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Unraveling the history of adaptation in an island model: Cape Verde Arabidopsis

Periodic Reporting for period 3 - CVI_ADAPT (Unraveling the history of adaptation in an island model: Cape Verde Arabidopsis)

Reporting period: 2018-11-01 to 2020-04-30

Islands have played a pivotal role in evolutionary theory since Darwin and Wallace. Due to their isolation, they can represent natural laboratories, or uncomplicated microcosms where fundamental principles of the evolutionary process can be revealed. One area where island systems can provide a crucial advance is in evolutionary genetics. Here, a primary goal is to reconstruct the mechanisms, mode, and tempo of evolution by identifying specific adaptive functional variants and studying the historical dynamics of these in nature. However, even with recent advances in tools and technologies (e.g. affordable genome-wide sequencing, developments in genome manipulation), the complexity of most natural systems makes this a challenging task. In this research, we examine the evolutionary history of intriguing populations at the edge of the species range (Cape Verde Islands) to comprehensively characterize the adaptive process in this tractable and ecologically relevant island system.

A single individual Arabidopsis thaliana plant was collected 30 years ago from Cape Verde. Since Arabidopsis can be inbred, one plant can be propagated for many generations and it’s progeny can be used again and again for research. Due to its location far from other sampled Arabidopsis plants and divergent traits, progeny of this plant have been used extensively over the past 30 years to study the genetic basis of trait variation. From this work, we know a lot about the plant both at the level of its traits: strong seed dormancy, fast flowering, open stomata and a procumbent growth habit and at the level of the genetic loci and variants that underlie its trait differentiation. In this project, we went back to the site of collection of this plant and collected populations across the two Cape Verde Islands where Arabidopsis is found. Here, we combine field monitoring, population genetic analyses, trait mapping, powerful genome editing technology (CRISPR), and spatially explicit modelling to reconstruct the detailed history of adaption. By applying the wealth of tools available in Arabidopsis thaliana to this intriguing natural population, we are working to uncover general principles of adaptation and produce a roadmap and toolkit for future research in diverse systems to predict outcomes of environmental change.
At the outset of the funding period, in order to identify the closest outgroup to the Cape Verde populations, we sequenced the genomes of 78 Africans (mainly from the Moroccan Atlas Mountains) including herbarium specimen from locations where seeds were not available (South Africa and Algeria). In addition, to identify potential outgroup populations, we sequenced 48 individuals from the Canary Islands and 14 individuals from Madeira. By comparison to samples from Cvi-0 we have now identified a set of closest relatives and are using these as our outgroup individuals for crosses and phenotyping.

An unexpected bonus also came out of this work. We were surprised to find that the samples we sequenced from Africa all clustered far from the well-studied Eurasian populations and that they best represent the origin of the A. thaliana species, relative to all other sampled and sequenced individuals. That is, they carry more diversity at the S-locus (the locus involved in transition to selfing) and across the genome in general than other sampled populations. In addition, we inferred historical population sizes for each worldwide region and found evidence that the ancient population size was largest in Africa. We published these results in PNAS last year (Durvasula et. al., PNAS 2017).

As I mentioned above, we also sequenced Madeirans and Canary Islands populations. The Madeiran population appeared to diverge long ago (~80-90 kya) and turned out to be useful for making additional inferences about population history in Eurasia. Briefly, this population serves as a banked ancestor of the now-admixed Iberian relict population. Having this ‘parent’ population allowed us to gain new insights into the history of admixture and timing of population expansions in Eurasia. Another surprising result in this paper was that we found evidence for positive natural selection via a selective sweep for the ancestral haplotype of a well-studied inversion polymorphism on Chromosome 1. This was surprising because in Eurasia it is the derived haplotype that shows evidence of a sweep. We have been in discussions with a group that is following this result up to examine the pattern in more detail. Our study of Madeiran population history is published in Molecular Biology and Evolution, (Fulgione et al., MBE 2017).

In both studies we find surprising consistency between major climatic shifts and the timing of inferred migrations and population splits. A postdoc working on the project and I recently published an insight article describing these patterns and relating our work to other recent work in A. thaliana population history (Fulgione and Hancock, New Phytologist 2018).

References
Durvasula, A., Fulgione, A, Gütaker, R, Alacakaptan, S, Flood, P, Neto, C, Tsuchimatsu, T, Burbano, HA, Pico, XA, Alonso-Blanco, C, Hancock, AM. African genomes illuminate the early history of Arabidopsis thaliana, Proceedings of the National Academy of Sciences 2017, 114(20), 5213-5218.

Fulgione, A., Koornneef, M., Roux, F., Hermisson, J., Hancock, AM., Madeiran Arabidopsis thaliana Reveals Ancient Long-Range Colonization and Clarifies Demography in Eurasia, Molecular Biology and Evolution 2018, 35, 564–574.

Fulgione, A., Hancock, AM., Archaic lineages broaden our view on the history of Arabidopsis thaliana, New Phytologist 2018, Jun 4. Doi: 10.1111/nph. 15244.
We have identified new functional variants and are testing the effects of these on survival and reproductive success and modelling the evolutionary histories of these.
Picture taken in Fogo, Cape Verde Islands
Arabidopsis thaliana plant growing in Fogo, Cape Verde Islands
Picture taken in Cape Verde Islands
Arabidopsis thaliana plant growing in Fogo, Cape Verde Islands