Abstract
A threatened but under-studied component offreshwater biodiversity in North America is thenative freshwater mussels (Bivalvia:Unionoidea: Margaritiferidae and Unionidae). Genetic data suggest that these mussel speciesgenerally exhibit levels of variability similarto other invertebrates. We surveyed allozymevariation in the Louisiana Pearlshell, Margaritifera hembeli (Margaritiferidae), athreatened freshwater mussel. Five examinedpopulations are monomorphic for 25 allozymeloci, the first report of a native freshwatermussel species with extensive allozymemonomorphism. Low genetic diversity appears tobe characteristic of margaritiferids, as anANOVA indicated that mussels of the familyMargaritiferidae have significantly lowerlevels of heterozygosity than the mussels ofthe family Unionidae. Margaritiferids havestrong habitat preferences and modification ofhabitat leads to rapid loss of populations.Although bottlenecks are known to cause lowgenetic variability, margaritiferids mayexhibit meta-population structure withextinction/re-colonization dynamics leading tolow genetic variability. Margaritiferidsgenerally exhibit a patchy distribution with acolonization rate that is approximately twicethat of extinction. Tests of themetapopulation hypothesis will requireadditional allozyme population genetic data aswell as hypervariable microsatellite loci.
Similar content being viewed by others
References
Abell R (2002) Conservation biology for the biodiversity crisis: a freshwater follow-up. Conserv. Biol., 16, 1435–1437.
Araujo R, Ramos M-A (2000) Status and conservation of the giant European freshwater pearl mussel (Margaritifera auricularia) (Splengler, 1793) (Bivalvia: Unionoidea). Biol. Conserv., 96, 233–239.
Avise JC (1996) Introduction: the scope of conservation genetics. In: Conservation Genetics: Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 1–9. Chapman & Hall, New York.
Badino G, Celebrano G, Nagel K-O (1991) Unio elongatulus and Unio pictorum (Bivalvia: Unionidae): molecular genetics and relationships of Italian and Central European populations. Boll. Mus. reg. Sci. nat. Torino, 9, 261–274.
Bauer G (1987) Reproductive strategy of the freshwater Pearl mussel Margaritifera margaritifera. J. Anim. Ecol., 56, 691–704.
Bauer G (1992) Variation in life span and size of the freshwater Pearl Mussel. J. Anim. Ecol., 61, 425–436.
Berg DJ, Cantonwine EG, Hoeh WR, Guttman SI (1998) Genetic structure of Quadrula quadrula (Bivalvia: Unionidae): little variation across large distances. J. Shellfish Res., 17, 1365–1373.
Berg DJ, Haag WR, Guttman SI, Sickel JB (1995) Mantle biopsy: a technique for nondestructive tissue sampling of freshwater mussels. J. N. Am. Benthol. Soc., 14, 577–581.
Bijlsma R, Bundgaard J, van Putten WF (1999) Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. J. Evol. Biol., 12, 1125–1137.
Bolden SR, Brown KM (2002) Role of stream, habitat, and density in predicting translocation success in the threatened Louisiana pearlshell, Margaritifera hembeli (Conrad). J. N. Am. Benthol. Soc., 21, 89–96.
Bonnell ML, Selander RK (1974) Elephant seals: genetic variation and near extinction. Science, 184, 908–909.
Chesney HCG, Oliver PG, Davis GM (1993) Margaritifera durrovensis Phillips, 1928: taxonomic status, ecology and conservation. J. Conch., 34, 267–299.
Clark JA, May RM (2002) Taxonomic bias in conservation research. Science, 297, 191–192.
Coker RE, Shira AF, Clark W, Howard AD (1921) Natural history and propagation of fresh-water mussels. U.S. Bureau of Fisheries Bulletin, 37, 77–181.
Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity, 83, 260–270.
Davis GM (1984) Genetic relationships among some North American Unionidae (Bivalvia): sibling species, convergence, and cladistic relationships. Malacologia, 25, 629–648.
Davis GM, Fuller SLH (1981) Genetic relationships among recent Unionacea (Bivalvia) of North America. Malacologia, 20, 217–253.
Davis GM, Heard WH, Fuller SLH, Hesterman C (1981) Molecular genetics and speciation in Elliptio and its relationships to other taxa of North American Unionidae (Bivalvia). Biol. J. Linnean Soc., 15, 131–150.
DeRose MA, Roff DA (1999) A comparison of inbreeding depression in life history and morphological traits in animals. Evolution, 53, 1288–1292.
Haag C, Hottinger JW, Riek M, Ebert D (2002) Strong inbreeding depression in a Daphnia metapopulation. Evolution, 56, 518–526.
Haag WR, Warren MJ (1998) Role of ecological factors and reproductive strategies in structuring freshwater mussel communities. Can. J. Fish. Aquat. Sci., 55, 297–306.
Hansson B, Westerberg L (2002) On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol., 11, 2467–2474.
Hansten C, Pekkarinen M, Valovirta I (1997) Effect of transplantation on the gonad development of the freshwater pearl mussel, Margaritifera margaritifera (L.). Boreal Environment Research, 2, 247–256.
Hastie LC, Boon PJ, Young MR, Way S (2001) The effects of a major flood on an endangered freshwater mussel population. Biol. Conserv., 98, 107–115.
Hastie LC, Young MR, Boon PJ, Cosgrove PJ, Henninger B (2000) Sizes, densities and age structures of Scottish Margaritifer margaritifera (L.) populations. Aquatic Conserv.: Mar. Freshw. Ecosyst., 10, 229–247.
Heard WH (1970) Hermaphroditism in Margaritifera falcata (Gould) (Pelecypoda: Margaritiferidae). Nautilus, 83, 113–114.
Hedrick P, Kalinowski ST (2000) Inbreeding depression in conservation biology. Ann. Rev. Ecol. Syst., 31, 139–162.
Hedrick PW (1996) Bottleneck(s) or metapopulation in cheetahs. Conserv. Biol., 10, 897–899.
Hedrick PW, Gilpin ME (1997) Genetic effective size of a metapopulation. In: Metapopulation Biology (eds. Hanski IA, Gilpin ME), pp. 166–182. Academic Press, San Diego, CA.
Hoeh WR, Black MB, Gustafson R, Bogan AE, Lutz RA, Vrijenhoek RC (1998) Testing alternative hypotheses of Neotrigonia (Bivalvia: Trigonioida) phylogenetic relationships using cytocrhome c oxidase subunit I sequences. Malacalogia, 40, 267–278.
Hoeh WR, Bogan AE, Heard WH (2001) A phylogenetic perspective on the evolution of morphological and reproductive characteristics in the Unionoida. In: Ecology and Evolution of the Freshwater Mussels Unionoida (eds. Bauer G, Wachtler K), Springer-Verlag, Berline Heidelberg.
Hornbach DJ, March JG, Deneka T, Nels J, Troelstrup H, Perry JA (1996) Factors influencing the distribution and abundance of the endangered Winged Mapleleaf mussel Quadrula fragosa in the St. Croix River, Minnesota and Wisconsin. Amer. Mid. Nat., 136, 278–286.
Johnson PD, Brown KM (1998) Intraspecific life history variation in the threatened Louisiana pearlshell mussel, Margaritifera hembeli. Freshwater Biol., 40, 317–329.
Johnson PD, Brown KM (2000) The importance of microhabitat factors and habitat stability to the threatened Louisiana pearlshell, Margaritifera hembeli (Conrad). Can. J. Zool., 78, 271–277.
Johnson RL, Liang FQ, Farris JL (1998) Genetic diversity among four Amblemini species (Bivalvia: Unionidae) in the Cache and White Rivers, Arkansas. Southwest. Nat., 43, 321–332.
Kandl KL, Liu H-P, Butler RS, Hoeh WR, Mulvey M (2001) A genetic approach to resolving taxonomic ambiguity among Pleurobema (Bivalvia: Unionidae) of the eastern Gulf coast. Malacalogia, 43, 87–101.
Kat PW (1983a) Genetic and morphological divergence among nominal species of North American Anodonta (Bivalvia: Unionidae). Malacologia, 23, 361–374.
Kat PW (1983b) Morphologic divergence, genetics, and speciation among Lampsilis (Bivalvia: Unionidae). J. Moll. Stud., 49, 133–145.
Kat PW (1983c) Patterns of electrophoretic and morphologic variability in a widely distributed unionid: an initial survey. Neth. J. Zool., 33, 21–40.
Kat PW, Davis GM (1984) Molecular genetics of peripheral populations of Nova Scotian Unionidae (Mollusca: Bivalvia). Biol. J. Linnean Soc., 22, 157–185.
Keller LF, Waller DM(2002) Inbreeding effects in wild populations. Trends Ecol. Evol., 17, 230–241.
Kesler DH, Bailey RC (1993). Density and ecomorphology of a freshwater mussel (Elliptio complanata, Bivaliva: Unionidae) in a Rhode Island lake. J. N. Am. Benthol. Soc., 12, 259–264.
Lydeard C, Roe KJ (1998) Phylogenetic systematics: the missing ingredient in the conservation of freshwater unionid bivalves. Fisheries, 23, 16–17.
Machordom A, Araujo R, Erpenbeck D, Ramos M-A (2003) Phylogeography and conservation genetics of endangered European Margaritiferidae (Bivalvia: Unionoidea). Biol. J. Linnean Soc., 78, 235–252.
Merola M (1994) A reassessment of homozygosity and the case for inbreeding depression in the cheetah, Acinonyx jubatus: implications for conservation. Conserv. Biol., 8, 961–971.
Mulvey M, Liu H-P, Kandl KL (1998) Application of molecular genetic markers to conservation of freshwater bivalves. J. Shell-fish Res., 17, 1395–1405.
Mulvey M, Lydeard C, Pyer DL, Hicks KM, Brim-Box J, Williams JD, Butler RS (1997) Conservation genetics of North American freshwater mussels Amblema and Megalonaias. Conserv. Biol., 11, 868–878.
Murphy RW, Sites JW, Buth DG, Haufler, CH (1996) Proteins I: Isozyme electrophoresis. In: Molecular Systematics (eds. Hillis DM, Moritz C, Mable BK). Sinauer Associates Inc., Sunderland, Massachusetts.
Nagel KO, Badino G (2001) Population genetics and systematics of European Unionoidea. In: Ecology and Evolution of the Freshwater Mussels Unionoida (eds. Bauer G, Wachtler K). Springer-Verlag, Berlin.
Nagel KO, Badino G, Alessandria B (1996) Population genetics of European Anodontinae (Bivalvia: Unionidae). J. Moll. Stud., 62, 343–357.
Neves RJ (1992) A state-of-the-unionids address. In: Conservation and Management of Freshwater Mussels (eds. Cummings KS, Buchanan AC, Koch LM), pp. 1–10. Upper Mississippi River Conservation Committee, St. Louis, MO.
Nevo E, Beiles A, Ben-Shlomo R (1983) The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: Evolutionary Dynamics of Genetic Diversity (ed. Levin S). Springer-Verlag, Berlin.
O'Brien SJ (1994) Genetic and phylogenetic analyses of endangered species. Annu. Rev. Genet., 28, 467–489.
O'Brien SJ, Wildt DE, Goldman D, Merril CR, Bush M (1983) The cheetah is depauperate in genetic variation. Science, 221, 459–462.
Pamilo P, Palsson S (1998) Associative overdominance, heterozygosity and fitness. Heredity, 81, 381–389.
Pannell JR, Charlesworth B (2000) Effects of metapopulation processes on measures of genetic diversity. Phil. Trans. R. Soc. [Biol], 355, 1851–1864.
Payne BS, Miller AC (2000) Recruitment of Fusconia ebena (Bivalvia: Unionidae) in relation to discharge of the lower Ohio river. Amer. Mid. Nat., 144, 328–341.
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv. Biol., 17, 230–237.
Ricciardi A, Neves RJ, Rasmussen JB (1998) Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion. J. Anim. Ecol., 67, 613–619.
SAS Institute Inc. (1989) SAS/STAT Users Guide, Version 6, fourth edition, Vol. 2. SAS Institute Inc., Cary, NC.
Shaw CR, Prasad R (1970) Starch gel electrophoresis of enzymes-a compilation of recipes. Biochem. Genet., 4, 297–320.
Shively SH (1999) 1999 Survey for the Louisiana Pearlshell (Margaritifera hembeli) in Grant Parish, LA. Louisiana Natural Heritage Program, Louisiana Department of Wildlife and Fisheries, Baton Rouge, LA.
Shively SH, Vermillion WG (1998) 1998 Survey for the Louisiana Pearlshell (Margaritifera hembeli) in Rapides Parish, LA. Louisiana Natural Heritage Program, Louisiana Department of Wildlife and Fisheries, Baton Rouge, LA.
Smith DG (2001) Systematics and distribution of the Recent Margaritiferidae. In: Evolution of the Freshwater Mussels Unionoida (eds. Bauer G, Wachtler K). Springer-Verlag, Berlin.
Stein BA, Master LL, Morse LE (2002) Taxonomic bias and vulnerable species. Science, 297, 1807.
Stiven AE, Alderman J (1992) Genetic similarities among certain freshwater mussel populations of the Lampsilis genus in North Carolina. Malacologia, 34, 355–369.
Strayer DL, Ralley J (1993) Microhabitat use by an assemblage of stream-dwelling unionaceans (Bivalvia), including two rare species of Alasmidonta. J. N. Am. Benthol. Soc., 12, 247–258.
van der Schalie H (1970) Hermaphroditism among North American freshwater mussels. Malacologia, 10, 93–112.
Vannote RL, Minshall GW (1982) Fluvial processes and local lithology controlling abundance, structure, and composition of mussel beds. Proc. Natl. Acad. Sci. USA, 79, 4103–4107.
Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. In: Conservation Genetics (eds. Loeschcke V, Tomiuk J, Jain SK). Birkhauser Verlag, Basel, Switzerland.
Vrijenhoek RC (1996) Conservation genetics of North American desert fishes. In: Conservation Genetics: Case Histories from Nature (eds. Avise JC, Hamrick JL), pp. 367–397. Chapman & Hall, New York.
Williams JD, Melvin J, Warren L, Cummings KS, Harris JL, Neves RJ (1992) Conservation status of freshwater mussels of the United States and Canada. Fisheries, 18, 6–22.
WWF (1990) Louisiana Pearlshell. In: The official World Wildlife Fund Guide to Endangered Species of North America (eds. Matthews JR, Moseley CJ). Walton Beacham, Washington, D.C.
Young MR, Williams JC (1983) Redistribution and local recolonisation by the freshwater pearl mussel Margaritifera margaritifera. J. Conch., 31, 225–234.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Curole, J.P., Foltz, D.W. & Brown, K.M. Extensive allozyme monomorphism in a threatened species of freshwater mussel, Margaritifera hembeli Conrad (Bivalvia: Margaritiferidae). Conservation Genetics 5, 271–278 (2004). https://doi.org/10.1023/B:COGE.0000030005.14751.76
Issue Date:
DOI: https://doi.org/10.1023/B:COGE.0000030005.14751.76