Phylogeography, evolutionary history and effects of glaciations in a species (Zootoca vivipara) inhabiting multiple biogeographic regions

Abstract

Aim: During glaciations, the distribution of temperate species inhabiting the Northern Hemisphere generally contracts into southern refugia; and in boreo-alpine species of the Northern Hemisphere, expansion from Northern refugia is the general rule. Little is known about the drivers explaining vast distributions of species inhabiting multiple biogeographic regions (major biogeographic regions defined by the European Environmental Agency). Here we investigate the fine-scale phylogeography and evolutionary history of the Eurasian common lizard (Zootoca vivipara), the terrestrial reptile with the world's widest and highest latitudinal distribution, that inhabits multiple biogeographic regions. Location: Eurasia. Methods:We generated the largest molecular dataset to date of Z. vivipara, ran phylogenetic analyses, reconstructed its evolutionary history, determined the location of glacial refuges and reconstructed ancestral biogeographic regions. Results:The phylogenetic analyses revealed a complex evolutionary history, driven by expansions and contractions of the distribution due to glacials and interglacials, and the colonization of new biogeographic regions by all lineages of Z. vivipara.Many glacial refugia were detected, most were located close to the southern limit of the Last Glacial Maximum. Two subclades recolonized large areas covered by permafrost during the last glaciation: namely, Western and Northern Europe and North-Eastern Europe and Asia. Main conclusions:In Z. vivipara, most of the glacial refugia were located in the South of their current distribution. Previous studies suggested the existence of Northern refuges, but the species' inability to overwinter on permafrost and the lack of genetic support suggest that the presence of a refugia in the north of the Alps is unlikely. This species currently inhabits boreo-alpine climates and retracted during previous glaciations into southern refugia, as temperate species. Two clades exhibited enormous geographic expansion that started from two distinct glacial refugia.These phylogeographic patterns were highly congruent with those of Vipera berus.Together they suggest that glacial retraction, the location of the refugia and absence of competition may have promoted the enormous geographic expansion of two clades.

Reversals in complex traits uncovered as reticulation events: Lessons from the evolution of parity‐mode, chromosome morphology, and maternal resource transfer

“…Here we tested, whether reticulation may explain potential reversals of complex traits, using two datasets with potential reversals in parity mode evolution that exhibited sufficient genetic coverage and reversals in other complex traits (W chromosome morphology and maternal resource transfer). Contrary to Dollo's law (1983), which states “that organisms cannot return, even partially, to a previous state already realized in its ancestral series”, the here derived phylogenetic trees for Cyprinodontiformes (Figure a) and Z. vivipara (Figure a) point to three reversals with statistical support in Cyprinodontiformes (a reversal to oviparity in the ancestor of T. gracilis and two reversals to placentotrophy in the ancestors of P. hollandi and P. elongate ; Figure ), which are congruent with conclusions from previous studies (Helmstetter et al, ; Pollux et al, ), and two reversals in Z. vivipara (one reversal to oviparity in the ancestor clade B and a reversal to the ancestral chromosome morphology in clade F; Figure a), which is also congruent with previous conclusions (Horreo, Palaez, Breedveld, et al, ).…”

“…In addition, we selected Zootoca vivipara , because models of parity‐mode evolution suggest the existence of a reversal from viviparity to oviparity (Surget‐Groba et al, ) and because the combination between phylogenetic and morphological studies suggest that a reversal may exist in the evolution of chromosome evolution (Horreo, Palaez, Breedveld, et al, ; Kupriyanova et al, ). Zootoca vivipara is the terrestrial squamate species with the largest natural distribution, ranging from northwest Spain and Ireland in the West to the Peninsula of Sakhalin (Russia) and Hokkaido (Japan) in the East, and from the southern Balkan (Bulgaria) and the Pyrenees in the south to the Arctic Circle.…”

“…It has seven well‐defined clades (Surget‐Groba et al, ), a bimodal reproductive pattern, and is a model species for the study of evolution, population dynamics, behavior, coloration, and physiology (Fitze & Le Galliard, ; Gonzalez‐Jimena & Fitze, ; Horvathova et al, ; San‐Jose, Peñalver‐Alcázar, Milá, Gonzalez‐Jimena, & Fitze, ). Because the existing genetic coverage was not sufficient for the envisaged analyses, we amplified three nuclear (nZV1, nZV2, and nZV3; Horreo, Peláez, Suárez, & Fitze, ) and three mitochondrial gene fragments (16S rDNA, 16S: Clary & Wolstenholme, ; cytochrome B, cytB: Smith & Patton, ; and NADH dehydrogenase 2, ND2: Macey, Larson, Ananjeva, Fang, & Papenfuss, ) in 24 individuals belonging to all extant clades (three individuals per clade; Surget‐Groba et al, ), except for clade B, from which 9 individuals were used, three per subclade; Horreo, Palaez, Breedveld, et al, ; Mila, Surget‐Groba, Heulin, Gosá, & Fitze, ) and two outgroups (Tables S2 and S3) following original protocols (Horreo, Peláez, Suárez, & Fitze, ). One specimen per population was used (Table S2).…”

“…Potential reversals have been detected in other complex traits (Oakley & Cunningham, ; Whiting et al, ), but discussion about their existence was less intense and for some traits discussion was almost absent (e.g., chromosome morphology, maternal resource transfer). For example, the combination of phylogenetic studies (Horreo, Palaez, Breedveld, et al, ) and studies on the chromosome morphology of Zootoca vivipara (Kupriyanova, Kuksin, & Odierna, ), suggests that there may exist a reversal in the morphology of the W chromosome, but this hypothesis has not been tested so far. Similarly, phylogenetic analyses of Cyprinodontiformes suggest reversals to oviparity (Helmstetter et al, ) and reversals in maternal resource transfer from placentotrophy to lecithotrophy (Pollux, Meredith, Springer, Garland, & Reznick, ).…”

Northern areas as refugia for temperate species under current climate warming: Atlantic salmon (Salmo salarL.) as a model in northern Europe

“…These patterns have been especially well documented in the northern hemisphere, especially in Europe and North America, with putative refugia and patterns of recolonization described for many organisms (Bidegaray‐Batista et al ., ; Deffontaine et al ., ; Horreo et al . , ; Nesbø et al ., ). However, under current global climate warming, this pattern may be reversed and in the future species may be pushed poleward, to find refuge in areas of their current northern distribution.…”