Skip to main content

Advertisement

SpringerLink
Log in

Mitochondrial DNA variation and population genetic structure of the blue crab Callinectes sapidus in the eastern United States

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The blue crab (Callinectes sapidus) is an ecologically important component of estuarine ecosystems throughout the eastern United States and supports both commercial and recreational fisheries of high economic importance. We investigated the population genetic structure of blue crabs in the waters of the eastern United States using restriction fragment length polymorphism analysis of the mitochondrial DNA (mtDNA) molecule. Genetic diversity was notably high; nucleotide diversities were in the range 1.0%–2.6%, haplotype diversities were in the range 0.7–1.0, and 79% of the haplotypes occurred in single individuals. A mismatch analysis of pairwise haplotype differences indicated that C. sapidus experienced a historic period of rapid population expansion. The relationship among mtDNA haplotypes was complex and may represent pre- and post-expansion lineage sorting. Genetic differentiation of the collections was suggested by a significant analysis of molecular variance (AMOVA), but no geographic patterns to the differences nor geographic partitioning of haplotypes was evident. Nevertheless, blue crabs showed a significant cline in haplotype diversity along Atlantic Ocean coastal waters—haplotype diversity decreased with increasing latitude—and a distinctly low haplotype diversity in the northernmost New York collection. The putative population expansion and development of the cline in genetic diversity are consistent with a historic range expansion northward along the Atlantic Ocean coast, perhaps as a result of Pleistocene-era climatic fluctuations. The cline in diversity parallels a cline in allele frequencies at an esterase locus previously observed through allozyme electrophoresis. The combination of a distinct cline and the geographically widespread distribution of common and closely related haplotypes suggests that short-term gene flow in blue crabs is regional whereas long-term gene flow is long-distance. Management of this species should focus on maintaining local blue crab populations and habitats to ensure the long-term sustainability of the species and its fishery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4A, B

Similar content being viewed by others

References

  • Abele LG (1982) Biogeography. In: Abele LG (ed) The biology of Crustacea, vol 1. Academic, New York, pp 241–304

  • Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504

    CAS  PubMed  Google Scholar 

  • Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol 20:99–105

    CAS  PubMed  Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Article  Google Scholar 

  • Baker AM, Mather PB, Hughes JM (2001) Evidence for long-distance dispersal in a sedentary passerine, Gymnorhina tibicen (Artamidae). Biol J Linn Soc 72:333–343

    Article  Google Scholar 

  • Benefield RL, Linton T (1990) Movement study of blue crabs in Trinity Bay. Texas Parks and Wildlife Department, Coastal Fisheries Division. Manag Data Ser 16:1–11

    Google Scholar 

  • Benzie JAH, Ballment E, Frusher S (1993) Genetic structure of Penaeus monodon in Australia: concordant results from mtDNA and allozymes. Aquaculture 111:89–93

    Article  CAS  Google Scholar 

  • Bert TM, McCarthy KJ, Cruz-Lopez H, Bogdanowicz S (1996) Character discriminatory power, character-set congruence, and the classification of individuals from hybrid zones: an example using stone crabs (Menippe). Evolution 50:655–671

    Google Scholar 

  • Brooker AL, Benzie JAH, Blair D, Versini J-J (2000) Population structure of the giant tiger prawn Penaeus monodon in Australian waters, determined using microsatellite markers. Mar Biol 136:149–157

    Article  Google Scholar 

  • Buroker NE (1983) Population genetics of the American oyster Crassostrea virginica along the Atlantic coast and the Gulf of Mexico. Mar Biol 75:99–112

    Google Scholar 

  • Caley MJ, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open marine populations. Annu Rev Ecol Syst 27:477–500

    Article  Google Scholar 

  • Churchill EP Jr (1919) Life history of the blue crab. Bull Bur Fish 356:93–128

    Google Scholar 

  • Cowen RK, Lwiza KMM, Sponaugle S, Paris CB, Olson DB (2000) Connectivity of marine populations: open or closed? Science 287:857–859

    Article  CAS  PubMed  Google Scholar 

  • Epifanio CE, Garvine RW (2001) Larval transport on the Atlantic continental shelf of North America: a review. Estuar Coast Shelf Sci 52:51–77

    Article  Google Scholar 

  • 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 131:479–491

    CAS  PubMed  Google Scholar 

  • Fedorov V, Jaarola M, Fredga K (1996) Low mitochondrial DNA variation and recent colonization of Scandinavia by the wood lemming. Mol Ecol 5:577–581

    Article  CAS  Google Scholar 

  • Felsenstein J (1993) PHYLIP (Phylogeny Inference Package) version 3.5c. Department of Genetics, University of Washington, Seattle (distributed by the author)

  • Gonzalez-Villaseñor LI, Powers DA (1990) Mitochondrial-DNA restriction-site polymorphisms in the teleost Fundulus heteroclitus support secondary intergradation. Evolution 44:27–37

    CAS  Google Scholar 

  • Harris RE Jr (1982) Life history, ecology, and stock assessment of the blue crab Callinectes sapidus of the United States Atlantic coast—a review. Proceeding of the Blue Crab Colloquium, pp 59–63

  • Hellberg ME, Balch DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1710

    Article  CAS  PubMed  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Johnson DR, Perry HM (1999) Blue crab larval dispersion and retention in the Mississippi Bight. Bull Mar Sci 65:129–149

    Google Scholar 

  • Karl SA, Avise JC (1992) Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256:100–102

    CAS  PubMed  Google Scholar 

  • Kordos LM, Burton RS (1993) Genetic differentiation of Texas Gulf coast populations of the blue crab, Callinectes sapidus. Mar Biol 117:227–233

    Google Scholar 

  • Lavery S, Moritz C, Fielder DR (1996) Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Mol Ecol 5:557–570

    Article  Google Scholar 

  • Marko PB (1998) Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution 52:757–774

    Google Scholar 

  • McElroy D, Moran P, Bermingham E, Kornfield I (1992) REAP: an integrated environment for the manipulation and phylogenetic analysis of restriction data. J Hered 83:157–158

    CAS  PubMed  Google Scholar 

  • McMillen-Jackson AL, Bert TM, Steele P (1994) Population genetics of the blue crab Callinectes sapidus: modest population structuring in a background of high gene flow. Mar Biol 118:53–65

    Google Scholar 

  • Mead LS, Tilley SG, Katz LA (2001) Genetic structure of the blue ridge dusky salamander (Desmognathus orestes): inferences from allozymes, mitochondrial DNA, and behavior. Evolution 55:2287–2302

    CAS  PubMed  Google Scholar 

  • National Marine Fisheries Service (2003) Fisheries of the United States 2002. United States Department of Commerce, NOAA, NMFS

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • Nei M, Tajima F (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97:145–163

    Google Scholar 

  • Oesterling MJ, Adams CA (1982) Migration of blue crabs along Florida’s Gulf Coast. Gulf States Marine Fisheries Commission, Ocean Springs, Mississippi. Report no. 7, pp 37–57

  • Ovenden JR, Brasher DJ, White RWG (1992) Mitochondrial DNA analyses of the red rock lobster Jasus edwardsii supports an apparent absence of population subdivision throughout Australia. Mar Biol 112:319–326

    CAS  Google Scholar 

  • Pellegrin G Jr, Guillory V, Prejean P, Perry H, Warren J, Steele P, Wagner T, Heath S (2001) Length-based estimates of total mortality for Gulf of Mexico blue crab. Proceedings of the Blue Crab Mortality Symposium, 28–29 May 1999, Lafayette. Louisiana Gulf States Marine Fisheries Commission, number 90, pp 42–49

  • Perry HM, Stuck KC (1982) The life history of the blue crab in Mississippi with notes on larval distribution. Gulf States Marine Fisheries Commission, Ocean Springs, Mississippi. Report no. 7, pp 17–22

  • Prim RC (1957) Shortest connection networks and some generalizations. Bell Syst Tech J 36:1389–1401

    Google Scholar 

  • Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124:397–406

    CAS  PubMed  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Roff DA, Bentzen P (1989) The statistical analysis of mitochondrial DNA polymorphism: chi-square and the problem of small samples. Mol Biol Evol 6:539–545

    CAS  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rohlf FJ (1992) NTSYS-pc. Numerical taxonomy and multivariate analysis system, version 1.7. Exeter Software, New York

  • Roman MR, Boicourt WC (1999) Dispersion and recruitment of crab larvae in the Chesapeake Bay plume: physical and biological controls. Estuaries 22:563–574

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Silberman JD, Sarver SK, Walsh PJ (1994) Mitochondrial DNA variation in seasonal cohorts of spiny lobster (Panulirus argus) postlarvae. Mol Mar Biol Biotechnol 3:165–170

    CAS  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279

    Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  Google Scholar 

  • Steele P (1991) Population dynamics and migration of the blue crab, Callinectes sapidus (Rathbun), in the eastern Gulf of Mexico. Proc Gulf Caribb Fish Inst 40:241–244

    Google Scholar 

  • Sulkin SD, van Heukelem W (1982) Larval recruitment in the crab Callinectes sapidus Rathbun: an amendment to the concept of larval retention in estuaries. In: Kennedy VS (ed) Estuarine comparisons. Academic, New York, pp 459–475

  • Swofford DL (1993) PAUP: phylogenetic analysis using parsimony, version 3.1 Computer program distributed by the Illinois Natural History Survey, Champaign, Illinois

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  Google Scholar 

  • Thomas CD, Bodsworth EJ, Wilson RJ, Simmons AD, Davies ZG, Musche M, Conradt L (2001) Ecological and evolutionary processes at expanding range margins. Nature 411:577–581

    Article  CAS  PubMed  Google Scholar 

  • Turgeon J, Bernatchez L (2001) Clinal variation at microsatellite loci reveals historical secondary intergradation between glacial races of Coregonus artedi (Teleosti: Coregoninae). Evolution 55:2274–2286

    CAS  PubMed  Google Scholar 

  • Williams AB (1984) Shrimps, lobsters, and crabs of the Atlantic coast of the eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, D.C.

  • Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–400

    Google Scholar 

  • Wilson RR Jr, Tringali MD (1990) Improved methods for isolation of fish mtDNA by ultracentrifugation and visualization of restriction fragments using fluorochrome dye: results from Gulf of Mexico clupeids. Fish Bull 88:611–615

    CAS  Google Scholar 

  • Wirgin I, Waldman JR, Rosko J, Gross R, Collins MR, Rogers SG, Stabile J (2000) Genetic structure of Atlantic sturgeon populations based on mitochondrial DNA control region sequences. Trans Am Fish Soc 129:476–486

    CAS  Google Scholar 

Download references

Acknowledgements

We thank the many individuals from all over the eastern United States who graciously provided us with blue crabs, especially P. Steele. We also thank T. Thompson, S. Butler, C. Crawford, and S. Lotz for their help with DNA extractions; P. Steele, S. Karl, and three anonymous reviewers for reviewing the manuscript; the Florida Marine Research Institute editorial staff for editorial assistance; and L. French for producing the map of collection locations. This study was conducted as part of A.L.M.-J.’s dissertation work and was funded by an Interjurisdictional Marine Fisheries Research Grant from the National Oceanographic and Atmospheric Administration to the Florida Marine Research Institute, a Lerner-Gray grant to A.L.M.-J., and the State of Florida. The views expressed herein are solely those of the authors and are not necessarily shared by the funding agencies. The performance of these experiments complied with the current laws of the United States.

Author information

Authors and Affiliations

  1. Florida Marine Research Institute, 100 8th Avenue S.E., St. Petersburg, FL 33701, USA

    A. L. McMillen-Jackson & T. M. Bert

Authors
  1. A. L. McMillen-Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. M. Bert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. L. McMillen-Jackson.

Additional information

Communicated by P.W. Sammarco, Chauvin

Rights and permissions

Reprints and permissions

About this article

Cite this article

McMillen-Jackson, A.L., Bert, T.M. Mitochondrial DNA variation and population genetic structure of the blue crab Callinectes sapidus in the eastern United States. Marine Biology 145, 769–777 (2004). https://doi.org/10.1007/s00227-004-1353-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-004-1353-3

Keywords

Search

Navigation