Climatic adaptation explains responses to Pleistocene oscillations and diversification in European vipers

Abstract

AimAllopatric speciation is the primary mode of diversification in the Mediterranean Basin. However, the contribution of climatic adaptation during this process is contradictory. In this work, we investigate the eco‐evolutionary processes that drove diversification in this region, using European vipers as a case study. We describe the climatic requirements of different lineages to compare their responses to the Pleistocene climatic oscillations and tackle the evolutionary mechanisms underlying their diversification.LocationEurasia and North Africa.TaxonEuropean vipers (genus Vipera).MethodsWe used ecological niche modelling (ENM) to identify the climatic requirements of 24 Vipera lineages and infer past range dynamics associated with their diversification during the Pleistocene. To test whether climatic niches varied across lineages, we calculated the phylogenetic signal of different climatic variables and examined the relationship with phylogenetic relatedness. To investigate climatic niche evolution and test for phylogenetic niche conservatism (PNC), we quantified pairwise niche overlap in sister phylogenetic units under a 3D hypervolume approach.ResultsENM identified temperature annual range, precipitation of wettest month and precipitation of driest quarter as the most important climatic variables related to the distribution of most lineages, validating Pelias clade as cold‐adapted, and Vipera 1 and Vipera 2 as warm‐adapted clades. Projections to past conditions varied among clades, with Pelias and Vipera 1 having more similar responses, while Vipera 2 exhibited greater variability. We found significant phylogenetic signal in one temperature‐related and two humidity‐related climatic variables and detected high complexity in ecological niche evolution across the phylogeny, both rejecting the hypothesis of PNC.Main ConclusionsClimatic adaptation played a significant role in driving diversification among European vipers. Cold‐adapted and warm‐adapted lineages presented similar climatic requirements and remarkable responses to Pleistocene stages, resulting in an intricate pattern of niche divergence along the phylogeny that favours local adaptation rather than PNC.

Inferring current and Last Glacial Maximum distributions are improved by physiology‐relevant climatic variables in cold‐adapted ectotherms

“…This spatial diversity in biophysical conditions is relevant in terms of local selective forces especially for cold‐adapted species. Notably, past climatic environments may have influenced the mechanisms of differentiation between lineages, as well as their persistence (Horreo et al., 2021; Lucchini et al., 2023; Martínez‐Freiría et al., 2020). Furthermore, studies are required to address potential ecophysiological variations among lineages to better understand cold‐climate adaptations (Lourdais et al., 2013).…”

“…Climatic oscillations, such as those occurring during the Pleistocene (2.6 to 0.2 Mya), are recognized as major drivers of diversification worldwide (Hewitt, 2000(Hewitt, , 2004. Phylogeographic studies have recurrently linked the uncovered patterns of intraspecific genetic structure and diversity to the repeated warming-cooling cycles of the Pleistocene (Calatayud et al, 2019;Ehl et al, 2021;Lucchini et al, 2023). Over these cycles, species were forced to retract or spread in accordance with their ecological and physiological tolerances (Stewart et al, 2010).…”

“…We developed predictions from two sets of predictors, that is physiologically meaningful climatic variables (PMV) and freely available BioV that have been widely used to describe ectotherms realized climatic niche (e.g. Lucchini et al., 2023; Martínez‐Freiría et al., 2020). We then assessed and compared their ability to predict current and LGM species ranges, considering phylogeographic data indicating the Pleistocene refugia locations for the latter.…”

Range-Wide Phylogeography and Ecological Niche Modeling Provide Insights into the Evolutionary History of the Mongolian Racerunner (Eremias argus) in Northeast Asia

“…For example, Plethodon serratus has been shown to fit a model of GM expansion [8], which is contrary to the common assumption of contraction into refugia during the LGM. Recently, another good case for testing the responses of cold-adapted and warm-adapted ectotherms in the Northern Hemisphere has been documented in European vipers [9]. Thus, the effects of the Pleistocene glacial cycles on the biotic elements are expected to vary between regions and differ between species, depending largely on the natural history and adaptation (e.g., environmental tolerance and dispersal ability) of organisms (e.g., [10][11][12][13]).…”