Ancient and recent hybridization in the Oreochromis cichlid fishes

Ciezarek, Adam G., Mehta, Tarang K., Man, Angela, Ford, Antonia G. P., Kavembe, Geraldine Dorcas, Kasozi, Nasser, Ngatunga, Benjamin P., Shechonge, Asilatu H., Tamatamah, Rashid, Nyingi, Dorothy Wanja, Cnaani, Avner, Ndiwa, Titus C., Di Palma, Federica, Turner, George F., Genner, Martin J. and Haerty, Wilfried ORCID: https://orcid.org/0000-0003-0111-191X (2024) Ancient and recent hybridization in the Oreochromis cichlid fishes. Molecular Biology and Evolution, 41 (7). ISSN 0737-4038

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Abstract

Cichlid fishes of the genus Oreochromis (tilapia) are among the most important fish for inland capture fisheries and global aquaculture. Deliberate introductions of non-native species for fisheries improvement and accidental escapees from farms have resulted in admixture with indigenous species. Such hybridization may be detrimental to native biodiversity, potentially leading to genomic homogenization of populations and the loss of important genetic material associated with local adaptation. By contrast, introgression may fuel diversification when combined with ecological opportunity, by supplying novel genetic combinations. To date, the role of introgression in the evolutionary history of tilapia has not been explored. Here we studied both ancient and recent hybridization in tilapia, using whole genome resequencing of 575 individuals from 23 species. We focused on Tanzania, a natural hotspot of tilapia diversity, and a country where hybridization between exotic and native species in the natural environment has been previously reported. We reconstruct the first genome-scale phylogeny of the genus and reveal prevalent ancient gene flow across the Oreochromis phylogeny. This has likely resulted in the hybrid speciation of one species, O. chungruruensis. We identify multiple cases of recent hybridization between native and introduced species in the wild, linked to the use of non-native species in both capture fisheries improvement and aquaculture. This has potential implications for both conservation of wild populations and the development of the global tilapia aquaculture industry.

Item Type:	Article
Additional Information:	Data Availability Statement: All raw-read data generated is available in the European Nucleotide Archive (project PRJEB77041). All inferred phylogenetic trees and their underlying datasets are available in Dryad (https://doi.org/10.5061/dryad.p2ngf1w0c). All custom R and Python scripts are available in Zenodo (https://doi.org/10.5281/zenodo.12549228). Any further data is available upon request. Funding Information: The authors declare no competing interests. Sequencing and library construction were delivered via the BBSRC National Capability in Genomics and Single Cell (BB/CCG1720/1) at Earlham Institute by members of the Genomics Pipelines Group. The computing infrastructure and data center delivered via the NBI Research Computing are supported by the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation, Core Capability Grant BB/CCG1720/1. This work was funded by BBSRC/Natural Environment Research Council (NERC) award BB/M026736/1 (G.F.T., M.J.G., F.D.P.), and Leverhulme Trust Africa Awards AA100023 and AA130107 (M.J.G., B.P.N., G.F.T., R.T.). W.H. and F.D.P. acknowledge the support of the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation; this research was funded by the BBSRC Core Strategic Programme Grant BB/CSP1720/1 and its constituent work packages-BBS/E/T/000PR9818. A.C., W.H., F.D.P. were supported through BBSRC GCRF funding (BB/P028098/1). Samples from Tanzania were collected across 2013-2016 under permit numbers 2012-393-ER-2011-103, 2014-374-ER-2011-103, 2015-83-NA-2011-103, and 2016-293-NA-2011-103. Reference samples from Uganda (Lake Albert) were collected in 2015 under permit number FS06/15/04. This study was approved by the Agricultural Research Organization Committee for Ethics in Using Experimental Animals and was carried out in compliance with the current laws governing biological research in Israel (Approval number: IL-568/15). We are grateful for the technical and logistical support from staff of the Tanzania Fisheries Research Institute. We thank Alan Smith, Steph Bradbeer, Carlos Gracida Juarez, and Mar\u00EDa Lorena Romero-Martinez for assistance with sample collection and DNA extraction. Acknowledgements: The authors declare no competing interests. Sequencing and library construction were delivered via the BBSRC National Capability in Genomics and Single Cell (BB/CCG1720/1) at Earlham Institute by members of the Genomics Pipelines Group. The computing infrastructure and data center delivered via the NBI Research Computing are supported by the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation, Core Capability Grant BB/CCG1720/1. This work was funded by BBSRC/Natural Environment Research Council (NERC) award BB/M026736/1 (G.F.T., M.J.G., F.D.P.), and Leverhulme Trust Africa Awards AA100023 and AA130107 (M.J.G., B.P.N., G.F.T., R.T.). W.H. and F.D.P. acknowledge the support of the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation; this research was funded by the BBSRC Core Strategic Programme Grant BB/CSP1720/1 and its constituent work packages\u2014BBS/E/T/000PR9818. A.C., W.H., F.D.P. were supported through BBSRC GCRF funding (BB/P028098/1). Samples from Tanzania were collected across 2013\u20132016 under permit numbers 2012-393-ER-2011-103, 2014-374-ER-2011-103, 2015-83-NA-2011-103, and 2016-293-NA-2011-103. Reference samples from Uganda (Lake Albert) were collected in 2015 under permit number FS06/15/04. This study was approved by the Agricultural Research Organization Committee for Ethics in Using Experimental Animals and was carried out in compliance with the current laws governing biological research in Israel (Approval number: IL-568/15). We are grateful for the technical and logistical support from staff of the Tanzania Fisheries Research Institute. We thank Alan Smith, Steph Bradbeer, Carlos Gracida Juarez, and Mar\u00EDa Lorena Romero-Martinez for assistance with sample collection and DNA extraction.
Uncontrolled Keywords:	cichlid,hybridizations,introgression,oreochromis,phylogenomics,speciation,ecology, evolution, behavior and systematics,molecular biology,genetics,sdg 15 - life on land ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School:	Faculty of Science > School of Biological Sciences University of East Anglia Research Groups/Centres > Theme - ClimateUEA
UEA Research Groups:	Faculty of Medicine and Health Sciences > Research Centres > Norwich Institute for Healthy Aging
Related URLs:	http://www.scopus.com/inward/record.url?...
Depositing User:	LivePure Connector
Date Deposited:	23 Oct 2024 10:30
Last Modified:	01 Nov 2024 12:30
URI:	https://ueaeprints.uea.ac.uk/id/eprint/97137
DOI:	10.1093/molbev/msae116

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