Parallel adaptation in autopolyploid Arabidopsis arenosa is 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. 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 discover significant parallelism in candidate genes involved in ion homeostasis. We further model parallel selection and infer 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.

Repeated genetic adaptation to altitude in two tropical butterflies

“…High altitude differentiation at the same locus could be driven by the same or different haplotypes under selection. For instance, different de-novo mutations at one locus were recently found to confer parallel adaptation to toxic soils in Arabidopsis , although most parallel regions were sourced from a common pool of standing alleles 75 . To test whether our candidate regions shared the same haplotypes, we performed local Principal Component Analyses (PCA) with outlier windows of each SHDR (Fig.…”

A simple conceptual framework and nomenclature for studying repeated, parallel and convergent evolution

“…De novo mutation can happen repeatedly (Konečná et al, 2021;Fulgione et al, 2022), especially in hotspots of adaptive variation, as discussed above (Xie et al, 2019). Repeated events of gene flow have also been shown (Jones et al, 2018;Giska et al, 2019;Stolle et al, 2022), and there can be a repeated recruitment of standing genetic variation in di erent lineages (Lai et al, 2019;Konečná et al, 2021). This, once again, highlights the need of coherent language.…”

“…A final, yet important consideration about these three patterns, concerns the 'repeated' nature of genome patterns, as all three can occur repeatedly, and result in repeated phenotypic evolution. De novo mutation can happen repeatedly (Konečná et al, 2021;Fulgione et al, 2022), especially in hotspots of adaptive variation, as discussed above (Xie et al, 2019). Repeated events of gene flow have also been shown (Jones et al, 2018;Giska et al, 2019;Stolle et al, 2022), and there can be a repeated recruitment of standing genetic variation in di erent lineages (Lai et al, 2019;Konečná et al, 2021).…”

“…It is often the case that the genomic origin involves a complex genetic basis, where a mix of shared and non-shared genetic mechanisms may underpin a phenotype in di erent lineages (Table 1; see below on stickleback). Others consider that parallel evolution occurs when di erent mutations occur in di erent lineages, and these confer the same derived phenotype (Konečná et al, 2021).…”

“…Second, vague or imprecise terms are likely to impact early career researchers and newcomers to the field, who are sedimenting their knowledge, creating a superfluous barrier to their understanding. For instance, in biodiversity genomics parallel evolution has been used to refer to 'parallel changes at the molecular sequence level' (Natarajan et al, 2015), 'parallel replacements/substitutions' (Natarajan et al, 2015;Mendes et al, 2016;Lee et al, 2018), 'parallel evolution and fixation of mutations' (Stern, 2013), 'parallel selection on standing genetic variation' (Pease et al, 2016), 'parallel adaptation' (Stoltzfus & McCandlish, 2017;Bohutínská et al, 2021;Konečná et al, 2021;Szukala et al, 2022), 'parallel evolution of phenotypes' (Colosimo et al, 2005;Szukala et al, 2022), among other terms. Third, because nuances in the terms are likely field-specific (when considering developmental biology, physiology, ecology, genomics as di erent fields within biology), they may obstruct multidisciplinary e orts.…”