extra-Mediterranean Refugia Research Articles

The opposed forces of differentiation and admixture across glacial cycles in the butterfly Aglais urticae.

Glacial cycles lead to periodic population interbreeding and isolation in warm-adapted species, which impact genetic structure and evolution. However, the effects of these processes on highly mobile and more cold-tolerant species are not well understood. This study aims to shed light on the phylogeographic history of Aglais urticae, a butterfly species with considerable dispersal ability, and a wide Palearctic distribution reaching the Arctic. Through the analysis of genomic data, four main genetic lineages are identified: European, Sierra Nevada, Sicily/Calabria/Peloponnese, and Eastern. The results indicate that the Sardo-Corsican endemic taxon ichnusa is a distinct species. The split between the relict lineages in southern Europe and the main European lineage is estimated to have happened 400-450 thousand years ago, with admixture observed during the Quaternary glacial cycles, and still ongoing, albeit to a much smaller extent. These results suggest that these lineages may be better treated as subspecific parapatric taxa. Ecological niche modelling supported the existence of both Mediterranean and extra-Mediterranean refugia during the glacial periods, with the main one located on the Atlantic coast. Nevertheless, gene flow between populations was possible, indicating that both differentiation and admixture have acted continuously across glacial cycles in this cold-tolerant butterfly, generally balancing each other but producing differentiated lineages in the southern peninsulas. We conclude that the population dynamics and the processes shaping the population genetic structure of cold-adapted species during the Quaternary ice ages may be different than those classically accepted for warm-adapted species.

A dynamic history of admixture from Mediterranean and Carpathian glacial refugia drives genomic diversity in the bank vole.

Understanding the historical contributions of differing glacial refugia is key to evaluating the roles of microevolutionary forces, such as isolation, introgression, and selection in shaping genomic diversity in present‐day populations. In Europe, where both Mediterranean and extra‐Mediterranean (e.g., Carpathian) refugia of the bank vole (Clethrionomys glareolus) have been identified, mtDNA indicates that extra‐Mediterranean refugia were the main source of colonization across the species range, while Mediterranean peninsulas harbor isolated, endemic lineages. Here, we critically evaluate this hypothesis using previously generated genomic data (>6,000 SNPs) for over 800 voles, focusing on genomic contributions to bank voles in central Europe, a key geographic area in considering range‐wide colonization. The results provide clear evidence that both extra‐Mediterranean (Carpathian) and Mediterranean (Spanish, Calabrian, and Balkan) refugia contributed to the ancestry and genomic diversity of bank vole populations across Europe. Few strong barriers to dispersal and frequent admixture events in central Europe have led to a prominent mid‐latitude peak in genomic diversity. Although the genomic contribution of the centrally located Carpathian refugium predominates, populations in different parts of Europe have admixed origins from Mediterranean (28%–47%) and the Carpathian (53%–72%) sources. We suggest that the admixture from Mediterranean refugia may have provisioned adaptive southern alleles to more northern populations, facilitating the end‐glacial spread of the admixed populations and contributing to increased bank vole diversity in central Europe. This study adds critical details to the complex end‐glacial colonization history of this well‐studied organism and underscores the importance of genomic data in phylogeographic interpretation.

Molecular biogeography of the fungus-dwelling saproxylic beetle Bolitophagus reticulatus indicates rapid expansion from glacial refugia

Abstract The geographical distributions of species associated with European temperate broadleaf forests have been significantly influenced by glacial–interglacial cycles. During glacial periods, these species persisted in Mediterranean and extra-Mediterranean refugia and later, during interglacial periods, expanded northwards. The widespread saproxylic beetle Bolitophagus reticulatus depends closely on European temperate broadleaf forests. It usually develops in the tinder fungus Fomes fomentarius, a major decomposer of broadleaf-wood. We sampled B. reticulatus in sporocarps from European beech (Fagus sylvatica) and Oriental beech (Fagus orientalis) across Europe and the Caucasus region. We analysed mitochondrial gene sequences (cox1, cox2, cob) and 17 microsatellites to reconstruct the geographical distribution of glacial refugia and postglacial recolonization pathways. We found only marginal genetic differentiation of B. reticulatus, except for a significant split between populations of the Caucasus region and Europe. This indicates the existence of past refugia south of the Great Caucasus, and a contact zone with European populations in the Crimean region. Further potential refugia might have been located at the foothills of the Pyrenees and in the Balkan region. Our genetic data suggest a phalanx-wise recolonization of Europe, a reflection of the high mobility of B. reticulatus.

The Carpathians hosted extra-Mediterranean refugia-within-refugia during the Pleistocene Ice Age: genomic evidence from two newt genera

Part of Europe’s temperate species survived the Pleistocene glacial cycles in refugia north of the Mediterranean peninsulas. For one such extra-Mediterranean refugia, the Carpathians, an intricate ‘refugia-within-refugia’ scenario has been suggested, involving species surviving in multiple discrete glacial refugia. We test the Carpathian refugia-within-refugia hypothesis, employing genome-wide multilocus data sets for two newt species (Triturus cristatus and Lissotriton montandoni). We first use Bayesian clustering to delineate intraspecific evolutionary lineages. The number of intraspecific lineages identified, and the allocation of localities to these lineages, were used to construct testable hypotheses on the spatial arrangement of glacial refugia in both newt species. Next we employ approximate Bayesian computation to date whether these lineages are of Holocene ( 12 Ka) origin. We identify three intraspecific evolutionary lineages for T. cristatus and two for L. montandoni. For both newt species, intraspecific divergence is rooted in the Pleistocene, in line with species survival in distinct range fragments during the last glacial period. Hence, our findings firmly support the Carpathian refugia-within-refugia hypothesis. Furthermore, we show that mitochondrial DNA overestimates the age of intraspecific evolutionary lineages and we urge caution in basing refugia-within-refugia scenarios on mitochondrial DNA alone.

Extra-Mediterranean glacial refugia in a Mediterranean faunal element: the phylogeography of the chalk-hill blue Polyommatus coridon (Lepidoptera, Lycaenidae)

Most warm-adapted Central European species are thought to have survived ice ages exclusively in Mediterranean refugia. During recent years, this point of view has been questioned. Therefore, we tested the hypothesis that extra-Mediterranean refugia also played a role in warm-adapted insect species and selected the chalk-hill blue, Polyommatus coridon. We sequenced two mitochondrial loci (COI, CR) in 150 individuals from 30 populations covering nearly the complete range. Minimum spanning networks and other statistical analyses concordantly revealed four genetic lineages with strong phylogeographic signal: a western group in Italy, France and western/central Germany, an eastern lineage in the Balkan Peninsula, the Carpathian Basin and eastern Central Europe, an Alpine group with populations in the Alps and southern Germany and a Pyrenean group. Our results are generally consistent with previous analyses for P. coridon based on allozymes and DNA sequences, but provide additional insights. We propose that these four lineages have evolved during allopatry in different glacial refugia, two in typical Mediterranean refugia (Apennines and Balkan Peninsulas), but two in extra-Mediterranean areas south of the Alps and Pyrenees. This supports survival of warm-adapted organisms in these regions in close geographic proximity to the refugia of high mountain species.

Phylogeography of social polymorphism in a boreo-montane ant.

BackgroundThe disjunct distribution of several Palearctic species has been widely shaped by the changes in climatic conditions during the Quaternary. The observed genetic differentiation or reproductive isolation between extant populations may be the outcome of their contemporary geographic separation or reproductive incompatibility due to differences in phenotypic traits which have evolved in isolated refugia. In the boreal ant Leptothorax acervorum, colonies from central and peripheral populations differ in social structure: colonies from Central and Northern Europe may contain several equally reproductive queens (facultative polygyny), while in colonies from peripheral populations in Spain only one the most dominant of several queens lays eggs (functional monogyny). By reconstructing the specie’s evolutionary and demographic history in Southwestern Europe we examine whether variation in social organization is associated with restricted gene flow between the two social forms.ResultsWe show that multi-queen colonies from all so far known inner Iberian populations of L. acervorum are functionally monogynous, whereas multi-queen colonies from all Pyrenean populations are polygynous, like those from other previously studied areas in Europe. Our analyses revealed complex spatial-genetic structure, but no association between spatial-genetic structure and social organization in SW-Europe. The population in the western Pyrenees diverged most strongly from other Iberian populations. Moreover, microsatellite data suggest the occurrence of recent bottlenecks in Pyrenean and inner Iberian populations.ConclusionsOur study shows a lack of reproductive isolation between the two social forms in SW-Europe. This in turn suggests that demographic and spatial patterns in genetic variation as well as the distribution of social phenotypes are better explained by co-variation with climatic, ecological, and historical factors. Moreover, we for the first time show the existence of substantial spatial-genetic structure in L. acervorum, suggesting the existence of multiple refugia in SW-Europe, including two extra-Mediterranean refugia in France. While gene flow among inner Iberian refugia may have been larger during the late glacial, extra-Mediterranean refugia in southern France may have contributed to the post-glacial recolonization of W-Europe.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0711-3) contains supplementary material, which is available to authorized users.

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

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.

Extra-Mediterranean refugia: The rule and not the exception?

Some decades ago, biogeographers distinguished three major faunal types of high importance for Europe: (i) Mediterranean elements with exclusive glacial survival in the Mediterranean refugia, (ii) Siberian elements with glacial refugia in the eastern Palearctic and only postglacial expansion to Europe and (iii) arctic and/or alpine elements with large zonal distributions in the periglacial areas and postglacial retreat to the North and/or into the high mountain systems. Genetic analyses have unravelled numerous additional refugia both of continental and Mediterranean species, thus strongly modifying the biogeographical view of Europe. This modified notion is particularly true for the so-called Siberian species, which in many cases have not immigrated into Europe during the postglacial period, but most likely have survived the last, or even several glacial phases, in extra-Mediterranean refugia in some climatically favourable but geographically limited areas of southern Central and Eastern Europe. Recently, genetic analyses revealed that typical Mediterranean species have also survived the Last Glacial Maximum in cryptic northern refugia (e.g. in the Carpathians or even north of the Alps) in addition to their Mediterranean refuge areas.