environmental conditions. Here, we used a widely distributed lizard (Eremias argus ) collected from different populations situated across China to assess how climatic conditions and/or available resources at different altitudes shape the geographical patterns of lizard body size across populations. We used body size data from locations differing in altitudes across China to construct linear mixed models to test the relationship between lizard body size and ecological and climate conditions across altitudes. Lizard populations showed significant differences in body size across altitudes. Furthermore, we found that variation in body size among populations was also explained by climatic and seasonal changes along the altitudinal gradient. Specifically, body size decreased with colder and drier environmental conditions at high altitudes, resulting in a reversal of Bergmann’s rule. Limited resources at high altitudes, as measured by net primary productivity, may also constrain body size. Therefore, our study demonstrates that the intraspecific variation in female lizards’ body size may be strongly influenced by multifarious local environments as adaptive plasticity for female organisms to possibly maximise reproductive ecology along geographic clines.
Keywords: Bergmann’s rule, Squamates, Resource availability, Geographical gradients, Climate
1.0 Introduction
Body size is a fundamental but critical trait of organisms, and variation in body size within and between species is often tightly linked to important life history traits, such as fecundity, growth, and survival (Roff, 2002; Pincheira-Donoso et al., 2008; Meiri, 2018; Lu et al., 2018a; Meiri et al., 2020; Deme et al., 2022a; 2022b; Wu et al., 2022). Originally described for endothermic species, Bergmann’s rule predicts that species occupying colder environments will have larger body sizes when compared to species occupying warmer environments (Bergmann, 1847). Indeed, almost all endotherms adhere to Bergmann’s rule (see reviews by Blackburn et al., 1999; Freckleton et al., 2003). However, ectotherms often do not (Forsman and Shine, 1995; Sears and Angilletta, 2004; Norris et al., 2021); with some ectotherm species showing no observable clines in body size and others reversing Bergmann’s rule (Forsman and Shine, 1995; Sears and Angilletta, 2004; Olalla-Tárraga and Rodríguez, 2007; Meiri et al., 2013; Lu et al., 2018a; Norris et al., 2021). This is perhaps not surprising, as the original explanation for Bergman’s rule does not apply to ectotherms (Watt et al., 2010), since they generate little internal body heat, and a larger body would therefore heat up more slowly as well (Stevenson, 1985). The proximate underlying factors influencing clines in body size among ectotherms are instead likely complex and multifarious (Sears and Angilletta, 2004; Pincheira-Donoso and Meiri, 2013; Pincheira-Donoso et al., 2019). Thus, unraveling the specific factors explaining clines of body size in ectotherms is necessary to properly understand the evolution of body size and its ecological consequences (Collar et al., 2010).
Plastic and evolutionary responses to altitudinal clines may influence inter- and intraspecific variation in body size among ectotherms (Lu et al., 2018a; Meiri, 2018; Norris et al., 2021; Giovanna et al., 2022), due to the often rapid changes in annual and seasonal variation in temperature and precipitation across altitude (Liang et al., 2021; Anderson et al., 2022). For instance, studies have suggested that ectotherm body sizes may increase at low elevations with optimal seasonal environments (seasonal environments that allow ectotherms to have more active time) (Slavenko et al., 2019), likely because optimal seasonal environments allow for increased time available for ectotherms to acquire resources (Horváthová et al., 2013). Moreover, lizard species at high altitudes may have small body sizes due to short warmer seasons, unfavourable conditions, and constrained active time (Meiri et al., 2013; Meiri, 2018). Therefore, a potentially important driver of body size variation across ectotherms may be the direct and/or indirect relationship between favourable environmental (climatic) conditions and lizards’ foraging behaviour for available resources (van der Meer, 2019; Lu et al., 2018a; Lu et al., 2018b). Thus, environments at high altitudes with unfavourable climate conditions that may constrain lizards’ foraging behaviour for the limited resources may impose underlying constraints on body size within populations of ectothermic species (Velasco et al., 2020; Giovanna et al., 2022).
As their wide distribution across climatic zones globally, lizards are excellent models for understanding how climatic conditions along geographic clines influence interspecific variation in body size (Velasco et al., 2020). China, has a rich diversity of over 212 species of lizards belonging to 10 families (Zhao et al., 1999; Zhou et al., 2019; Wang et al., 2020). However, how body size varies with geographic and climatic clines has only recently been explored for this region, especially when considering body size variation across populations (see, Guo, 2016; Liang et al., 2021). For example, female lizards inhabiting colder environments at higher gradients within China (from tropical to temperate regions) were found to possess small body sizes as adaptive plasticity for reproductive ecology (Lu et al., 2018a; Deme et al., 2022b), suggesting that the body sizes of the female lizards may as well follow climatic clines for adaptation to environmental (climatic) conditions (Feldman and Meiri, 2014; Brusch et al., 2022). Indeed, this is a large gap considering that the impact of climate conditions on lizard body size has been extensively studied in other regions of the world (e.g., Ashton and Feldman, 2003; Angilletta et al., 2004; Sears, 2005; Olalla-Tárraga et al., 2006; Olalla-Tárraga and Rodríguez, 2007; Olalla-Tárraga, 2011; Pincheira-Donoso and Meiri, 2013; Zamora-Camacho et al., 2014; Rivas et al., 2018; Slavenko et al., 2019; Tarr et al., 2019; Wishingrad and Thomson, 2020; Norris et al., 2021). To address this gap in our knowledge, we set out to evaluate the predictors of female body size within populations of the Lacertid lizard, the Mongolia racerunner (Eremias argus ), a widespread species occupying a wide altitudinal range across China (30 m to 2975m asl, Figure 1).
Here, we focus only on the female E. argus lizards because maternal body size is highly important for maternal fitness, which may depend on seasonal, climatic, and geographic variation among populations (Deme et al., 2022b). Eremias argus lizard populations occupying high altitudes across China may experience unique local climatic conditions and unpredictable seasonal changes (Deme et al., 2022a), which may be different for other lizards globally, because of regional differences in climatic conditions (see, Sinervo et al., 2010; Meiri et al., 2013; Meiri, 2018). As studies have suggested that lizard populations across China that occupy unfavourable environments, which may reduce lizards’ body size (Liang et al., 2021; Wang et al., 2021), we set out to ask (i) whether E. argus follow a reverse Bergmann’s cline across altitudes to physiologically adapt to local environmental changes? (ii) if variation in resource availability, climate, and seasonality across altitudes will explain the patterns of lizards’ body sizes. We predict that a) lizards in colder environments will have small body sizes as physiological adaptive plasticity to reduce physiological costs along altitudes (Meiri et al., 2020; Brusch et al., 2022), with lizard species occupying high altitudes may have small body sizes, thereby reversing Bergmann’s rule; b) high altitudes with rapid transitions between seasons may constraint the body sizes of lizards since short seasonal changes at high altitudes may imply less active time and fewer resources available for species (Ashton and Feldman, 2003; Sears, 2005; Meiri et al., 2007; Slavenko et al., 2021).