Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline

Abstract

Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CT ), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co-expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity-limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.

Seedling response to water stress in valley oak (Quercus lobata) is shaped by different gene networks across populations

“…Differential expression (DE) analyses comparing water‐stressed plants to controls have been used to identify candidate drought response genes in a wide range of species, including wild barley (Hübner, Korol, & Schmid, ), eucalyptus (Villar et al, ), fir (Behringer, Zimmermann, Ziegenhagen, & Liepelt, ), pine and spruce ⁠(Yeaman et al, ), poplar species (Cohen et al, ; Street et al, ), switchgrass (Meyer et al, ) and oaks (Gugger, Peñaloza‐Ramírez, Wright, & Sork, ; Steele, ). Using weighted gene co‐expression network analysis (WGCNA, Langfelder & Horvath, ), co‐expressed genes are grouped into eigengenes, or modules, which can be considered putative functional categories regulated in the same way and can be tested for differences across conditions (Campbell‐Staton, Bare, Losos, Edwards, & Cheviron, ; Kenkel & Matz, ; Passow et al, ; Rose, Seneca, & Palumbi, ).…”

Plasticity and local adaptation explain lizard cold tolerance

“…In this issue of Molecular Ecology , Campbell‐Staton et al. () address these broad questions by investigating cold tolerance adaptation in the green anole lizard ( Anolis carolinensis ) across a latitudinal transect. By integrating physiological data, gene expression data and acclimation experiments, the authors disentangle the mechanisms underlying cold adaptation.…”

“…In this issue of Molecular Ecology , Campbell‐Staton, Bare, Losos, Edwards, and Cheviron () use the green anole lizard ( Anolis carolinensis ; Figure ) as a model system to identify mechanisms that enable ectothermic lineages with tropical origins to colonize more temperate climatic niches. By sampling anole populations across a latitudinal transect, they tested the broad question of whether success in higher latitudes, with lower temperatures, occurs through phenotypic plasticity or the evolution of heritable genetic variation.…”

“…Schematic of Anolis carolinensis populations (black dots) analysed in Campbell‐Staton et al. (), which were situated along a latitudinal transect through Texas and Oklahoma. Along this cline, cold tolerance increases with latitude, while phenotypic plasticity remains constant.…”

“…A major contribution of the work of Campbell‐Staton et al. () is providing one of the first illustrations of the molecular mechanisms that may enable adaptation of lower CT min and, thus, the expansion of tropical vertebrates into more temperate climates. Using liver gene expression data from control and acclimation treatment samples from various latitudes, the authors identify 15 clustered sets of co‐expressed genes that were significantly associated with oxygen demand, including functions such as oxygen transport and aerobic respiration.…”