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Open Access Highly Accessed Research article

Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard

Daniele Salvi*, D James Harris, Antigoni Kaliontzopoulou, Miguel A Carretero and Catarina Pinho

Author Affiliations

CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto; Campus Agrário de Vairão, 4485-661, Vairão, Portugal

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BMC Evolutionary Biology 2013, 13:147  doi:10.1186/1471-2148-13-147

Published: 11 July 2013

Abstract

Background

Pleistocene climatic oscillations have played a major role in structuring present-day biodiversity. The southern Mediterranean peninsulas have long been recognized as major glacial refugia, from where Northern Europe was post-glacially colonized. However, recent studies have unravelled numerous additional refugia also in northern regions. We investigated the phylogeographic pattern of the widespread Western Palaearctic lizard Podarcis muralis, using a range-wide multilocus approach, to evaluate whether it is concordant with a recent expansion from southern glacial refugia or alternatively from a combination of Mediterranean and northern refugia.

Results

We analyzed DNA sequences of two mitochondrial (cytb and nd4) and three nuclear (acm4, mc1r, and pdc) gene fragments in individuals from 52 localities across the species range, using phylogenetic and phylogeographic methods. The complex phylogeographic pattern observed, with 23 reciprocally monophyletic allo- parapatric lineages having a Pleistocene divergence, suggests a scenario of long-term isolation in multiple ice-age refugia across the species distribution range. Multiple lineages were identified within the three Mediterranean peninsulas – Iberia, Italy and the Balkans - where the highest genetic diversity was observed. Such an unprecedented phylogeographic pattern - here called “refugia within all refugia” – compasses the classical scenario of multiple southern refugia. However, unlike the southern refugia model, various distinct lineages were also found in northern regions, suggesting that additional refugia in France, Northern Italy, Eastern Alps and Central Balkans allowed the long-term persistence of this species throughout Pleistocene glaciations.

Conclusions

The phylogeography of Podarcis muralis provides a paradigm of temperate species survival in Mediterranean and extra-Mediterranean glacial refugia. Such refugia acted as independent biogeographic compartments for the long-term persistence of this species, for the differentiation of its genetic lineages, and for the short-distance post-glacial re-colonization of neighbouring areas. This finding echoes previous findings from recent phylogeographic studies on species from temperate ecoregions, thus suggesting the need for a reappraisal of the role of northern refugia for glacial persistence and post-glacial assembly of Holarctic biota.

Keywords:
Podarcis muralis; Phylogeography; Western Palaearctic; Glacial refugia; Mediterranean peninsulas; Genetic diversity; Temperate species