Migration history of Avicennia marina populations: a legacy of mangrove expansion on the Sunda Shelf

Ludwig Triest^1,2*Thi Thuy Hang Phan³Quang Doc Luong³Anne Bousquet-Mélou⁴Bich Thi Ngoc Do¹Tim Sierens¹Farid Dahdouh-Guebas²Nico Koedam^2,5,6Tom Van der Stocken¹

• ¹Vrije University Brussels, Brussels, Belgium
• ²Université libre de Bruxelles, Brussels, Belgium
• ³Hue University, Hue, North Central Coast, Vietnam
• ⁴Aix-Marseille Université, Marseille, Provence-Alpes-Côte d'Azur, France
• ⁵Ghent University, Ghent, East Flanders, Belgium
• ⁶Centre for Environmental Sciences, University of Hasselt, Diepenbeek, Limburg, Belgium

Mangrove forests maintain connectivity and stay genetically linked through ocean-dispersed propagules. Avicennia species exhibit a pronounced genetic structure following a stepping stone migration model, with connectivity patterns linked to strength and direction of ocean-surface currents. Present-day spatial genetic structure of A. marina populations are an imprint of connectivity. This allows to estimate their migration history in relation to coastal configuration and Holocene sea-level rise. We examined the genetic diversity, structure, as well as the demographic and evolutionary history of establishment for ten A. marina sites across coastal stretches of Vietnam, using nuclear microsatellite markers in 558 individual trees. Additionally, genome skimming of 24 samples allowed detailed analysis of complete chloroplast genome and nuclear ribosomal cistron sequences. Although A. marina grew mixed with A. alba, a NewHybrids analysis ensured only pure A. marina were considered in this study.Microsatellites revealed an overall low allelic diversity, though inbreeding, recent bottlenecks and strong differentiation of populations were detected. Genetic breaks along the coast were confirmed through AMOVA, structure, and barrier analyses, while RST > FST indicated an evolutionary signal of divergence consistent with isolation-by-distance. Migrate-n model tests and divMigrate analysis supported northward unidirectional stepping stone migration history. Approximate Bayesian Computation (ABC) demographic analysis indicated a Holocene expansion whereas an origin model demonstrated discrete migration events across Vietnam, with southern populations most closely related to a bottlenecked ancestral population.A haplotype network considering complete chloroplast genomes, revealed identical or nearly similar propagule sources of A. marina throughout central and northern Vietnam, thereby following most recent Holocene expansion on the northwestern Sunda Shelf. Microsatellites, chloroplast and rRNA cistron sequences confirmed uniqueness of A. marina from the southernmost peninsula and their far relatedness with other populations in Southeast Asia, suggesting a longer-term persistence since gradual Shelf flooding. It is additionally proposed that, besides ocean currents, coastal landforms such as shallow areas with broad river delta plumes, a wide mouth or strong discharge such as for the Mekong and Red River, may have caused a regional substructure and provide a quasi-permanent barrier to alongshore currents and mangrove connectivity. Perspectives on conservation issues of the species are provided.