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Evolutionary Dynamics of American Manatee Species on the Northern Coast of South America: Origins and Maintenance of an Interspecific Hybrid Zone

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Abstract

Interspecific hybridization has been historically neglected in research and conservation practice, but it is a common phenomenon in nature, and several models have been developed to characterize it genetically. Even though Trichechus inunguis (Amazonian manatee) and T. manatus (West Indian manatee) exhibit large morphological, karyotypic, and molecular differences, a hybrid zone was identified on the northern coast of South America, from the Amazon River estuary toward the Guianas coastline. Two major populations or evolutionarily significant units (ESUs) within T. manatus, namely, the Caribbean and Atlantic, were separated and their differentiation was likely promoted or reinforced by the interspecific hybridization zone. We used nuclear and mtDNA sequences to reconstruct manatee speciation, population diversification through time and space, and secondary contact, which resulted in a hybrid zone. In this hybrid zone, the genetic contribution of each parental species was estimated, and different models for generating the current scenario were tested using statistical phylogeographic tools. All the results suggest a long hybridization history, during which a stable and structured hybrid swarm is generated. The coastline hybrid zone is composed of individuals with a lesser genomic contribution from T. inunguis; this zone works as a genetic sink that restricts gene flow between neighbouring Atlantic (Brazil) and Caribbean (all others) T. manatus populations, which further reinforces the isolation and differentiation of the Brazilian manatees.

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Data Availability

The datasets analysed during the current study are referenced in the text and are publicly available (see SI, Table S1). New sequences have been deposited in GenBank under ID OR594249, OR594250, OR594251, OR594252, OR594253, OR594254, OR594255, OR594256, OR594257, OR594258 and OR594259.

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Acknowledgements

CSL was supported by a CAPES (Brazil) Ph.D. fellowship, and FRS was supported by a CNPq (Brazil) research fellowship. This project was performed under ICMBio/SISBIO permit 45028 and received funding support from FAPEMIG, CNPq, Programa Petrobras Socioambiental – PETROBRAS (Projeto Manati), and Fundação Grupo O Boticário from Brazil. Samples from Florida (USA) and Puerto Rico were obtained from Robert K. Bonde (USGS/Florida, USA). We thank ICMBio (CMA and CEPENE) for supplying the 19 T. manatus samples from the northeast coast of Brazil. Samples from French Guiana were originally kept in the database JAGUARS at Cayenne, French Guiana. The JAGUARS tissue collection is supported by the Collectivité Territoriale de Guyane and the Direction Générale des Territoires et de la Mer, Guyane. The use of the genetic resources was declared to the French Ministry of Environment under the reference TSP 48704 in compliance with the Access and Benefit Sharing procedure implemented by the Loi pour la Reconquête de la Biodiversité. The research with Access to Genetic Resources of Brazil is registered under number ADDD66D in the SisGen platform of the Ministry of Environment.

Funding

This project received funding support from FAPEMIG, CNPq, Programa Petrobras Socioambiental – PETROBRAS (Projeto Manati), and Fundação Grupo O Boticário from Brazil.

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Authors and Affiliations

Authors

Contributions

D.N.A. extraction and sequencing: C.S.L.; Phylogenetic and dating analysis: C.S.L. and R.F.M.; Demographic modelling: A.C.; Interpretation of biological data: C.S.L., R.F.M., A.C., B.T., M.M., V.L.C., A.C.M., and F.R.S.; Writing of the manuscript: C.S.L., R.F.M., A.C., and F.R.S.; all authors approved the final version of the manuscript.

Corresponding author

Correspondence to Fabrício Rodrigues Santos.

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Ethical Approval

Manatee samples were derived from previously collected material under the CEUA/UFMG ethical protocol 202/2007.

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The authors declare no competing interests.

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de Lima, C.S., de Magalhães, R.F., Camargo, A. et al. Evolutionary Dynamics of American Manatee Species on the Northern Coast of South America: Origins and Maintenance of an Interspecific Hybrid Zone. Evol Biol (2024). https://doi.org/10.1007/s11692-024-09629-4

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