Expansion of the mangrove species Rhizophora mucronata in the Western Indian Ocean launched contrasting genetic patterns

Ludwig Triest,Dennis De Ryck,Hajaniaina Andrianavalonarivo Ratsimbazafy,Tom Van Der Stocken,Nico Koedam,Marc Kochzius,Tim Sierens,Magdalene Ngeve,Sophie Lorent,Rosa Van Der Ven

doi:10.1038/s41598-021-84304-8

Abstract

Estimates of population structure and gene flow allow exploring the historical and contemporary processes that determine a species’ biogeographic pattern. In mangroves, large-scale genetic studies to estimate gene flow have been conducted predominantly in the Indo-Pacific and Atlantic region. Here we examine the genetic diversity and connectivity of Rhizophora mucronata across a > 3,000 km coastal stretch in the Western Indian Ocean (WIO) including WIO islands. Based on 359 trees from 13 populations and using 17 polymorphic microsatellite loci we detected genetic breaks between populations of the (1) East African coastline, (2) Mozambique Channel Area (3) granitic Seychelles, and (4) Aldabra and northern Madagascar. Genetic structure, diversity levels, and patterns of inferred connectivity, aligned with the directionality of major ocean currents, driven by bifurcation of the South Equatorial Current, northward into the East African Coastal Current and southward into the Mozambique Channel Area. A secondary genetic break between nearby populations in the Delagoa Bight coincided with high inbreeding levels and fixed loci. Results illustrate how oceanographic processes can connect and separate mangrove populations regardless of geographic distance.

Highlights

Estimates of population structure and gene flow allow exploring the historical and contemporary processes that determine a species’ biogeographic pattern
As a null-hypothesis, we considered that over a broad geographical scale, R. mucronata populations in the Western Indian Ocean (WIO) would comprise a single evolutionarily significant unit and hypothesise that (1) highest genetic diversity levels will be found for populations located in the core region of the species’ distribution, whereas lower levels of genetic diversity will be found for populations on remote small islands; (2) spatial patterns of genetic differentiation will align with patterns of dominant contemporary ocean currents
Information retrieved from nuclear microsatellites in Rhizophora mucronata from the Western Indian Ocean (WIO) showed a clear genetic structure, largely corresponding to the dominant ocean currents in the region

Summary

Introduction

Estimates of population structure and gene flow allow exploring the historical and contemporary processes that determine a species’ biogeographic pattern. A recent quantitative assessment of this research revealed important taxonomic and geographical biases, with mangrove population connectivity having received minimal attention compared to for example fish, seagrasses and corals[1] Efforts to fill this gap are valuable, as connectivity determines the genetic diversity and structure of populations, increases the effective population size, while high connectivity can replenish degraded sites. The spatial scale of connectivity depends on the additive effect of different factors, such as propagule traits, the timing of propagule release, physical barriers, the availability of suitable habitats, and the spatiotemporal characteristics of the dispersal vectors[13] Oceanographic features such as eddies and regions of convergence may constrain, delay or prevent gene flow between nearby populations, rendering the isolation-by-distance (IBD) model too simplistic to explain observed genetic differentiation[14]. As more species are being studied, biogeographical “barriers” seem more permeable than previously thought and act as filters rather than impenetrable b arriers[18]

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