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Marine Biology

, Volume 149, Issue 2, pp 213–226 | Cite as

Genetic structure and phylogeography of the lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts

  • Bryan J. Cassone
  • Elizabeth G. Boulding
Research Article

Abstract

Marine invertebrates with high larval dispersal capacity typically exhibit low degrees of population differentiation, which reflects both contemporary and historical processes. We sampled 346 individuals from seven populations of the lined shore crab, Pachygrapsus crassipes Randall, along the northeastern Pacific Coast and Korea during summer 2003. DNA sequence analysis of 613 bp of the mitochondrial COI gene showed that overall gene diversity (h) was high (0.92±0.01), whereas overall nucleotide diversity (π) was low (0.009±0.005). A total of 154 mtDNA haplotypes were identified; however, 114 were present in only one individual. Analysis of molecular variance revealed significant genetic structuring at Point Conception, CA, USA, that is likely due to the oceanographic circulation patterns, which result in asymmetrical migration of haplotypes. However, genetic variation among eastern Pacific populations was generally low, probably because of high contemporary gene flow and recent common ancestry of haplotypes. Mismatch analysis and nested clade analysis suggested that the population history of this region is characterized by two contiguous northwards range expansions, which are congruent with Late Pleistocene glacial cycles. Highly significant genetic differentiation was detected between eastern Pacific populations and Korea, indicating transpacific gene flow is restricted. Time of divergence between the two transpacific lineages was estimated between 0.8 and 1.2 Myrs ago. The small, recently founded population of P. crassipes at Bamfield, BC, Canada, did not appear to have undergone a founder effect.

Keywords

Mismatch Distribution Point Conception Nest Clade Analysis Sudden Population Expansion Effective Female Population Size 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We wish to thank C. Schubart for his P. transversus samples, as well as T. Crease, T. Zahradnik, R. McCarthy, and J. Ackerman for their valuable insight on various aspects of this study. We also greatly thank H.-J. Lee for collecting samples from Korea, and the directors and staff of Bamfield Marine Station, Oregon Institute of Marine Biology, Bodega Bay Marine Lab, and CICESE for field assistance. This work was supported by NSERC Discovery and PREA grants to E.G. Boulding. All experiments complied with the current laws of Canada.

References

  1. Addicott WO (1966) Late Pleistocene marine paleoecology and zoogeography in central California. US Geological Survey Professional Paper 523C, pp 1–21Google Scholar
  2. Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New YorkCrossRefGoogle Scholar
  3. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Beckwitt R (1985) Population genetics of the sand crab, Emerita analoga Stimpson, in southern California. J Exp Mar Biol Ecol 91:45–52CrossRefGoogle Scholar
  5. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568CrossRefGoogle Scholar
  6. Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past. Am Zool 39:131–145CrossRefGoogle Scholar
  7. Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45CrossRefGoogle Scholar
  8. Brant SV, Orti G (2003) Phylogeography of the northern short-tailed shrew, Blarina brevicauda (Insectivora: Soricidae): past fragmentation and postglacial recolonization. Mol Ecol 12:1435–1449CrossRefGoogle Scholar
  9. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: tempo and mode of evolution. J Mol Evol 18:225–239CrossRefGoogle Scholar
  10. Burton RS, Feldman M (1982) Population genetics of coastal and estuarine invertebrates: does larval behavior influence population structure? In: Kennedy VS (ed) Estuarine comparisons. Academic, New York, pp 537–551CrossRefGoogle Scholar
  11. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  12. Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969PubMedPubMedCentralGoogle Scholar
  13. Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 126:443–450CrossRefGoogle Scholar
  14. Ewens WJ (1972) The sampling theory of selectively neutral haplotypes. Theor Popul Biol 3:87–112CrossRefGoogle Scholar
  15. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 13:479–491Google Scholar
  16. Felsenstein (1993) PHYLIP version 3.5c. University of Washington, SeattleGoogle Scholar
  17. Folmer OM, Black R, Hoeh R, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  18. Fratini S, Vannini M (2002) Genetic differentiation in the mud crab Scylla serrata (Decapoda: Portunidae) within the Indian Ocean. J Exp Mar Biol Ecol 272:103–116CrossRefGoogle Scholar
  19. Gaylord B, Gaines SD (2000) Temperature or transport? Range limits in marine species mediated solely by flow. Am Nat 155:769–789CrossRefGoogle Scholar
  20. Graves JE (1998) Molecular insights into the population structures of cosmopolitan marine fishes. J Hered 89:427–437CrossRefGoogle Scholar
  21. Grigg RW, Hey R (1992) Paleoceanography of the tropical eastern Pacific Ocean. Science 255:172–178CrossRefGoogle Scholar
  22. Harpending H (1994) Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600Google Scholar
  23. Harpending H, Sherry ST, Rogers AR, Stoneking M (1993) The genetic structure of ancient human populations. Curr Anthropol 34:483–496CrossRefGoogle Scholar
  24. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond Ser B Biol Sci 270:313–321CrossRefGoogle Scholar
  25. Hedgecock D (1986) Is gene flow from pelagic larval dispersal important in the adaptation and evolution of marine invertebrates? Bull Mar Sci 39:550–565Google Scholar
  26. Hellberg ME (1998) Sympatric sea shells along the sea’s shore: the geography of speciation in the marine gastropod Tegula. Evolution 52:1311–1324CrossRefGoogle Scholar
  27. Hellberg ME, Balch DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1709CrossRefGoogle Scholar
  28. Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  29. Hiatt RW (1948) The biology of the lined shore crab, Pachygrapsus crassipes Randall. Pac Sci 2:135–213Google Scholar
  30. Hudson RR (1990) Gene genealogies and the coalescent process. In: Futyama J, Antonovics JD (eds) Oxford surveys in evolutionary biology. Oxford University Press, New YorkGoogle Scholar
  31. Hui CA (1992) Walking of the shore crab Pachygrapsus crassipes in its two natural environments. J Exp Biol 165:213–227Google Scholar
  32. Jablonski D, Flessa K, Valentine JW (1985) Biogeography and paleobiology. Paleobiology 11:75–90CrossRefGoogle Scholar
  33. Jin L, Nei M (1990) Limitations of the evolutionary parsimony method of phylogenetic analysis. Mol Biol Evol 7:82–102PubMedGoogle Scholar
  34. Jukes TH, Cantor CH (1969) Evolution of protein molecules. In: Munro HM (ed) Mammalian protein metabolism. Academic, New York, pp 21–123CrossRefGoogle Scholar
  35. Ketchum BH (1954) Relation between circulation and planktonic populations in estuaries. Ecology 35:191–200CrossRefGoogle Scholar
  36. Kimura M (1980) A simple model for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  37. Knowlton K, Keller BD (1986) Larvae which fall short of their potential: highly localized recruitment in an alpheid shrimp with extended larval development. Bull Mar Sci 39:213–223Google Scholar
  38. Knowlton N, Weight NA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond Ser B Biol Sci 265:2257–2263CrossRefGoogle Scholar
  39. Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845CrossRefGoogle Scholar
  40. Langor DW, Sperling FAH (1997) Mitochondrial DNA sequence divergence in weevils of the Pissodes strobi species complex (Coleoptera: Curculionidae). Insect Mol Biol 6:255–265CrossRefGoogle Scholar
  41. Lavery S, Moritz C, Fielder DR (1996) Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Mol Ecol 5:557–570CrossRefGoogle Scholar
  42. Levin LA, Huggett D, Myers P, Bridges T, Weaver J (1993) Rare-earth tagging methods for the study of larval dispersal by marine invertebrates. Limnol Oceanogr 38:246–360CrossRefGoogle Scholar
  43. Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New YorkGoogle Scholar
  44. Marko P (1998) Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution 52:757–774CrossRefGoogle Scholar
  45. Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155CrossRefGoogle Scholar
  46. McConaugha JR (1992) Decapod larvae: dispersal, mortality, and ecology. A working hypothesis? Am Zool 32:512–573CrossRefGoogle Scholar
  47. Merkouris SE, Seeb LW, Murphy MC (1998) Low levels of genetic diversity in highly exploited populations of Alaskan tanner crabs, Chionoecetes bairdi, and Alaskan and Atlantic snow crabs, C. opilio. Fish Bull 96:525–537Google Scholar
  48. Morris RH, Abbott DP, Haderlie EC (1980) Intertidal invertebrates of California. Stanford University Press, StanfordGoogle Scholar
  49. Newman WA (1979) California transition zone: significance of short-range endemics. In: Gray J, Boucot AJ (eds) Historical biogeography, plate tectonics, and the changing environment. Oregon State University Press, Corvallis, pp 399–416Google Scholar
  50. Newton CR (1988) Significance of “Tethyan” fossils in the American Cordillera. Science 242:385–390CrossRefGoogle Scholar
  51. Ohta T (1992) Theoretical study of near neutrality. II. Effect of subdivided population structure with local extinction and recolonization. Genetics 130:917–923PubMedPubMedCentralGoogle Scholar
  52. Page RDM (2001) Treeview version 1.6.6. University of Glasgow, GlasgowGoogle Scholar
  53. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  54. Pogson GH, Taggart CT, Mesa KA, Boutlier RG (2001) Isolation by distance in the Atlantic cod, Gadus morhua, at large and small geographic scales. Evolution 55:131–146CrossRefGoogle Scholar
  55. Posada DK, Crandall KA, Templeton AR (2000) GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol Ecol 9:487–488CrossRefGoogle Scholar
  56. Raimondi PT, Keough MJ (1990) Behavioural variability in marine larvae. Aust J Ecol 4:427–437CrossRefGoogle Scholar
  57. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615CrossRefGoogle Scholar
  58. Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  59. Rohling EJ, Fenton M, Jorissen FJ, Bertrand P, Ganssen G, Caulet JP (1998) Magnitudes of sea-level lowstands of the past 500,000 years. Nature 394:162–165CrossRefGoogle Scholar
  60. Saiki RK, Gelfand DH, Stoffel SJ, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487–491CrossRefGoogle Scholar
  61. Saitu N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  62. Scheltema RS (1971) Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic invertebrates. Biol Bull Mar Biol Lab (Woods Hole) 140:284–322CrossRefGoogle Scholar
  63. Scheltema RS (1975) Relationship of larval dispersal, gene flow and natural selection to geographic variation of benthic invertebrates in estuaries and along coastal regions. Estuarine Res 1:372–389Google Scholar
  64. Schlotterbeck RE (1976) The larval development of the lined shore crab, Pachygrapsus crassipes Randall, 1840 (Decapoda Brachyura, Grapsidae) reared in the laboratory. Crustaceana 30:184–200CrossRefGoogle Scholar
  65. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedPubMedCentralGoogle Scholar
  66. Schneider S, Roessli D, Excoffier L (2000) Arlequin, version 2.0000: a software program for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  67. Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365CrossRefGoogle Scholar
  68. Shanks AL (1983) Surface slicks associated with tidally forced internal waves may transport pelagic larvae and benthic invertebrates and fishes shoreward. Mar Ecol Prog Ser 13:311–315CrossRefGoogle Scholar
  69. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  70. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  71. Slatkin M, Voelm L (1991) Fѕт in a hierarchical island model. Genetics 127:627–629PubMedPubMedCentralGoogle Scholar
  72. Sousa WP (1993) Size-dependent predation on the salt-marsh snail Cerithidea californica Haldeman. J Exp Mar Biol Ecol 166:19–37CrossRefGoogle Scholar
  73. Tam YK, Kornfield I, Ojeda FP (1996) Divergence and zoogeography of mole crabs, Emerita spp. (Decapoda: Hippidae), in the Americas. Mar Biol 125:489–497Google Scholar
  74. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypothesis about gene flow and population history. Mol Ecol 7:381–397CrossRefGoogle Scholar
  75. Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809CrossRefGoogle Scholar
  76. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping IV. Nested analyses with the cladogram uncertainty and recombination. Genetics 134:659–669PubMedPubMedCentralGoogle Scholar
  77. Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophilia. Genetics 117:343–351PubMedPubMedCentralGoogle Scholar
  78. Thompson JD, Higins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  79. Uthicke S, Benzie JH (2003) Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific. Mol Ecol 12:2635–2648CrossRefGoogle Scholar
  80. Wares JP, Gaines SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55:295–306CrossRefGoogle Scholar
  81. Warner GF (1977) The biology of crabs. Elek Science, LondonGoogle Scholar
  82. Watterson GA (1978) The homozygosity test of neutrality. Genetics 88:405–417PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Department of Integrative BiologyUniversity of GuelphGuelphCanada

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