Slippery slopes: montane isolation and elevational shifts shape the evolution and diversity of Iberolacerta lizards

Abstract

Understanding the processes driving the diversity of mountain herpetofauna requires a comprehensive examination of species diversification across evolutionary scales. Here, we investigate the phylogeography of Iberolacerta, a genus of eight lizard species mainly restricted to high elevations in southwestern Europe. Using genomic data, we reconstructed a nuclear phylogeny that aligns with mitochondrial evidence in supporting the divergence of all currently recognized species. Notably, we detect historical nuclear gene flow between I. cyreni and I. martinezricai in Central Spain, suggesting past range overlap, reminiscent of previously observed mitochondrial introgression between I. galani and I. monticola, and the lack of divergence between disjoint populations of I. monticola. Bioclimatic projections accordingly depict broader historical ranges during the last glacial maximum compared to interglacial and current conditions. At the intraspecific level, genomic analyses of four high-elevation species reveal that genetic structure is mainly shaped by isolation-by-distance and, in I. cyreni, by separation among mountain ranges, while heterozygosity generally decreases with elevation. These findings are consistent with the impact of glacial-interglacial cycles on the genetic diversity of montane taxa: populations experience genetic isolation and altitudinal bottlenecks during interglacial periods, but are reconnected and admix in lowland areas during glacial periods. These processes are expected to leave contrasting signatures between the mitochondrial and nuclear genomes, as well as between slow- and fast-evolving molecular markers. From a conservation perspective, our results highlight that the genetically richest – and potentially most adaptive – populations occur at the lowland edges of the species’ ranges, where they are also most vulnerable to climate change.