Integrative inference of population history in the Ibero-Maghrebian endemic Pleurodeles waltl (Salamandridae)

Abstract

Inference of population histories from the molecular signatures of past demographic processes is challenging, but recent methodological advances in species distribution models and their integration in time-calibrated phylogeographic studies allow detailed reconstruction of complex biogeographic scenarios. We apply an integrative approach to infer the evolutionary history of the Iberian ribbed newt (Pleurodeles waltl), an Ibero-Maghrebian endemic with populations north and south of the Strait of Gibraltar. We analyzed an extensive multilocus dataset (mitochondrial and nuclear DNA sequences and ten polymorphic microsatellite loci) and found a deep east-west phylogeographic break in Iberian populations dating back to the Plio-Pleistocene. This break is inferred to result from vicariance associated with the formation of the Guadalquivir river basin. In contrast with previous studies, North African populations showed exclusive mtDNA haplotypes, and formed a monophyletic clade within the Eastern Iberian lineage in the mtDNA genealogy. On the other hand, microsatellites failed to recover Moroccan populations as a differentiated genetic cluster. This is interpreted to result from post-divergence gene flow based on the results of IMA2 and Migrate analyses. Thus, Moroccan populations would have originated after overseas dispersal from the Iberian Peninsula in the Pleistocene, with subsequent gene flow in more recent times, implying at least two trans-marine dispersal events. We modeled the distribution of the species and of each lineage, and projected these models back in time to infer climatically favourable areas during the mid-Holocene, the last glacial maximum (LGM) and the last interglacial (LIG), to reconstruct more recent population dynamics. We found minor differences in climatic favourability across lineages, suggesting intraspecific niche conservatism. Genetic diversity was significantly correlated with the intersection of environmental favourability in the LIG and LGM, indicating that populations of P. waltl are genetically more diverse in regions that have remained environmentally favourable through the last glacial cycle, particularly southern Iberia and northern Morocco. This study provides novel insights into the relative roles of geology and climate on the biogeography of a biodiversity hotspot.