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

Periodic Reporting for period 4 - CVI_ADAPT (Unraveling the history of adaptation in an island model: Cape Verde Arabidopsis)

Reporting period: 2020-05-01 to 2021-04-30

Determining the genetic mechanisms underlying adaptation to challenging environments is a central goal in biology and also has practical applications for a broad range of critical issues in agriculture, conservation and medicine. Potential uses include developing sustainable crops tailored to local environments, managing vulnerable populations and species, and mitigating emerging risks from pathogens. However, reconstructing the details of adaptation is challenging and requires knowledge of the traits important for adaptation, the genetic variants that underlie these and a reconstruction of the evolutionary histories of these variants and traits.

Due to their isolation, islands can represent natural laboratories, or uncomplicated microcosms where fundamental principles of the evolutionary process can be revealed. 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.

There are several ways in which the results from this project may result in long-term benefits to advance knowledge and to eventually provide improvements to society. In this research, we have identified functional genetic loci that underlie adaptation to rapid shifts in climate (to a shorter growing season) and variation in soil mineral nutrients, photosynthetic efficiency, DNA methylation, and drought tolerance. These could potentially be used as starting points for agricultural improvement. We have established collaborations with organisations in Cape Verde that will continue after the funding ends.
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. 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. We wrote a perspective describing these patterns and relating our work to other recent work in A. thaliana population history (Fulgione and Hancock, New Phytologist 2018). More recently, we annotated structural variation using short-read sequencing data in a worldwide data set and conducted analyses to identify regions of the genome that were especially prone to or resistant to structural variation. We found that defense response genes were prone to contain structural variation and showed evidence that balancing selection was operating on these.

We have submitted two papers for publication that deal specifically with adaptation within the Cape Verde Islands (CVI) and are writing up several others. The first of the submitted papers releases the genetic data for the project and is the first description of the island population history. This paper shows that the CVI populations are as distinct as new species, that they adapted through multivariate changes involving several traits, and that an important early step in adaptation was convergent loss of function in two major flowering time genes (FRI and FLC). In the second paper, we show evidence for a two-step adaptive walk that rewired nutrient transport.

Tergemina, E., et al., A two-step adaptive walk rewires nutrient transport in a novel edaphic environment, in review.

Fulgione, A.*, Neto, C.*, et al., Parallel reduction in flowering time from new mutations enabled evolutionary rescue in colonizing Arabidopsis lineages, accepted Nature Communications, * represents multiple first authors.

Göktay, M., Fulgione, A., Hancock, A.M. A new catalogue of structural variants in A. thaliana lines from Africa, Eurasia and North America reveals a signature of balancing selection at defense response genes, Molecular Biology and Evolution 2021, doi:10.1093/molbev/msaa309.

Durvasula, A.*, Fulgione, A.*, et al., 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