Unidirectional trans‐Atlantic gene flow and a mixed spawning area shape the genetic connectivity of Atlantic bluefin tuna

Author:

Díaz‐Arce Natalia1,Gagnaire Pierre‐Alexandre2,Richardson David E.3,Walter John F.4,Arnaud‐Haond Sophie5,Fromentin Jean‐Marc5,Brophy Deirdre6,Lutcavage Molly7,Addis Piero8,Alemany Francisco9,Allman Robert10,Deguara Simeon11,Fraile Igaratza12,Goñi Nicolas12,Hanke Alex R.13,Karakulak F. Saadet14,Pacicco Ashley15,Quattro Joseph M.16,Rooker Jay R.17,Arrizabalaga Haritz12,Rodríguez‐Ezpeleta Naiara1ORCID

Affiliation:

1. AZTI, Marine Research Basque Research and Technology Alliance (BRTA) Sukarrieta Spain

2. ISEM, Univ Montpellier, CNRS, EPHE, IRD Montpellier France

3. Northeast Fisheries Science Center, National Marine Fisheries Service National Oceanic and Atmospheric Administration (NOAA) Narragansett Rhode Island USA

4. Southeast Fisheries Sciences Center National Marine Fisheries Service, National Oceanic and Atmospheric Administration (NOAA) Miami Florida USA

5. MARBEC, Univ Montpellier, Ifremer, IRD, CNRS Sète France

6. Marine and Freshwater Research Center Atlantic Technological University (ATU) Galway City Ireland

7. Large Pelagics Research Center, School for the Environment University of Massachusetts Boston Gloucester Massachusetts USA

8. Department of Environmental and Life Science University of Cagliari Cagliari Italy

9. International Commission for the Conservation of Atlantic Tunas, GBYP Madrid Spain

10. National Marine Fisheries Service, Southeast Fisheries Science Center, Panama City Laboratory Panama City Florida USA

11. AquaBio Tech Ltd., Central Complex Mosta Malta

12. AZTI, Marine Research Basque Research and Technology Alliance (BRTA) Pasaia Spain

13. St Andrews Biological Station Fisheries and Oceans Canada St. Andrews New Brunswick Canada

14. Faculty of Aquatic Sciences Istanbul University Istanbul Turkey

15. Cooperative Institute for Marine and Atmospheric Studies Rosenstiel School of Marine, Atmospheric and Earth Science University of Miami Miami Florida USA

16. Department of Biological Sciences University of South Carolina Columbia South Carolina USA

17. Department of Marine Biology Texas A&M University at Galveston Galveston Texas USA

Abstract

AbstractThe commercially important Atlantic bluefin tuna (Thunnus thynnus), a large migratory fish, has experienced notable recovery aided by accurate resource assessment and effective fisheries management efforts. Traditionally, this species has been perceived as consisting of eastern and western populations, spawning respectively in the Mediterranean Sea and the Gulf of Mexico, with mixing occurring throughout the Atlantic. However, recent studies have challenged this assumption by revealing weak genetic differentiation and identifying a previously unknown spawning ground in the Slope Sea used by Atlantic bluefin tuna of uncertain origin. To further understand the current and past population structure and connectivity of Atlantic bluefin tuna, we have assembled a unique dataset including thousands of genome‐wide single‐nucleotide polymorphisms (SNPs) from 500 larvae, young of the year and spawning adult samples covering the three spawning grounds and including individuals of other Thunnus species. Our analyses support two weakly differentiated but demographically connected ancestral populations that interbreed in the Slope Sea. Moreover, we also identified signatures of introgression from albacore (Thunnus alalunga) into the Atlantic bluefin tuna genome, exhibiting varied frequencies across spawning areas, indicating strong gene flow from the Mediterranean Sea towards the Slope Sea. We hypothesize that the observed genetic differentiation may be attributed to increased gene flow caused by a recent intensification of westward migration by the eastern population, which could have implications for the genetic diversity and conservation of western populations. Future conservation efforts should consider these findings to address potential genetic homogenization in the species.

Publisher

Wiley

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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