Extra-Mediterranean glacial refuges in barred and common grass snakes (Natrix helvetica, N. natrix)

Carolin Kindler,Uwe Fritz,Eva Graciá

doi:10.1038/s41598-018-20218-2

Abstract

Extra-Mediterranean glacial refugia of thermophilic biota, in particular in northern latitudes, are controversial. In the present study we provide genetic evidence for extra-Mediterranean refugia in two species of grass snake. The refuge of a widely distributed western European lineage of the barred grass snake (Natrix helvetica) was most likely located in southern France, outside the classical refuges in the southern European peninsulas. One genetic lineage of the common grass snake (N. natrix), distributed in Scandinavia, Central Europe and the Balkan Peninsula, had two distinct glacial refuges. We show that one was located in the southern Balkan Peninsula. However, Central Europe and Scandinavia were not colonized from there, but from a second refuge in Central Europe. This refuge was located in between the northern ice sheet and the Alpine glaciers of the last glaciation and most likely in a permafrost region. Another co-distributed genetic lineage of N. natrix, now massively hybridizing with the aforementioned lineage, survived the last glaciation in a structured refuge in the southern Balkan Peninsula, according to the idea of ‘refugia-within-refugia’. It reached Central Europe only very recently. This study reports for the first time the glacial survival of a thermophilic egg-laying reptile species in Central Europe.

Highlights

Climatic oscillations in the Pleistocene induced large-scale range shifts of many animal and plant species all over the world[1]
Our analyses of genetic diversities of mitochondrial DNA (mtDNA) suggest for the blue lineage of the barred grass snake (Natrix helvetica) and the red lineage of the common grass snake (N. natrix) glacial refugia in the south, close to the Mediterranean Sea or inland of the southern Balkan Peninsula
Such refugia are thought to be located in the southern peninsulas[1,4,5,34,35,36,37]

Summary

Introduction

Climatic oscillations in the Pleistocene induced large-scale range shifts of many animal and plant species all over the world[1]. Its northern range extension is controversial, with unambiguous records up to central Sweden and southern Finland and debated records close to the Arctic Circle further north in Fennoscandia[9,13,14] In any case, these two grass snake species are cold-tolerant compared to many other egg-laying reptile species[9]. These two grass snake species are cold-tolerant compared to many other egg-laying reptile species[9] This suggests that extra-Mediterranean refugia might have existed, like recently shown for the more thermophilic wall lizard (Podarcis muralis). For this species, extra-Mediterranean refugia were inferred for southern France, northern Italy, the eastern Alps and the Central Balkans[8]. The southern Balkan records of the yellow lineage are separated by an enigmatic distribution gap from the northern records, whereas the red lineage is continuously distributed from the southern Balkans to Central Europe (Fig. 1)[11,15]

Methods

Results

Conclusion