Parallel adaptation in autopolyploidArabidopsis arenosais dominated by repeated recruitment of shared alleles

Abstract

Relative contributions of pre-existing vs de novo genomic variation to adaptation are poorly understood, especially in polyploid organisms, which maintain increased variation. We assess this in high resolution using autotetraploid Arabidopsis arenosa, which repeatedly adapted to toxic serpentine soils that exhibit skewed elemental profiles. Leveraging a fivefold replicated serpentine invasion, we assess selection on SNPs and structural variants (TEs) in 78 resequenced individuals and discovered substantial parallelism in candidate genes involved in ion homeostasis. We further modelled parallel selection and inferred repeated sweeps on a shared pool of variants in nearly all these loci, supporting theoretical expectations. A single, striking exception is represented by TWO PORE CHANNEL 1, which exhibits convergent evolution from independent de novo mutations at an identical, otherwise conserved site at the calcium channel selectivity gate. Taken together, this suggests that polyploid populations can rapidly adapt to environmental extremes, calling on both pre-existing variation and novel polymorphisms.

Genomic basis and phenotypic manifestation of (non-)parallel serpentine adaptation inArabidopsis arenosa

“…For each population pair, we transplanted young seedlings into serpentine and non-serpentine soils from their original sites (i.e., S1 plant cultivated in S1 and N1 soil and vice versa) in a common garden (Faculty of Science Charles University, 200 m; methodological details are provided in Supplementary Methods) and tested for the interaction between the soil treatment and substrate of origin in selected fitness indicators (described further) as a proxy of local substrate adaptation. We observed initial differences already in germination and young rosette sizes (Konečná et al, 2021), and thus continued with the cultivation for the entire growing season until seed set.…”

“…Although occurring worldwide, serpentine outcrops are typically scattered as small edaphic ‘islands’, being surrounded by other less toxic substrates. This setup triggers parallel evolution via repeated colonization from the surrounding non-toxic substrates, which has been recently shown in the case of an autotetraploid Arabidopsis arenosa (Konečná et al, 2021). In its genetically highly diverse autotetraploid cytotype, low neutral genetic differentiation and recent split times between geographically proximal serpentine and non-serpentine populations indicate recent postglacial serpentine invasions that happened at least five times independently (Konečná et al, 2021).…”

“…We used already published individual resequencing data for serpentine (S1, S2, and S3) and non-serpentine (N1, N2, and N3) populations (7-8 individuals per population, 47 in total) from the study of Konečná et al (2021). Raw data are available as a BioProject PRJNA667586 and PRJNA325082.…”

“…Here, we used reciprocal transplants and asked to what extent the phenotypic evolution is repeatable during rapid parallel edaphic adaptation across three serpentine – non-serpentine A. arenosa population pairs. We hypothesize that in this recently postglacially diversified system with pervasive sharing of adaptive polymorphism (Konečná et al, 2021), genetic and phenotypic parallelism will be largely congruent. We quantified (i) genomic parallelism at genes (shared selection candidate loci) and functional pathways (shared gene ontology categories) and (ii) parallel phenotypic changes by scoring a diverse set of traits: fitness proxies, morphological functional traits and ion uptake.…”

Novelty and Convergence in Adaptation to Whole Genome Duplication

“…Evidence for this has come from both plants ( Arabidopsis arenosa/Arabidopsis lyrata [ Schmickl and Koch 2011 ]) and animals (the frog genus Neobatrachus [ Novikova et al 2020 ], reviewed in Schmickl and Yant 2021 ). In both examples WGD led to niche expansion ( Molina-Henao and Hopkins 2019 ; Novikova et al 2020 ) and the invasion of particularly challenging environments relative to the diploid: in the case of polyploid frogs, the desert ( Novikova et al 2020 ) and polyploid A. arenosa , metal-contaminated mines and serpentine barrens ( Arnold et al 2016 ; Preite et al 2019 ; Konečná et al 2021 ). Thus, although clear challenges must be overcome to function as a polyploid ( Bomblies et al 2015 ; Yant and Bomblies 2015 ; Baduel, Hunter, et al 2018 ), novel population genomic and ecological opportunities await a lineage that successfully adapts to a WGD state ( Yant and Bomblies 2015 ; Baduel, Hunter, et al 2018 ).…”