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.
Highlights
Pleistocene climatic oscillations have played a major role in structuring present-day biodiversity
In Europe, the genetic structure of temperate organisms has been mainly explained by cycles of contraction toward glacial refugia located in southern peninsulas and postglacial recolonization of northern regions, tracking the expansion of suitable habitats [5,6] southern peninsular refugia are thought to have played a major role in the long-term maintenance of genetic diversity and differentiation, and relatively few patterns and routes of colonization have been described as paradigms for the post-glacial arrival of species in Northern Europe [6,7,8]
In recent decades, the phylogeography of the Western Palaearctic has been mainly centered around the southern refugia model, which sets a sharp dichotomy between Mediterranean peninsulas and Northern Europe, the former being areas of long-term persistence of temperate species and sources for the postglacial assembly of northern biotas
Summary
Pleistocene climatic oscillations have played a major role in structuring present-day biodiversity. Mounting examples from plants, insects, mammals, amphibians, and reptiles show that in many temperate species the southern refugia model is insufficient to explain the observed genetic patterns, which would be better explained by a scenario of ice-age survival in a combination of Mediterranean and extra-Mediterranean refugia [13,14,15,16,17] This changing view with respect to geographical location of refugia has had direct implications for the inferred scenarios of recolonization for many widespread species from the Western Palaearctic. This is true even in emblematic species, such as the brown bear and the common beech, the phylogeographic patterns of which were previously upheld as paradigms of postglacial recolonization routes (exclusively) from southern refugia [6,7] In these species, the existence of additional extra-Mediterranean refugia has recently become evident through the analysis of fossil DNA and palaeobotanical data, respectively. These evidence suggests that range shifts and expansions in these species could have been much smaller than previously thought [18,19,20,21]
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