Phylogenomic and population genomic analyses reveal the spatial-temporal dynamics of diversification of the Nigella arvensis complex (Ranunculaceae) in the Aegean archipelago.

ABSTRACT

The continental-shelf islands of the Aegean Sea provide an ideal geographical setting for evolutionary-biogeographical studies but disentangling the relationships between palaeogeographical history and the times, orders of modes of taxon divergence is not straightforward. Here, we used phylogenomic and population genomic approaches, based on orthologous gene sequences and transcriptome-derived SNP data, to reconstruct the spatial-temporal evolution of the Aegean Nigella arvensis complex (Ranunculaceae; 11 out of 12 taxa). The group's early diversification in the Early/Mid-Pliocene (c. 3.77 Mya) resulted in three main lineages (Greek mainland vs. central Aegean + Turkish mainland/eastern Aegean islands), while all extant taxa are of Late Plio-/Early Pleistocene origin (c. 3.30-1.59 Mya). Demographic modelling of the outcrossing taxa uncovered disparate modes of (sub)speciation, including divergence with gene flow on the Greek mainland, para- or peripatric diversification across eastern Aegean islands, and a 'mixing-isolation-mixing (MIM)' mode of subspeciation in the Cyclades. The two selfing species (N. stricta, N. doerfleri) evolved independently from the outcrossers. Present-day island configurations are clearly insufficient to explain the spatial-temporal history of lineage diversification and modes of (sub)speciation in Aegean Nigella. Moreover, our identification of positively selected genes in almost all taxa calls into question that this plant group represents a case of 'non-adaptive' radiation. Our study revealed an episodic diversification history of the N. arvensis complex, giving new insight into the modes and drivers of island speciation and adaption across multiple spatiotemporal scales.