Madeiran Arabidopsis thaliana Reveals Ancient Long-Range Colonization and Clarifies Demography in Eurasia

Abstract

The study of model organisms on islands may shed light on rare long-range dispersal events, uncover signatures of local evolutionary processes, and inform demographic inference on the mainland. Here, we sequenced the genomes of Arabidopsis thaliana samples from the oceanic island of Madeira. These samples include the most diverged worldwide, likely a result of long isolation on the island. We infer that colonization of Madeira happened between 70 and 85 ka, consistent with a propagule dispersal model (of size ≥10), or with an ecological window of opportunity. This represents a clear example of a natural long-range dispersal event in A. thaliana. Long-term effective population size on the island, rather than the founder effect, had the greatest impact on levels of diversity, and rates of coalescence. Our results uncover a selective sweep signature on the ancestral haplotype of a known translocation in Eurasia, as well as the possible importance of the low phosphorous availability in volcanic soils, and altitude, in shaping early adaptations to the island conditions. Madeiran genomes, sheltered from the complexities of continental demography, help illuminate ancient demographic events in Eurasia. Our data support a model in which two separate lineages of A. thaliana, one originating in Africa and the other from the Caucasus expanded and met in Iberia, resulting in a secondary contact zone there. Although previous studies inferred that the westward expansion of A. thaliana coincided with the spread of human agriculture, our results suggest that it happened much earlier (20–40 ka).

On the postglacial spread of human commensal Arabidopsis thaliana: journey to the East

“…), and this scenario is consistent with the observation that the Iberian relicts had admixture with the European group at c . 20 ka (Fulgione et al ., ). Finally, at around 10 ka, the weedy nonrelict group expanded across Eurasia.…”

Archaic lineages broaden our view on the history of Arabidopsis thaliana

“…Contrary to the idea that the center of A. thaliana diversity lies within Eurasia, the joint analysis of variation across continents revealed evidence for deep divergence among several relict lineages (1001 Genomes Consortium, ; Durvasula et al ., ; Fulgione et al ., ; Zeng et al ., ; Zou et al ., ). Particularly surprising was the finding that all African populations, including South Africans and Tanzanians, are native and that all sampled African individuals represent relicts when compared to the major Eurasian clade (Durvasula et al ., ).…”

“…These two factors limited the scope of the conclusions that could be drawn. However, several recent studies examined complete genome sequences of accessions from outside Eurasia, including Africa (Durvasula et al ., ), Madeira (Fulgione et al ., ) and Central Asia (Zeng et al ., ; Zou et al ., ) and compared them to results from across Eurasia (1001 Genomes Consortium, ). These studies reveal several surprises and helped to reconcile previous inconsistencies, as outlined below.…”

“…Particularly surprising was the finding that all African populations, including South Africans and Tanzanians, are native and that all sampled African individuals represent relicts when compared to the major Eurasian clade (Durvasula et al ., ). Other notable findings are that the island of Madeira harbors the most extremely diverged individuals sampled to date (Fulgione et al ., ) and that diverged samples from Central Asia (Tibet, Zeng et al ., ; Yunnan, Zou et al ., ; Western Himalayas, Tyagi et al ., ; the Altai Mountains, Yin et al ., ) suggest additional refugia.…”

“…45 ka (Durvasula et al ., ; Zou et al ., ). This expanding lineage mixed with archaics in Iberia, resulting in the admixed Iberian relicts (Fulgione et al ., ), represented as brown and blue stripes.…”