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

Abstract

BackgroundPleistocene 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.ResultsWe 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.ConclusionsThe 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.

A combination of long term fragmentation and glacial persistence drove the evolutionary history of the Italian wall lizard Podarcis siculus

“…The number of mtDNA lineages and their high level of divergence are, to the best of our knowledge, among the highest ever observed in any vertebrate species from the area. A similar high number of mtDNA lineages can be observed in the congeneric Podarcis muralis [28]. However, in this species the genetic divergences among lineages is much lower than the one observed in P. siculus .…”

“…The hypothesis of glacial expansion and local persistence, reported in a growing number of Palearctic and Nearctic species [28, 98, 99], was criticized for the possible inaccuracy of molecular clock rates [100, 101]. However, our claim is supported not only by the estimated time of divergence but also by the evidence of large amount of new environment with high suitability, predicted by SDM, which appear during LGM in different southern Italian regions.…”

“…The geographic boundary observed between the Tyrrenian clade T and the Adriatic clade A2, whose split is dated at 1.9 Mya (Early Pleistocene), has been reported in various taxa [20, 28, 75]. The genetic discontinuites seem to be located in different geographic positions.…”

“…The rise of highly divergent genetic lineages in these areas is probably closely linked to these paleo-island systems. However, the northern and central Apennines have also played a role in generating long-term genetic discontinuity, suggesting the presence of additional cryptic refugia in the central and northern portions of the Italian Peninsula [28, 29]. …”

Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast

“…Magri 2008;Canestrelli et al 2010), its northern part has long been acknowledged as an area of postglacial (re)colonization (e.g. Salvi et al 2013;Vilaça et al 2014). Although the majority of the studies that support the refugia-within-refugia scenario (Gómez and Lunt 2007) have been undertaken in the Iberian Peninsula, including those on freshwater mussels (e.g.…”