Pleistocene diversification in Morocco and recent demographic expansion in the Mediterranean pond turtleMauremys leprosa

Abstract

Quaternary climatic oscillations and geographic barriers have strongly influenced the distribution and diversification of thermophilic species occurring in the Mediterranean Basin. The Western Mediterranean pond turtle, Mauremys leprosa, is widely distributed throughout the Iberian Peninsula, southern France and most of the Maghreb region, with two subspecies currently recognized. In this work, we used 566 samples, including 259 new individuals, across the species range, and sequenced two mitochondrial markers (cytochrome b gene and control region; 163 samples in a concatenated mtDNA dataset) and one nuclear intron (R35; 23 samples representing all identified sublineages) to study the evolutionary history of M. leprosa. We combined phylogenetic methods and phylogeographic continuous diffusion models with spatial analysis. Our results (1) show a high level of genetic structure in Morocco originated during the Pleistocene; (2) reveal two independent population expansion waves from Morocco to Tunisia and to southern Europe, which later expanded throughout the Iberian Peninsula, and (3) identify several secondary contact zones in Morocco. Our study also sheds new light on the role of geographical features (Moroccan mountains ranges and the Strait of Gibraltar) and Pleistocene climatic oscillations in shaping genetic diversity and structure of M. leprosa, and underlines the importance of the Maghreb as a differentiation centre harbouring distinct glacial refugia.

Phylin 2.0: Extending the phylogeographical interpolation method to include uncertainty and user‐defined distance metrics

“…When tested individually against genetic distances, all three isolation models partially explained the genetic divergence but the resistance isolation model showed the highest coefficient. This was expected as topography and the seawater barrier greatly impacted the biogeographical history and contemporary patterns of genetic diversity and structure of the species (Veríssimo et al, ).…”

“…The distribution of M. leprosa is known to be restricted to terrestrial and freshwater habitats from low to medium altitudes. Both altitude and sea water increase the resistance to dispersion for this species (Veríssimo et al, ). The optimization procedure determined the parameters for a logistic model of resistance that provided the best fit for the presence of the species and the genetic data.…”

“…This reinforced the connectivity between samples, even in the presence of substantial sampling gaps in Algeria. The populations of M. leprosa are highly structured with most of their diversity occurring in Morocco (Veríssimo et al, ). The connectivity within the B3 lineage was difficult to assess due to lack of sampling in Algeria (Veríssimo et al, ).…”

“…When including seawater as a barrier to gene flow, the expected connectivity between samples improved, even with the obvious lack of sampling in this region. Although the Mediterranean Sea is a permeable barrier, exchange between the two continents probably occurred at its narrowest passage in the Strait of Gibraltar (Velo‐Antón et al, ; Velo‐Antón, Pereira, Fahd, Teixeira, & Fritz, ; Veríssimo et al, ). Using the resistance information when calculating pairwise distances between samples is forcing the Strait of Gibraltar to act as the single point of connectivity between the two continents, resulting in larger distances between points separated by seawater and, thus, providing a better description of the genetic structure.…”

“…The study area comprises the entire distribution of Mauremys leprosa (12.19°W, 11.21°E, 27.70°N, 43.81°N; see Figure S2), as defined by the occurrence data from the Spanish (Pleguezuelos, Màrquez, & Lizana, , http://siare.herpetologica.es/bdh/distribucion) and Portuguese atlases (Loureiro, Ferrand, Carretero, & Paulo, ) of amphibians and reptiles, and from previous publications (Veríssimo et al, ), but discarding the few populations in southern France which have been admixed with accidental or intentional introductions from Africa (Palacios et al, ; Veríssimo et al, ). The Moroccan populations of M. leprosa contain all the genetic lineages found within the species, with two of them expanding to Tunisia and the Iberian Peninsula, respectively (Veríssimo et al, ). Genetic diversity in this species is highly structured by the Atlas Mountains, which act as a barrier to gene flow.…”