Discussion
Association of key life history traits, such as body size, with environmental factors shape the adaptation of species to local environments (e.g., Blackburn et al., 1999; Freckleton et al., 2003; Morrison and Hero, 2003; Pincheira-Donoso and Tregenza, 2011; Meiri et al., 2013; Volynchik, 2014; Hille and Cooper, 2015; Laiolo and Obeso 2015; Lack et al., 2016 Meiri et al., 2020; Velasco et al., 2020; Wang et al., 2021; Deme et al., 2022a; Giovanna et al., 2022; Szymkowiak and Schmidt, 2022). Indeed, we found that geographical patterns of female body size were influenced by the coupling effects of the seasonal and annual changes in the climatic conditions along altitudinal gradients, suggesting a possible adaptation of E. argus lizards to the changing environmental conditions. The climate-body size relationship across populations of E. argus lizards in our study showed a reversal of Bergmann’s rule: female lizards occupying warmer environments at low altitudes had bigger body sizes. Further, we found that populations at low latitudes with an abundance of available resources and highly seasonal environments, such as increased precipitation, had significantly larger body sizes. Thus, our study suggests that the intraspecific variation in the geographical patterns of body size along altitudinal clines was primarily driven by multifarious local environmental conditions such as climatic conditions, highly seasonal environments and available resources.
Geographic patterns of body size are thought to be primarily influenced by climatic gradients, as summarized by Bergmann’s rule (Bergmann, 1847; Ashton and Feldman, 2003; Sears, 2005). Based on Bergmann’s rule, there is a general understanding that the body sizes of endotherms increase toward high latitudes or altitudes (see Ashton and Feldman, 2003; Meiri and Dayan, 2003; Pincheira-Donoso et al., 2008; Pincheira-Donoso and Meiri, 2013; Moreno Azocar et al., 2015). In a reversal to Bergmann’s rule, we found evidence that female lizards at lower altitudes in warmer environments had larger body sizes. Our finding concurs with other previous studies showing ectotherms may sometimes reverse Bergmann’s rule (Ashton and Feldman, 2003; Sears, 2005). In contrast studies have shown some ectotherms follow Bergmann’s rule, possessing large body sizes at high latitudes (e.g., Angilletta et al., 2004). The original explanation for Bergman’s rule did not account for the peculiarity of ectotherms (Watt et al., 2010) in their inability to generate significant internal body heat, and consequently that a larger bodied ectotherm would therefore heat up more slowly (Stevenson, 1985) and would lack the ability to conserve heat in colder environments (Liang et al., 2021). Further, possessing larger bodies in colder environments may be deleterious to some ectotherm species (Jadin et al., 2019; Velasco et al., 2020; Slavenko et al., 2021); since ectotherms with large body sizes that slowly heat up in colder environments show constrained thermoregulatory behavior (Pincheira-Donoso et al., 2008; Anderson et al., 2022; Szymkowiak and Schmidt, 2022).
Expressly, our results found evidence for the influence of both resource availability and seasonality (i.e., precipitation seasonality) on female body size, with smaller body sizes associated with decreased seasonality and lower primary productivity. Previous studies have suggested that highly seasonal changes in rainfall significantly influence the abundance of available resources for female lizards (Valenzuela-Sánchez et al., 2015; Meiri et al., 2020; Slavenko et al., 2021), which is positively related to large body sizes (Liang et al., 2021). Perhaps this is not surprising since unpredictable seasonal changes at high altitudes may suggest scarce resources for lizards (Deme et al., 2022a; Anderson et al., 2022). Previous studies have shown that abundant available resources for lizards to feed mostly impact the growth rate along geographic clines, which may be a function of body size variations in lizards (e.g., Lu et al., 2018a, 2018b), suggesting that non-climatic factors such as available resources can also influence the variation in the body sizes of lizards. For instance, available resources as a function of habitat productivity in novel environments influenced body size variations in other ectotherm species like insects, fishes and amphibians (Morrison and Hero, 2003; Laiolo and Obeso, 2015; Riesch et al., 2018; Giovanna et al., 2022). Perhaps, the variations in non-climatic factors across environments also play significant roles in determining shifts in phenotypic traits, such as variation in the body size of species. However, our understanding of how the variations of these climatic and non-climatic factors along geographic clines can directly or indirectly impact ectotherms’ body sizes in the context of rapidly changing climates may still be limited.
Thus, clinal variation in body sizes across populations within ectothermic species may be a result of adaptive plasticity to changing environmental conditions (Riesch et al., 2018; Giovanna et al., 2022). Organismal body size, as a function of growth and development rates, is influenced by the interplay of intrinsic and extrinsic factors (Duellman and Trueb 1986). For example, extrinsic and intrinsic factors such as temperature, habitat type, food availability, egg size, yolk reserves, and competition have all been shown to influence the body sizes of ectotherms across environments (Fischer et al., 2003; Laiolo and Obeso, 2015; Riesch et al., 2018), which ultimately can affect the reproductive ecology of ectotherms (Fielding et al., 1999; Morrison and Hero, 2003; Deme et al., 2022a). While the patterns of female body size across altitudes and environments found in our study may be a results of non-adaptive plasticity, or even fixed genetic differences between populations, we suggest that this pattern may be a result of adaptive phenotypic plasticity (Ghalambor et al., 2007; Szymkowiak and Schmidt, 2022). However, further experiments, such as common garden studies, would be needed to test this hypothesis. Understanding the underlying cause of the altitudinal body size differences is important in order to predict how these populations will response to future changes in climate (Merilä and Hendry, 2014). The pace of climate change is expected to be more rapid at high altitudes (Pepin et al. , 2015). Phenotypic plasticity in body size may allow lizard populations to quickly respond to changes in climatic conditions across populations, but may consequently shield body size from selection, slowing the pace of evolutionary change (Diamond and Martin 2021). In contrast if body size differences between populations is largely due to genetic divergence, these population may evolve on response to changing climates, but it is unclear whether the rate of evolution could keep pace with the rate of climatic change (Diamond and Martin 2020).