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The population genomic structure of green turtles (Chelonia mydas) suggests a warm-water corridor for tropical marine fauna between the Atlantic and Indian oceans during the last interglacial

Abstract

The occasional westward transport of warm water of the Agulhas Current, “Agulhas leakage”, around southern Africa has been suggested to facilitate tropical marine connectivity between the Atlantic and Indian oceans, but the “Agulhas leakage” hypothesis does not explain the signatures of eastward gene flow observed in many tropical marine fauna. We investigated an alternative hypothesis: the establishment of a warm-water corridor during comparatively warm interglacial periods. The “warm-water corridor” hypothesis was investigated by studying the population genomic structure of Atlantic and Southwest Indian Ocean green turtles (N = 27) using 12,035 genome-wide single nucleotide polymorphisms (SNPs) obtained via ddRAD sequencing. Model-based and multivariate clustering suggested a hierarchical population structure with two main Atlantic and Southwest Indian Ocean clusters, and a Caribbean and East Atlantic sub-cluster nested within the Atlantic cluster. Coalescent-based model selection supported a model where Southwest Indian Ocean and Caribbean populations diverged from the East Atlantic population during the transition from the last interglacial period (130–115 thousand years ago; kya) to the last glacial period (115–90 kya). The onset of the last glaciation appeared to isolate Atlantic and Southwest Indian Ocean green turtles into three refugia, which subsequently came into secondary contact in the Caribbean and Southwest Indian Ocean when global temperatures increased after the Last Glacial Maximum. Our findings support the establishment of a warm-water corridor facilitating tropical marine connectivity between the Atlantic and Southwest Indian Ocean during warm interglacials.

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Fig. 1: Map showing the sampling locations (stars) and sample sizes per location used in the present study: Caribbean (CA), East Atlantic (EA) and Southwest Indian Ocean (SWO) as well as a proposed phylogeography based upon the findings of the present and previous studies (Encalada et al. 1996; Bourjea et al. 2007; Naro-Maciel et al. 2014; Jensen et al. 2019).
Fig. 2: Migration and population divergence models tested in the present study using data from the Caribbean (CA; θ1), East Atlantic (EA; θ2) and Southwest Indian Ocean (SWO; θ3).
Fig. 3: Genetic differentiation as a function of sample size based upon simulated data.
Fig. 4: Mean likelihood of K (left; A and C) and ∆K (right panels; B and D) for up to K = 5 clusters with 15 replicates per K estimated using STRUCTURE.
Fig. 5: Posterior group membership probabilities estimated using model-based clustering.
Fig. 6: Co-ancestry matrix showing the degree of shared ancestry among Caribbean (CA), East Atlantic (EA) and Southwest Indian Ocean (SWO) samples.

Data availability

Raw sequencing data has been deposited in Dryad (https://doi.org/10.5061/dryad.31zcrjdmd). Simulation scripts have been deposited in Zenodo (https://doi.org/10.5281/zenodo.5513679) and are also available at GitHub (https://github.com/jpvdz/green-turtle-sims).

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Acknowledgements

We thank all volunteers of Sea Turtle Conservation Bonaire who contributed to sample collection in Bonaire, in particular Hans and Jannie Koning, and Gielmon “Funchi“ Egberts. We thank Géraud Leroux for providing samples from the Barren Isles, Madagascar, and thank Nuno dos Santos for providing samples from Príncipe Island, São Tomé and Príncipe. This study was carried out as part of the project “Ecology and conservation of green and hawksbill turtles in the Dutch Caribbean” funded by the Netherlands Organization of Scientific Research (NWO-ALW 858.14.090).

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JPZ designed the study with input from PJP. JPZ, MJAC and MN collected samples in Bonaire. MN and KS provided logistical-, and field support in Bonaire. FH arranged and coordinated sample collection in Madagascar. AAN arranged and coordinated sample collection in São Tomé and Príncipe. JPZ and MB performed DNA extractions. MB created ddRAD libraries. JPZ performed bioinformatic-, and data analyses. MJAC, MN, LEB and PJP obtained funding. JPZ and PJP coordinated the writing of the manuscript with input from all authors.

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Correspondence to Jurjan P. van der Zee.

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van der Zee, J.P., Christianen, M.J.A., Bérubé, M. et al. The population genomic structure of green turtles (Chelonia mydas) suggests a warm-water corridor for tropical marine fauna between the Atlantic and Indian oceans during the last interglacial. Heredity 127, 510–521 (2021). https://doi.org/10.1038/s41437-021-00475-0

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