Abstract
The taxonomic status of hake (Merluccius spp.) in the northeastern Pacific is unclear. Hakes in this region are Merluccius productus, M. angustimanus, M. hernandezi, and a morphotype known as dwarf hake. Of these, only the first two species are currently valid. Descriptions in previous studies have been limited by overlapping morphological characteristic, lack of biological material, and limited numbers of sampling localities. To clarify their taxonomy, 461 hake were obtained from eight localities along the North American coast for morphological and mitochondrial DNA sequence analyses (cytochrome b, cytochrome c oxidase subunit I, and 16S ribosomal rDNA). Morphological and molecular analyses suggest that hake in this region represent a continuum of a single species with some levels of morphological and genetic intra-specific variation. In light of these results, we propose that M. productus is the only species of hake present along the North American and northern Central American coast.
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References
Ahlstrom EH (1969) Distributional atlas of fish larvae in the California Current region: jack mackerel, Trachurus symmetricus, and Pacific hake, Merluccius productus, 1951 through 1966. Calif Coop Ocean Fish Invest Atlas 11:v–xiii, 1–187
Ahlstrom EH, Counts RC (1955) Eggs and larvae of the Pacific hake, Merluccius productus. Fish Bull 56:295–329
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693
Ambrose DA (1996) Merlucciidae: hakes. In: Moser HG (ed) The early stages of the fishes in the California Current Region. Calif Coop Ocean Fish Invest Atlas 33, pp 508–511
Astrin JJ, Huber BA, Misof B, Klütsch CFC (2006) Molecular taxonomy in pholcid spiders (Pholcidae, Araneae): evaluation of species identification methods using CO1 and 16S rRNA. Zool Scr 35:441–457
Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol 20:99–105
Ayres WO (1855) Description of new species of Californian fishes. Proc Calif Acad Nat Sci 1:23–77
Bailey KM, Francis RC, Stevens PR (1982) The life history and fishery of Pacific whiting, Merluccius productus. Calif Coop Ocean Fish Invest Rep 23:81–98
Balart-Páez EF (2005) Biología y ecología de la merluza bajacaliforniana, Merluccius angustimanus Garman, 1899, en la costa occidental de Baja California Sur, México. Doctoral Thesis, Universidad Autónoma de Nuevo León, Monterrey
Beal CH (1948) Reconnaissance of the geology and oil possibilities of Baja California, Mexico. Geol Soc Am Mem 31:1–138
Bermingham E, Lessios HA (1993) Rate variation of protein and mitochondrial DNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc Natl Acad Sci USA 90:2734–2738
Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In: Kocher TD, Stepien CA (eds) Molecular systematics of fishes. Academic Press, New York, pp 113–128
Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57:1599–1609
Billington N, Hebert PDN (1991) Mitochondrial DNA diversity in fishes and its implications for introductions. Can J Fish Aquat Sci 48:80–94
Blackburn M (1967) Synopsis of biological information on the Australian anchovy Engraulis australis (White). Calif Coop Ocean Fish Invest Rep 11:34–43
Camper JD, Barber RC, Richardson LR, Gold JR (1993) Mitochondrial DNA variation among red snapper (Lutjanus campechanus) from the Gulf of Mexico. Mol Mar Biol Biotech 2:154–161
Campo D, Machado-Schiaffino G, Perez J, Garcia-Vazquez E (2007) Phylogeny of the genus Merluccius based on mitochondrial and nuclear genes. Gene 406:171–179
Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591
Cohen DM, Inada T, Iwamoto T, Scialabba N (1990) FAO species catalogue. Vol. 10. Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Fish Synop, Roma
Crisci JV, López-Armengol MF (1983) Introducción a la teoría y práctica de la taxonomía numérica. Secretaría General de la Organización de los Estados Americanos. Programa Regional de Desarrollo Científico y Tecnológico, Washington, DC
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886
Dodson JJ, Carscadden JE, Bernatchez L, Colombani F (1991) Relationship between spawning mode and phylogenetic structure in mitochondrial DNA of north Atlantic capelin Mallotus villosus. Mar Ecol Prog Ser 76:103–113
Félix-Uraga R, Quiñónez-Velázquez C, Hill KT, Gómez-Muñoz VM, Melo-Barrera FN, García-Franco W (2005) Pacific sardine (Sardinops sagax) stock discrimination off the west coast of Baja California and southern California using otolith morphometry. Calif Coop Ocean Fish Invest Rep 46:113–121
Felsenstein J (1985) Confidence limits on phylogenies: and approach using the bootstrap. Evolution 39:783–791
Franca P (1962) Considérations sur la taxonomie des Merluccius de I’Atlantique oriental. Trabalhos do Centro de Biologia Piscatoria. Mem Junta Inv Ultram 2:7–48
Frost KJ (1981) Descriptive key to the otoliths of Gadid fishes of the Bering, Chukchi, and Beaufort seas. Arctic 34:55–59
Garman S (1899) Report on an exploration off the west coasts of México, Central and South America, and off the Galapagos Islands, in charge of Alexander Agassiz, by the U. S. Fish Commission steamer “Albatros” during 1891, XXVI (The Fishes). Mem Mus Comp Zool Harvard Coll 24:1–431
Ginsburg I (1954) Whitings on the coasts of the America continents. Fish Bull 96:187–208
Gold JR, Richardson LR, Furman C, Sun F (1994) Mitochondrial DNA diversity and population structure in marine fish species from the Gulf of Mexico. Can J Fish Aquat Sci 51:205–214
Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426
Grant WS, Leslie RW (2001) Inter-ocean dispersal is an important mechanism in the zoogeography of hakes (Pisces: Merluccius spp). J Biogeogr 28:699–721
Grant WS, Leslie RW, Becker II (1987) Genetic stock structure of the southern African hakes Merluccius capensis and M. paradoxus. Mar Ecol Prog Ser 41:9–20
Graves JE (1995) Conservation genetics of fishes in the pelagic marine realm. In: Avise JC, Hamrick JL (eds) Conservation genetics: case histories from nature. Chapman and Hall, New York, pp 335–366
Guichenot A (1848) Historia física y política de Chile (en Gay, C.). Zool 2:328–330
Hadfield AJ, Ivantsoff V, Johnston PG (1979) Clinal variation in electrophoretic and morphological characters between two nominal species of the genus Pseudomugil (Pisces: Atheriniformes: Pseudomugilidae). Aust J Mar Freshwat Res 30:375–386
Ho J (1990) Phylogeny and biogeography of hakes (Merluccius; Teleostei): a cladistic analysis. Fish Bull 88:95–104
Hubbs CL (1925) Racial and seasonal variation in the Pacific herring, California sardine and California anchovy. Calif Fish Game Comm Fish Bull 8:1–23
Hubbs CL, Hubbs C (1953) An improved graphical analysis and comparison of series of samples. Syst Zool 2:49–57
Hubbs CL, Lagler KF (1958) Fishes of the Great Lakes Region. Cranbrook Inst Sci Bull 26:1–213
Huelsenbeck JP, Ronquist R (2001) Mr Bayes: Bayesian inferences of phylogeny. Bioinformatics 17:754–755
Huelsenbeck JP, Hillis DM, Jones R (1996) Parametric bootstrapping in molecular phylogenetics: applications and performance. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies and protocols. Wiley-Liss, New York, pp 19–45
ICZN (1999) International code of zoological nomenclature. The International Trust for Zoological Nomenclature, London
Inada T (1981) Studies on the Merluccid fishes. Bull Far Seas Fish Res Lab 18:1–172
Inada T (1995) Merlucciidae. In: Fisher W, Krupp F, Schneider W, Sommer C, Carpenter KE, Niem VH (eds) Guía FAO para la identificación de especies para los fines de la pesca. Pacífico centro-oriental. Volumen III. Vertebrados Parte 2. FAO, Rome, pp 1272–1274
Iwamoto E, Ford MJ, Gustafson RG (2004) Genetic population structure of Pacific hake, Merluccius productus, in the Pacific Northwest. Environ Biol Fish 69:187–199
Johns GC, Avise JC (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15:1481–1490
Jordan AD, Moller PR, Nielsen JG (2003) Revision of the Arctic cod genus Arctogadus. J Fish Biol 62:1339–1352
Kabata Z, Ho J (1981) The origin and dispersal of hake (genus Merluccius: Pices: Teleostei) as indicated by its copepod parasites. Oceanogr Mar Biol Annu Rev 19:381–404
Kartavtsev YP, Lee JS (2006) Analysis of nucleotide diversity at the cytochrome b and cytochrome oxidase 1 genes at the population, species and genus levels. Russ J Genet 42:341–362
Kartavtsev YP, Jung SO, Lee YM, Byeon HK, Lee JS (2007) Complete mitochondrial genome of the bullhead torrent catfish, Liobagrus obesus (Siluriformes, Amblycipididae): genome description and phylogenetic considerations inferred from the Cyt b and 16S rRNA genes. Gene 396:13–27
Knowlton N, Weight LA, Solorzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260:1629–1632
Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca XF, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200
Lankford TE, Billerbeck JM, Conover DO (2001) Evolution of intrinsic growth and energy acquisition rates: II. Trade-offs with vulnerability to predation in Menidia menidia. Evolution 55:1873–1881
Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam
Lloris D, Matallanas J, Oliver P (2003) Merluzas del mundo. (Familia Merlucciidae). Catalogo comentado e ilustrado de las merluzas conocidas. FAO Catalogo de especies para fines de la pesca, Roma
Lozano-Cabo F (1965) Las merluzas atlánticas. Publ Téc J Est Pesca 4:11–31
Lundy CJ, Moran P, Rico C, Milner RS, Hewitt GM (1999) Macrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius), a commercially important fish. Mol Ecol 8:1889–1898
Martínez E (1976) Variabilidad de los caracteres merísticos en Merluccius gayi (Guichenot, 1848) en la costa de Chile. Rev Biol Mar 16:71–93
Mathews CP (1985) Meristic studies of the Gulf of California species of Merluccius, with a description of a new species. J Nat Hist 19:697–718
Mayr E (1969) Principles of systematic zoology. McGraw-Hill, New York
McDowall RM (2008) Jordan’s and other ecogeographical rules, and the vertebral number in fishes. J Biogeogr 35:501–508
McHugh J (1951) Meristic variations and populations of northern anchovy (Engraulis mosdax). Scripps Inst Oceanogr Bull 6:123–160
Meyer A (1993) Evolution of mitochondrial DNA in fishes. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Elsevier, Amsterdam, pp 1–38
Miller DJ (1956) Anchovy. Calif Coop Ocean Fish Invest Rept 1:20–26
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University
Ovenden JR (1990) Mitochondrial DNA and marine stock assessment: a review. Aust J Mar Freshwat Res 41:835–853
Peregrino-Uriarte AB, Pacheco-Aguilar R, Yepiz-Plascencia G (2007) Diferencias en los genes 16SrRNA y citocromo c oxidasa subunidad I de las lisas Mugil cephalus y Mugil curema y los robalos Centropomus viridis y Centropomus robalito. Cienc Mar 33:95–104
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UK
Quinteiro J, Vidal R, Rey-Méndez M (2000) Phylogeny and biogeographic history of hake (genus Merluccius) inferred from DNA control-region sequences. Mar Biol 136:163–174
Riddle BR, Hafner DJ, Alexander LF, Jaeger JR (2000) Cryptic vicariance in the historical assembly of a Baja California peninsular desert biota. PNAS 97:14438–14443
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Roldán MI, García-Marín JL, Utter FM, Pla C (1998) Population genetic structure of European hake, Merluccius merluccius. Heredity 81:327–334
Roldán MI, García-Marín JL, Utter FM, Pla C (1999) Genetic relationships among Merluccius species. Heredity 83:79–86
Rosel PE, Kocher TD (2002) DNA-based identification of larval cod in stomach contents of predatory fishes. J Exp Mar Biol Ecol 267:75–88
Rozas J, Sanchéz-DelBarrio JC, Messenguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Saunders MW, Leaman BM, McFarlane GA (1997) Influence of ontogeny and fishing mortality on the interpretation of sablefish, Anoplopoma fimbria, life history. NOAA Tech Rept NMFS 130:81–92
Shields GF, Gust JR (1995) Lack of geographic structure in mitochondrial DNA sequences of Bering Sea walleye pollock, Theragra chalcogramma. Mol Mar Biol Biotechnol 4:69–82
Short JA, Gburski CM, Kimura DK (2006) Using otolith morphometrics to separate small Walleye Pollock Theragra chalcogramma from Artic Cod Boregadus saida in mixed samples. Alaska Fish Res Bull 12:147–152
Smith PE, Moser HG (2003) Long-term trends and variability in the larvae of Pacific sardine and associated fish species of the California Current region. Deep-Sea Res II 50:2519–2536
Smith PJ, Patchell GJ, Benson PG (1979) Glucosephosphate isomerase and isocitrate dehydrogenase polymorphisms in the hake, Merluccius australis. N Z J Mar Freshw Res 13:545–547
StatSoft (2004) STATISTICA, Version 7. Tulsa, OK
Swain DP (1992) The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution 46:987–997
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA). Software version 4.0. Mol Biol Evol 24:1596–1599
Teletchea F, Laudet V, Hänni C (2006) Phylogeny of the Gadidae (sensu Svetovidov, 1948) based on their morphology and two mitochondrial genes. Mol Phylogenet Evol 38:189–199
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Utter FM, Hodgins HO (1971) Biochemical polymorphisms in the Pacific hake (Merluccius productus). Rapp P-V Reun Cons Perm Int Explor Mer 161:87–89
Utter FM, Stormont CJ, Hodgins HO (1970) Esterase polymorphism in vitreous fluid of Pacific hake, Merluccius productus. Anim Blood Grps Biochem Genet 1:69–82
Vrooman AM, Paloma PA (1977) Dwarf hake off the coast of Baja California, México. Calif Coop Ocean Fish Invest Rep 19:67–72
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Phil Trans R Soc B 360:1–11
Xia X, Xie Z (2001) DAMBE: data analysis in molecular biology and evolution. J Hered 92:371–373
Yamahira K, Lankford TE Jr, Conover DO (2006) Intra- and interspecific latitudinal variation in vertebral number of Menidia spp. (Teleostei: Atherinopsidae). Copeia 2006:431–436
Acknowledgments
Hake samples were provided by Manuel Nevares, Mike Canino, Maria de L. Gonzalez-Rugge, Hugo Cirilo, and Eva F. Isaak Vissuet. Special thanks to the crews of the INP and CIBNOR vessels for cruises to obtain samples; the Pacific Choice Seafood of California, and the commercial shrimp fleets of the Pacific coast of Costa Rica. We thank Lucía Campos-Dávila at the Colección Ictiológica at CIBNOR. This project was funded by the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación de México and the Consejo Nacional de Ciencia y Tecnología (SAGARPA-CONACYT grant 2005-12058 to FJGDL. CASS and MBC received CONACYT fellowships. Additional advice was received from Gil Rosenthal, Darrin Hulsey, Ingo Schlupp, and Miguel Cordoba.
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Silva-Segundo, C.A., Brito-Chavarria, M., Balart, E.F. et al. Clarifying the taxonomic status of Merluccius spp. in the northeastern Pacific: a combined morphological and molecular approach. Rev Fish Biol Fisheries 21, 259–282 (2011). https://doi.org/10.1007/s11160-010-9166-6
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DOI: https://doi.org/10.1007/s11160-010-9166-6