Phylogeographic surveys and apomictic genetic connectivity in the North Atlantic red seaweed Mastocarpus stellatus

Abstract

The North Atlantic red alga Mastocarpus stellatus is characterized by two life histories (sexual-type and direct-type), which correspond to two geographically isolated breeding groups. These features enable M. stellatus to be an interesting model to investigate how environmental shift and apomictic propagation have influenced its population genetic structure, historical demography and distribution dynamic. To test these ideas, we obtained 456 specimens from 15 locations on both sides of the North Atlantic and sequenced portion of the nuclear internal transcribed spacer (ITS), mitochondrial cox2-3 region (COX) and plastid RuBisCo spacer (RLS). Median-joining networks and ML trees inferred from COX and RLS consistently revealed two gene lineages (mtDNA: CN, CS; cpDNA: RN, RS). The concatenated COX and RLS markers yielded three cytotypes: a northern CN-RN, a southern CS-RS and a mixed cytotype CS-RN, which enabled us to roughly separate samples into D (direct-type life-cycle) and S (sexual-type life-cycle) groups (northern CN-RN and mixed cytotype CS-RN=D; southern CS-RS=S). Pairwise FST analysis of the D group revealed a high level of genetic differentiation both along European coasts and across the Atlantic basin. Bayesian skyline plots (BSPs) and IMa analyses indicated that M. stellatus underwent slight demographic expansion at the late-Pleistocene, with the beginning of divergence between lineages dating to c. 0.189Ma (95%HPD: 0.083-0.385Ma). IMa analyses also revealed asymmetric genetic exchange among European populations and a predominant postglacial trans-Atlantic migration from Norway and Galway Bay to North America. Our study highlights the importance of phylogeographic approaches to discover the imprints of climate change, life histories and gene flow in driving population genetic connectivity and biogeographic distribution of intertidal seaweeds in the North Atlantic.