Genomic Patterns of Local Adaptation under Gene Flow in Arabidopsis lyrata

Abstract

Short-scale local adaptation is a complex process involving selection, migration, and drift. The expected effects on the genome are well grounded in theory but examining these on an empirical level has proven difficult, as it requires information about local selection, demographic history, and recombination rate variation. Here, we use locally adapted and phenotypically differentiated Arabidopsis lyrata populations from two altitudinal gradients in Norway to test these expectations at the whole-genome level. Demography modeling indicates that populations within the gradients diverged <2 kya and that the sites are connected by gene flow. The gene flow estimates are, however, highly asymmetric with migration from high to low altitudes being several times more frequent than vice versa. To detect signatures of selection for local adaptation, we estimate patterns of lineage-specific differentiation among these populations. Theory predicts that gene flow leads to concentration of adaptive loci in areas of low recombination; a pattern we observe in both lowland-alpine comparisons. Although most selected loci display patterns of conditional neutrality, we found indications of genetic trade-offs, with one locus particularly showing high differentiation and signs of selection in both populations. Our results further suggest that resistance to solar radiation is an important adaptation to alpine environments, while vegetative growth and bacterial defense are indicated as selected traits in the lowland habitats. These results provide insights into genetic architectures and evolutionary processes driving local adaptation under gene flow. We also contribute to understanding of traits and biological processes underlying alpine adaptation in northern latitudes.

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…All calculations were performed using ScanTools_ProtEvol, and custom R scripts (github.com/mbohutinska/ProtEvol/selScans.R). Our FST-based detection of outlier windows was not largely biased towards regions with low recombination rate (as estimated based on the available A. lyrata recombination map 39 and also from our diploid population genomic data; Supplementary Text 2, Supplementary Figs. 8, 9).…”

“…To address our hypothesis at deeper phylogenetic scales, we performed a meta-analysis of gene-and function-level parallelism by complementing our data with gene candidate lists from six genome-wide studies of alpine adaptation from the Brassicaceae family [36][37][38][39][40][41] (species diverging 0.5 -18 millions of years ago 48,49 , Supplementary Tables 8, 9). We found significant parallelism both at the level of candidate genes (overlaps between 19 % of species pairs were significant, all within the Arabidopsis genus, p < 0.05, Fisher's exact test, Fig.…”

“…We analyzed all variants within 25 kb of the gene (both upstream and downstream) to capture the decay of genetic diversity to neutrality with genetic distance from the selected site. We used Ne = 800 000 inferred from A. thaliana genome-wide mutation rate 88 and nucleotide diversity in our sequence data ( Supplementary Table 4) and a recombination rate of 3.7e -8 determined from the closely related A. lyrata 39 . To determine whether the signal of parallel selection originated from adaptation to the foothill rather than alpine environment, we ran the method assuming that parallel selection acted on (i) two alpine populations or (ii) two foothill populations.…”

“…Here, we aimed to test this hypothesis and investigate whether allele reuse is a major mechanism. We used replicated instances of adaptation to a challenging alpine environment, spanning a range of divergence from populations to tribes within the plant family Brassicaceae [36][37][38][39][40][41] (Fig. 1a).…”

Impact of demography on linked selection in two outcrossing Brassicaceae species

“…Additionally, the effect of positive selection has been found to be stronger in C. grandiflora (Gossmann et al, 2010) which may also affect the diversity patterns. In turn, the recent colonization history of the studied A. lyrata population has been associated with local adaptation (Leinonen et al, 2009) which is likely to have shaped patterns of diversity at adaptive loci (Hämälä & Savolainen, 2019;Mattila et al, 2016;Mattila et al, 2017;Toivainen, Pyhäjärvi, Niittyvuopio, & Savolainen, 2014). However, the estimated proportion of adaptive substitutions relative to neutral divergence was <5% in both species.…”