Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard

Maravillas Ruiz Miñano,Christopher P Burridge,Weizhao Yang,Daniele Salvi,Geoffrey M While,Tobias Uller

doi:10.1038/s41437-022-00518-0

Maravillas Ruiz Miñano, Christopher P Burridge + Show 4 more

Open Access

https://doi.org/10.1038/s41437-022-00518-0

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Abstract

Species distributed across climatic gradients will typically experience spatial variation in selection, but gene flow can prevent such selection from causing population genetic differentiation and local adaptation. Here, we studied genomic variation of 415 individuals across 34 populations of the common wall lizard (Podarcis muralis) in central Italy. This species is highly abundant throughout this region and populations belong to a single genetic lineage, yet there is extensive phenotypic variation across climatic regimes. We used redundancy analysis to, first, quantify the effect of climate and geography on population genomic variation in this region and, second, to test if climate consistently sorts specific alleles across the landscape. Climate explained 5% of the population genomic variation across the landscape, about half of which was collinear with geography. Linear models and redundancy analyses identified loci that were significantly differentiated across climatic regimes. These loci were distributed across the genome and physically associated with genes putatively involved in thermal tolerance, regulation of temperature-dependent metabolism and reproductive activity, and body colouration. Together, these findings suggest that climate can exercise sufficient selection in lizards to promote genetic differentiation across the landscape in spite of high gene flow.

Highlights

Understanding how the spatial distribution of environments shapes population differentiation is a shared goal of biogeography, ecology, and evolutionary biology
A redundancy analysis on these four significant distance-based Moran Eigenvector Maps (dbMEMs) as response variables resulted in four canonical axes that together explained 6.0% of the variation (F4,29 = 1.52, P < 0.001; Fig. 2; Table 1)
We investigated the relationship of genome-wide single nucleotide polymorphisms (SNPs) with climatic and spatial data across 34 populations of the common wall lizard (Podarcis muralis) in central Italy

Summary

Introduction

Understanding how the spatial distribution of environments shapes population differentiation is a shared goal of biogeography, ecology, and evolutionary biology. The balance between selection and gene flow determines the extent to which populations will diverge genetically along environmental gradients and exhibit adaptation to local environmental conditions (Savolainen et al 2013; Tigano and Friesen 2016; Yeaman and Otto 2011). Local adaptation is common in nature (e.g., Fraser et al 2011; Halbritter et al 2018; Hargreaves et al 2020) and can occur even with high levels of gene flow if selection is strong (Yeaman and Otto 2011; Savolainen et al: 2013; Tigano and Friesen 2016). Common garden experiments suggest that local physiological adaptation along climatic gradients is very common (Pettersen 2020) In line with these phenotypic effects, genotypeenvironment associations have been able to identify genetic differentiation of particular loci associated with climate (e.g., Rodríguez et al 2017; Prates et al 2018; Farleigh et al 2021; see Campbell-Staton et al 2016, 2017, 2020). It remains poorly understood to what extent climate is able to cause genome-wide population differentiation when the opportunity for gene flow is high

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