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).