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

atlantic bluefin tuna genetic connectivity introgression large migratory fish single-nucleotide polymorphisms

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
03 Nov 2023
Historique:
revised: 02 10 2023
received: 21 06 2023
accepted: 19 10 2023
pubmed: 3 11 2023
medline: 3 11 2023
entrez: 3 11 2023
Statut: aheadofprint

Résumé

The 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.

Identifiants

pubmed: 37921120
doi: 10.1111/mec.17188
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Department of Agriculture and Fisheries of the Basque Government
ID : GENGES/Doctoral grant
Organisme : ICCAT Atlantic Wide Research Program for Bluefin Tuna (GBYP), funded by the European Community (Grant SI2/542789), Canada, Croatia, Japan, Norway, Turkey, United States (NMFS NA11NMF4720107), Chinese Taipei, and the ICCAT Secretariat

Informations de copyright

© 2023 John Wiley & Sons Ltd.

Références

Aalto, E. A., Dedman, S., Stokesbury, M. J. W., Schallert, R. J., Castleton, M., & Block, B. A. (2023). Evidence of bluefin tuna (Thunnus thynnus) spawning in the Slope Sea region of the Northwest Atlantic from electronic tags. ICES Journal of Marine Science., 80, 861-877.
Aalto, E. A., Ferretti, F., Lauretta, M. V., Walter, J. F., Stokesbury, M. J. W., Schallert, R. J., & Block, B. A. (2021). Stock-of-origin catch estimation of Atlantic bluefin tuna (Thunnus thynnus) based on observed spatial distributions. Canadian Journal of Fisheries and Aquatic Sciences, 78, 1193-1204.
Aarestrup, K., Baktoft, H., Birnie-Gauvin, K., Sundelöf, A., Cardinale, M., Quilez-Badia, G., Onandia, I., Casini, M., Nielsen, E. E., Koed, A., Alemany, F., & MacKenzie, B. R. (2022). First tagging data on large Atlantic bluefin tuna returning to Nordic waters suggest repeated behaviour and skipped spawning. Scientific Reports, 12, 11772.
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., … Zinner, D. (2013). Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
Alemany, F., Quintanilla, L., Velez-Belchí, P., García, A., Cortés, D., Rodríguez, J. M., Fernández de Puelles, M. L., González-Pola, C., & López-Jurado, J. L. (2010). Characterization of the spawning habitat of Atlantic bluefin tuna and related species in the Balearic Sea (western Mediterranean). Progress in Oceanography, 86, 21-38.
Alexander, D. H., Novembre, J., & Lange, K. (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research, 19, 1655-1664.
Alvarado Bremer, J. R., Viñas, J., Mejuto, J., Ely, B., & Pla, C. (2005). Comparative phylogeography of Atlantic bluefin tuna and swordfish: The combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Molecular Phylogenetics and Evolution, 36, 169-187.
Aranda, G., Aragón, L., Corriero, A., Mylonas, C. C., la Gándara, F. D., Belmonte, A., & Medina, A. (2011). GnRHa-induced spawning in cage-reared Atlantic bluefin tuna: An evaluation using stereological quantification of ovarian post-ovulatory follicles. Aquaculture, 317, 255-259.
Arnold, M. L., & Martin, N. H. (2009). Adaptation by introgression. Journal of Biology, 8, 82.
Arregui, I., Galuardi, B., Goñi, N., Lam, C. H., Fraile, I., Santiago, J., Lutcavage, M., & Arrizabalaga, H. (2018). Movements and geographic distribution of juvenile bluefin tuna in the Northeast Atlantic, described through internal and satellite archival tags. ICES Journal of Marine Science, 75, 1560-1572.
Baglin, R. (1976). A preliminary study of the gonadal development and fecundity of the western Atlantic bluefin tuna. Collective Volume of Scientific Papers ICCAT, 5, 279-289.
Barth, J. M. I., Berg, P. R., Jonsson, P. R., Bonanomi, S., Corell, H., Hemmer-Hansen, J., Jakobsen, K. S., Johannesson, K., Jorde, P. E., Knutsen, H., Moksnes, P.-O., Star, B., Stenseth, N. C., Svedäng, H., Jentoft, S., & André, C. (2017). Genome architecture enables local adaptation of Atlantic cod despite high connectivity. Molecular Ecology, 26, 4452-4466.
Barth, J. M. I., Damerau, M., Matschiner, M., Jentoft, S., & Hanel, R. (2017). Genomic differentiation and demographic histories of Atlantic and Indo-Pacific yellowfin tuna (Thunnus albacares) populations. Genome Biology and Evolution, 9, 1084-1098.
Barth, J. M. I., Villegas-Ríos, D., Freitas, C., Moland, E., Star, B., André, C., Knutsen, H., Bradbury, I., Dierking, J., Petereit, C., Righton, D., Metcalfe, J., Jakobsen, K. S., Olsen, E. M., & Jentoft, S. (2019). Disentangling structural genomic and behavioural barriers in a sea of connectivity. Molecular Ecology, 28, 1394-1411.
Begg, G. A., Friedland, K. D., & Pearce, J. B. (1999). Stock identification and its role in stock assessment and fisheries management: An overview. Fisheries Research, 43, 1-8.
Berg, P. R., Star, B., Pampoulie, C., Sodeland, M., Barth, J. M. I., Knutsen, H., Jakobsen, K. S., & Jentoft, S. (2016). Three chromosomal rearrangements promote genomic divergence between migratory and stationary ecotypes of Atlantic cod. Scientific Reports, 6, 23246.
Bernatchez, L. (2016). On the maintenance of genetic variation and adaptation to environmental change: Considerations from population genomics in fishes. Journal of Fish Biology, 89, 2519-2556.
Bernatchez, L., Wellenreuther, M., Araneda, C., Ashton, D. T., Barth, J. M. I., Beacham, T. D., Maes, G. E., Martinsohn, J. T., Miller, K. M., Naish, K. A., Ovenden, J. R., Primmer, C. R., Young Suk, H., Therkildsen, N. O., & Withler, R. E. (2017). Harnessing the power of genomics to secure the future of seafood. Trends in Ecology & Evolution, 32, 665-680.
Block, B. A., Teo, S. L. H., Walli, A., Boustany, A., Stokesbury, M. J. W., Farwell, C. J., Weng, K. C., Dewar, H., & Williams, T. D. (2005). Electronic tagging and population structure of Atlantic bluefin tuna. Nature, 434, 1121-1127.
Bonanomi, S., Pellissier, L., Therkildsen, N. O., Hedeholm, R. B., Retzel, A., Meldrup, D., Olsen, S. M., Nielsen, A., Pampoulie, C., Hemmer-Hansen, J., Wisz, M. S., Grønkjaer, P., & Nielsen, E. E. (2015). Archived DNA reveals fisheries and climate induced collapse of a major fishery. Scientific Reports, 5, 15395.
Brauer, C. J., Sandoval-Castillo, J., Gates, K., Hammer, M. P., Unmack, P. J., Bernatchez, L., & Beheregaray, L. B. (2023). Natural hybridization reduces vulnerability to climate change. Nature Climate Change, 13, 282-289.
Brophy, D., Rodríguez-Ezpeleta, N., Fraile, I., & Arrizabalaga, H. (2020). Combining genetic markers with stable isotopes in otoliths reveals complexity in the stock structure of Atlantic bluefin tuna (Thunnus thynnus). Scientific Reports, 10, 14675.
Brown-Peterson, N. J., Wyanski, D. M., Saborido-Rey, F., Macewicz, B. J., & Lowerre-Barbieri, S. K. (2011). A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries, 3, 52-70.
Chow, S., & Kishino, H. (1995). Phylogenetic relationships between tuna species of the genus Thunnus (Scombridae: Teleostei): Inconsistent implications from morphology, nuclear and mitochondrial genomes. Journal of Molecular Evolution, 41, 741-748.
Ciezarek, A. G., Osborne, O. G., Shipley, O. N., Brooks, E. J., Tracey, S. R., McAllister, J. D., Gardner, L. D., Sternberg, M. J. E., Block, B., & Savolainen, V. (2018). Phylotranscriptomic insights into the diversification of endothermic Thunnus tunas. Molecular Biology and Evolution, 36, 84-96.
Clarkson, C. S., Weetman, D., Essandoh, J., Yawson, A. E., Maslen, G., Manske, M., Field, S. G., Webster, M., Antão, T., MacInnis, B., Kwiatkowski, D., & Donnelly, M. J. (2014). Adaptive introgression between anopheles sibling species eliminates a major genomic Island but not reproductive isolation. Nature Communications, 5, 4248.
Collette, B. B., Carpenter, K. E., Polidoro, B. A., Juan-Jordá, M. J., Boustany, A., Die, D. J., Elfes, C., Fox, W., Graves, J., Harrison, L. R., McManus, R., Minte-Vera, C. V., Nelson, R., Restrepo, V., Schratwieser, J., Sun, C. L., Amorim, A., Brick Peres, M., Canales, C., … Yáñez, E. (2011). High value and long life-double jeopardy for tunas and billfishes. Science, 333, 291-292.
da Fonseca, R., Campos, P., Rey de la Iglesia, A., Barroso, G., Bergeron, L., Nande, M., Tuya, F., Abidli, S., Pérez, M., Riveiro, I., Carrera, P., Jurado-Ruzafa, A., Santamaria, M. T. G., Faria, R., Machado, A., Fonseca, M., Froufe, E., & Castro, L. F. C. (2022). Population genomics reveals the underlying structure of the small pelagic European sardine and suggests low connectivity within Macaronesia. Authorea. https://doi.org/10.22541/au.161628445.52373083/v3
Díaz-Arce, N., Arrizabalaga, H., Murua, H., Irigoien, X., & Rodríguez-Ezpeleta, N. (2016). RAD-seq derived genome-wide nuclear markers resolve the phylogeny of tunas. Molecular Phylogenetics and Evolution, 102, 202-207.
Durand, E. Y., Patterson, N., Reich, D., & Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Molecular Biology and Evolution, 28, 2239-2252.
Duranton, M., Allal, F., Valière, S., Bouchez, O., Bonhomme, F., & Gagnaire, P. A. (2020). The contribution of ancient admixture to reproductive isolation between European sea bass lineages. Evolution Letters, 4, 226-242.
Erauskin-Extramiana, M., Arrizabalaga, H., Hobday, A. J., Cabré, A., Ibaibarriaga, L., Arregui, I., Murua, H., & Chust, G. (2019). Large-scale distribution of tuna species in a warming ocean. Global Change Biology, 25, 2043-2060.
Etter, P. D., Bassham, S., Hohenlohe, P. A., Johnson, E. A., & Cresko, W. A. (2012). SNP discovery and genotyping for evolutionary genetics using RAD sequencing. In V. Orgogozo & M. Rockman (Eds.), Molecular methods for evolutionary genetics (pp. 157-178). Springer.
Faillettaz, R., Beaugrand, G., Goberville, E., & Kirby, R. R. (2019). Atlantic multidecadal oscillations drive the basin-scale distribution of Atlantic bluefin tuna. Science Advances, 5, eaar6993.
Foll, M., & Gaggiotti, O. (2008). A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics, 180, 977-993.
Fraser, D. J., & Bernatchez, L. (2001). Adaptive evolutionary conservation: Towards a unified concept for defining conservation units. Molecular Ecology, 10, 2741-2752.
Fromentin, J. M. (2009). Lessons from the past: Investigating historical data from bluefin tuna fisheries. Fish and Fisheries, 10, 197-216.
Fromentin, J. M., Bonhommeau, S., Arrizabalaga, H., & Kell, L. T. (2014). The spectre of uncertainty in management of exploited fish stocks: The illustrative case of Atlantic bluefin tuna. Marine Policy, 47, 8-14.
Fromentin, J. M., & Powers, J. E. (2005). Atlantic bluefin tuna: Population dynamics, ecology, fisheries and management. Fish and Fisheries, 6, 281-306.
Fromentin, J. M., Reygondeau, G., Bonhommeau, S., & Beaugrand, G. (2014). Oceanographic changes and exploitation drive the spatio-temporal dynamics of Atlantic bluefin tuna (Thunnus thynnus). Fisheries Oceanography, 23, 147-156.
Fuentes-Pardo, A. P., Farrell, E. D., Pettersson, M. E., Sprehn, C. G., & Andersson, L. (2023). The genomic basis and environmental correlates of local adaptation in the Atlantic horse mackerel (Trachurus trachurus). Evolutionary Applications, 16, 1201-1219.
Gagnaire, P. A., Broquet, T., Aurelle, D., Viard, F., Souissi, A., Bonhomme, F., Arnaud-Haond, S., & Bierne, N. (2015). Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evolutionary Applications, 8, 769-786.
Galuardi, B., Royer, F., Golet, W., Logan, J., Neilson, J., & Lutcavage, M. (2010). Complex migration routes of Atlantic bluefin tuna (Thunnus thynnus) question current population structure paradigm. Canadian Journal of Fisheries and Aquatic Sciences, 67, 966-976.
Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., Li, H., Zhai, W., & Fritz, M. H. Y. (2010). A draft sequence of the neandertal genome. Science, 328, 710-722.
Gutenkunst, R. N., Hernandez, R. D., Williamson, S. H., & Bustamante, C. D. (2009). Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genetics, 5, e1000695.
Hauser, L., & Carvalho, G. R. (2008). Paradigm shifts in marine fisheries genetics: Ugly hypotheses slain by beautiful facts. Fish and Fisheries, 9, 333-362.
Hedrick, P. W. (2013). Adaptive introgression in animals: Examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606-4618.
Hernández, C. M., Richardson, D. E., Rypina, I. I., Chen, K., Marancik, K. E., Shulzitski, K., & Llopiz, J. K. (2022). Support for the Slope Sea as a major spawning ground for Atlantic bluefin tuna: Evidence from larval abundance, growth rates, and particle-tracking simulations. Canadian Journal of Fisheries and Aquatic Sciences, 79, 814-824.
Hoban, S., Arntzen, J. A., Bruford, M. W., Godoy, J. A., Rus Hoelzel, A., Segelbacher, G., Vilà, C., & Bertorelle, G. (2014). Comparative evaluation of potential indicators and temporal sampling protocols for monitoring genetic erosion. Evolutionary Applications, 7, 984-998.
Hoey, J. A., Able, K. W., & Pinsky, M. L. (2022). Genetic decline and recovery of a demographically rebuilt fishery species. Molecular Ecology, 31, 5684-5698.
Hoffmann, A. A., & Sgrò, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470, 479-485.
Horton, T. W., Block, B. A., Drumm, A., Hawkes, L. A., O'Cuaig, M., Maoiléidigh, N. Ó., O'Neill, R., Schallert, R. J., Stokesbury, M. J. W., & Witt, M. J. (2020). Tracking Atlantic bluefin tuna from foraging grounds off the west coast of Ireland. ICES Journal of Marine Science, 77, 2066-2077.
Huang, K., Andrew, R. L., Owens, G. L., Ostevik, K. L., & Rieseberg, L. H. (2020). Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype. Molecular Ecology, 29, 2535-2549.
Huerta-Sánchez, E., Jin, X., Asan, Z., Bianba, B. M., Peter, N., Vinckenbosch, Y., Liang, X., Yi, M., He, M., Somel, P., Ni, B., Wang, X. O., Huasang, J., Luosang, Z. X. P., Cuo, K., Li, G., Gao, Y., Yin, W., Wang, X., … Nielsen, R. (2014). Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature, 512, 194-197.
Hutchinson, W. F. (2008). The dangers of ignoring stock complexity in fishery management: The case of the North Sea cod. Biology Letters, 4, 693-695.
ICCAT. (2017). Report of the standing committee on research and statistics (SCRS). ICCAT. https://www.iccat.int/Documents/Meetings/Docs/2017_SCRS_REP_ENG.pdf
ICCAT. (2019). Report of the standing committee on research and statistics (SCRS). ICCAT. http://www.iccat.int/Documents/Meetings/Docs/2019/REPORTS/2019_SCRS_ENG.pdf
ICCAT. (2021). 2020 SRCS advice to the commission. ICCAT. https://www.iccat.int/Documents/BienRep/REP_EN_20-21_I-1.pdf
ICCAT. (2023). Recommendation by ICCAT Establishing a Management Procedure for Atlantic Bluefin Tuna to be Used for both the Western Atlantic and Eastern Atlantic and Mediterranean Management Areas. 8. https://www.iccat.int/Documents/Recs/compendiopdf-e/2022-09-e.pdf
Jansen, T., Nielsen, E. E., Rodriguez-Ezpeleta, N., Arrizabalaga, H., Post, S., & MacKenzie, B. R. (2021). Atlantic bluefin tuna (Thunnus thynnus) in Greenland - Mixed-stock origin, diet, hydrographic conditions, and repeated catches in this new fringe area. Canadian Journal of Fisheries and Aquatic Sciences, 78, 400-408.
Jay, P., Whibley, A., Frézal, L., Rodríguez de Cara, M. Á., Nowell, R. W., Mallet, J., Dasmahapatra, K. K., & Joron, M. (2018). Supergene evolution triggered by the introgression of a chromosomal inversion. Current Biology, 28, 1839-1845.
Jiménez-Mena, B., Le Moan, A., Christensen, A., van Deurs, M., Mosegaard, H., Hemmer-Hansen, J., & Bekkevold, D. (2020). Weak genetic structure despite strong genomic signal in lesser sandeel in the North Sea. Evolutionary Applications, 13, 376-387.
Johnstone, C., Pérez, M., Malca, E., Quintanilla, J. M., Gerard, T., Lozano-Peral, D., Alemany, F., Lamkin, J., García, A., & Laiz-Carrión, R. (2021). Genetic connectivity between Atlantic bluefin tuna larvae spawned in the Gulf of Mexico and in the Mediterranean Sea. PeerJ, 9, e11568.
Jombart, T., & Ahmed, I. (2011). Adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27, 3070-3071.
Kerr, L. A., Hintzen, N. T., Cadrin, S. X., Clausen, L. W., Dickey-Collas, M., Goethel, D. R., Hatfield, E. M. C., Kritzer, J. P., & Nash, R. D. M. (2016). Lessons learned from practical approaches to reconcile mismatches between biological population structure and stock units of marine fish. ICES Journal of Marine Science, 74, 1708-1722.
Kerr, L. A., Whitener, Z. T., Cadrin, S. X., Morse, M. R., Secor, D. H., & Golet, W. (2020). Mixed stock origin of Atlantic bluefin tuna in the U.S. rod and reel fishery (gulf of Maine) and implications for fisheries management. Fisheries Research, 224, 105461.
Kulathinal, R. J., Stevison, L. S., & Noor, M. A. (2009). The genomics of speciation in drosophila: Diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genetics, 5, e1000550.
Le Moan, A., D. Bekkevold, J. Hemmer-Hansen. (2021). Evolution at two time-frames: Ancient structural variants involved in post-glacial divergence of the European plaice (Pleuronectes platessa). Heredity, 126, 668-683.
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. 1303.3997 [q-Bio].
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & Subgroup, G. P. D. P. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079.
Lischer, H. E. L., & Excoffier, L. (2011). PGDSpider: An automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics, 28, 298-299.
Lowe, W. H., & Allendorf, F. W. (2010). What can genetics tell us about population connectivity? Molecular Ecology, 19, 3038-3051.
Luu, K., Bazin, E., & Blum, M. G. B. (2017). Pcadapt: An R package to perform genome scans for selection based on principal component analysis. Molecular Ecology Resources, 17, 67-77.
Mamoozadeh, N. R., Graves, J. E., & McDowell, J. R. (2020). Genome-wide SNPs resolve spatiotemporal patterns of connectivity within striped marlin (Kajikia audax), a broadly distributed and highly migratory pelagic species. Evolutionary Applications, 13, 677-698.
Mariani, S., & Bekkevold, D. (2014). Chapter fourteen-the nuclear genome: Neutral and adaptive markers in fisheries science. In S. X. Cadrin, L. A. Kerr, & S. Mariani (Eds.), Stock identification methods (second edition) (pp. 297-327). Academic Press.
Mather, F. J., Mason, J. M., & Jones, A. C. (1995). Historical document: Life history and fisheries of Atlantic bluefin tuna (p. 165). NOAA Technical Memorandum, NMFS-SEFSC.
McPherson, G. (1991). Reproductive biology of yellowfin tuna in the eastern Australian fishing zone, with special reference to the North-Western Coral Sea. Marine and Freshwater Research, 42, 465-477.
Mérot, C., Berdan, E. L., Cayuela, H., Djambazian, H., Ferchaud, A. L., Laporte, M., Normandeau, E., Ragoussis, J., Wellenreuther, M., & Bernatchez, L. (2021). Locally adaptive inversions modulate genetic variation at different geographic scales in a seaweed Fly. Molecular Biology and Evolution, 38, 3953-3971.
Muhling, B. A., Lee, S. K., Lamkin, J. T., & Liu, Y. (2011). Predicting the effects of climate change on bluefin tuna (Thunnus thynnus) spawning habitat in the Gulf of Mexico. ICES Journal of Marine Science, 68, 1051-1062.
Nikolic, N., Devloo-Delva, F., Bailleul, D., Noskova, E., Rougeux, C., Delord, C., Borsa, P., Liautard-Haag, C., Hassan, M., Marie, A. D., Feutry, P., Grewe, P., Davies, C., Farley, J., Fernando, D., Biton-Porsmoguer, S., Poisson, F., Parker, D., … Arnaud-Haond, S. (2023). Stepping up to genome scan allows stock differentiation in the worldwide distributed blue shark Prionace glauca. Molecular Ecology, 32, 1000-1019.
Nøttestad, L., Boge, E., & Ferter, K. (2020). The comeback of Atlantic bluefin tuna (Thunnus thynnus) to Norwegian waters. Fisheries Research, 231, 105689.
Oosting, T., Star, B., Barrett, J. H., Wellenreuther, M., Ritchie, P. A., & Rawlence, N. J. (2019). Unlocking the potential of ancient fish DNA in the genomic era. Evolutionary Applications, 12, 1513-1522.
Ovenden, J. R., Berry, O., Welch, D. J., Buckworth, R. C., & Dichmont, C. M. (2015). Ocean's eleven: A critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries. Fish and Fisheries, 16, 125-159.
Patterson, N. J., Moorjani, P., Luo, Y., Mallick, S., Rohland, N., Zhan, Y., Genschoreck, T., Webster, T., & Reich, D. (2012). Ancient admixture in human history. Genetics:Genetics., 112, 145037.
Pickrell, J. K., & Pritchard, J. K. (2012). Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8, e1002967.
Porch, C. E., Bonhommeau, S., Diaz, G. A., Arrizabalaga, H., & Melvin, G. (2019). The journey from overfishing to sustainability for Atlantic bluefin tuna, Thunnus thynnus. In B. Block (Ed.), The future of bluefin tunas: Ecology, fisheries management, and conservation (pp. 3-44). John Hopkins University Press.
Portik, D. M., Leaché, A. D., Rivera, D., Barej, M. F., Burger, M., Hirschfeld, M., Rödel, M. O., Blackburn, D. C., & Fujita, M. K. (2017). Evaluating mechanisms of diversification in a Guineo-Congolian tropical forest frog using demographic model selection. Molecular Ecology, 26, 5245-5263.
Puncher, G. N., Cariani, A., Maes, G. E., Van Houdt, J., Herten, K., Cannas, R., Rodriguez-Ezpeleta, N., Albaina, A., Estonba, A., Lutcavage, M., Hanke, A., Rooker, J., Franks, J. S., Quattro, J. M., Basilone, G., Fraile, I., Laconcha, U., Goñi, N., Kimoto, A., … Tinti, F. (2018). Spatial dynamics and mixing of bluefin tuna in the Atlantic Ocean and Mediterranean Sea revealed using next-generation sequencing. Molecular Ecology Resources, 18, 620-638.
Puncher, G. N., Hanke, A., Busawon, D., Sylvester, E. V. A., Golet, W., Hamilton, L. C., & Pavey, S. A. (2022). Individual assignment of Atlantic bluefin tuna in the northwestern Atlantic Ocean using single nucleotide polymorphisms reveals an increasing proportion of migrants from the eastern Atlantic Ocean. Canadian Journal of Fisheries and Aquatic Sciences, 79, 111-123.
Puncher, G. N., Rowe, S., Rose, G. A., Leblanc, N. M., Parent, G. J., Wang, Y., & Pavey, S. A. (2019). Chromosomal inversions in the Atlantic cod genome: Implications for management of Canada's northern cod stock. Fisheries Research, 216, 29-40.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A., Bender, D., Maller, J., Sklar, P., de Bakker, P. I., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559-575.
Ravier, C., & Fromentin, J. M. (2004). Are the long-term fluctuations in Atlantic bluefin tuna (Thunnus thynnus) population related to environmental changes? Fisheries Oceanography, 13, 145-160.
Raymond, M. (1995). GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. The Journal of Heredity, 86, 248-249.
Reiss, H., Hoarau, G., Dickey-Collas, M., & Wolff, W. J. (2009). Genetic population structure of marine fish: Mismatch between biological and fisheries management units. Fish and Fisheries, 10, 361-395.
Richardson, D. E., Marancik, K. E., Guyon, J. R., Lutcavage, M. E., Galuardi, B., Lam, C. H., Walsh, H. J., Wildes, S., Yates, D. A., & Hare, J. A. (2016a). Discovery of a spawning ground reveals diverse migration strategies in Atlantic bluefin tuna (<em>Thunnus thynnus</em>). Proceedings of the National Academy of Sciences, 113, 3299-3304.
Richardson, D. E., Marancik, K. E., Guyon, J. R., Lutcavage, M. E., Galuardi, B., Lam, C. H., Walsh, H. J., Wildes, S., Yates, D. A., & Hare, J. A. (2016b). Reply to Safina and Walter et al: Multiple lines of evidence for size-structured spawning migrations in western Atlantic bluefin tuna. Proceedings of the National Academy of Sciences, 113, E4262-E4263.
Roberts, D. G., Gray, C. A., West, R. J., & Ayre, D. J. (2010). Marine genetic swamping: Hybrids replace an obligately estuarine fish. Molecular Ecology, 19, 508-520.
Rochette, N. C., Rivera-Colón, A. G., & Catchen, J. M. (2019). Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology, 28, 4737-4754.
Rodríguez-Ezpeleta, N., Díaz-Arce, N., Walter, J. F., III, Richardson, D. E., Rooker, J. R., Nøttestad, L., Hanke, A. R., Franks, J. S., Deguara, S., Lauretta, M. V., Addis, P., Varela, J. L., Fraile, I., Goñi, N., Abid, N., Alemany, F., Oray, I. K., Quattro, J. M., Sow, F. N., … Arrizabalaga, H. (2019). Determining natal origin for improved management of Atlantic bluefin tuna. Frontiers in Ecology and the Environment, 17, 439-444.
Rooker, J. R., Arrizabalaga, H., Fraile, I., Secor, D. H., Dettman, D. L., Abid, N., Addis, P., Deguara, S., Karakulak, F. S., Kimoto, A., Sakai, O., Macías, D., & Santos, M. N. (2014). Crossing the line: Migratory and homing behaviors of Atlantic bluefin tuna. Marine Ecology Progress Series, 504, 265-276.
Rooker, J. R., Fraile, I., Liu, H., Abid, N., Dance, M. A., Itoh, T., Kimoto, A., Tsukahara, Y., Rodriguez-Marin, E., & Arrizabalaga, H. (2019). Wide-ranging temporal variation in transoceanic movement and population mixing of bluefin tuna in the North Atlantic Ocean. Frontiers in Marine Science, 6, 398.
Rooker, J. R., Secor, D. H., DeMetrio, G., Kaufman, A. J., Ríos, A. B., & Ticina, V. (2008). Evidence of trans-Atlantic movement and natal homing of bluefin tuna from stable isotopes in otoliths. Marine Ecology Progress Series, 368, 231-239.
Rypina, I. I., Chen, K., Hernández, C. M., Pratt, L. J., & Llopiz, J. K. (2019). Investigating the suitability of the Slope Sea for Atlantic bluefin tuna spawning using a high-resolution ocean circulation model. ICES Journal of Marine Science, 76, 1666-1677.
Safina, C. (2016). Data do not support new claims about bluefin tuna spawning or abundance. Proceedings of the National Academy of Sciences, 113, E4261.
Schaefer, K. (1996). Spawning time, frequency, and batch fecundity of yellowfin tuna, Thunnus albacares, near Clipperton atoll in the eastern Pacific ocien. Fishery Bulletin, 94, 98-112.
Secor, D. H., Rooker, J. R., Gahagan, B. I., Siskey, M. R., & Wingate, R. W. (2015). Depressed resilience of bluefin tuna in the western Atlantic and age truncation. Conservation Biology, 29, 400-408.
Siskey, M. R., Wilberg, M. J., Allman, R. J., Barnett, B. K., & Secor, D. H. (2016). Forty years of fishing: Changes in age structure and stock mixing in northwestern Atlantic bluefin tuna (Thunnus thynnus) associated with size-selective and long-term exploitation. ICES Journal of Marine Science, 73, 2518-2528.
Stephenson, R. L. (1999). Stock complexity in fisheries management: A perspective of emerging issues related to population sub-units. Fisheries Research, 43, 247-249.
Suda, A., Nishiki, I., Iwasaki, Y., Matsuura, A., Akita, T., Suzuki, N., & Fujiwara, A. (2019). Improvement of the Pacific bluefin tuna (Thunnus orientalis) reference genome and development of male-specific DNA markers. Scientific Reports, 9, 14450.
Thorstensen, M. J., Euclide, P. T., Jeffrey, J. D., Shi, Y., Treberg, J. R., Watkinson, D. A., Enders, E. C., Larson, W. A., Kobayashi, Y., & Jeffries, K. M. (2022). A chromosomal inversion may facilitate adaptation despite periodic gene flow in a freshwater fish. Ecology and Evolution, 12, e8898.
Tigano, A., & Friesen, V. L. (2016). Genomics of local adaptation with gene flow. Molecular Ecology, 25, 2144-2164.
Valenzuela-Quiñonez, F. (2016). How fisheries management can benefit from genomics? Briefings in Functional Genomics, 15, 352-357.
Viñas, J., Gordoa, A., Fernández-Cebrián, R., Pla, C., Vahdet, Ü., & Araguas, R. M. (2011). Facts and uncertainties about the genetic population structure of Atlantic bluefin tuna (Thunnus thynnus) in the Mediterranean. Implications for fishery management. Reviews in Fish Biology and Fisheries, 21, 527-541.
Walter, J. F., Porch, C. E., Lauretta, M. V., Cass-Calay, S. L., & Brown, C. A. (2016). Implications of alternative spawning for bluefin tuna remain unclear. Proceedings of the National Academy of Sciences, 113, E4259-E4260.
Waples, R. (1998). Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. Journal of Heredity, 89, 438-450.
Waples, R. S. (2022). What is Ne, anyway? Journal of Heredity, 113, 371-379.
Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R., & Hebert, P. D. (2005). DNA barcoding Australia's fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 360(1462), 1847-1857. https://doi.org/10.1098/rstb.2005.1716
Wellenreuther, M., & Bernatchez, L. (2018). Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution, 33, 427-440.
Xuereb, A., D'Aloia, C. C., Andrello, M., Bernatchez, L., & Fortin, M. J. (2021). Incorporating putatively neutral and adaptive genomic data into marine conservation planning. Conservation Biology, 35, 909-920.
Yang, J., Lee, S. H., Goddard, M. E., & Visscher, P. M. (2011). GCTA: A tool for genome-wide complex trait analysis. The American Journal of Human Genetics, 88, 76-82.

Auteurs

Natalia Díaz-Arce (N)

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

Pierre-Alexandre Gagnaire (PA)

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

David E Richardson (DE)

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

John F Walter (JF)

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

Sophie Arnaud-Haond (S)

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

Jean-Marc Fromentin (JM)

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

Deirdre Brophy (D)

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

Molly Lutcavage (M)

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

Piero Addis (P)

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

Francisco Alemany (F)

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

Robert Allman (R)

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

Simeon Deguara (S)

AquaBio Tech Ltd., Central Complex, Mosta, Malta.

Igaratza Fraile (I)

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

Nicolas Goñi (N)

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

Alex R Hanke (AR)

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

F Saadet Karakulak (FS)

Faculty of Aquatic Sciences, Istanbul University, Istanbul, Turkey.

Ashley Pacicco (A)

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

Joseph M Quattro (JM)

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

Jay R Rooker (JR)

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

Haritz Arrizabalaga (H)

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

Naiara Rodríguez-Ezpeleta (N)

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

Classifications MeSH