The sweet tabaiba or there and back again: phylogeographic history of the Macaronesian Euphorbia balsamifera

Ann Bot. 2024 Jan 10:mcae001. doi: 10.1093/aob/mcae001. Online ahead of print.

Abstract

Background and aims: Biogeographic relationships between the Canary Islands and northwest Africa are often explained by oceanic dispersal and geographic proximity. Sister-group relationships between Canarian and eastern African/Arabian taxa, the "Rand Flora" pattern, are rare among plants, and have been attributed to the extinction of northwestern African populations. Euphorbia balsamifera is the only representative species of this pattern that is distributed in the Canary Islands and northwest Africa; it is also one of few species present in all seven islands. Previous studies placed E. balsamifera African populations as sister to the Canarian populations, but they were based on herbarium samples with highly degraded DNA. Here, we test the extinction hypothesis by sampling new continental populations; we also expand the Canarian sampling to examine the dynamics of island colonization and diversification.

Methods: Using target enrichment with genome skimming, we reconstructed phylogenetic relationships within E. balsamifera, and between this species and its disjunct relatives. A SNP dataset obtained from the target sequences was used to infer population-genetic diversity patterns. We employed convolutional neural networks (CNNs) to discriminate among alternative Canary Islands colonization scenarios.

Key results: Results confirm the Rand Flora sister-group relationship between western E. balsamifera and E. adenensis in the Eritreo-Arabian region, and recover an eastern-western geographic structure among E. balsamifera Canarian populations. CNNs supported a scenario of east-to-west island colonization, followed by population extinctions in Lanzarote and Fuerteventura and recolonization from Tenerife and Gran Canaria; a signal of admixture between the eastern island and northwest African populations was recovered.

Conclusions: Populations of E. balsamifera from northwest Africa are not the remnants of an ancestral stock, but originated from migration events from Lanzarote and Fuerteventura. These results support the Surfing Syngameon Hypothesis for the colonization of the Canary Islands by E. balsamifera, but also a recent back-colonization to the continent.

Keywords: Africa; Canary Islands; Hyb-Seq; Population Genomics; Rand Flora; Single-Nucleotide Polymorphism; back-colonization; convoluted neural networks; island colonization models.