Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana

Abstract Background Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and per...

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Main Authors: Antonio R. Castilla, Belén Méndez-Vigo, Arnald Marcer, Joaquín Martínez-Minaya, David Conesa, F. Xavier Picó, Carlos Alonso-Blanco
Format: Article
Language:English
Published: BMC 2020-06-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-020-01635-2
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author Antonio R. Castilla
Belén Méndez-Vigo
Arnald Marcer
Joaquín Martínez-Minaya
David Conesa
F. Xavier Picó
Carlos Alonso-Blanco
author_facet Antonio R. Castilla
Belén Méndez-Vigo
Arnald Marcer
Joaquín Martínez-Minaya
David Conesa
F. Xavier Picó
Carlos Alonso-Blanco
author_sort Antonio R. Castilla
collection DOAJ
description Abstract Background Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and persist in changing environments. We tested three major hypotheses accounting for genetic differentiation—isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR)—in the annual plant Arabidopsis thaliana across the Iberian Peninsula, the region with the largest genomic diversity. To that end, we sampled, genotyped with genome-wide SNPs, and analyzed 1772 individuals from 278 populations distributed across the Iberian Peninsula. Results IBD, and to a lesser extent IBE, were the most important drivers of genetic differentiation in A. thaliana. In other words, dispersal limitation, genetic drift, and to a lesser extent local adaptation to environmental gradients, accounted for the within- and among-population distribution of genetic diversity. Analyses applied to the four Iberian genetic clusters, which represent the joint outcome of the long demographic and adaptive history of the species in the region, showed similar results except for one cluster, in which IBR (a function of landscape heterogeneity) was the most important driver of genetic differentiation. Using spatial hierarchical Bayesian models, we found that precipitation seasonality and topsoil pH chiefly accounted for the geographic distribution of genetic diversity in Iberian A. thaliana. Conclusions Overall, the interplay between the influence of precipitation seasonality on genetic diversity and the effect of restricted dispersal and genetic drift on genetic differentiation emerges as the major forces underlying the evolutionary trajectory of Iberian A. thaliana.
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spelling doaj.art-bfc19d79f3eb45c3af783a4910b2c5e22022-12-21T21:49:15ZengBMCBMC Evolutionary Biology1471-21482020-06-0120111310.1186/s12862-020-01635-2Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thalianaAntonio R. Castilla0Belén Méndez-Vigo1Arnald Marcer2Joaquín Martínez-Minaya3David Conesa4F. Xavier Picó5Carlos Alonso-Blanco6Centre for Applied Ecology “Prof. Baeta Neves”, InBIO, School of Agriculture, University of LisbonDepartamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC)CREAF, Centre de Recerca Ecològica i Aplicacions ForestalsBCAM - Basque Center for Applied MathematicsDepartament d’Estadística i Investigació Operativa, Universitat de ValènciaDepartamento de Ecología Integrativa, Estación Biológica de Doñana (EBD), Consejo Superior de Investigaciones Científicas (CSIC)Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC)Abstract Background Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and persist in changing environments. We tested three major hypotheses accounting for genetic differentiation—isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR)—in the annual plant Arabidopsis thaliana across the Iberian Peninsula, the region with the largest genomic diversity. To that end, we sampled, genotyped with genome-wide SNPs, and analyzed 1772 individuals from 278 populations distributed across the Iberian Peninsula. Results IBD, and to a lesser extent IBE, were the most important drivers of genetic differentiation in A. thaliana. In other words, dispersal limitation, genetic drift, and to a lesser extent local adaptation to environmental gradients, accounted for the within- and among-population distribution of genetic diversity. Analyses applied to the four Iberian genetic clusters, which represent the joint outcome of the long demographic and adaptive history of the species in the region, showed similar results except for one cluster, in which IBR (a function of landscape heterogeneity) was the most important driver of genetic differentiation. Using spatial hierarchical Bayesian models, we found that precipitation seasonality and topsoil pH chiefly accounted for the geographic distribution of genetic diversity in Iberian A. thaliana. Conclusions Overall, the interplay between the influence of precipitation seasonality on genetic diversity and the effect of restricted dispersal and genetic drift on genetic differentiation emerges as the major forces underlying the evolutionary trajectory of Iberian A. thaliana.http://link.springer.com/article/10.1186/s12862-020-01635-2Genetic diversityGenetic structureIberian PeninsulaNested maximum-likelihood population effect modelsPrecipitation seasonalitySpatial hierarchical Bayesian models
spellingShingle Antonio R. Castilla
Belén Méndez-Vigo
Arnald Marcer
Joaquín Martínez-Minaya
David Conesa
F. Xavier Picó
Carlos Alonso-Blanco
Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
BMC Evolutionary Biology
Genetic diversity
Genetic structure
Iberian Peninsula
Nested maximum-likelihood population effect models
Precipitation seasonality
Spatial hierarchical Bayesian models
title Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
title_full Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
title_fullStr Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
title_full_unstemmed Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
title_short Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana
title_sort ecological genetic and evolutionary drivers of regional genetic differentiation in arabidopsis thaliana
topic Genetic diversity
Genetic structure
Iberian Peninsula
Nested maximum-likelihood population effect models
Precipitation seasonality
Spatial hierarchical Bayesian models
url http://link.springer.com/article/10.1186/s12862-020-01635-2
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