Local adaptation in mainland anole lizards: Integrating population history and genome–environment associations

Abstract

Environmental gradients constrain physiological performance and thus species’ ranges, suggesting that species occurrence in diverse environments may be associated with local adaptation. Genome–environment association analyses (GEAA) have become central for studies of local adaptation, yet they are sensitive to the spatial orientation of historical range expansions relative to landscape gradients. To test whether potentially adaptive genotypes occur in varied climates in wide‐ranged species, we implemented GEAA on the basis of genomewide data from the anole lizards Anolis ortonii and Anolis punctatus, which expanded from Amazonia, presently dominated by warm and wet settings, into the cooler and less rainy Atlantic Forest. To examine whether local adaptation has been constrained by population structure and history, we estimated effective population sizes, divergence times, and gene flow under a coalescent framework. In both species, divergence between Amazonian and Atlantic Forest populations dates back to the mid‐Pleistocene, with subsequent gene flow. We recovered eleven candidate genes involved with metabolism, immunity, development, and cell signaling in A. punctatus and found no loci whose frequency is associated with environmental gradients in A. ortonii. Distinct signatures of adaptation between these species are not associated with historical constraints or distinct climatic space occupancies. Similar patterns of spatial structure between selected and neutral SNPs along the climatic gradient, as supported by patterns of genetic clustering in A. punctatus, may have led to conservative GEAA performance. This study illustrates how tests of local adaptation can benefit from knowledge about species histories to support hypothesis formulation, sampling design, and landscape gradient characterization.

Selection at behavioural, developmental and metabolic genes is associated with the northward expansion of a successful tropical colonizer

“…We note that there are redundant patterns between GWSS in green anoles, such as the repeated finding that candidate genes for positive selection are involved in metabolism, muscular development and physiology (Campbell‐Staton et al, ; Prates et al, ; Tamate et al, ; Tollis et al, ), even in extremely recent adaptation (Tamate et al, ). Although this is encouraging, we urge to apply caution since most developmental genes tend to be longer than other annotated genes in the green anole (Figure ), which can make them easier to detect by GWSS.…”

“…We identified genes belonging to GO categories of interest (Immune response, GO:0006955; somitogenesis and limb development, GO:0001756 and GO:0060173; Reproduction, GO:0000003; Behavior, GO:0007610) and tested whether these candidates displayed more frequent evidence of selection. These functions were chosen as they are likely important from an ecological perspective in green anoles, based on previous studies (Campbell‐Staton et al, ; Prates et al, ; Rodríguez et al, ). We also investigated whether genes involved in response to cold displayed more signatures of selection than expected by chance, using a list of 1,375 genes highlighted in a recent transcriptomic study (Campbell‐Staton et al, ).…”

“…In Anolis cybotes , an anole from Hispaniola, many genes involved in bone development, blood pressure or lipid metabolism were found to be involved in adaptation to elevation (Rodríguez et al, ). In A. punctatus , genes involved in metabolism, immunity and development are also associated with variation in climatic regimes across the distribution area (Prates, Penna, Rodrigues, & Carnaval, ). Combined with previous physiological studies (Campbell‐Staton et al, ), these results already provide a set of relevant candidate functions that should be further investigated to identify possible convergence for adaptation in squamates.…”

“…In Anolis cybotes, an anole from Hispaniola, many genes involved in bone development, blood pressure or lipid metabolism were found to be involved in adaptation to elevation (Rodríguez et al, 2017). In A. punctatus, genes involved in metabolism, immunity and development are also associated with variation in climatic regimes across the distribution area (Prates, Penna, Rodrigues, & Carnaval, 2018).…”

Rain forest shifts through time and riverine barriers shaped the diversification of South American terrestrial pit vipers (Bothrops jararacussu species group)

“…More recently, however, biogeographers have addressed the idea of 'mega-refugia' that would correspond to presently disjunct Neotropical forested biomes. Under this new interpretation, habitats such as Amazonia and the Atlantic Forest have acted as historically linked refuge areas; pulses of rain forest expansion led to species interchange across regions, followed by lineage divergence and speciation after forest separation (Dal Vechio, Prates, Grazziotin, Zaher, & Rodrigues, 2018;Prates et al, 2017;Prates, Penna, Rodrigues, & Carnaval, 2018;Prates, Rivera, et al, 2016a).…”