Rapid Parallel Adaptation to Anthropogenic Heavy Metal Pollution

Abstract

The impact of human-mediated environmental change on the evolutionary trajectories of wild organisms is poorly understood. In particular, species’ capacities to adapt rapidly (in hundreds of generations or less), reproducibly and predictably to extreme environmental change is unclear. Silene uniflora is predominantly a coastal species, but it has also colonised isolated, disused mines with phytotoxic, zinc-contaminated soils. To test whether rapid, parallel adaptation to anthropogenic pollution has taken place, we used reduced representation sequencing (ddRAD) to reconstruct the evolutionary history of geographically proximate mine and coastal population pairs and found largely independent colonisation of mines from different coastal sites. Furthermore, our results show that parallel evolution of zinc tolerance has occurred without gene flow spreading adaptive alleles between mine populations. In genomic regions where signatures of selection were detected across multiple mine-coast pairs, we identified genes with functions linked to physiological differences between the putative ecotypes, although genetic differentiation at specific loci is only partially shared between mine populations. Our results are consistent with a complex, polygenic genetic architecture underpinning rapid adaptation. This shows that even under a scenario of strong selection and rapid adaptation, evolutionary responses to human activities (and other environmental challenges) may be idiosyncratic at the genetic level and, therefore, difficult to predict from genomic data.

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

“…It is rather surprising given the large pool of variation shared in this polyploid and recently diverged system (Konečná et al, 2021). However, it is consistent with an array of other studies showing similar levels of parallelism (Lai et al, 2019; Preite et al, 2019; Ji et al, 2020; Bohutínská et al, 2021; James, Wilkinson, et al, 2021; Papadopulos et al, 2021). Although, possibly high number of false-positive candidates resulting from F ST scans can lead to a decrease in the percentage of parallels.…”

“…This is rather surprising given the large pool of variation shared in this polyploid and recently diverged system (Konečná et al, 2021). However, it is consistent with an array of other studies showing similar levels of parallelism (Lai et al, 2019; Preite et al, 2019; Ji et al, 2020; Bohutínská et al, 2021; James, Wilkinson, et al, 2021; Papadopulos et al, 2021). Although, a possibly high number of false-positive candidates resulting from F ST scans and limits in the detection of soft sweeps (Hoban et al, 2016) can lead to a decrease in the percentage of parallels, another mechanism beyond sharing the same genes in repeated adaptation shall be sought, likely related to genetic redundancy and overall polygenic architecture of serpentine adaptation as it is explained below.…”

“…This shows the important role of genetic redundancy in rapid adaptations with a polygenic basis (Boyle et al, 2017; Barghi et al, 2020; Láruson et al, 2020). That genetic redundancy is an important factor underlying parallel adaptation towards complex environmental challenges that have been also shown in other systems such as in alpine Heliosperma pusillum (Trucchi et al, 2017; Szukala et al, 2021) or dune Senecio lauttus (James, Allsopp, et al, 2021), but also from more narrowly defined environments – metal-polluted mines in Silene uniflora (Papadopulos et al, 2021) or temperature adaptations in Drosophila simulans (Barghi et al, 2019). In summary, given the expected polygenic basis of adaptation, it is unlikely that limited gene-level parallelism simply reflects genetic architecture but rather represents an effect of genetic redundancy.…”

Rapid phenotypic differentiation and local adaptation in Japanese knotweed s.l. (Reynoutria japonica and R. × bohemica, Polygonaceae) invading novel habitats

“…In this study, we investigated how one of the world’s most invasive plants may be adapting to three different habitats on Long Island, NY. Many studies have demonstrated that significant differences in habitat characteristics can result in adaptive differentiation within species, even under high levels of gene flow between habitats (Antonovics and Bradshaw, 1970; Linhart and Grant, 1996; Sambatti and Rice, 2006; Papadopulos et al, 2021; Zerebecki et al, 2021 but see Leimu and Fischer, 2008). Introduced species in particular have been highlighted because they can evolve rapidly in response to novel conditions (Lee, 2002; Leger and Rice, 2007; Dlugosch and Parker, 2008).…”

Innate, High Tolerance to Zinc and Lead in Violets Confirmed at the Suspended Cell Level

“…Thus, adaptive tolerance would refer to the species whose individuals inhabiting only polluted areas possess this trait as a result of natural selection, whereas constitutive (innate) tolerance would refer to the species where all individuals (from polluted and non-polluted sites) manifest this feature. It has been confirmed that in some pseudometallophytes from other genera (e.g., Arabidopsis halleri , Silene uniflora ) sufficient genetic variation allows populations to adapt quickly to a single physiological stress (heavy metal) repeatedly in different places [ 26 , 27 ]. However, multiple origins of metallicolous populations have never been confirmed in violets.…”