Taxonomic re-appraisal for toothfish (Dissostichus: Notothenioidea) across the Antarctic Polar Front using genomic and morphological studies.
Dissostichus australis
endemism
mtDNA
new species
nuclear SNP analysis
southern Atlantic
Journal
Journal of fish biology
ISSN: 1095-8649
Titre abrégé: J Fish Biol
Pays: England
ID NLM: 0214055
Informations de publication
Date de publication:
May 2022
May 2022
Historique:
revised:
03
02
2022
received:
15
11
2021
accepted:
14
02
2022
pubmed:
18
2
2022
medline:
25
5
2022
entrez:
17
2
2022
Statut:
ppublish
Résumé
The Patagonian toothfish, Dissostichus eleginoides, is one of the largest predatory fishes inhabiting Southern Ocean waters spanning the Antarctic Polar Front (APF), a prominent biogeographic boundary restricting gene flow and driving species divergence between Antarctic and sub-Antarctic waters. In the light of emerging threats to toothfish conservation and sustainability, this study investigated genetic [mtDNA sequences and genome wide nuclear single nucleotide polymorphisms (SNPs)] and morphological data to critically evaluate the taxonomic status of toothfish north (Chile and Patagonian shelf) and south (South Georgia and South Sandwich Islands) of the APF. mtDNA revealed reciprocally monophyletic lineages on either side of the APF with coalescent analysis indicating these diverged during the Pleistocene. Integration with data from other sources suggests the Chilean/Patagonian lineage is endemic. SNP analysis confirmed restricted nuclear gene flow between both groups and revealed a consensus suite of positive outlier SNPs compatible with adaptive divergence between these groups. Finally, several morphological features permit unequivocal assignment of individuals to either of the clades. Based on the genetic, phenotypic and ecological divergence, the authors propose that toothfish on either side of the APF be recognised as distinct species, with the name D. eleginoides used for toothfish occurring in South American waters north of the APF and toothfish south of the APF being classified using the new name D. australis reflecting their southern distribution.
Substances chimiques
DNA, Mitochondrial
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1158-1170Informations de copyright
© 2022 Fisheries Society of the British Isles.
Références
Allcock, A. L., & Strugnell, J. M. (2012). Southern Ocean diversity: New paradigms from molecular ecology. Trends in Ecology & Evolution, 27, 520-528.
Appleyard, S. A., Williams, R., & Ward, R. D. (2004). Population genetic structure of Patagonian toothfish in the West Indian Ocean sector of the Southern Ocean. CCAMLR Science, 11, 21-32.
Arkhipkin, A. I., & Laptikhovsky, V. V. (2010). Convergence in life-history traits in migratory deep-water squid and fish. ICES Journal of Marine Science, 67, 1444-1451.
Bierne, N., Welch, J., Loire, E., Bonhomme, F., & David, P. (2011). The coupling hypothesis: Why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044-2072.
Brigden, K. E., Marshall, C. T., Scott, B. E., Young, E. F., & Brickle, P. (2017). Interannual variability in reproductive traits of the Patagonian toothfish Dissostichus eleginoides around the sub-Antarctic Island of South Georgia. Journal of Fish Biology, 91, 278-301.
Brickle, P. (2003)The parasite ecology of the Patagonian toothfish (Dissostichus eleginoides Smitt, 1898). (Ph.D. thesis). University of Aberdeen, 211 pp..
Brickle, P., MacKenzie, K., & Pike, A. (2005). Parasites of the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, in different parts of the sub-Antarctic. Polar Biology, 28, 663-671.
Brown, J., Brickle, P., & Scott, B. E. (2013). Investigating the movements and behaviour of Patagonian toothfish (Dissostichus eleginoides Smitt, 1898) around The Falkland Islands using satellite linked archival tags. Journal of Experimental Marine Biology and Ecology, 443, 65-74.
Canales-Aguirre, C. B., Ferrada-Fuentes, S., Galleguillos, R., Oyarzun, F. X., & Hernandez, C. E. (2018). Population genetic structure of Patagonian toothfish (Dissostichus eleginoides) in the Southeast Pacific and Southwest Atlantic Ocean. PeerJ, 6, e4173.
Candy, S. G., Welsford, D. C., Lamb, T., Verdouw, J. J., & Hutchins, J. J. (2011). Estimation of natural mortality for the Patagonian toothfish at Heard and McDonald Islands using catch-at-age and aged mark-recapture data from the main trawl ground. CCAMLR Science, 18, 29-45.
Carreira, G. P., Shaw, P. W., Goncalves, J. M., & McKeown, N. J. (2017). Congruent molecular and morphological diversity of macaronesian limpets: Insights into eco-evolutionary forces and tools for conservation. Frontiers in Marine Science, 4, 75.
Ceballos, S. G., Roesti, M., Matschiner, M., Fernández, D. A., Damerau, M., Hanel, R., & Salzburger, W. (2019). Phylogenomics of an extra-Antarctic notothenioid radiation reveals a previously unrecognized lineage and diffuse species boundaries. BMC Evolutionary Biology, 19, 1-14.
Collins, M. A., Brickle, P., Brown, J., & Belchier, M. (2010). The Patagonian toothfish: Biology, ecology and fishery. Advances in Marine Biology, 58, 227-300.
Collins, R. A., & Cruickshank, R. H. (2013). The seven deadly sins of DNA barcoding. Molecular Ecology Resources, 13, 969-975.
Cumming, R. A., Nikula, R., Spencer, H. G., & Waters, J. M. (2014). Transoceanic genetic similarities of kelp-associated sea slug populations: Long-distance dispersal via rafting? Journal of Biogeography, 41, 2357-2370.
Cziko, P. A., & Cheng, C. H. C. (2006). A new species of Nototheniid (Perciformes: Notothenioidei) fish from McMurdo Sound, Antarctica. Copeia, 2006(4), 752-759.
De Mita, S., Thuillet, A. C., Gay, L., Ahmadi, N., Manel, S., Ronfort, J., & Vigouroux, Y. (2013). Detecting selection along environmental gradients: Analysis of eight methods and their effectiveness for outbreeding and selfing populations. Molecular Ecology, 22, 1383-1399.
Dornburg, A., Federman, S., Lamb, A. D., Jones, C. D., & Near, T. J. (2017). Cradles and museums of Antarctic teleost biodiversity. Nature Ecology & Evolution, 1, 1379-1384.
Dray, S., & Dufour, A. B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22(4), 1-20. https://doi.org/10.18637/jss.v022.i04.
Eastman, J. T. (2005). The nature of the diversity of Antarctic fishes. Polar Biology, 28, 93-107.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611-2620.
Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10, 564-567.
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.
Gonzalez-Wevar, C. A., Gerard, K., Rosenfeld, S., Saucede, T., Naretto, J., Diaz, A., … Poulin, E. (2019). Cryptic speciation in Southern Ocean Aequiyoldia eightsii (Jay, 1839): Mio-Pliocene trans-Drake Passage separation and diversification. Progress in Oceanography, 174, 44-54.
Gonzalez-Wevar, C. A., Hune, M., Canete, J. I., Mansilla, A., Nakano, T., & Poulin, E. (2012). Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: Lessons from the limpet Nacella magellanica (Gmelin, 1791). BMC Evolutionary Biology, 12, 1-17.
Gonzalez-Wevar, C. A., Hune, M., Segovia, N. I., Nakano, T., Spencer, H. G., Chown, S. L., … Poulin, E. (2017). Following the Antarctic circumpolar current: Patterns and processes in the biogeography of the limpet Nacella (Mollusca: Patellogastropoda) across the Southern Ocean. Journal of Biogeography, 44, 861-874.
Gonzalez-Wevar, C. A., Nakano, T., Canete, J. I., & Poulin, E. (2010). Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean. Molecular Phylogenetics and Evolution, 56, 115-124.
Gonzalez-Wevar, C. A., Nakano, T., Canete, J. I., & Poulin, E. (2011). Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Molecular Ecology, 20, 1936-1951.
Gonzalez-Wevar, C. A., Segovia, N. I., Rosenfeld, S., Noll, D., Maturana, C. S., Hune, M., … Poulin, E. (2021). Contrasting biogeographical patterns in Margarella (Gastropoda: Calliostomatidae: Margarellinae) across the Antarctic polar front. Molecular Phylogenetics and Evolution, 156, 107039.
Grant, W. S. (2015). Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. Journal of Heredity, 106, 333-346.
Grilly, E., Reid, K., Lenel, S., & Jabour, J. (2015). The price of fish: A global trade analysis of Patagonian (Dissostichus eleginoides) and Antarctic toothfish (Dissostichus mawsoni). Marine Policy, 60, 186-196.
Gwilliam, M. P., Winkler, A. C., Potts, W. M., Santos, C. V., Sauer, W. H. H., Shaw, P. W., & McKeown, N. J. (2018). Integrated genetic and morphological data support eco-evolutionary divergence of Angolan and south African populations of Diplodus hottentotus. Journal of Fish Biology, 92, 1163-1176.
Hey, J. (2010). Isolation with migration models for more than two populations. Molecular Biology and Evolution, 27, 905-920.
Hey, J., & Nielsen, R. (2004). Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics, 167, 747-760.
Ho, S. Y. W., Phillips, M. J., Cooper, A., & Drummond, A. J. (2005). Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution, 22, 1561-1568.
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111-120.
Kock, K. H. (1992). Antarctic fish and fisheries. Cambridge, UK: Cambridge University Press.
Kruskal, J. B. (1964). Nonmetric multidimensional scaling: A numerical method. Psychometrika, 29, 115-129. https://doi.org/10.1007/BF02289694.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecualr evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870-1874.
Laptikhovsky, V., & Brickle, P. (2005). The Patagonian toothfish fishery in Falkland Islands' waters. Fisheries Research, 74, 11-23.
Lee, B., Brewin, P. E., Brickle, P., & Randhawa, H. (2018). Use of otolith shape to inform stock structure in Patagonian toothfish (Dissostichus eleginoides) in the South-Western Atlantic. Marine and Freshwater Research, 69, 1238-1247. https://doi.org/10.1071/MF17327.
Legendre, P., Oksanen, J., & ter Braak, C. J. (2011). Testing the significance of canonical axes in redundancy analysis. Methods in Ecology and Evolution, 2(3), 269-277. https://doi.org/10.1111/j.2041-210X.2010.00078.x.
Lestrel, P. E. (1997). Fourier descriptors and their applications in biology. Cambridge: Cambridge University Press.
Li, S., & Chou, H. H. (2004). Lucy 2: An interactive DNA sequence quality trimming and vector removal tool. Bioinformatics, 20, 2865-2866.
Libungan, L. A., & Pálsson, S. (2015). ShapeR: An R package to study otolith shape variation among fish populations. PLoS One, 10(3), e0121102. https://doi.org/10.1371/journal.pone.0121102.
Matschiner, M., Hanel, R., & Salzburger, W. (2009). Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Molecular Ecology, 18, 2574-2587.
McKeown, N. J., Arkhipkin, A. I., & Shaw, P. W. (2017). Regional genetic population structure and fine scale genetic cohesion in the southern blue whiting Micromesistius australis. Fisheries Research, 185, 176-184.
McKeown, N. J., Arkhipkin, A. I., & Shaw, P. W. (2015). Integrating genetic and otolith microchemistry data to understand population structure in the Patagonian Hoki (Macruronus magellanicus). Fisheries Research, 164, 1-7.
McKeown, N. J., Carpi, P., Silva, J. F., Healey, A. J. E., Shaw, P. W., & van der Kooij, J. (2020). Genetic population structure and tools for the management of European sprat (Sprattus sprattus). ICES Journal of Marine Science, 77, 2134-2143.
Meredith, M. P., Watkins, J. L., Murphy, E. J., Cunningham, N. J., Wood, A. G., Korb, R., … Vivier, F. (2003). An anticyclonic circulation above the Northwest Georgia rise, Southern Ocean. Geophysical Research Letters, 30(20), 5.
Milano, I., Babbucci, M., Cariani, A., Atanassova, M., Bekkevold, D., Carvalho, G. R., et al. (2014). Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Molecular Ecology, 23, 118-135.
Mortimer, E., van Vuuren, B. J., Lee, J. E., Marshall, D. J., Convey, P., & Chown, S. L. (2011). Mite dispersal among the Southern Ocean islands and Antarctica before the last glacial maximum. Proceedings of the Royal Society B-Biological Sciences, 278, 1247-1255.
Narum, S. R., & Hess, J. E. (2011). Comparison of F-ST outlier tests for SNP loci under selection. Molecular Ecology Resources, 11, 184-194.
Nielsen, E. E., Cariani, A., Mac Aoidh, E., Maes, G. E., Milano, I., Ogden, R., et al. (2012). Gene-associated markers provide tools for tackling illegal fishing and false eco-certification. Nature Communications, 3(1), 1-7.
Norman, J. R. (1937). Coast fishes part II. The Patagonian region. Discovery Reports, 16, 1-150.
Nosil, P., Funk, D. J., & Ortiz-Barrientos, D. (2009). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375-402.
Nylander, J. A. A., Ronquist, F., Huelsenbeck, J. P., & Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology, 53, 47-67.
Ott, A., Liu, S., Schnable, J. C., Yeh, C. T. E., Wang, K. S., & Schnable, P. S. (2017). tGBS® genotyping-by-sequencing enables reliable genotyping of heterozygous loci. Nucleic Acids Research, 45(21), e178.
Poulin, E., Gonzalez-Wevar, C., Diaz, A., Gerard, K., & Hune, M. (2014). Divergence between Antarctic and south American marine invertebrates: What molecular biology tells us about scotia arc geodynamics and the intensification of the Antarctic circumpolar current. Global and Planetary Change, 123, 392-399.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
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.
Roe, A. D., & Sperling, F. A. H. (2007). Population structure and species boundary delimitation of cryptic Dioryctria moths: An integrative approach. Molecular Ecology, 16, 3617-3633.
Rogers, A. D., Morley, S., Fitzcharles, E., Jarvis, K., & Belchier, M. (2006). Genetic structure of Patagonian toothfish (Dissostichus eleginoides) populations on the Patagonian shelf and Atlantic and western Indian Ocean sectors of the Southern Ocean. Marine Biology, 149, 915-924.
Shaw, P. W., Arkhipkin, A. I., & Al-Khairulla, H. (2004). Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: The effect of the Antarctic polar front and deep-water troughs as barriers to genetic exchange. Molecular Ecology, 13, 3293-3303.
Smitt, F. A. (1898). Poissons de l'expedition scientifique a la terra de feu. Bihang till Kongl Svenska Vetenskaps-Akademiens Handlingar. Brandweek, 24 IV, 1-80.
Strugnell, J. M., Rogers, A. D., Prodohl, P. A., Collins, M. A., & Allcock, A. L. (2008). The thermohaline expressway: The Southern Ocean as a Centre of origin for deep-sea octopuses. Cladistics, 24, 853-860.
Thorpe, S. E., Heywood, K. J., Brandon, M., & Stevens, D. P. (2002). Variability of the southern Antarctic circumpolar current front north of South Georgia. Journal of Marine Systems, 37, 87-105.
Toomey, L., Welsford, D., Appleyard, S. A., Polanowski, A., Faux, C., Deagle, B. E., … Jarman, S. (2016). Genetic structure of Patagonian toothfish populations from otolith DNA. Antarctic Science, 28, 347-360.
Trathan, P. N., Garcia-Borboroglu, P., Boersma, D., Bost, C. A., Crawford, R. J. M., Crossin, G. T., et al. (2015). Pollution, habitat loss, fishing, and climate change as critical threats to penguins. Conservation Biology, 29, 31-41.
Van Ginneken, M., Decru, E., Verheyen, E., & Snoeks, J. (2017). Morphometry and DNA barcoding reveal cryptic diversity in the genus Enteromius (Cypriniformes: Cyprinidae) from The Congo basin, Africa. European Journal of Taxonomy, 310, 1-32.
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York: Springer.
Vitalis, R., Dawson, K., & Boursot, P. (2001). Interpretation of variation across marker loci as evidence of selection. Genetics, 158, 1811-1823.
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370.
Williams, R., Tuck, G. N., Constable, A. J., & Lamb, T. (2002). Movement, growth and available abundance to the fishery of Dissostichus eleginoides Smitt,1898 at heard Island, derived from tagging experiments. CCAMLR Science, 9, 33-48.
Winnepenninckx, B., Backeljau, T., & Dewachter, R. (1993). Extraction of high-molecular-weight DNA from mollusks. Trends in Genetics, 9, 407-407.