, Volume 810, Issue 1, pp 207–225 | Cite as

Signature of postglacial colonization on contemporary genetic structure and diversity of Quadrula quadrula (Bivalvia: Unionidae)

  • Philip T. Mathias
  • Jordan R. Hoffman
  • Chris C. Wilson
  • David T. ZanattaEmail author


Contemporary species distributions and geographic patterns of genetic structure largely reflect pre-historic events, often with subsequent alterations from human influences. The geographic genetic structure of a relatively common and widespread unionid species, Quadrula quadrula, was investigated to reconstruct its postglacial history. Hypotheses regarding colonization routes of Q. quadrula into the Great Lakes basin after the most recent glacial retreat were tested. Samples were collected from Q. quadrula at sites spanning hypothesized glacial refugia and postglacial expansion routes in the Mississippi River drainage, including the Ohio and Missouri rivers, and the Great Lakes. Broad-scale phylogeography and population structure were assessed by sequencing a fragment of the mitochondrial CO1 gene and genotyping eight microsatellites. Results of analyses showed marked differences among the Great Lakes, Mississippi River, and Ohio River drainages, and suggested colonization of the Great Lakes basin from a Mississippian source. Populations showed patterns of isolation by distance: geographic and genetic distances were significantly correlated among Great Lakes populations based on colonization through the Chicago–Illinois outlet, but not when following the Wabash–Maumee outlet. All evidence indicates that postglacial colonization of the Great Lakes basin occurred almost exclusively through the Chicago–Illinois outlet, with subsequent expansion into the lower Great Lakes.


Great Lakes Freshwater mussels Phylogeography Mitochondrial DNA Microsatellites Conservation genetics 



This work was made possible through funding from the Endangered Species Recovery Fund of World Wildlife Fund Canada, Fisheries and Oceans Canada, Ontario Ministry of Natural Resources and Forestry (OMNRF), Central Michigan University (CMU), and the Conchologists of America, Inc. Stipend support was awarded to PTM and JRH by Central Michigan University. This article is contribution 77 of the Central Michigan University Institute for Great Lakes Research. Dr. Heather Galbraith (Trent University/United States Geological Survey—USGS), Dr. Daniel Spooner (Trent University/USGS), Caleigh Smith (OMNRF), Kristyne Wozney (OMNRF), Amy Mathias (Trent University), Anne Kidde (OMNRF), Ryan Hill (OMNRF), Brant Fisher (Indiana Department of Natural Resources), Steve McMurray (Missouri Department of Conservation; MDOC), Scott Faiman (MDOC), Jeremy Tiemann and the Illinois Natural History Survey (INHS) 2010 Stream Team, Steve Kahl (Shiawassee National Wildlife Refuge, United States Fish and Wildlife Service; USFWS), Dr. Todd Crail (University of Toledo), Dr. Daelyn Woolnough (CMU), Andy Harris (CMU), Matt Rowe (CMU), Jennifer Bergner (CMU), Daryl Kuipers (CMU), Katie Colaccino (CMU), Ben Boecher (CMU), Joe Bailey (CMU), Briana Collins (CMU), Mariah Scott (CMU), Kile Kucher (USFWS/CMU), Robert Mathias, and James Miller provided valuable assistance with both field and lab work. The Indiana Department of Natural Resources, Illinois Department of Natural Resources, Ohio Department of Natural Resources, Missouri Department of Conservation, Michigan Department of Natural Resources, United States Fish and Wildlife Service, Ontario Ministry of Natural Resources and Forestry, and Fisheries and Oceans Canada provided scientific collection permits for specimen collection.

Supplementary material

10750_2016_3076_MOESM1_ESM.docx (69 kb)
Appendix 1–3 (DOCX 70 kb)
10750_2016_3076_MOESM2_ESM.xls (84 kb)
Appendix 4 Pairwise population differentiation (F ST below diagonal and D est above diagonal) with each site represented by a rectangle separated by drainage. The Lake Michigan drainage is abbreviated as Lk MI (XLS 84 kb)
10750_2016_3076_MOESM3_ESM.jpg (599 kb)
Appendix 5 Delta-K graphs for STRUCTURE analyses with a priori (A) and without a priori (C) population assignments. Mean natural log-likelihood graphs for STRUCTURE analyses with a priori (B) and without a priori (D) population assignments (JPEG 600 kb)


  1. Astanei, I., E. Gosling, J. Wilson & E. Powell, 2005. Genetic variability and phylogeography of the invasive zebra mussel, Dreissena polymorpha (Pallas). Molecular Ecology 14: 1655–1666.CrossRefPubMedGoogle Scholar
  2. Bailey, R. M. & G. R. Smith, 1981. Origin and geography of the fish fauna of the Laurentian Great Lakes basin. Canadian Journal of Fisheries and Aquatic Sciences 38: 1539–1561.CrossRefGoogle Scholar
  3. Berg, D. J., W. R. Haag, S. I. Guttman & J. B. Sickel, 1995. Mantle biopsy: a technique for nondestructive tissue-sampling of freshwater mussels. Journal of the North American Benthological Society 14: 577–581.CrossRefGoogle Scholar
  4. Berg, D. J., E. G. Cantonwine, W. R. Hoeh & S. I. Guttman, 1998. Genetic structure of Quadrula quadrula (Bivalvia: Unionidae): little variation across large distances. Journal of Shellfish Research 17: 1365–1373.Google Scholar
  5. Berg, D. J., A. D. Christian & S. I. Guttman, 2007. Population genetic structure of three freshwater mussel (Unionidae) species within a small stream system: significant variation at local spatial scales. Freshwater Biology 52: 1427–1439.CrossRefGoogle Scholar
  6. Bernatchez, L. & C. C. Wilson, 1998. Comparative phylogeography of Nearctic and Palearctic fishes. Molecular Ecology 7: 431–452.CrossRefGoogle Scholar
  7. Bierne, N., S. Launey, Y. Naciri-Graven & F. Bonhomme, 1998. Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics 148: 1893–1906.PubMedPubMedCentralGoogle Scholar
  8. Bogan, A. E. & K. J. Roe, 2008. Freshwater bivalve (Unioniformes) diversity, systematics, and evolution: status and future directions. Journal of the North American Benthological Society 27: 349–369.CrossRefGoogle Scholar
  9. Brookfield, J. F. Y., 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5: 453–455.CrossRefPubMedGoogle Scholar
  10. Campbell, D. C., J. M. Serb, J. E. Buhay, K. J. Roe, R. L. Minton & C. Lydeard, 2005. Phylogeny of North American amblemines (Bivalvia, Unionoida): prodigious polyphyly proves pervasive across genera. Invertebrate Biology 124: 131–164.CrossRefGoogle Scholar
  11. Chapuis, M. P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621–631.CrossRefPubMedGoogle Scholar
  12. Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.CrossRefPubMedGoogle Scholar
  13. COSEWIC, 2006. COSEWIC assessment and status report on the Mapleleaf Mussel, Quadrula quadrula (Saskatchewan-Nelson population and Great Lakes-Western St. Lawrence population) in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa.Google Scholar
  14. Daugherty, D. J. & T. M. Sutton, 2005. Seasonal movement patterns, habitat use, and home range of flathead catfish in the lower St. Joseph River, Michigan. North American Journal of Fisheries Management 25: 256–269.CrossRefGoogle Scholar
  15. Dyke, A., 2004. An outline of North American deglaciation with emphasis on central and northern Canada. In Ehlers, J. & Gibbard P. L. (eds), Quarternary glaciations-extent and chronology, Part II, vol 2b. Elsevier, Amsterdam: 373–424.Google Scholar
  16. Earl, D. A. & B. M. von Holdt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.CrossRefGoogle Scholar
  17. Elderkin, C. L., A. D. Christian, C. C. Vaughn, J. L. Metcalfe-Smith & D. J. Berg, 2007. Population genetics of the freshwater mussel, Amblema plicata (Say 1817) (Bivalvia: Unionidae): evidence of high dispersal and post-glacial colonization. Conservation Genetics 8: 355–372.CrossRefGoogle Scholar
  18. Elderkin, C. L., A. D. Christian, J. L. Metcalfe-Smith & D. J. Berg, 2008. Population genetics and phylogeography of freshwater mussels in North America, Ellipto dilatata and Actinonaias ligamentina (Bivalvia: Unionidae). Molecular Ecology 17: 2149–2163.CrossRefPubMedGoogle Scholar
  19. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefPubMedGoogle Scholar
  20. Excoffier, L. & H. E. L. Lischer, 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.CrossRefPubMedGoogle Scholar
  21. Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.PubMedPubMedCentralGoogle Scholar
  22. Ferguson, C. D., M. J. Blum, M. L. Raymerm, M. S. Eackles & D. E. Krane, 2013. Population structure, multiple paternity, and long-distance transport of spermatozoa in freshwater mussel Lampsilis cardium (Bivalvia: Unionidae). Freshwater Science 32: 267–282.CrossRefGoogle Scholar
  23. Fetzner, W. J. & K. A. Crandall, 2003. Linear habits and the nested clade analysis: an empirical evaluation of geographic versus river distances using an Ozark crayfish (Decapoda: Cambaridae). Evolution 57: 2101–2118.CrossRefPubMedGoogle Scholar
  24. FMCS (Freshwater Mollusk Conservation Society), 2016. A national strategy for the conservation of native freshwater mollusks. Freshwater Mollusk Biology and Conservation 19: 1–21.Google Scholar
  25. Froufe, E., C. Sobral, A. Teixeira, R. Sousa, S. Varandas, D. C. Aldridge & M. Lopes-Lima, 2014. Genetic diversity of the pan-European freshwater mussel Anodonta anatina (Bivalvia: Unionoida) based on CO1: new phylogenetic insights and implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems 24: 561–574.CrossRefGoogle Scholar
  26. Galbraith, H. S., D. T. Zanatta & C. C. Wilson, 2015. Comparative analysis of riverscape genetic structure in rare, threatened and common freshwater mussels. Conservation Genetics 16: 845–857.CrossRefGoogle Scholar
  27. Garner, J. T. & S. W. McGregor, 2001. Current status of freshwater mussels (Unionidae, Margaritiferidae) in the muscle shoals area of Tennessee River in Alabama (Muscle Shoals revisited again). American Malacological Bulletin 16: 155–170.Google Scholar
  28. Geist, J. & R. Kuehn, 2005. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Molecular Ecology 14: 425–439.CrossRefPubMedGoogle Scholar
  29. Grabarkiewicz, J. & T. D. Crail, 2006. Freshwater Mussels of the Maumee Drainage, 2nd edn. Special Publication Funded by the USEPA, USFWS, OEEF, and OEPA, Toledo, OH.Google Scholar
  30. Graf, D. L., 2002. Historical biogeography and late glacial origin of the freshwater pearly mussel (Bivalvia: Unionidae) faunas of Lake Erie, North America, Vol. 6. Occasional Papers on Mollusks, The Department of Mollusks, Museum of Comparative Zoology, Harvard University, Cambridge, MA: 175–211.Google Scholar
  31. Griekspoor, A. & T. Groothuis, 2006. 4PEAKS.
  32. Haag, W. R., 2012. North American Freshwater Mussels: Natural History, Ecology, and Conservation. Cambridge University Press, New York.CrossRefGoogle Scholar
  33. Hedrick, P. W., 2005. Genetics of Populations, 3rd ed. Jones and Bartlett Publishers, Boston, MA.Google Scholar
  34. Hemmingsen, A. H., K. J. Roe & J. M. Serb, 2009. Isolation and characterization of nine microsatellite markers for the endangered winged-mapleleaf mussel, Quadrula fragosa (Bivalvia, Unionidae). Molecular Ecology Resources 9: 1460–1466.CrossRefPubMedGoogle Scholar
  35. Herdendorf, C. E., 2013. Research overview: Holocene development of Lake Erie. Ohio Journal of Science 112: 24–36.Google Scholar
  36. Hewitt, T. L., J. L. Bergner, D. A. Woolnough & D. T. Zanatta, 2016. Phylogeography of the freshwater mussel species Lasmigona costata: testing postglacial colonization hypotheses. Hydrobiologia. doi: 10.1007/s10750-016-2834-3.Google Scholar
  37. Hoftyzer, E., J. D. Ackerman, T. J. Morris & G. L. Mackie, 2008. Genetic and environmental implications of reintroducing laboratory-raised unionid mussels to the wild. Canadian Journal of Fisheries and Aquatic Sciences 65: 1217–1229.CrossRefGoogle Scholar
  38. Hubley, R. C., 1963. Movement of tagged channel catfish in the upper Mississippi River. Transactions of American Fisheries Society 92: 165–168.CrossRefGoogle Scholar
  39. Inoue, K., E. M. Monroe, C. L. Elderkin & D. J. Berg, 2013. Phylogeographic and population genetic analyses reveal Pleistocene isolation followed by high gene flow in a wide ranging, but endangered, freshwater mussel. Heredity 112: 282–290.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Jones, J. W., E. M. Hallerman & R. J. Neves, 2006a. Genetic management guidelines for captive propagation of freshwater mussels (Unionoidea). Journal of Shellfish Research 25: 527–535.CrossRefGoogle Scholar
  41. Jones, J. W., R. J. Neves, S. A. Ahlstedt & E. M. Hallerman, 2006b. A holistic approach to taxonomic evaluation of two closely related endangered freshwater mussel species, the oyster mussel, Epioblasma capsaeformis and tan riffleshell, Epioblasma florentina walkeri (Bivalvia:Unionidae). Journal of Molluscan Studies 72: 267–283.CrossRefGoogle Scholar
  42. Jost, L., 2008. Gst and its relatives do not measure differentiation. Molecular Ecology 17: 4015–4026.CrossRefPubMedGoogle Scholar
  43. Kelly, M. W. & J. M. Rhymer, 2005. Population genetic structure of a rare unionid (Lampsilis cariosa) in a recently glaciated landscape. Conservation Genetics 6: 789–802.CrossRefGoogle Scholar
  44. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson & D. G. Higgins, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.CrossRefPubMedGoogle Scholar
  45. Larson, G. & R. Schaetzl, 2001. Origin and evolution of the Great Lakes. Journal of Great Lakes Research 27: 518–546.CrossRefGoogle Scholar
  46. Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan, P. Bouchet, S. A. Clark, K. S. Cummings, T. J. Frest, O. Gargonminy, D. G. Herbert, R. Hershler, K. E. Perez, B. Roth, M. Seddon, E. E. Strong & F. G. Thompson, 2004. The global decline of nonmarine mollusks. BioScience 54: 321–330.CrossRefGoogle Scholar
  47. Maddison, W. P. & D. R. Maddison, 2008. MESQUITE: A Modular System for Evolutionary Analysis, Version 3.0.
  48. Mandrak, N. E. & E. J. Crossman, 1992. Postglacial dispersal of freshwater fishes into Ontario. Canadian Journal of Zoology 70: 2247–2259.CrossRefGoogle Scholar
  49. Mantel, N., 1967. The detection of disease clustering a generalized regression approach. Cancer Research 27: 209–220.PubMedGoogle Scholar
  50. Masatoshi Nei (1972) Genetic distance between populations. The American Naturalist 106 (949): 283–292CrossRefGoogle Scholar
  51. McGoldrick, D. J., D. Hedgecock, L. J. English, P. Baoprasertkul & R. D. Ward, 2000. The transmission of microsatellite alleles in Australian and North American stocks of the Pacific oyster (Crassostrea gigas): selection and null alleles. Journal of Shellfish Research 19: 779–788.Google Scholar
  52. Metcalfe-Smith, J., A. MacKenzie, I. Carmichael & D. McGoldrick, 2005. Photo Field Guide to the Freshwater Mussels of Ontario. St. Thomas Field Naturalist Club Inc, St. Thomas, ON, Canada.Google Scholar
  53. Moritz, C., 1994. Defining ‘Evolutionarily Significant Units’ for conservation. Trends in Ecology & Evolution 9: 373–375.CrossRefGoogle Scholar
  54. Nagel, K. O., G. Badino & B. Alessandria, 1996. Population genetics of European Anodontinae (Bivalvia: Unionidae). Journal of Molluscan Studies 62: 343–357.CrossRefGoogle Scholar
  55. Oesch, R. D., 1995. Missouri Naiades, A Guide to the Mussels of Missouri. Missouri Department of Conservation, Jefferson City, MO.Google Scholar
  56. Paterson, W. L., T. A. Griffith, R. A. Krebs, L. E. Burlakova & D. T. Zanatta, 2015. An evaluation of the genetic structure of Mapleleaf mussels (Quadrula quadrula) in the Lake Erie watershed. Journal of Great Lakes Research 41: 1123–1130.CrossRefGoogle Scholar
  57. Peakall, R. & P. E. Smouse, 2006. GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.CrossRefGoogle Scholar
  58. Pemberton, J. M., J. Slate, D. R. Bancroft & J. A. Barrett, 1995. Nonamplifying alleles at microsatellite loci: a caution for parentage and population studies. Molecular Ecology 4: 249–252.CrossRefPubMedGoogle Scholar
  59. Posada, D., 2004. Collapse: Describing haplotypes from sequence alignments. Available at, accessed December, 2015.
  60. Pritchard, J. K., 2010. Documentation for Structure Software: Version 2.3., accessed December, 2015.
  61. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  62. Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.CrossRefGoogle Scholar
  63. Rice, W. R., 1989. Analyzing of statistical tests. Evolution 43: 223–225.CrossRefPubMedGoogle Scholar
  64. Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.PubMedGoogle Scholar
  65. Sambrook, J., E. F. Fritsch & T. Maniatas, 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  66. Scott, W. B. & E. J. Crossman, 1973. Freshwater Fishes of Canada. Fisheries Research Board of Canada. The Bryant Press Limited, Ottawa.Google Scholar
  67. Shrader, T. M., B. Moody & M. Buckman, 2003. Population dynamics of channel catfish in Brownlee Reservoir and the Snake River, Oregon. North American Journal of Fisheries Management 23: 822–834.CrossRefGoogle Scholar
  68. Soltis, D. E., A. B. Morris, J. S. McLachlan, P. S. Manos & P. S. Soltis, 2006. Comparative phylogeography of unglaciated eastern North America. Molecular Ecology 15: 4261–4293.CrossRefPubMedGoogle Scholar
  69. Takezaki, N., M. Nei & K. Tamura, 2010. POPTREE2: software for constructing population trees from allele frequency data and computing other population statistics with Windows interface. Molecular Biology and Evolution 27: 747–752.CrossRefPubMedGoogle Scholar
  70. van der Schalie, H., 1945. The value of mussel distribution in tracing stream confluence. Papers of the Michigan Academy of Science, Arts, and Letters 30: 355–372.Google Scholar
  71. van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley, 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  72. Vaughn, C. C. & D. E. Spooner, 2006. Unionid mussels influence macroinvertebrate assemblage structure in streams. Journal of the North American Benthological Society 25: 691–700.CrossRefGoogle Scholar
  73. Vokoun, J. C. & C. E. Rabeni, 2005. Home range and space use patterns of flathead catfish during the summer-fall period in two Missouri streams. Transactions of the American Fisheries Society 134: 509–517.CrossRefGoogle Scholar
  74. Watters, G. T., 1992. Unionids, fishes, and the species-area curve. Journal of Biogeography 19: 481–490.CrossRefGoogle Scholar
  75. Watters, G. T., M. A. Hoggarth & D. H. Stansbery, 2009. The Freshwater Mussels of Ohio. The Ohio State University Press, Columbus, OH.Google Scholar
  76. WDNR (Wisconsin Department of Natural Resources), 2003. Freshwater Mussels of the Upper Mississippi River. Wisconsin Department of Natural Resources, Madison, WI.Google Scholar
  77. Williams, J. D., M. L. Warren, K. S. Cummings, J. L. Harris & R. J. Neves, 1993. Conservation status of freshwater mussels of the United States and Canada. Fisheries 18: 6–22.CrossRefGoogle Scholar
  78. Williams, J. D., A. E. Bogan & J. T. Garner, 2008. Freshwater Mussels of Alabama and the Mobile Basin in Georgia, Mississippi, and Tennessee. University of Alabama Press, Tuscaloosa, AL.Google Scholar
  79. Willson, W. E., 1966. Indiana, A History. Indiana University Press, Bloomington, IN.Google Scholar
  80. Zanatta, D. T. & A. T. Harris, 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: 267–279.CrossRefGoogle Scholar
  81. Zanatta, D. T. & R. W. Murphy, 2007. Range-wide population genetic analysis of the endangered northern riffleshell mussel, Epioblasma torulosa rangiana (Bivalvia: Unionoida). Conservation Genetics 8: 1393–1404.CrossRefGoogle Scholar
  82. Zanatta, D. T. & R. W. Murphy, 2008. The phylogeographic and management implications of genetic population structure in the imperiled snuffbox mussel, Epioblasma triquetra (Bivalvia: Unionidae). Biological Journal of the Linnaean Society 93: 371–384.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Philip T. Mathias
    • 1
  • Jordan R. Hoffman
    • 1
  • Chris C. Wilson
    • 2
  • David T. Zanatta
    • 1
    Email author
  1. 1.Institute for Great Lakes Research, Biology DepartmentCentral Michigan UniversityMount PleasantUSA
  2. 2.Aquatic Research and Monitoring Section, Ontario Ministry of Natural Resources and ForestryTrent UniversityPeterboroughCanada

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