Population structure and mantle display polymorphisms in the wavy-rayed lampmussel, Lampsilis fasciola (Bivalvia: Unionidae)

Canadian Journal of Zoology

Volumn 85, Issue 11, 2007, Pages 1169-1181

  Zanatta, David T ^a,c   Fraley, Stephen J ^b   Murphy, Robert W ^a  

^a DEPARTMENT OF NATURAL HISTORY   (Canada)

^b North Carolina Wildlife Resources Commission   (United States)

^c TRENT UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DRAINAGE; FISH; LAKES;

GENE FLOW; LAMPSILIS FASCIOLA;

POLYMORPHISM;

BIVALVE; CONSERVATION GENETICS; ENDANGERED SPECIES; GENE FLOW; GENETIC ANALYSIS; GENETIC STRUCTURE; GENETIC VARIATION; GENOTYPE; MOLECULAR ANALYSIS; MORPHOLOGY; POLYMORPHISM; POPULATION STRUCTURE; REINTRODUCTION; SPECIES CONSERVATION;

GREAT LAKES [NORTH AMERICA]; LAKE ONTARIO; LITTLE TENNESSEE RIVER; NORTH AMERICA; NORTH CAROLINA; UNITED STATES;

BIVALVIA; FASCIOLA; LAMPSILIS FASCIOLA; UNIONIDAE;

EID: 39649089876     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/Z07-089     Document Type: Article

References (75)

1. Avilés, J.M., and Møller, A.P. 2004. How is host egg mimicry maintained in the cuckoo (Cunculus canorus)? Biol. J. Linn. Soc. 82: 57-68. doi:10.1111/j.1095-8312.2004.00311.x.
2. Avise, J.C., Power, A.J., and Walker, D. 2004. Genetic sex determination, gender identification and pseudohermaphroditism in the knobbed welk, Busycon carica (Mollusca: Melongenidae). Proc. R. Soc. Lond. B Biol. Sci. 271: 641-646. doi:10.1098/rspb.2003.2533.
3. Berg, D.J., Haag, W.R., Guttman, S.I., and Sickel, J.B. 1995. Mantle biopsy: a technique for nondestructive tissue-sampling of freshwater mussels. J. North Am. Benthol. Soc. 14: 577-581. doi:10.2307/1467542.
4. Brookfield, J.F.Y. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5: 453-455. doi:10.1046/j.1365-294X.1996.00098.x.
5. Calkin, P.E., and Feenstra, B.H. 1985. Evolution of the Erie-Basin Great Lakes. In Quartenary evolution of the Great Lakes. Edited by P.F. Karrow and P.E. Calkin. Geological Association of Canada, Ottawa, Ont. Spec. Pap. 30. pp. 149-170.
6. Cornuet, J.M., and Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144: 2001-2014.
7. Cornuet, J.M., Piry, S., Luikart, G., Estoup, A., and Solignac, M. 1999. New methods employing multilocus genotypes to select or exclude populations as origins of individuals.. Genetics, 153: 1989-2000.
8. COSEWIC. 2005. Guidelines for recognizing designatable units below the species level. Available from www.cosewic.gc.ca/eng/sct2/sct2_5_e.cfm [accessed 9 May 2007].
9. COSEWIC. 2006. Canadian species at risk. Committee on the Status of Endangered Wildlife in Canada, Ottawa, Ont., Canada.
10. Dakin, E.E., and Avise, J.C. 2004. Microsatellite null alleles in parentage analysis. Heredity, 93: 504-509. doi:10.1038/sj.hdy.6800545.
11. Dodd, B.J., Barnhart, M.C., Rogers-Lowery, C.L., Fobian, T.B., and Dimock, R.V. 2005. Cross-resistance of largemouth bass to glochidia of unionid mussels. J. Parasitol. 91: 1064-1072. doi:10.1645/GE-511R.1.
12. Dodd, B.J., Barnhart, M.C., Rogers-Lowery, C.L., Fobian, T.B., and Dimock, R.V. 2006. Persistence of host response against glochidia larvae in Micropterus salmoides. Fish Shellfish Immunol. 21: 473-484. doi:10.1016/j.fsi.2006.02.002.
13. Eackles, M.S., and King, T.L. 2002. Isolation and characterization of microsatellite loci in Lampsilis abrupta (Bivalvia: Unionidae) and cross-species amplification within the genus. Mol. Ecol. Notes, 2: 559-562. doi:10.1046/j.1471-8286.2002.00323.x.
14. Environmental Systems Research Institute. 2001. ArcView 3.2a. ESRI, Inc., Redlands, Calif.
15. Excoffier, L., Smouse, P.E., and Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics, 131: 479-491.
16. Fanelli, D., Henshaw, M., Cervo, R., Turillazzi, S., Queller, D.C., and Strassmann, J.E. 2005. The social parasite wasp Polistes atrimandibularis does not form host races. J. Evol. Biol. 18: 1362-1367. doi:10.1111/j.1420-9101.2005.00927.x.
17. Geist, J., and Kuehn, R. 2005. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Mol. Ecol. 14: 425-439. doi:10.1111/j.1365-294X.2004.02420.x.
18. Geist, J., Rottmann, O., Schroder, W., and Kuhn, R. 2003. Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea). Mol. Ecol. Notes, 3: 444-446. doi:10.1046/j.1471-8286.2003.00476.x.
19. Gibbs, H.L., Sorenson, M.D., Marchetti, K., Brooke, M.de L., Davies, N.B., and Nakamura, H. 2000. Genetic evidence for female host-specific races of the common cuckoo. Nature (London), 407: 183-186. doi:10.1038/35025058.
20. Goudet, J. 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. J. Hered. 86: 485-486.
21. Graf, D.L. 1997. Sympatric speciation of freshwater mussels (Bivalvia: Unionoidea): a model. Am. Malacol. Bull. 14: 35-40.
22. Graf, D.L. 2002. Historical biogeography and late glacial origin of the freshwater pearly mussel (Bivalvia: Unionidae) faunas of Lake Erie, North America. Occasional Papers on Mollusks, The Department of Mollusks, Museum of Comparative Zoology, Harvard University, Cambridge, Mass. 6: 175-211.
23. Green, D.M. 2005. Designatable units for status assessment of endangered species. Conserv. Biol. 19: 1813-1820. doi:10.1111/j.1523-1739.2005. 00284.x.
24. Haag, W.R., and Warren, M.L. 1999. Mantle displays of freshwater mussels elicit attacks from fish. Freshw. Biol. 42: 35-40. doi:10.1046/j.1365- 2427.1999.00454.x.
25. Haag, W.R., Butler, R.S., and Hartfield, P.D. 1995. An extraordinary reproductive strategy in freshwater bivalves: prey mimicry to facilitate larval dispersal. Freshw. Biol. 34: 471-476. doi:10.1111/j.1365-2427.1995. tb00904.x.
26. Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K., and Zimmer, E.A. 1996. Nucleic acids. IV. Sequencing and cloning. In Molecular systematics. 2nd ed. Edited by D.M. Hillis, C. Moritz, and B.K. Mable. Sinauer Associates, Inc., Sunderland, Mass. pp. 321-381.
27. Hoeh, W.R., Stewart, D.T., and Guttman, S.I. 2002. High fidelity of mitochondrial genome transmission under the doubly uniparental mode of inheritance in freshwater mussels (Bivalvia: Unionoidea). Evolution, 56: 2252-2261.
28. Johnson, R.L., Liang, F.Q., Milam, C.D., and Farris, J.L. 1998. Genetic diversity and cellulolytic activity among several species on unionid bivalves in Arkansas. J. Shellfish Res. 17: 1375-1382.
29. Jones, J.W., Culver, M., David, V., Struthers, J., Johnson, N.A., Neves, R.J., O'Brien, S.J., and Hallerman, E.M. 2004. Development and characterization of microsatellite loci in the endangered oyster mussel Epioblasma capsaeformis (Bivalvia: Unionidae). Mol. Ecol. Notes, 4: 649-652. doi:10.1111/j.1471-8286.2004.00762.x.
30. Jones, J.W., Neves, R.J., Ahlstedt, S.A., and Hallerman, E.M. 2006. 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). J. Molluscan Stud. 72: 267-283. doi:10.1093/mollus/eyl004.
31. Kelly, M.W., and Rhymer, J.M. 2005. Population genetic structure of a rare unionid (Lampsilis cariosa) in a recently glaciated landscape. Conserv. Genet. 6: 789-802. doi:10.1007/s10592-005-9037-1.
32. Kraemer, L.R. 1970. The mantle flap in three species of Lampsilis (Pelecypoda: Unionidae). Malacologia, 10: 225-282.
33. Kumar, S., Tamura, K., and Nei, M. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5: 150-163. doi:10.1093/bib/5.2.150.
34. Luikart, G., and Cornuet, J.-M. 1998. Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv. Biol. 12: 228-237. doi:10.1046/j.1523-1739.1998.96388.x.
35. Maynard Smith, J. 1966. Sympatric speciation. Am. Nat. 100: 637-650. doi:10.1086/282457.
36. McGoldrick, D.J., Hedgecock, D., English, L.J., Baoprasertkul, P., and Ward, R.D. 2000. The transmission of microsatellite alleles in Australian and North American stocks of the Pacific oyster (Crassostrea gigas): selection and null alleles. J. Shellfish Res. 19: 779-788.
37. McNichols, K.A., and Mackie, G.L. 2002. Fish host determination of endangered freshwater mussels in the Sydenham River, Ontario, Canada. Final report for a study funded by Endangered Species Recovery Fund in 2002.
38. McNichols, K.A., and Mackie, G.L. 2003. Fish host determination of endangered freshwater mussels in the Sydenham River, Ontario, Canada. Final report for a study funded by Endangered Species Recovery Fund in 2003.
39. McNichols, K.A., Mackie, G.L., and Ackerman, J.D. 2004. Fish host determination of endangered freshwater mussels in the Sydenham River, Ontario, Canada. Final report for a study funded by Endangered Species Recovery Fund in 2004.
40. Metcalfe-Smith, J.L., Staton, S.K., and West, E.L. 2000a. Status of the wavy-rayed lampmussel, Lampsilis fasciola (Bivalvia: Unionidae), in Ontario and Canada. Can. Field-Nat. 114: 457-470.
41. Metcalfe-Smith, J.L., Mackie, G.L., Di Maio, J., and Staton, S.K. 2000b. Changes over time in the diversity and distribution of freshwater mussels (Unionidae) in the Grand River, southwestern Ontario. J. Great Lakes Res. 26: 445-459.
42. Moritz, C. 1994. Defining 'Evolutionary Significant Units' for conservation. Trends Ecol. Evol. 9: 373-375. doi:10.1016/0169-5347(94) 90057-4.
43. Morris, T.J. 2006. National recovery strategy for the wavyrayed lampmussel (Lampsilis fasciola, Rafinesque 1820) in Canada. Species at Risk Act Recovery Strategy Series, Fisheries and Oceans Canada, Ottawa, Ont.
44. Nagel, K.-O., Badino, G., and Alessandria, B. 1996. Population genetics of European Anodontinae (Bivalvia: Unionidae). J. Molluscan Stud. 62: 343-357. doi:10.1093/mollus/62.3.343.
45. National Native Mussel Conservation Committee. 1998. National strategy for the conservation of native freshwater mussels. J. Shellfish Res. 17: 1419-1428.
46. Nei, M. 1972. Genetic distance between populations. Am. Nat. 106: 283-292. doi:10.1086/282771.
47. Nei, M., Tajima, F., and Tateno, Y. 1983. Accuracy of genetic distances and phylogenetic trees from molecular data. J. Mol. Evol. 19: 153-170. doi:10.1007/BF02300753.
48. Ota, T. 1993. DISPAN: genetic distance and phylogenetic analyses software. Pennsylvania State University, University Park, Penn.
49. Paetkau, D., Calvert, W., Stirling, I., and Strobeck, C. 1995. Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4: 347-354.
50. Petit, R.J., El-Mousadik, A., and Pons, O. 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12: 844-855. doi:10.1046/j.1523-1739.1998.96489.x.
51. Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L., and Estoup, A. 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95: 536-539. doi:10.1093/jhered/esh074.
52. Rannala, B., and Mountain, J.L. 1997. Detecting immigration by using multilocus genotypes. Proc. Natl. Acad. Sci. U.S.A. 94: 9197-9201. doi:10.1073/pnas.94.17.9197.
53. Raymond, M., and Rousset, F. 1995. GENEPOP. Version 1.2. Population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249.
54. Raymond, M., Vaanto, R.L., Thomas, F., Rousset, F., De Meuss, T., and Renaud, F. 1997. Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Mar. Ecol. Prog. Ser. 156: 225-237. doi:10.3354/meps156225.
55. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution, 43: 223-225. doi:10.2307/2409177.
56. Schloesser, D.W., and Nalepa, T.F. 1994. Dramatic decline of unionid bivalves in offshore waters of western Lake Erie after infestation by the zebra mussel, Dreissena polymorpha. Can. J. Fish. Aquat. Sci. 51: 2234-2242.
57. Schloesser, D.W., Metcalfe-Smith, J.L., Kovalak, W.P., Longton, G.D., and Smithee, R.D. 2006. Extirpation of freshwater mussels (Bivalvia: Unionidae) following the invasion of Dreissenid mussels in an interconnecting river of the Laurentian Great Lakes. Am. Midl. Nat. 155: 307-320. doi:10.1674/0003- 0031(2006)155[307:EOFMBU]2.0.CO;2.
58. Schneider, S., Roessli, D., and Excoffier, L. 2000. Arlequin. Version 2.000. A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland.
59. Schuelke, M. 2000. An economic method for the fluorescent labeling of PCR fragments. Nat. Biotechnol. 18: 233-234. doi:10.1038/72708.
60. Serb, J.M. 2006. Discovery of genetically distinct sympatric lineages in the freshwater mussel Cyprogenia aberti (Bivalvia: Unionidae). J. Molluscan Stud. 72: 425-434. doi:10.1093/mollus/eyl021.
61. Serb, J.M., and Barnhart, M.C. 2007. Congruence and conflict between molecular and reproductive characters when assessing biological diversity in the western fanshell Cyprogenia aberti (Bivalvia: Unionidae). Ann. Mo. Bot. Gard., In press.
62. Shaw, K.M., King, T.L., Lellis, W.A., and Eackles, M.S. 2006. Isolation and characterization of microsatellite loci in Alasmidonta heterodon (Bivalvia: Unionidae). Mol. Ecol. Notes, 6: 365-367. doi:10.1111/j.1471- 8286.2005.01235.x.
63. VanArnum, C.J., Buynak, G.L., and Ross, J.R. 2004. Movement of smallmouth bass in Elkhorn Creek, Kentucky. N. Am. J. Fish. Manage. 24: 311-315. doi:10.1577/M02-107.
64. Van Oosterhout, C., Hutchinson, W.F., Willis, D.P.M., and Shipley, P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes, 4: 535-538. doi:10.1111/j.1471-8286.2004.00684.x.
65. Van Valen, L. 1973. A new evolutionary law. Evol. Theory, 1: 1-30.
66. Villella, R.F., King, T.L., and Starliper, C.E. 1998. Ecological and evolutionary concerns in freshwater bivalve relocation programs. J. Shellfish Res. 17: 1407-1413.
67. Watters, G.T., and O'Dee, S.H. 1996. Shedding of untransformed glochidia by fishes parasitized by Lampsilis fasciola Rafinesque, 1820 (Mollusca: Bivalvia: Unionidae): evidence of acquired immunity in the field? J. Freshwat. Ecol. 11: 383-388.
68. Weir, B.S., and Cockerham, C.C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38: 1358-1370. doi:10.2307/2408641.
69. Zale, A.V., and Neves, R.J. 1982. Fish hosts of four species of lampsiline mussels (Mollusca: Unionidae) in Big Moccasin Creek, Virginia. Can. J. Zool. 60: 2535-2542.
70. Zanatta, D.T., and Murphy, R.W. 2006a. Development and characterization of microsatellite markers for the endangered northern riffleshell mussel Epioblasma torulosa rangiana (Bivalvia: Unionidae). Mol. Ecol. Notes, 6: 850-852. doi:10.1111/j.1471-8286.2006.01367.x.
71. Zanatta, D.T., and Murphy, R.W. 2006b. The evolution of active host-attraction strategies in the freshwater mussel tribe Lampsilini (Bivalvia: Unionidae). Mol. Phylogenet. Evol. 41: 195-208. doi:10.1016/j.ympev.2006. 05.030.
72. Zanatta, D.T., and Murphy, R.W. 2007a. Range-wide population genetic analysis of the endangered northern riffleshell mussel, Epioblasma torulosa rangiana (Bivalvia: Unionoida). Conserv. Genet. 8: 1393-1404. doi:10.1007/s10592-007-9290-6.
73. Zanatta, D.T., and Murphy, R.W. 2007b. The phylogeographic and management implications of genetic population structure in the imperiled snuffbox mussel, Epioblasma triquetra (Bivalvia: Unionidae). Biol. J. Linn. Soc. In press.
74. Zanatta, D.T., Mackie, G.L., Metcalfe-Smith, J.L., and Woolnough, D.A. 2002. A refuge for native freshwater mussels (Bivalvia: Unionidae) from impacts of the exotic zebra mussel (Dreissena polymorpha) in Lake St. Clair. J. Gt. Lakes Res. 28: 479-489.
75. Zouros, E., and Foltz, D.W. 1984. Possible explanations of heterozygote deficiency in bivalve mollusks. Malacologia, 25: 583-591.