Countergradient Variation in Reptiles: Thermal Sensitivity of Developmental and Metabolic Rates Across Locally Adapted Populations

Abstract

Environmental temperature is a key driver of variation in developmental physiological rates in reptiles. Cooler temperatures extend development time and can increase the amount of energy required to achieve hatching success, which can pose fitness consequences later in life. Yet, for locally-adapted populations, genetic variation can oppose environmental variation across ecological gradients, known as countergradient variation (CnGV). Biologists often seek to understand the presence of phenotypic variation, yet the absence of such variation across environmental gradients can also reveal insights into the mechanisms underlying local adaptation. While evidence for genetic variation opposing environmental variation in physiological rates has been summarized in other taxa, the generality of CnGV variation in reptiles is yet unknown. Here I present a summary of studies measuring development time and metabolic rates in locally-adapted populations across thermal clines for 15 species of reptiles across 8 families. CnGV in development time is found to be common, while no clear pattern emerges for the thermal sensitivity of metabolic rates across locally-adapted populations. CnGV in development time may be an adaptive response in order to decrease the costly development in cool climates, however, empirical work is needed to disentangle plastic from genetic responses, and to uncover potentially general mechanisms of local thermal adaptation in reptiles.

Population divergence in maternal investment and embryo energy use and allocation suggests adaptive responses to cool climates

“…As a potential compensation for this energy cost, high‐altitude embryos increase developmental rate without a concomitant increase in metabolic rate, and therefore expend less energy completing development at one and the same incubation temperature than embryos from lower altitudes. These results are consistent with thermal adaptation via countergradient variation in development time, as observed previously (Conover & Present, 1990; Laugen et al, 2003; Pettersen, 2020), but conclusive demonstration of local adaptation would require additional data on fitness (Kawecki & Ebert, 2004). Further investigation is needed to establish whether embryonic responses are consistently more important than maternal effects for adaptive responses to cool climate in lizards, or if the results here reflect ancestral levels of standing genetic variation, for example.…”

“…Consistent with these potential mechanisms to reduce development time in cool climates, there is a growing body of evidence in fish, amphibians and reptiles that populations in cool climates have evolved faster developmental rates, such that they hatch at comparably similar dates, to populations in warmer climates (known as countergradient variation; (Conover & Present, 1990; Laugen et al, 2003; Pettersen, 2020)). Local adaptation in developmental rates is most easily exemplified by common garden studies, whereby individuals from cold‐adapted populations (e.g.…”

“…low latitude and altitude) populations when placed under common conditions (Laugen et al, 2003). Despite clear evidence that countergradient variation represents local adaptation to cool climates (Pettersen, 2020), which of the above mechanisms are responsible for increasing in developmental rate is poorly understood (however see Du et al, 2010). It is also unclear whether faster developmental rates necessitate increased metabolic rates and therefore, cost of development.…”

Thermal–metabolic phenotypes of the lizard Podarcis muralis differ across elevation, but converge in high-elevation hypoxia

“…Biochemical reactions accelerate as temperature increases (until an upper limit is reached) and, correspondingly, maximum performance, growth and metabolism should increase with higher body temperatures (Hamilton, 1973;Huey and Bennett, 1987). Counter-gradient variation (Conover and Schultz, 1995;Pettersen, 2020) in upper physiological limits, as we observed here, may be attributable to a greater basking need to compensate for limited thermal resources (Michniewicz and Aubret, 2010;Hodgson and Schwanz, 2019). This compensation may drive thermal physiological and behavioral evolution for increased thermal limits and preferences in cold climate reptiles relative to warm climate reptiles (Hertz and Huey, 1981;Huey et al, 2009;Llewelyn et al, 2017).…”

How do fluctuating temperatures alter the cost of development?

“…Both metabolic and developmental rates can vary between populations, reflecting either local adaptation (Conover & Schultz, 1995; Demarco, 1992; Pettersen, 2020) or plasticity (Cordero et al, 2017; Gangloff et al, 2019; Macagno et al, 2018). In wall lizards, developmental rate shows counter-gradient variation, whereby embryos from cooler, high altitude and latitude populations develop faster than those from warm climates when placed under common garden conditions (Pettersen et al, 2022; While et al, 2015).…”