Genomic signatures of convergent adaptation to Alpine environments in three Brassicaceae species

Abstract

It has long been discussed to what extent related species develop similar genetic mechanisms to adapt to similar environments. Most studies documenting such convergence have either used different lineages within species or surveyed only a limited portion of the genome. Here, we investigated whether similar or different sets of orthologous genes were involved in genetic adaptation of natural populations of three related plant species to similar environmental gradients in the Alps. We used whole‐genome pooled population sequencing to study genome‐wide SNP variation in 18 natural populations of three Brassicaceae (Arabis alpina, Arabidopsis halleri, and Cardamine resedifolia) from the Swiss Alps. We first de novo assembled draft reference genomes for all three species. We then ran population and landscape genomic analyses with ~3 million SNPs per species to look for shared genomic signatures of selection and adaptation in response to similar environmental gradients acting on these species. Genes with a signature of convergent adaptation were found at significantly higher numbers than expected by chance. The most closely related species pair showed the highest relative over‐representation of shared adaptation signatures. Moreover, the identified genes of convergent adaptation were enriched for nonsynonymous mutations, suggesting functional relevance of these genes, even though many of the identified candidate genes have hitherto unknown or poorly described functions based on comparison with Arabidopsis thaliana. We conclude that adaptation to heterogeneous Alpine environments in related species is partly driven by convergent evolution, but that most of the genomic signatures of adaptation remain species‐specific.

Genomic basis of parallel adaptation varies with divergence inArabidopsisand its relatives

“…We also did not find any evidence that our gene reuse candidates were under weaker selective constraint than other genic loci genome-wide. Nevertheless, we cannot exclude that changes in constraint contribute to the decreasing probability of gene reuse across Brassicaceae, as was also reported in (61). Second, protein evolution studies reported patterns of diminishing amino acid convergence over time due to the decreasing probability of hemiplasy, i.e., the gene tree discordance caused by incomplete lineage sorting and introgression (32, 33, 62).…”

Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives

“…Nevertheless, we cannot exclude that changes in constraint contribute to the decreasing probability of gene reuse across Brassicaceae, as was also reported in ref. 61. Second, protein evolution studies reported patterns of diminishing amino acid convergence over time due to the decreasing probability of hemiplasy (i.e., the gene tree discordance caused by incomplete lineage sorting and introgression) (33,34,62).…”

Arabis alpina: A perennial model plant for ecological genomics and life‐history evolution

“…Resequencing of 35 individuals from across the species range (Laenen et al, 2018) and 304 from the western Swiss Alps (Rogivue et al, 2019) represent outstanding examples for sequencing of natural plant populations, and the publicly available data offer opportunities for future population genomic analyses. Additional genomic resources for A. alpina include the whole-chloroplast genome sequence (Melodelima & Lobréaux, 2013) and a more fragmented reference genome assembly using individual and pooled-sample sequencing of a Swiss population (Rellstab et al, 2020).…”