Integrating genetics, physiology and morphology to study desert adaptation in a lizard species

Integration of multiple approaches is key to understand the evolutionary processes of local adaptation and speciation. Reptiles have successfully colonized desert environments, that is, extreme and arid conditions that constitute a strong selective pressure on organisms. Here, we studied genomic, physiological and morphological variations of the lizard Liolaemus fuscus to detect adaptations to the Atacama Desert. By comparing populations of L. fuscus inhabiting the Atacama Desert with populations from the Mediterranean forests from central Chile, we aimed at characterizing features related to desert adaptation. We combined ddRAD sequencing with physiological (evaporative water loss, metabolic rate and selected temperature) and morphological (linear and geometric morphometrics) measurements. We integrated the genomic and phenotypic data using redundancy analyses. Results showed strong genetic divergence, along with a high number of fixed loci between desert and forest populations. Analyses detected 110 fixed and 30 outlier loci located within genes, from which 43 were in coding regions, and 12 presented non-synonymous mutations. The candidate genes were associated with cellular membrane and development. Desert lizards presented lower evaporative water loss than those from the forest. Morphological data showed that desert lizards had smaller body size, different allometry, larger eyeballs and more dorsoventrally compressed heads. Our results suggest incipient speciation between desert and forest populations. The adaptive signal must be cautiously interpreted since genetic drift could also contribute to the divergence pattern. Nonetheless, we propose water and resource availability, and changes in habitat structure, as the most relevant challenges for desert reptiles. This study provides insights of the mechanisms that allow speciation as well as desert adaptation in reptiles at multiple levels, and highlights the benefit of integrating independent evidence.