Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2016-09-14
Page range: 38–60
Abstract views: 87
PDF downloaded: 6

Phylogeny and genetic variation within the widely distributed Bluntnose Minnow, Pimephales notatus (Cyprinidae), in North America

Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA. phone: (314) 997-3932; Fax: (314) 977-3658.
Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA. phone: (314) 997-3932; Fax: (314) 977-3658.
Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA. phone: (314) 997-3932; Fax: (314) 977-3658.
Department of Biology, Saint Louis University, 3507 Laclede Avenue, St. Louis, MO 63103, USA. phone: (314) 997-3932; Fax: (314) 977-3658.
Pisces range expansion diversification genetic variation phylogeography

Abstract

This study represents a phylogenetic analysis of Pimephales notatus, a widely distributed North American cyprinid fish species, using one mitochondrial (cytb) and two nuclear (S7 and Rag1) genes. Despite the broad geographic distribution of this species that includes independent basins, results suggest a largely drainage-independent genetic structure. Results reveal a well-supported lineage in the Ozark Highlands, which is highly divergent from the remaining populations and may represent a long-term isolated lineage that should be considered as a separate conservation and management unit. All other remaining populations comprised a widely distributed lineage, covering most of the distribution for the species (from the Red River and tributaries of the Great Lakes in the north to the lower Mississippi and Mobile basin in the south, and from the Missouri River in the west to the Chesapeake and Albemarle Sound basins in the east). Phylogenetic, genetic diversity, and biogeographical data suggest that this wide-ranging lineage could have experienced a recent expansion to northern areas where populations exhibit little genetic variation. Results from molecular analyses reveal a distinctive lineage in the Ozarks and suggest that there is need for morphological analyses within P. notatus to determine its taxonomic status.

 

 

References

  1. Abell, R., Thieme, M.L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras-Balderas, S., Bussing, W., Stiassny, M., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Rebecca Ng, Sindorf, N., Robertson, J., Armijo, E., Higgins, J.V., Heibel, T.J., Wikramanayake, E., Olson, D., López, H.L., Reis, R.E., Lundberg, J.G., Pérez, M.H.S. & Petry, P. (2008) Freshwater ecoregions of the world: A new map of biogeographic units for freshwater biodiversity conservation. Bioscience, 58, 403–414.
    http://dx.doi.org/10.1641/B580507

    Bandelt, H.-J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.
    http://dx.doi.org/10.1093/oxfordjournals.molbev.a026036

    Beachum, C.E. (2014) Correlating temperature and streamflow with species traits in the bluntnose minnow (Pimephales notatus). Ph.D. dissertation. Saint Louis University, St. Louis, Missouri, 106 pp.

    Beachum, C.E., Michel, M.J. & Knouft, J.H. (2016) Differential responses of body shape to local and reach scale stream flow in two freshwater fish species. Ecology of Freshwater Fish, 25, 446–454.
    http://dx.doi.org/10.1111/eff.12225

    Berendzen, P.B., Simons, A.M. & Wood, R.M. (2003) Phylogeography of the northern hogsucker, Hypentelium nigricans (Teleostei: Cypriniformes): genetic evidence for the existence of the ancient Teays River. Journal of Biogeography, 30, 1139–1152.
    http://dx.doi.org/10.1046/j.1365-2699.2003.00888.x

    Berendzen, P.B., Dugan, J.F. & Gamble, T. (2010) Post-glacial expansion into the Paleozoic Plateau: evidence of an Ozarkian refugium for the Ozark minnow Notropis nubilus (Teleostei: Cypriniformes). Journal of Fish Biology, 77, 1114–1136.
    http://dx.doi.org/10.1111/j.1095-8649.2010.02769.x

    Bernatchez, L. & Wilson, C.C. (1998) Comparative phylogeography of Neartic and Paleartic fishes. Molecular Ecology, 7, 431–452.
    http://dx.doi.org/10.1046/j.1365-294x.1998.00319.x

    Bielawski, J.P., Brault, A. & Gold, J.R. (2002) Phylogenetic relationships within the genus Pimephales as inferred from ND4 and ND4L nucleotide sequences. Journal of Fish Biology, 61, 293–297.
    http://dx.doi.org/10.1111/j.1095-8649.2002.tb01754.x

    Blanton, R.E., Page, L.M. & Ennis, B.M. (2011) Phylogenetic relationships of Opsopoeodus emiliae, with comments on the taxonomic implications of discordance among datasets. Copeia, 2011, 82–92.
    http://dx.doi.org/10.1643/CI-10-004

    Blatchley, W.S. (1885) A review of the species of the genus Pimephales. Proceedings of the Academy of Natural Sciences of Philadelphia, 37, 63–65.

    Buth, D.G. & Mayden, R.L. (1981) Taxonomic status and relationships among populations of Notropis pilsbryi and N. zonatus (Cypriniformes: Cyprinidae) as shown by the glucosephosphate isomerase, lactate dehydrogenase and phosphoglucomutase enzyme systems. Copeia, 1981, 583–590.
    http://dx.doi.org/10.2307/1444562

    Chow, S. & Hazama, K. (1998) Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology, 7, 1255–1256.

    Coburn, M.M. & Cavender, T.M. (1992) Interrelationships of North American cyprinid fishes. In: Mayden, R.L. (Ed.), Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, pp. 328–373.

    Cross, F.B., Mayden, R.L. & Stewart, J.D. (1986) Fishes in the western Mississippi Basin (Missouri, Arkansas and Red Rivers). In: Hocutt, C.H. & Wiley, E.O. (Eds.), The Zoogeography of North American Freshwater Fishes. John Wiley and Sons, New York, pp. 363–412.

    Dillman, C.B., Wagner, B.K. & Wood, R.M. (2010) Phylogenetic estimation of species limits in dwarf crayfishes from the Ozarks: Orconectes macrus and Orconectes nana (Decapoda: Cambaridae). Southeastern Naturalist, 9 (3), 185–198.
    http://dx.doi.org/10.1656/058.009.s309

    Echelle, A.A., Schwemm, M.R., Land, N.J., Nagle, B.C., Simons, A.M., Unmack, P.J., Fisher, W.L. & Hoagstrom, C.W. (2014) Molecular systematics and historical biogeography of the Nocomis biguttatus species group (Teleostei: Cyprinidae): Nuclear and mitochondrial introgression and a cryptic Ozark species. Molecular Phylogenetics and Evolution, 81, 109–119.
    http://dx.doi.org/10.1016/j.ympev.2014.09.011

    Echelle, A.A., Michael R., Schwemm, M.R., Lang, N.J., Baker, J.S., Wood, R.M., Near, T.J. & Fisher, W.L. (2015) Molecular systematics of the least darter (Percidae: Etheostoma microperca): Historical biogeography and conservation implications. Copeia, 103 (1), 87–98.
    http://dx.doi.org/10.1643/CG-14-082

    Egge, J.D. & Simons, A.M. (2006) The challenge of truly cryptic diversity: diagnosis and description of a new madtom catfish (Ictaluridae: Noturus). Zoologica Scripta, 35, 581–595.
    http://dx.doi.org/10.1111/j.1463-6409.2006.00247.x

    Excoffier, L. & Lischer, H.E. (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.
    http://dx.doi.org/10.1111/j.1755-0998.2010.02847.x

    Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
    http://dx.doi.org/10.2307/2408678

    Foster, K., Bower, L. & Piller, K. (2015) Getting in shape: habitat-based morphological divergence for two sympatric fishes. Biological Journal of the Linnean Society, 114, 152–162.
    http://dx.doi.org/10.1111/bij.12413

    Fu, Y.X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.

    Galloway, W.E., Whiteaker, T.L. & Ganey-Curry, P. (2011) History of Cenozoic North American drainage basin evolution, sediment yield, and accumulation in the Gulf of Mexico basin. Geosphere, 7, 938–973.
    http://dx.doi.org/10.1130/GES00647.1

    Gilbert, C.R. (1998) Type catalog of recent and fossil North American freshwater fishes: families Cyprinidae, Catostomidae, Ictaluridae, Centrarchidae, and Elassomatidae. Florida Museum of Natural History Special Publication, 1, 1–284.

    Grobman, A.B. (1943) Notes on salamanders with the description of a new species of Cryptobranchus. Occasional Papers of the Museum of Zoology University of Michigan, 470, 1–13.

    Halas, D. & Simons, A.M. (2014) Cryptic speciation reversal in the Etheostoma zonale (Teleostei: Percidae) species group, with an examination of the effect of recombination and introgression on species tree inference. Molecular Phylogenetics and Evolution, 70, 13–28.
    http://dx.doi.org/10.1016/j.ympev.2013.08.014

    Harpending, R.C. (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology, 66, 591–600.

    Hewitt, G. (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913.
    http://dx.doi.org/10.1038/35016000

    Hoagstrom, C.W., Visotheary, U. & Taylor, K. (2014) Miocene rivers and taxon cycles clarify the comparative biogeography of North American highland fishes. Journal of Biogeography, 41, 644–658.
    http://dx.doi.org/10.1111/jbi.12244

    Hollingsworth, P.R., Simons, A.M., Fordyce, J.A. & Hulsey, C.D. (2013) Explosive diversification following a benthic to pelagic shift in freshwater fishes. BMC Evolutionary Biology, 13 (Article 272), 1–11.
    http://dx.doi.org/10.1186/1471-2148-13-272

    Hudson, R.R., Slatkin, M., Maddison, W.P. (1992) Estimation of levels of gene flow from DNA sequence data. Genetics, 132, 583–589.

    Hubbs, C.L. & Black, J.D. (1947) Revision of Ceratichthys, a genus of American cyprinid fishes. Miscellaneous Publications Museum of Zoology, University of Michigan, 66, 1–56.

    Huelsenbeck, J.P. & Ronquist, F.R. (2001) Mr. Bayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
    http://dx.doi.org/10.1093/bioinformatics/17.8.754

    Jacquemin, S.J., Martín, E. & Piron, M. (2013) Morphology of bluntnose minnow Pimephales notatus (Cyprinidae) covaries with habitat in a central Indiana watershed. American Midland Naturalist, 169, 137–146.
    http://dx.doi.org/10.1674/0003-0031-169.1.137

    Jenkins, R.E. & Burkhead, N.M. (1994) Freshwater Fishes of Virginia. American Fisheries Society, Bethesda, MD, 1079 pp.

    Kraatz, W.C. (1928) Study of the food of the blunt-nosed minnow, Pimephales notatus. Ohio Journal of Science, 28 (2), 86–98.

    Kinziger, A.P. (2003) Evidence supporting two new forms and one previously described race within the Cottus carolinae species-complex from the Ozark Highlands. American Midland Naturalist, 149, 418–424.
    http://dx.doi.org/10.1674/0003-0031(2003)149[0418:ESTNFA]2.0.CO;2

    Kinziger, A.P., Goodman, D.H. & Studebaker, R.S. (2007) Mitochondrial DNA variation in the Ozark Highland members of the banded sculpin Cottus carolinae complex. Transactions of the American Fisheries Society, 136, 1742–1749.
    http://dx.doi.org/10.1577/T06-025.1

    Kinziger, P.A. & Wood, R.M. (2010) Cottus immaculatus, a new species of sculpin (Cottidae) from the Ozark Highlands of Arkansas and Missouri, USA. Zootaxa, 2340, 50–64.

    Librado, P. & Rojas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA 958 polymorphism data. Bioinformatics, 25, 1451–1452.
    http://dx.doi.org/10.1093/bioinformatics/btp187

    Lopez, J.A., Chen, W.-J. & Orti, G. (2004) Esociform phylogeny. Copeia, 2004 (3), 449–464.
    http://dx.doi.org/10.1643/cg-03-087r1

    Li, C., Bessert, M.L., Macrander, J. & Orti, G. (2009) Low variation but strong population structure in mitochondrial control region of the plains topminnow, Fundulus sciadicus. Journal of Fish Biology, 74, 1037–1048.
    http://dx.doi.org/10.1111/j.1095-8649.2008.02097.x

    Li, Y.C. & Gold, J.R. (1991) Cytogenetics studies in North American minnows (Cyprinidae). XXII. Chromosomal NORs in the genus Pimephales. Canadian Journal of Zoology, 69, 2826–2830.
    http://dx.doi.org/10.1139/z91-398

    Mayden, R.L. (1985) Biogeography of Ouachita highland fishes. Southwestern Naturalist, 30, 195–211.
    http://dx.doi.org/10.2307/3670734

    Mayden, R.L. (1987a) Historical ecology and North American highland fishes: A research program in community ecology. In: Matthews, W.J. & Heins, D.C. (Eds.), Community and Evolutionary Ecology of North American Stream Fishes. University of Oklahoma Press, Norman, pp. 210–222.

    Mayden, R.L. (1987b) Pleistocene glaciation and historical biogeography of North American highland fishes. In: Johnson, W.C. (Ed.), Quaternary environments of Kansas. Kansas Geological Survey, Guidebook Series 5, pp. 141–151.

    Mayden, R.L. (1988a) Vicariance biogeography, parsimony, and evolution in North American freshwater fishes. Systematic Zoology, 37 (4), 329–355.
    http://dx.doi.org/10.2307/2992197

    Mayden, R.L. (1988b) Systematics of the Notropis zonatus species group, with description of a new species from the Interior Highlands of North America. Copeia, 1988 (1), 153–173.
    http://dx.doi.org/10.2307/1445934

    Mayden, R.L. (1989) Phylogenetic studies of North American minnows, with emphasis on the genus Cyprinella (Teleostei: Cypriniformes). Miscellaneous Publications, University of Kansas Museum of Natural History, 80, 1–189.
    http://dx.doi.org/10.5962/bhl.title.5480

    Mayden, R.L. (2010) Systematics of the Etheostoma punctulatum species group (Teleostei: Percidae), with descriptions of new species. Copeia, 2010 (4), 716–734.
    http://dx.doi.org/10.1643/CG-10-056

    Morris, A. & Page, L.M. (1981) Variation in western logperches (Pisces: Percidae), with description of a new subspecies from the Ozarks. Copeia, 1981, 95–108.
    http://dx.doi.org/10.2307/1444044

    Near, T.J., Page, L.M. & Mayden, R.L. (2001) Intraspecific phylogeography of Percina evides (Percidae: Etheostomatinae): an additional test of the Central Highlands pre-Pleistocene vicariance hypothesis. Molecular Ecology, 10, 2235–2240.
    http://dx.doi.org/10.1046/j.1365-294X.2001.01362.x

    Oberdorff, T., Hugueny, B. & Guegan, J-F. (1997) Is there an influence of historical events on contemporary fish species richness in rivers? Comparisons between Western Europe and North America. Journal of Biogeography, 24, 461–467.
    http://dx.doi.org/10.1111/j.1365-2699.1997.00113.x

    Page, L.M. & Burr, B.M. (1991) A Field Guide to Freshwater Fishes of North America North of Mexico. The Peterson Field Guide Series, Houghton-Mifflin Co., Boston, MA, 432 pp.

    Panijpan, B., Laosinchai, P., Senapin, S., Kowasupat, C., Ruenwongsa, P., Kuhne, L. & Phiwsaiya, K. (2015) Mitochondrial COI and nuclear RAG1 DNA sequences and analyses of the three morphologically established species in the genus Trichopsis (Perciformes: Osphronemidae) reveal new/cryptic species. Meta Gene, 4, 17–28.
    http://dx.doi.org/10.1016/j.mgene.2015.02.003

    Pflieger W.L. (1971) A distributional study of Missouri fishes. University of Kansas Publications, Museum of Natural History, 20, 225–570.

    Posada, D. & Crandall, K.A. (1998) Modeltest: Testing the models of DNA substitution. Bioinformatics, 14, 817–818.
    http://dx.doi.org/10.1093/bioinformatics/14.9.817

    Provan, J. & Bennet, K.D. (2008) Phylogeographic insights into cryptic glacial regugia. Trends in Ecology and Evolution, 23 (10), 561–571.
    http://dx.doi.org/10.1016/j.tree.2008.06.010

    Pyron, M., Fincel, M. & Dang, M. (2007) Sexual size dimorphism and ecomorphology of spotfin shiner (Cyprinella spiloptera) from the Wabash River watershed. Journal of Freshwater Ecology, 22, 697–696.
    http://dx.doi.org/10.1080/02705060.2007.9664829

    Ramirez-Soriano, A., Ramos-Onsins, S.E., Rozas, J., Calafell, F. & Navarro, A. (2008) Statistical power analyses of neutrality test under demographic expansions, contractions and bottlenecks with recombination. Genetics, 179, 555–567.
    http://dx.doi.org/10.1534/genetics.107.083006

    Ray, J.M., Wood, R.M. & Simons, A.M. (2006) Phylogeography and post-glacial colonization patterns of the rainbow darter, Etheostoma caeruleum (Teleostei: Percidae). Journal of Biogeography, 33, 1550–1558.
    http://dx.doi.org/10.1111/j.1365-2699.2006.01540.x

    Robins, C.R. & Robinson, H.W. (1985) Cottus hypselurus, a new cottid fish from the Ozark uplands, Arkansas and Missouri. American Midland Naturalist, 114, 360–373.
    http://dx.doi.org/10.2307/2425610

    Robinson, H.W. (1986) Zoogeographic implications of the Mississippi River Basin. In: Hocutt, C.H. & Wiley, E.O. (Eds.), The Zoogeography of North American Freshwater Fishes. John Wiley and Sons, New York, pp. 267–285.

    Roe, K.J., Mayden, R.L. & Harris, P.M. (2008) Systematics and zoogeography of the Rock Bases (Centrarchidae: Ambloplites). Copeia, 2008 (4), 858–867.
    http://dx.doi.org/10.1643/CI-07-105

    Schönhuth, S. & Doadrio, I. (2003) Phylogenetic relationships of Mexican minnows of the genus Notropis (Actinopterygii: Cyprinidae). Biological Journal of the Linnean Society, 80, 323–337.
    http://dx.doi.org/10.1046/j.1095-8312.2003.00241.x

    Schönhuth, S., Blum, M.J., Lozano-Vilano, L., Neely, D.A., Romero-Varela, A., Espinosa, H., Perdices, A. & Mayden, R.L. (2011) Interbasin exchange and repeated headwater capture across the Sierra Madre Occidental inferred from the phylogeography of Mexican stonerollers. Journal of Biogeography, 38, 1406–1421.
    http://dx.doi.org/10.1111/j.1365-2699.2011.02481.x

    Schönhuth, S., Shiozawa, D.K., Dowling, T.E. & Mayden, R.L. (2012) Molecular systematics of western North American cyprinids (Cypriniformes: Cyprinidae). Zootaxa, 3586, 28–303.

    Schönhuth, S., Lozano-Vilano, L., Perdices, A., Espinosa, H. & Mayden, R.L. (2014) Phylogeny, genetic diversity and phylogeography of the genus Codoma (Teleostei, Cyprinidae). Zoologica Scripta, 44, 11–28.
    http://dx.doi.org/10.1111/zsc.12083

    Schmidt, T.R., Dowling, T.E. & Gold, J.R. (1994) Molecular systematics of the genus Pimephales (Teleostei: Cyprinidae). Southwestern Naturalist, 39, 241–248.
    http://dx.doi.org/10.2307/3671588

    Smith, G.R. (1981) Late Cenozoic freshwater fishes of North America. Annual Review of Ecology Evolution and Systematics, 12, 163–193.
    http://dx.doi.org/10.1146/annurev.es.12.110181.001115

    Stamatakis, A. (2006) RAxML-VI-HPC: Maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.
    http://dx.doi.org/10.1093/bioinformatics/btl446

    Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A fast bootstrapping algorithm for the RAxML Web-Servers. Systematic Biology, 57, 758–771.
    http://dx.doi.org/10.1080/10635150802429642

    Starnes, W.C. & Etnier, D.A. (1986) Drainage evolution and fish biogeography of the Tennessee and Cumberland rivers drainage realm. In: Hocutt, C.H. & Wiley, E.O. (Eds.), The Zoogeography of North American Freshwater Fishes. John Wiley and Sons, New York, pp. 325–362.

    Strange, R.M. & Burr, B.M. (1997) Intraspecific phylogeography of North American highland fishes: a test of the Pleistocene vicariance hypothesis. Evolution, 51, 885–897.
    http://dx.doi.org/10.2307/2411163

    Switzer, J.F. & Wood, R.M. (2009) Etheostoma erythrozonum, a new species of darter (Teleostei: Percidae) from the Meramec River drainage, Missouri. Zootaxa, 2095, 1–7.

    Swofford, D.L. (2001) PAUP*: Phylogenetic analysis using parsimony (* and other methods) Version 4.0b10. Sinauer, Sunderland, MA.

    Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.

    Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 634–640.

    Trautman, M.B. (1981) The Fishes of Ohio. Ohio State University Press Columbus, OH, 782 pp.

    Wood, R.M., Mayden, R.L., Matson, R.H., Kuhajda, B.R. & Layman, S.R. (2002) Systematics and biogeography of the Notropis rubellus species complex (Teleostei: Cyprinidae). Bulletin of the Alabama Museum of Natural History, 22, 37–80.

    Zanatta, D.T. & Harris, A.T. (2013) Phylogeography and genetic variability of the freshwater mussels (Bivalvia: Unionidae) Ellipse, Venustaconcha ellipsiformis (Conrad 1836), and Bleeding Tooth, V. pleasii (Marsh 1891). American Malacological Bulletin, 31 (2), 267–279.
    http://dx.doi.org/10.4003/006.031.0206