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 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.

Keywords: Genetic diversity; Genetic structure; Iberian Peninsula; Nested maximum-likelihood population effect models; Precipitation seasonality; Spatial hierarchical Bayesian models.

Fig. 1

Distribution of populations, genetic diversity and temporal habitat changes of Iberian Arabidopsis thaliana populations. a Geographic distribution of the 278 A. thaliana populations of study across the Iberian Peninsula. Red and blue dots represent populations with zero and non-zero genetic diversity (H_S) values, respectively. b Frequency distribution of populations with zero and non-zero H_S values as a function of altitude. Mean altitude for both groups of populations is almost identical, as indicated by dashed lines. c Frequency distribution of populations with zero and non-zero H_S values. d Frequency distribution of the average percentage change between year intervals for each habitat type. Data from digitalized orthophotographs available from each population. For the sake of clarity, only one X-axis is shown, indicating the accumulation of populations with average percentage changes around zero. The map of Fig. 1a was obtained from the National Center for Geographic Information (CNIG) of Spain

Fig. 2

Geographic distribution of genetic diversity within Iberian Arabidopsis thaliana populations estimated by spatial hierarchical Bayesian modeling. a Distribution of populations with zero (N = 66; absence of genetic diversity) and non-zero (N = 212; presence of genetic diversity) genetic diversity (H_S) values. Darker and lighter intensities indicate higher and lower odds for populations with non-zero and zero H_S values, respectively. b Distribution of populations with H_S values higher than zero (N = 212). Darker and lighter intensities indicate higher and lower H_S values, respectively. In both cases, the uncertainty of spatial hierarchical Bayesian model is given as standard deviation units in small maps. Darker and lighter intensities indicate higher and lower uncertainty, respectively

Fig. 3

Genetic structure of the 278 Arabidopsis thaliana populations of study across the Iberian Peninsula depicting the four genetic clusters (NW-C1, NE-C2, relict-C3 and SW-C4). a Results from the Bayesian clustering method implemented in STRUCTURE. b Results from the Discriminant Analysis of Principal Components (DAPC). c Geographic distribution of homogeneous populations from each genetic cluster. Homogeneous populations (N = 230) were those with average membership proportions among individuals within populations greater than 0.3 for only one genetic cluster. Mixed or heterogeneous populations (N = 48) are also shown in grey. The map of Fig. 3c was obtained from the National Center for Geographic Information (CNIG) of Spain

Fig. 4

Effects of isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR) on genetic differentiation in Arabidopsis thaliana. a Coefficients (± SD) of the top-ranked nested maximum-likelihood population effects models (NMLPE) testing the effect of IBD, IBE and IBR on genetic differentiation in A. thaliana. b Model averaged coefficients (± SD) for three Principal Component (PC) axes accounting for more than 75% of the total variance. Model averaging was conducted using the subsample of models exhibiting ∆AIC < 2 regarding the top-ranked model, if more than one. In all cases, model estimates for the analysis conducted for the entire Iberian Peninsula (IP) and the four genetic clusters (NW-C1, NE-C2, relict-C3, and SW-C4) are shown. Maps with the geographic distribution of populations used in each analysis are also given. Maps were obtained from the National Center for Geographic Information (CNIG) of Spain