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Mitochondrial DNA sequence revealed contrasting demographic history between the black bullhead (Ameiurus melas ) and its cryptic lineage in North America

Published online by Cambridge University Press:  24 December 2010

Abinash Padhi
Abinash Padhi*
Affiliation:
Department of Biological Science, University of Tulsa, 800 S. Tucker Drive, Oklahoma-74104, USA
*
aCorresponding author: [email protected]
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Abstract

The black bullhead, Ameiurus melas of the family Ictaluridae, is a freshwater fish native to North America that was introduced throughout Europe in the late 1800s. Using mitochondrial DNA (mtDNA) as a genetic marker, the present study investigates the genetic structure and historical demography of A. melas in North America. MtDNA-based phylogenetic analyses revealed the existence of two distinct lineages (A and B) of A. melas. While lineage A clustered with the previously reported sequences of A. melas, lineage B emerged as a unique clade like other species of the genus Ameiurus. Individuals belonging to lineage B were mostly from the south central region of the United States, the region that never glaciated during the last Ice Age. Results of a fossil-based molecular clock analysis suggest that lineage A and the paraphyletic lineage B of A. melas diverged from their respective common ancestors approximately 3 (±0.2) and 15.9 (±1.3) million years ago. Lineage B could possibly be a hybrid species, possessing the mtDNA haplotype of its maternal parent, an Ameiurus species that has gone extinct. While lineage A showed evidence of population expansion, lineage B did not show any evidence of population expansion, but rather is comprised of geographically structured populations.

Keywords

SiluriformesAmeiurusmtDNAPhylogenyCryptic speciesMolecular ClockPopulation dynamics
Type
Research Article
Information
Aquatic Living Resources , Volume 23 , Issue 3 , July 2010 , pp. 325 - 333
Copyright
© EDP Sciences, IFREMER, IRD 2010

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References

Références

Andersen B.G., Borns H.W., 1994, The Ice age world. Scandinavian University Press, Oslo.
Avise J.C., 2000, Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press.
Bernatchez, L., Wilson, C.C., 1998, Comparative phylogeography of Nearctic and Palearctic fishes. Mol. Ecol. 7, 431-452. CrossRefGoogle Scholar
Bossu, C.M., Near, T.J., 2009, Gene trees reveal repeated instances of mitochondrial DNA introgression in orangethroat darters (Percidae: Etheostoma). Syst. Biol. 58, 114-129. CrossRefGoogle Scholar
Clement, M., Posada, D., Crandall, K.A., 2000, TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657-1659. CrossRefGoogle Scholar
Colborn, J., Crabtree, R.E., Shaklee, J.B., Pfeiler, E., Bowen, B.W., 2001, The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shore fish. Evolution 55, 807-820. CrossRefGoogle Scholar
Culling, M.A., Janko, K., Boron, A., Vasil’ev, VP.,Cote, I.M., Hewitt, G.M., 2006, European colonization by the spined loach (Cobitis taenia) from Ponto-Caspian refugia based on mitochondrial DNA variation. Mol. Ecol. 15, 173-190. CrossRefGoogle ScholarPubMed
Fu, Y.X., 1997, Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915-925. Google ScholarPubMed
Gleeson, D.M., Howitt, R.L., Ling, N., 1999, Genetic variation, population structure and cryptic species within the black mudfish, Neochanna diversus, an endemic galaxiid from New Zealand. Mol. Ecol. 8, 47-57. CrossRefGoogle ScholarPubMed
Grant, B.R., Grant, P.R., 2002, Lack of premating isolation at the base of a phylogenetic tree. Am. Nat. 160, 1-19. CrossRefGoogle ScholarPubMed
Hardman, M., 2005, The phylogenetic relationships among non-diplomystid catfishes as inferred from mitochondrial cytochrome b sequences; the search for the ictalurid sister taxon (Otophysi: Siluriformes). Mol. Phylogenet. Evol. 37, 700-720. CrossRefGoogle Scholar
Hardman, M,Hardman, L.M., 2008, The relative importance of body size and paleoclimatic change as explanatory variables influencing lineage diversification rate: an evolutionary analysis of bullhead catfishes (Siluriformes: Ictaluridae). Syst. Biol. 57, 116-130. CrossRefGoogle Scholar
Hardman, M., Page, L.M., 2003, Phylogenetic relationships among bullhead catfishes of the genus Ameiurus (Siluriformes: Ictaluridae). Copeia 2003, 20-33. CrossRefGoogle Scholar
Hewitt, G.M., 1999, Post-glacial recolonization of European biota. Biol. J. Linn. Soc. 68, 87-112. CrossRefGoogle Scholar
Huelsenbeck, J.P., Ronquist, F., 2001, MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. CrossRefGoogle ScholarPubMed
Huelsenbeck, J.P., Rannala, B., 1997, Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276, 227-232. CrossRefGoogle Scholar
Hunnicutt, D.W., Cingolani, J.,Voss, M.A., 2005, Use of mtDNA to identify genetic introgression among related species of catfish. J. Great. Lakes Res. 31, 482-491. CrossRefGoogle Scholar
Keck B.P., Near T.J., 2009, Patterns of natural hybridization in darters (Percidae:Etheostomatinae). Copeia2009, 758-773.
Kidd, M.R., Kidd, C.E., Kocher, T.D., 2006, Axes of differentiation in the bower-building cichlids of Lake Malawi. Mol. Ecol. 15, 459-478. CrossRefGoogle ScholarPubMed
Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Paabo, S., Villablanca, F.X., Wilson, A.C., 1989, Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86, 6196-6120. CrossRefGoogle ScholarPubMed
Kuhner, M., Yamamato, J., Felsenstein, J., 1998, Maximum-likelihood estimation of population growth rates based on the coalescent. Genetics 149, 429-434. Google ScholarPubMed
Langley, C.H., Fitch, W.M., (1974), An examination of the constancy of the rate of molecular evolution. J. Mol. Evol. 3, 161–177. CrossRefGoogle ScholarPubMed
Leidy, J., 1889, Notice and description of fossils in caves and crevices of the limestone rocks of Pennsylvania. Annual Report Geological Survey Pennsylvania for 1887, 1-20. Google Scholar
Lessa, E.P., Cook, J.A., Patton, J.L., 2003, Genetic footprints of demographic expansion in North America, but not Amazonia, during the late Quaternary. Proc. Natl. Acad. Sci. USA 100, 10331-10334. CrossRefGoogle Scholar
Lundberg, J.G., 1975, The fossil catfishes of North America. Univ Mich Mus Palaeo Pap Palaeo 11, 1-51. Google Scholar
Lundberg J.G., 1992, The phylogeny of ictalurid catfishes: a synthesis of recent work. In: Mayden RL ed. Systematics, historical ecology, and North American freshwater fishes, Stanford, CA: Stanford University Press, 392-420
Maddison W.P., Maddison D., 2001, MacClade. Sunderland, MA: Sinauer Associates.
McDaniel, S.F., Shaw, A.J., 2003, Phylogeographic structure and cryptic speciation in the trans-Antarctic moss Pyrrhobryum mnioides . Evolution 57, 205-215. CrossRefGoogle Scholar
Meyer, A., Kocher, T.D., Basasibwaki, P., Wilson, A.C., 1990, Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347, 550–553. CrossRefGoogle Scholar
Murdoch, M.H., Hebert, D.N., 1997, Mitochondrial DNA evidence of distinct glacial refugia for brown bullhead (Ameiurus nebulosus) in the Great Lakes. Can. J. Fish. Aquat. Sci. 54, 1450-1460. CrossRefGoogle Scholar
Murphy, J.W., Collier, G.E., 1996, Phylogenetic relationships within the aplocheiloid fish genus Rivulus (Cyprinodontiformes, Rivulidae): implications for Caribbean and Central American biogeography. Mol. Biol. Evol. 13, 642-649. CrossRefGoogle Scholar
Musyl, M.K., Keenan, C.P., 1996, Evidence for cryptic speciation in Australian freshwater eel-tailed catfish, Tandanus tandanus (Teleostei: Plotosidae). Copeia 1996, 526-534. CrossRefGoogle Scholar
NatureServe., 2006, NatureServe Explorer: an online encyclopedia of life [web application]. Version 4.7. NatureServe, Arlington, Virginia. Available http://www.natureserve.org/explorer.
Near, T.J., Kassler, T.W., Koppelman, J.B., Dillman, C.B., Phillip, D.P., 2003, Speciation in North American black basses, Micropterus (Actinopterygii:Centrarchidae). Evolution 57, 1610-1628. CrossRefGoogle Scholar
Novomeska, A., Kovac, V., 2009, Life-history traits of non-native black bullhead Ameiurus melas with comments on its invasive potential. J. Appl. Ichthyol. 25, 79–84. CrossRefGoogle Scholar
Page L.M., Burr B.M., 1991, A field guide to freshwater fishes of North America north of Mexico. Boston, MA: Houghton Mifflin Co.
Palumbi S.R., Martin A., Romano S., McMillan W.O., Stice L., Grabowski G., 1991, The simple fool’s guide to PCR. Honolulu, University of Hawaii.
Posada, D., Crandall, K.A., 1998, Modeltest: testing the model of DNA substitution, Bioinformatics 14, 817-818. CrossRefGoogle ScholarPubMed
Rambout A., Drummond A.J., 2006, Tracer. Version 1.4 Available from http://evolve.zoo.ox.ac.uk/.
Rogers, A.R., 1995, Genetic evidence for a Pleistocene explosion. Evolution 49, 608-615. CrossRefGoogle ScholarPubMed
Rogers, A.R., Harpending, H., 1992, Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9, 552-569. Google ScholarPubMed
Sanderson, M.J., 2003, r8s: inferring absolute rates of molecular evolution and divergence times in absence of a molecular clock. Bioinformatics 19, 301–302. CrossRefGoogle ScholarPubMed
Schneider, S., Excoffier, L., 1999, Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: Application to human mitochondrial DNA. Genetics 152, 1079-1089. Google Scholar
Schneider S., Roessli D., Excoffier L., 2000, Arlequin: a software for population genetics data analysis, Ver. 3.0. Genetics and Biometry Laboratory, University of Geneva, Switzerland.
Scribner, K.T., Page, K.S., Bartron, M.L., 2001, Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Rev. Fish Biol. Fish. 10, 293–323. CrossRefGoogle Scholar
Shearer, T.L., Van Oppen, M.J., Romano, S.L., Wörheide, G., 2002, Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol. Ecol. 11, 2475-2487. CrossRefGoogle Scholar
Simon T.P., Wallus R., 2004, Reproductive Biology and Early Life History of Fishes in the Ohio River Drainage, Volume 3: Ictaluridae – Catfish and Madtoms. CRC Press, New York.
Smith, C.L., 1954, Pleistocene fishes of the Berends fauna of Beaver County, Oklahoma. Copeia 1954, 282-289. CrossRefGoogle Scholar
Smith, L.C., 1962, Some Pliocene fishes from Kansas, Oklahoma and Nebraska. Copeia 1962, 505-519. CrossRefGoogle Scholar
Swift, C., 1968, Pleistocene freshwater fishes from Ingleside Pit, San Patricio County, Texas. Copeia 1968, 63-69. CrossRefGoogle Scholar
Swofford D.L., 2002, PAUP*. Phylogenetic Analysis Using Parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates.
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. CrossRefGoogle ScholarPubMed
Teller, S., Bardack, D., 1975, New records of late Pleistocene vertebrates from the southern end of Lake Michigan. Am. Midland Nat. 94, 179-189. CrossRefGoogle Scholar
Weigel R.D., 1963, Fossil vertebrates of Vero, Florida. Florida Geological Survey, Special Publication No. 10, 1-59.
Welsh, S.A., Cincotta, D.A., 2004, Natural hybrids of the madtoms, Noturus flavus and Noturus insignis, from the Monongahela River drainage, West Virginia. Northeastern Naturalist 11, 399-406. CrossRefGoogle Scholar
Wheeler, A., 1978, Ictalurus melas (Rafinesque, 1820) and I. nebulosus (Lesueur, 1819): the North American catfishes in Europe. J. Fish Biol. 12, 435–439. CrossRefGoogle Scholar
Wirtz, P., 1999, Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour 58, 1–12. CrossRefGoogle ScholarPubMed