Tracing evolutionary trajectories in the presence of gene flow in South American temperate lizards (Squamata: Liolaemus kingii group)

Abstract

Evolutionary processes behind lineage divergence often involve multidimensional differentiation. However, in the context of recent divergences, the signals exhibited by each dimension may not converge. In such scenarios, incomplete lineage sorting, gene flow, and scarce phenotypic differentiation are pervasive. Here, we integrated genomic (RAD loci of 90 individuals), phenotypic (linear and geometric traits of 823 and 411 individuals, respectively), spatial, and climatic data to reconstruct the evolutionary history of a speciation continuum of liolaemid lizards (Liolaemus kingii group). Specifically, we (i) inferred the population structure of the group and contrasted it with the phenotypic variability; (ii) assessed the role of post-divergence gene flow in shaping phylogeographic and phenotypic patterns; and (iii) explored eco-geographic drivers of diversification across time and space. We inferred eight genomic clusters exhibiting leaky genetic borders coincident with geographic transitions. We also found evidence of post-divergence gene flow resulting in transgressive phenotypic evolution in one species. Predicted ancestral niches unveiled suitable areas in southern and eastern Patagonia during glacial and interglacial periods. Our study underscores integrating different data and model-based approaches to determine the underlying causes of diversification, a challenge faced in the study of recently diverged groups. We also highlight Liolaemus as a model system for phylogeographic and broader evolutionary studies.