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Population divergence in the sinistral whelks of North America, with special reference to the east Florida ecotone

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Abstract

This study evaluated models of species relationships among sinistral whelks in the genus Busycon in the Atlantic and Gulf of Mexico. Gene frequencies at eight polymorphic allozyme loci, shell morphology, anatomy, and partial DNA sequences for the cytochrome c oxidase I (COI) mitochondrial gene were examined in eight populations, ranging from New Jersey to the Yucatan peninsula, and from the dextrally coiled sister taxon Busycon carica (Gmelin, 1791). Whelks were collected in 1997 and 1998. The maximum COI sequence divergence recorded among 32 sinistral individuals was 1.96%, which together with the absence of any gross or qualitative morphological differences, suggested all eight populations should be considered conspecific. High levels of divergence between the allopatric western Atlantic and Gulf of Mexico populations, as revealed by fixed or nearly fixed differences at several allozyme-encoding loci were interpreted as evidence that the east Florida ecotone constitutes a significant barrier to gene flow. Size trimming also revealed several significant quantitative differences in shell and radular morphology between the three pooled Atlantic populations and five pooled Gulf populations. The Yucatan sample was the most distinctive conchologically, with heavy spines and tumid ridges, possibly related to stone crab predation. Based on the evidence all left-handed whelks of North America should be referred to the oldest available nomen, Busycon perversum (Linné, 1758), with three subspecies, B. perversum perversum along the Yucatan peninsula, B. perversum sinistrum (Hollister, 1958) in the northern and eastern Gulf of Mexico, and B. perversum laeostomum (Kent, 1982) in the Atlantic.

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References

  • Abbott RT (1974) American seashells, 2nd edn. Van Nostrand Reinhold, New York

  • Adamkewicz LS, Harasewych MG (1996) Systematics and biogeography of the genus Donax (Bivalvia: Donacidae) in eastern North America. Am Malacol Bull 13:97–103

    Google Scholar 

  • Anderson B, Eversole A, Anderson W (1989) Variations in shell and radula morphologies of knobbed whelks. J Shellfish Res 8:213–218

    Google Scholar 

  • Avise J (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76

    CAS  Google Scholar 

  • Avise J (2000) Phylogeography. Harvard University Press, Cambridge, Mass., USA

  • Baco A, Smith C, Peek A, Roderick G, Vrijenhoek R (1999) The phylogenetic relationships of whale-fall vesicomyid clams based on mitochondrial CO1 DNA sequences. Mar Ecol Prog Ser 182:137–147

    Google Scholar 

  • Bert T (1986) Speciation in western Atlantic stone crabs (genus Menippe): the role of geological processes and climatic events in the formation and distribution of species. Mar Biol 93:157–170

    Google Scholar 

  • Brown B, Smouse P, Epifania J, Kobak C (1999) Mitochondrial DNA mixed-stock analysis of American shad: coastal harvests are dynamic and variable. Trans Am Fish Soc 128:977–994

    Article  Google Scholar 

  • Buroker N (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 

  • Castagna M, Kraeuter J (1994) Age, growth rate, sexual dimorphism and fecundity of knobbed whelk Busycon carica (Gmelin, 1791) in a western mid-Atlantic lagoon system, Virginia. J Shellfish Res 13:581–585

    Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation, procedures. Evolution 21:550–570

    Google Scholar 

  • Clayton JW, Tretiak DN (1972) Amine-citrate buffers for pH control in starch gel electrophoresis. J Fish Res Board Can 29:1169–1172

    CAS  Google Scholar 

  • Collin R (2000) Phylogeny of the Crepidula plana (Gastropoda: Calyptraeidae) cryptic species complex in North America. Can J Zool 78:1500–1514

    Article  Google Scholar 

  • Conrad T (1840) Fossils of the medial tertiary of the United States, part I. Privately published, Philadelphia

  • Conrad T (1845) Descriptions of eight new fossil shells of the United States. Proc Acad Natl Sci USA 2:173–175

    Google Scholar 

  • Dayan N, Dillon Jr RT (1995) Florida as a biogeographic boundary: evidence from the population genetics of Littorina irrorata. Nautilus 108:49–54

    Google Scholar 

  • Dillon Jr RT (1985) Correspondence between the buffer systems suitable for electrophoretic resolution of bivalve and gastropod isozymes. Comp Biochem Physiol B Comp Biochem 82:643–645

    Article  Google Scholar 

  • Dillon Jr RT (1992) Electrophoresis IV, nuts and bolts. J World Aquac Soc 23:48–51

    Google Scholar 

  • Dillon Jr RT, Manzi J (1987) Hard clam (Mercenaria mercenaria) broodstocks: genetic drift and loss of rare alleles without reduction in heterozygosity. Aquaculture 60:99–105

    Article  Google Scholar 

  • Dillon Jr RT, Manzi J (1989a) Genetics and shell morphology in a hybrid zone between the hard clams Mercenaria mercenaria and M. campechiensis. Mar Biol 100:217–222

    Google Scholar 

  • Dillon Jr RT, Manzi J (1989b) Genetics and shell morphology of hard clams (Mercenaria) from Laguna Madre, Texas. Nautilus 103:73–77

    Google Scholar 

  • Dillon Jr RT, Manzi J (1992) Population genetics of the hard clam, Mercenaria mercenaria, at the northern limit of its range. Can J Fish Aquat Sci. 49:2574–2578

    Google Scholar 

  • Duggins C, Karlin AA, Mousseau T, Relyea K (1995) Analysis of a hybrid zone in Fundulus majalis in a northeastern Florida ecotone. Heredity 74:117–128

    Google Scholar 

  • Edwards A (1988) Latitudinal clines in shell morphologies of Busycon carica (Gmelin, 1791). J Shellfish Res 7:461–466

    Google Scholar 

  • Edwards A, Humphrey C (1981) An electrophoretic and morphological survey of Busycon occurring in Wassaw Sound, Georgia. Nautilus 95:144–150

    Google Scholar 

  • Felder D, Staton J (1994) Genetic differentiation in trans-Floridian species complexes of Sesarma and Uca (Decapoda: Brachyura). J Crustac Biol 14:191–209

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Freshwater D, Khyn-Hansen C, Sarver S, Walsh P (2000) Phylogeny of Opsanus spp. (Batrachiodidae) inferred from multiple mitochondrial-DNA sequences. Mar Biol 136:961–968

    Article  CAS  Google Scholar 

  • Geller J, Carlton J, Powers D (1993) Interspecific and intrapopulation variation in mitochondrial ribosomal DNA sequences of Mytilus spp. (Bivalvia: Mollusca). Mol Mar Biol Biotechnol 2:44–50

    CAS  PubMed  Google Scholar 

  • Grabau A (1903) Studies of Gastropoda. II. Fulgur and Sycotypus. Am Nat. 36:917–945

  • Harasewych MG, Adamkewicz S, Blake J, Saudek D, Spriggs T, Bult C (1997a) Phylogeny and relationships of pleurotomariid gastropods (Mollusca: Gastropoda): an assessment based on partial 18S rDNA and cytochrome c oxidase I sequences. Mol Mar Biol Biotechnol 6:1–20

    CAS  PubMed  Google Scholar 

  • Harasewych MG, Adamkewicz SL, Blake JA, Saudek D, Spriggs T, Bult CJ (1997b) Neogastropod phylogeny: a molecular perspective. J Molluscan Stud 63:327–351

    Google Scholar 

  • Hare M, Avise J (1996) Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305–2315

    Google Scholar 

  • Herke S, Foltz D (2002) Phylogeography of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Mar Biol 140:103–115

    Article  CAS  Google Scholar 

  • Hollister S (1958) A review of the genus Busycon and its allies, part I. Paleontogr Am 4:59–126

    Google Scholar 

  • Jozefowicz C, O’Foighil D (1998) Phylogenetic analysis of southern hemisphere flat oysters based on partial mitochondrial 16 s rDNA gene sequences. Mol Phylogenet Evol 10:426–435

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kent B (1983) An overlooked Busycon whelk (Melongenidae) from the eastern United States. Nautilus 96:99–104

    Google Scholar 

  • Lankford T, Target T, Gaffney P (1999) Mitochondrial DNA analysis of population structure in the Atlantic croaker, Micropogonias undulatus (Perciformes: Sciaenidae). Fish Bull (Wash DC) 97:884–890

    Google Scholar 

  • Leidy J (1889) Remarks on the nature of organic species. Trans Wagner Free Inst Sci 2:51–53

    Google Scholar 

  • McClure M, Greenbaum I (2000) Allozymic variation and biogeography of snapping shrimp (Alpheus) from the Gulf of Mexico and northwestern Atlantic coasts. Southwest Nat 44:462–469

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • O’Foighil D, Gaffney P, Hilbish T (1995) Differences in mitochondrial 16S ribosomal gene sequences allow discrimination among American [Crassostrea virginica (Gmelin)] and Asian [C. gigas (Thunberg), C. ariakensis Wakiya] oyster species. J Exp Mar Biol Ecol 192:211–220

    Article  Google Scholar 

  • O’Foighil D, Hilbish T, Showman R (1996) Mitochondrial gene variation in Mercenaria clam sibling species reveals a relict secondary contact zone in the western Gulf of Mexico. Mar Biol 126:675–683

    Google Scholar 

  • O’Foighil D, Gaffney P, Wilbur A, Hilbish T (1998) Mitochondrial cytochrome oxidase I gene sequences support an Asian origin for the Portuguese oyster Crassostrea angulata. Mar Biol 131:497–503

    Article  Google Scholar 

  • Petuch E (1994) Atlas of Florida fossil shells (Pliocene and Pleistocene marine gastropods). Chicago Spectrum Press and Graves Museum of Archaeology and Natural History, Chicago

  • Petuch EJ (2003) Cenozoic seas: the view from eastern North America. CRC Press, Boca Raton, Fla., USA

    Google Scholar 

  • Poulik M (1957) Starch gel electrophoresis in a discontinuous system of buffers. Nature 180:1477–1479

    CAS  PubMed  Google Scholar 

  • Puffer E, Emerson W (1954) Catalogue and notes on the gastropod genus Busycon. Proc Biol Soc Wash 67:115–147

    Google Scholar 

  • Pulley T (1959) Busycon perversum (L) and some related species. Rice Inst Pam 46:70–89

    Google Scholar 

  • Sarver S, Landrum M, Foltz D (1992) Genetics and taxonomy of ribbed mussels (Geukensia spp.). Mar Biol 113:385–390

    Google Scholar 

  • Scheltema R (1989) Planktonic and non-planktonic development among prosobranch gastropods and its relationship to the geographic range of species. In: Ryland J, Taylor P (eds) Reproduction, genetics and distributions of marine organisms. Olsen and Olsen, Fredensberg, Denmark, pp 183–188

  • Schultze S, Rice S, Simon J, Karl S (2000) Evolution of poecilogony and the biogeography of North American populations of the polychaete Streblospio. Evolution 54:1247–1259

    PubMed  Google Scholar 

  • Seyoum S, Tringali M, Bert T, McElroy D, Stokes R (2000) An analysis of genetic population structure in red drum, Sciaenops ocellatus, based on mtDNA control region sequences. Fish Bull (Wash DC) 98:127–138

    Google Scholar 

  • Shaw CR, Prasad R (1970) Starch gel electrophoresis of enzymes—a compilation of recipes. Biochem Genet 4:297–320

    CAS  PubMed  Google Scholar 

  • Simison W, Lindberg D (1999) Morphological and molecular resolution of a putative cryptic species complex: a case study of Notoacmea fascicularis (Menke, 1851) (Gastropoda: Patellogastropoda). J Molluscan Stud 65:99–109

    Article  Google Scholar 

  • Smith B (1939) Type specimen of Busycon perversum (Murex perversus Linné). Nautilus 53:23–26

    Google Scholar 

  • Swofford D (1998) PAUP, phylogenetic analysis using parsimony, version 4.0b10. Sinauer, Sunderland, Mass., USA

  • Swofford DL, Selander RB (1981) BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. J Hered 72:281–283

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties, weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Vermeij G (1987) Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J., USA

    Google Scholar 

  • Weins J, Servedio M (1998) Phylogenetic analysis and intraspecific variation: performance of parsimony, likelihood, and distance methods. Syst Biol 47:228–253

    Article  PubMed  Google Scholar 

  • Wilding C, Grahame J, Mill P (2000) Mitochondrial DNA COI haplotype variation in sibling species of rough periwinkles. Heredity 85:62–74

    Article  CAS  PubMed  Google Scholar 

  • Wilke T, Davis G (2000) Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): do their different life histories affect biogeographic patterns and gene flow? Biol J Linn Soc. 70:89–105

    Google Scholar 

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Acknowledgements

For help with obtaining whelks we thank B. Anderson, D. Barges, G. Boone, W. Frank, J. Gault, R. Haggerty, D. Ingral, J. Leal, H. Lee, H. Murphy, J. Nace, H. Nash, Patricio of Celestun, H. and F. White, P. Williams, M. Yianopolous. Laboratory assistance was provided by H. Agger, R. Adams, M. Adams, B. McClintock, D. McMillan, and R. Rowe. Illustrations of sinistral whelks were drawn by S. Ryan. We thank M. Rice, S. Reed and the Smithsonian Station at Fort Pierce for hosting us in Florida. This is Smithsonian Marine Station at Fort Pierce contribution number 558. This paper is dedicated to Constance E. Boone for her many years of devotion to teaching others about mollusks. The research was supported by the Sterling Turner Research Grant, Houston Museum of Natural Science, Houston, Texas and the Visiting Scientist Award, Smithsonian Marine Station at Fort Pierce to J.W. and M.G.H.

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Correspondence to J. Wise.

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Communicated by J.P. Grassle, New Brunswick

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Wise, J., Harasewych, M.G. & Dillon, R.T. Population divergence in the sinistral whelks of North America, with special reference to the east Florida ecotone. Marine Biology 145, 1167–1179 (2004). https://doi.org/10.1007/s00227-004-1411-x

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