Parallel reduction in flowering time from de novo mutations enable evolutionary rescue in colonizing lineages

ARTICLE https://doi.org/10.1038/s41467-022-28800-z OPEN Parallel reduction in flowering time from de novo mutations enable evolutionary rescue in colonizing lineages 1234567890():,; Andrea Fulgione1,2,3,9, Célia Neto 1,9, Ahmed F. Elfarargi 1, Emmanuel Tergemina 1, Shifa Ansari1, Mehmet Göktay1, Herculano Dinis4,5, Nina Döring1, Pádraic J. Flood1, Sofia Rodriguez-Pacheco1, Nora Walden 6,7, Marcus A. Koch 6, Fabrice Roux8, Joachim Hermisson2 & Angela M. Hancock 1,2 ✉ Understanding how populations adapt to abrupt environmental change is necessary to predict responses to future challenges, but identifying specific adaptive variants, quantifying their responses to selection and reconstructing their detailed histories is challenging in natural populations. Here, we use Arabidopsis from the Cape Verde Islands as a model to investigate the mechanisms of adaptation after a sudden shift to a more arid climate. We find genomewide evidence of adaptation after a multivariate change in selection pressures. In particular, time to flowering is reduced in parallel across islands, substantially increasing fitness. This change is mediated by convergent de novo loss of function of two core flowering time genes: FRI on one island and FLC on the other. Evolutionary reconstructions reveal a case where expansion of the new populations coincided with the emergence and proliferation of these variants, consistent with models of rapid adaptation and evolutionary rescue. 1 Max Planck Institute for Plant Breeding Research, Cologne, Germany. 2 Mathematics and Bioscience, Department of Mathematics and Max F. Perutz Labs, University of Vienna, Vienna, Austria. 3 Vienna Graduate School for Population Genetics, Vienna, Austria. 4 Parque Natural do Fogo, Direção Nacional do Ambiente, Praia, Santiago, Cabo Verde. 5 Associação Projecto Vitó, São Filipe, Fogo, Cabo Verde. 6 Centre for Organismal Studies (COS) Heidelberg, Biodiversity and Plant Systematics, Heidelberg University, Heidelberg, Germany. 7 Biosystematics, Wageningen University, Wageningen, The Netherlands. 8 LIPME, Université de Toulouse, INRAE, CNRS, Castanet-Tolosan, France. 9These authors contributed equally: Andrea Fulgione, Célia Neto. ✉email: NATURE COMMUNICATIONS | (2022)13:1461 | https://doi.org/10.1038/s41467-022-28800-z | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-022-28800-z O ne in eight of the world’s existing plant and animal species are at risk of extinction due to human-mediated environmental change1. To forecast and mitigate risk, it is necessary that we understand the mechanisms of adaptation to novel environmental challenges. On the one extreme, adaptation can be highly polygenic, with contributions from many small effect variants2–5. Conversely, when selection pressures are very strong and existing genetic variation is low, large-effect variants are expected to provide a crucial contribution to adaptation6–8. Theoretical models show the importance of genetic diversity and the strength of selection for shaping the architecture of adaptive response6,7,9–14. In practice, reconstructing detailed adaptive histories in natural populations is challenging. However, long-range colonization events can represent powerful natural experiments where populations are deposited in replicate in a new environment9,15–19. The resulting isolated populations provide an opportunity to examine evolutionary processes in the absence of confounding from admixture and secondary contact. A single Arabidopsis line from Cape Verde (Cvi-0) was collected 37 years ago20 and has since been studied extensively both at the phenotypic and genetic levels. This accession has been an enigma because it lies geographically and climatically far outside of the core range of Arabidopsis. The Cape Verde Islands (CVI) archipelago consists of ten islands located between 14.80 and 17.20 degrees north of the equator and 570 km from the coast of Senegal. The flora in CVI is a mix of native species that reached the islands via long-range dispersal from mainland Africa and Macaronesia and species introduced since 1456, when humans first settled in CVI21,22. Precipitation in CVI is limited and unpredictable—so that plants must grow quickly and reproduce in the short time when water is available21. The wealth of information for Cvi-0 together with the isolation of Arabidopsis in CVI provided a potentially powerful case to connect the genetic basis of adaptive change with ecological drivers and fitness differentials. Here, we sequence the genomes of 335 Arabidopsis lines from CVI and use a combination of population genetic inference and trait-mapping to reconstruct their evolutionary history. In small colonizing populations, the strength of genetic drift is strong14. However, in CVI Arabidopsis, where the colonizing population faced strong selection pressures, we find genome-wide signatures of adaptive evolution and show that parallel reduction in flowering time was a crucial first adaptive step. We identify functional variants responsible for an approximately 30-day reduction in flowering time and show these had a large selective advantage, consistent with expectations under the Fisher-Orr model of adaptation23,24. Finally, we discuss the relevance of our findings to observations in continental populations of A. thaliana and across species. Results Reconstructing demographic history of CVI Arabidopsis from genome-wide patterns of variation. We collected Arabidopsis across its distribution in CVI (Fig. 1a, Supplementary Fig. 1, Supplementary Data 1), where it is limited to the islands Santo Antão and Fogo, and sequenced complete genomes of 335 lines. Compared to Eurasian and Moroccan collection locations, the Arabidopsis habitat in Cape Verde is more arid (median aridity index in CVI: 0.21, Morocco: 0.25, Eurasia: 0.78; Mann–Whitney–Wilcoxon (MWW) for CVI-Eurasia: p = 3.41 × 10−35 and CVI-Morocco: p = 5.97 × 10−4) with higher precipitation seasonality (median in CVI: 144.24, Morocco: 54.00, Eurasia: 25.94; MWW CVI-Eurasia: p = 2.01 × 10−36 and CVI-Morocco: p = 3.8 × 10−11), and a shorter growing season (median in CVI: 3.5 months, Morocco: 8 months, Eurasia: 8 months; MWW CVI-Eurasia: p = 2.72 × 10−35 and CVIMorocco: p = 4.13 × 10−12) (Supplementary Fig. 2, Supplementary 2 Data 2). The strong climatic divergence of CVI suggests nascent CVI populations may have been subject to strong selection. We reconstructed the colonization history of CVI Arabidopsis by analysing CVI genomes together with published data25,26. Genome-wide, the two Cape Verde islands cluster tightly together and are nested within the Moroccan clade (Fig. 1b). Diversity within islands is 73.3- and 62.3-fold reduced compared to the continent (θW (Santo Antão) = 7.59 × 10−5, θW (Fogo) = 8.93 × 10−5, θW (Morocco) = 5.56 × 10−3; Supplementary Table 1) and there is almost no shared variation between the islands and Morocco or between the two Cape Verde Islands (F (...truncated)