Conservation Genetics

, 10:803 | Cite as

Limited genetic variation and structure in softshell clams (Mya arenaria) across their native and introduced range

  • C. A. StrasserEmail author
  • P. H. Barber
Research Article


To offset declines in commercial landings of the softshell clam, Mya arenaria, resource managers are engaged in extensive stocking of seed clams throughout its range in the northwest Atlantic. Because a mixture of native and introduced stocks can disrupt locally adapted genotypes, we investigated genetic structure in M. arenaria populations across its current distribution to test for patterns of regional differentiation. We sequenced mitochondrial cytochrome oxidase I for a total of 212 individuals from 12 sites in the northwest Atlantic (NW Atlantic), as well as two introduced sites, the northeast Pacific (NE Pacific), and the North Sea Europe (NS Europe). Populations exhibited extremely low genetic variation, with one haplotype dominating (65–100%) at all sites sampled. Despite being introduced in the last 150–400 years, both NE Pacific and NS Europe populations had higher diversity measures than those in the NW Atlantic and both contained private haplotypes at frequencies of 10–27% consistent with their geographic isolation. While significant genetic structure (F ST = 0.159, P < 0.001) was observed between NW Atlantic and NS Europe, there was no evidence for genetic structure across the pronounced environmental clines of the NW Atlantic. Reduced genetic diversity in mtDNA combined with previous studies reporting reduced genetic diversity in nuclear markers strongly suggests a recent population expansion in the NW Atlantic, a pattern that may result from the retreat of ice sheets during Pleistocene glacial periods. Lack of genetic diversity and regional genetic differentiation suggests that present management strategies for the commercially important softshell clam are unlikely to have a significant impact on the regional distribution of genetic variation, although the possibility of disrupting locally adapted stocks cannot be excluded.


Mya arenaria Bivalve COI Northwest Atlantic Genetic structure 



This work was supported by NSF grants OCE-0326734 and OCE-0215905 to L. Mullineaux and OCE-0349177 (Biological Oceanography) to PHB. Initial stages of this work were conducted as part of course BI536 (Molecular Ecology and Evolution) at Boston University and is contribution 003 from this course. We are grateful to the many people who collected samples for this study. We also thank L. Mullineaux, E. Crandall, E. Jones, J. Drew, D. Adams, and R. Jennings for helpful advice and discussion. E. Crandall, L. Mullineaux, S. Mills, and S. Beaulieu provided useful comments on early drafts. We also thank the two anonymous reviewers for their contributions to improving the manuscript. The experiments in this study comply with the current laws of the United States of America.


  1. Abraham BJ, Dillon PL (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (mid-Atlantic): Softshell clam. USFWS biological report TR EL-82-4, 18 ppGoogle Scholar
  2. Anonymous (2007) Massachusetts Commercial Shellfish Harvest; 1996–2000. Available at: Cited 8 Nov 2007
  3. Avise JC (2000) Phylogeography. Harvard University Press, Boston, MAGoogle Scholar
  4. Baker P, Austin JD, Bowen BW, Baker SM (2008) Range-wide population structure and history of the northern quahog (Merceneria merceneria) inferred from mitochondrial DNA sequence data. ICES J Mar Sci 65:155–163. doi: 10.1093/icesjms/fsn007 CrossRefGoogle Scholar
  5. Barber PH, Erdmann MV, Palumbi SR (2006) Comparative phylogeography of three codistributed stomatopods: origins and timing of regional lineage diversification in the coral triangle. Evol Int J Org Evol 60:1825–1839Google Scholar
  6. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188. doi: 10.1214/aos/1013699998 CrossRefGoogle Scholar
  7. Berry AJ, Ajioka JW, Kreitman M (1991) Lack of polymorphism on the Drosophila fourth chromosome resulting from selection. Genetics 129:1111–1117PubMedGoogle Scholar
  8. Billerbeck JM, Orti G, Conover DO (1997) Latitudinal variation in vertebral number has a genetic basis in the Atlantic silverside, Menidia menidia. Can J Fish Aquat Sci 54:1796–1801. doi: 10.1139/cjfas-54-8-1796 CrossRefGoogle Scholar
  9. Brousseau DJ (1978) Spawning cycle, fecundity, and recruitment in a population of soft-shell clam, Mya arenaria, from Cape Ann, Massachusetts. Fish Bull (Wash DC) 76:155–166Google Scholar
  10. Brousseau DJ (2005) Effects of natural mortality and harvesting on inshore bivalve population trends. In: Buchsbaum R, Pederson J, Robinson WE (eds) The decline of fisheries resources in New England: evaluating the impact of overfishing, contamination, and habitat degradation. MIT Sea Grant 05–5, Cambridge, MAGoogle Scholar
  11. Brown AF, Kann LM, Rand DM (2001) Gene flow versus local adaptation in the northern acorn barnacle, Semibalanus balanoides: insights from mitochondrial DNA variation. Evolution Int J Org Evolution 55:1972–1979Google Scholar
  12. Caporale DA, Beal BF, Roxby R, Van Beneden RJ (1997) Population structure of Mya arenaria along the New England coastline. Mol Mar Biol Biotechnol 6:33–39PubMedGoogle Scholar
  13. Carlton JT (1979) History, biogeography and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Dissertation, University of California DavisGoogle Scholar
  14. Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:265–270Google Scholar
  15. Chao A, Lee SM (1992) Estimating the number of classes via sample coverage. J Am Stat Assoc 87:210–217CrossRefGoogle Scholar
  16. Connell LB, MacQuarrie SP, Twarog BM, Iszard M, Bricelj VM (2007) Population differences in nerve resistance to paralytic shellfish toxins in softshell clam, Mya arenaria, associated with sodium channel mutations. Mar Biol (Berl) 150:1227–1236. doi: 10.1007/s00227-006-0432-z CrossRefGoogle Scholar
  17. Cronin TM (1988) Evolution of marine climates of the U.S. Atlantic coast during the past four million years. Phil Trans R Soc Lond. Ser B 318:661–678CrossRefGoogle Scholar
  18. Dahlgren TG, Weinberg JR, Halanych KM (2000) Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Mar Biol (Berl) 137:487–495. doi: 10.1007/s002270000342 CrossRefGoogle Scholar
  19. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320PubMedGoogle Scholar
  20. Drummond AJ, Rambaut A (2006) BEAST v.1.4. Available from
  21. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192. doi: 10.1093/molbev/msi103 PubMedCrossRefGoogle Scholar
  22. Engle VD, Summers JK (1999) Latitudinal gradients in benthic community composition in western Atlantic estuaries. J Biogeogr 26:1007–1023. doi: 10.1046/j.1365-2699.1999.00341.x CrossRefGoogle Scholar
  23. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  24. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  25. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  26. Gardner JPA, Kathiravetpillai G (1997) Biochemical genetic variation at a leucine aminopeptidase (LAP) locus in blue (Mytilus galloprovincialis) and greenshell (Perna canaliculus) mussel populations along a salinity gradient. Mar Biol (Berl) 128:619–625. doi: 10.1007/s002270050128 CrossRefGoogle Scholar
  27. Gardner JPA, Palmer NL (1998) Size-dependent, spatial and temporal genetic variation at a leucine aminopeptidase (LAP) locus among blue mussel (Mytilus galloprovincialis) populations along a salinity gradient. Mar Biol (Berl) 132:275–281. doi: 10.1007/s002270050393 CrossRefGoogle Scholar
  28. Hall CA Jr (1964) Shallow-water marine climates and molluscan provinces. Ecology 45:226–234. doi: 10.2307/1933835 CrossRefGoogle Scholar
  29. Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015. doi: 10.1046/j.1365-294X.2002.01495.x PubMedCrossRefGoogle Scholar
  30. Hart DL, Clark AG (1997) Population substructure. In: principles of population genetics. Sinauer, Sunderland, MA, pp 111–162Google Scholar
  31. Heck KL Jr, van Belle G, Simberloff D (1975) Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecology 56:1459–1461. doi: 10.2307/1934716 CrossRefGoogle Scholar
  32. Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79Google Scholar
  33. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913. doi: 10.1038/35016000 PubMedCrossRefGoogle Scholar
  34. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276Google Scholar
  35. Hidu H, Newell CR (1989) Culture and ecology of the soft-shelled clam Mya arenaria. In: Manzi JJ, Castagna M (eds) Clam mariculture in North America. Elsevier, AmsterdamGoogle Scholar
  36. Hutchins LW (1947) The bases for temperature zonation in geographical distribution. Ecol Monogr 17:325–335. doi: 10.2307/1948663 CrossRefGoogle Scholar
  37. King TL, Eackles MS, Gjetvaj B, Hoeh WR (1999) Intraspecific phylogeography of Lasmigona subviridis (Bivalvia: Unionidae): conservation implications of range discontinuity. Mol Ecol 8:S65–S78. doi: 10.1046/j.1365-294X.1999.00784.x PubMedCrossRefGoogle Scholar
  38. Lasota R, Hummel H, Wolowicz M (2004) Genetic diversity of European populations of the invasive soft-shell clam Mya arenaria (Bivalvia). J Mar Biol Assoc U K 84:1051–1056. doi: 10.1017/S0025315404010409h CrossRefGoogle Scholar
  39. MacNeal FS (1965) Evolution and distribution of the genus Mya, and tertiary migrations of mollusca. Prof Pap USGS 483(G):1–51Google Scholar
  40. Maddison DR, Maddison WP (2002) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland, MAGoogle Scholar
  41. Marcotti T, Leavitt DF (1997) The barnstable harbor shellfish recruitment enhancement project (BHSREP): a final report. Woods Hole Oceanographic Institution: T-97-001, 47 ppGoogle Scholar
  42. Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021PubMedGoogle Scholar
  43. May GE, Gelembiuk GW, Panov VE, Orlova MI, Lee CE (2006) Molecular ecology of zebra mussel invasions. Mol Ecol 15:1021–1031PubMedCrossRefGoogle Scholar
  44. Morgan RP, Block SB, Ulanowicz NI, Buys C (1978) Genetic variation in the soft-shelled clam, Mya arenaria. Estuaries 1:255–258. doi: 10.2307/1351528 CrossRefGoogle Scholar
  45. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi: 10.1007/s10592-005-9056-y CrossRefGoogle Scholar
  46. Newell CR, Hidu H (1982) The effects of sediment type on growth rate and shell allometry in the soft shelled clam, Mya arenaria L. J Exp Mar Biol Ecol 65:285–295. doi: 10.1016/0022-0981(82)90060-0 CrossRefGoogle Scholar
  47. Petersen KS, Rasmussen KL, Heinemeler J, Rud N (1992) Clams before Columbus? Nature 359:679CrossRefGoogle Scholar
  48. Porter SC (1989) Some geological implications of average quaternary glacial conditions. Quat Res 32:245–261. doi: 10.1016/0033-5894(89)90092-6 CrossRefGoogle Scholar
  49. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: 10.1093/bioinformatics/14.9.817 PubMedCrossRefGoogle Scholar
  50. Powers SP, Bishop MA, Grabowski JH, Peterson CH (2006) Distribution of the invasive bivalve Mya arenaria L. on intertidal flats of south central Alaska. J Sea Res 55:207–216. doi: 10.1016/j.seares.2005.10.004 CrossRefGoogle Scholar
  51. Present TMC, Conover DO (1992) Physiological basis of latitudinal frowth differences in Menidia menidia: variation in consumption or efficiency? Funct Ecol 6:23–31. doi: 10.2307/2389767 CrossRefGoogle Scholar
  52. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86. doi: 10.1093/molbev/msg009 PubMedCrossRefGoogle Scholar
  53. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  54. Shackleton NJ, Backman J, Zimmerman H, Kent DV, Hall MA et al (1984) Oxygen isotope calibration of the onset of ice-rafting and history of glaciation in the North Atlantic region. Nature 307:620–623. doi: 10.1038/307620a0 CrossRefGoogle Scholar
  55. Slatkin M (1985) Rare alleles as indicators of gene flow. Evol Int J Org Evol 39:53–65. doi: 10.2307/2408516 Google Scholar
  56. Smith MW, Chapman RW, Powers DA (1998) Mitochondrial DNA analysis of Atlantic coast, Chesapeake Bay, and Delaware Bay populations of the teleost Fundulus heteroclitus indicates temporally unstable distributions over geologic time. Mol Mar Biol Biotechnol 7:79–87Google Scholar
  57. Strasser M (1999) Mya arenaria—an ancient invader of the North Sea coast. Helgol Meersunters 52:309–324CrossRefGoogle Scholar
  58. Swofford DL (1998) Phylogenetic analysis using parsimony and other methods (PAUP*). Available from:, Sinauer, Sunderland, MA
  59. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  60. Upham W (1879a) The formation of Cape Cod. Am Nat 13:489–502. doi: 10.1086/272387 CrossRefGoogle Scholar
  61. Upham W (1879b) The formation of Cape Cod (Continued). Am Nat 13:552–565. doi: 10.1086/272404 CrossRefGoogle Scholar
  62. Waldman JR, Nolan K, Hart J, Wirgin II (1996) Genetic differentiation of three key anadromous fish populations of the Hudson River. Estuaries 19:759–768. doi: 10.2307/1352295 CrossRefGoogle Scholar
  63. Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  64. Waples RS, Do C (1994) Genetic risk associated with supplementation of Pacific salmonids: captive broodstock programs. Can J Fish Aquat Sci 51:310–329. doi: 10.1139/f94-318 CrossRefGoogle Scholar
  65. Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Mol Ecol 11:1131–1144. doi: 10.1046/j.1365-294X.2002.01510.x PubMedCrossRefGoogle Scholar
  66. Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evol Int J Org Evol 55:2455–2469Google Scholar
  67. Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276. doi: 10.1016/0040-5809(75)90020-9 PubMedCrossRefGoogle Scholar
  68. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  69. Yamahira K, Lankford TE Jr, Conover DO (2006) Intra- and interspecific latitudinal variation in vertebral number of Menidia spp. (Teleostei: Atherinopsidae). Copeia 2006:431–436. doi: 10.1643/0045-8511(2006)2006[431:IAILVI]2.0.CO;2 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Biology DepartmentBoston UniversityBostonUSA

Personalised recommendations