The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome-wide dynamics of local adaptation in a lizard.

Alejandro Llanos-Garrido,José A Díaz,Javier Pérez-Tris

doi:10.1002/ece3.5872

Abstract

Local adaptation is a dynamic process by which different allele combinations are selected in different populations at different times, and whose genetic signature can be inferred by genome‐wide outlier analyses. We combined gene flow estimates with two methods of outlier detection, one of them independent of population coancestry (CIOA) and the other one not (ROA), to identify genetic variants favored when ecology promotes phenotypic convergence. We analyzed genotyping‐by‐sequencing data from five populations of a lizard distributed over an environmentally heterogeneous range that has been changing since the split of eastern and western lineages ca. 3 mya. Overall, western lizards inhabit forest habitat and are unstriped, whereas eastern ones inhabit shrublands and are striped. However, one population (Lerma) has unstriped phenotype despite its eastern ancestry. The analysis of 73,291 SNPs confirmed the east–west division and identified nonoverlapping sets of outliers (12 identified by ROA and 9 by CIOA). ROA revealed ancestral adaptive variation in the uncovered outliers that were subject to divergent selection and differently fixed for eastern and western populations at the extremes of the environmental gradient. Interestingly, such variation was maintained in Lerma, where we found high levels of heterozygosity for ROA outliers, whereas CIOA uncovered innovative variants that were selected only there. Overall, it seems that both the maintenance of ancestral variation and asymmetric migration have counterbalanced adaptive lineage splitting in our model species. This scenario, which is likely promoted by a changing and heterogeneous environment, could hamper ecological speciation of locally adapted populations despite strong genetic structure between lineages.

Highlights

Aranjuez and the two western populations, located at opposite extremes of the genetic gradient identified by multidimensional scaling analysis (MDS) and admixture analyses, scored high homozygosity for the outliers detected by ROA
The large Psammodromus provides an example of local adaptation in which the phenotype of individuals fits better to the expected from habitat characteristics than from population ancestry
Our combined analysis of phenotypic variation, population genetic structure and genetic polymorphisms subject to selection, allowed us to explore the sources of genetic variants favored in different ecological contexts in this system

Summary

Introduction

This source of ancestral genetic variation should be detected by ROA in the form of divergent outliers with high levels of homozygosity in populations at the extremes of the phenotypic (and environmental) gradient, but with higher than average heterozygosity in the Lerma population. In order to improve the interpretation of our outlier analyses, we estimated gene flow among populations to test whether there could be less opposition to immigration of genetically western lizards in Lerma than in other populations of the eastern lineage.

Objectives

Results

Conclusion