Marine Biology

, Volume 151, Issue 5, pp 1863–1873 | Cite as

Geographical subdivision, demographic history and gene flow in two sympatric species of intertidal snails, Nerita scabricosta and Nerita funiculata, from the tropical eastern Pacific

  • L. A. Hurtado
  • M. Frey
  • P. Gaube
  • E. Pfeiler
  • T. A. MarkowEmail author
Research Article


The patchy distribution of rocky intertidal communities in the tropical eastern Pacific (TEP) may impose severe constraints on the genetic connectivity among populations of marine invertebrates associated with this habitat. In this study, we analyzed a portion of the mitochondrial cytochrome c oxidase subunit I (COI) gene in two sympatric species of marine snails, Nerita scabricosta and Nerita funiculata, common inhabitants of the rocky intertidal from the Gulf of California (Sea of Cortez) and outer Pacific coast of the southern Baja California (Baja) peninsula to northern South America, to assess genetic connectivity among populations of each species. One of our aims was to determine whether the morphological, behavioral, and ecological differences observed among populations of both species throughout their range in the TEP corresponded to population genetic differences. In addition, we were interested in elucidating the demographic history of both species. We found no evidence of genetic structure throughout the Gulf of California and outer coast of the Baja peninsula region for either species. Comparisons between Gulf of California/Baja and Panama populations, however, showed significant genetic differentiation for N. scabricosta, but not for N. funiculata. The genetic differences between Mexican and Panamanian populations of N. scabricosta were consistent with previously reported ecological and behavioral differences for this species between these two distant regions. However, previously reported size differences between northern and central/southern Gulf of California individuals of N. scabricosta do not correspond with our findings of genetic connectivity among these populations. Results from neutrality tests (Tajima’s D and Fu’s FS), the mismatch distribution, and Bayesian skyline analyses suggested that both species have experienced dramatic population expansions dating to the Pleistocene.


Mismatch Distribution Genetic Connectivity Population Genetic Differentiation Pairwise Sequence Divergence Tropical Eastern Pacific 
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.



We thank Mariana Mateos, Rick Grosberg, Geerat Vermeij, and Wain Evans for their helpful suggestions on the manuscript and/or study, and M. Mateos and Harilaos Lessios for collecting specimens. This study was supported by National Science Foundation grants HR-0123325, DEB-9510645 and DEB-0346773 to T.A. Markow and IBN-0416713 to R. Grosberg, and a grant of the Andrew W. Mellon Foundation to R. Grosberg.


  1. Alvarez-Borrego S (2002) Physical oceanography. In: Case TJ, Cody ML, Ezcurra E (eds) A new island biogeography of the Sea of Cortes. Oxford University Press, New York, pp 41–59Google Scholar
  2. Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504CrossRefGoogle Scholar
  3. Arnaud S, Monteforte M, Galtier N, Bonhomme F, Blanc F (2000) Population structure and genetic variability of pearl oyster Pinctada mazatlanica along Pacific coasts from Mexico to Panama. Conserv Genet 1:299–307CrossRefGoogle Scholar
  4. Aubert H, Lightner DV (2000) Identification of genetic populations of the Pacific blue shrimp Penaeus stylirostris of the Gulf of California, Mexico. Mar Biol 137:875–885CrossRefGoogle Scholar
  5. Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57:1599–1609CrossRefGoogle Scholar
  6. Bertness MD, Garrity SD, Levings SC (1981) Predation pressure and gastropod foraging: a temperate-tropical comparison. Evolution 35:995–1007CrossRefGoogle Scholar
  7. Bovbjerg RV (1984) Habitat selection in two intertidal snails, genus Nerita. Bull Mar Sci 34:185–196Google Scholar
  8. Briggs JC (1974) Marine zoogeography. McGraw-Hill, New YorkGoogle Scholar
  9. Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91: 6491–6495CrossRefGoogle Scholar
  10. Brusca RC (1980) Common intertidal invertebrates of the Gulf of California, 2nd edn. University of Arizona Press, TucsonGoogle Scholar
  11. Brusca RC, Brusca GJ (2003) Invertebrates. Sinauer Associates, SunderlandGoogle Scholar
  12. Calderón-Aguilera LE, Marinone SG, Aragón-Noriega EA (2003) Influence of oceanographic processes on the early life stages of the blue shrimp (Litopenaeus stylirostris) in the Upper Gulf of California. J Mar Syst 39:117–128CrossRefGoogle Scholar
  13. Castro R, Mascarenhas AS, Durazo R, Collins CA (2000) Seasonal variation of the temperature and salinity at the entrance to the Gulf of California, Mexico. Ciencias Marinas 26:561–583CrossRefGoogle Scholar
  14. Correa-Sandoval F, Carvacho-Bravo A (1992) Efecto de la “Barrera de las Islas” en la distribución de los braquiuros (Crustacea: Decapoda) en el Golfo de California. Proc San Diego Soc Nat Hist 26: 1–4Google Scholar
  15. Cushman JH (1989) Vertical size gradients and migratory patterns of two Nerita species in the northern Gulf of California. The Veliger 32:147–151Google Scholar
  16. de la Rosa-Vélez J, Escobar-Fernández R, Correa F, Maqueda-Cornejo M, de la Torre-Cueto J (2000) Genetic structure of two commercial penaeids (Penaeus californiensis and P. stylirostris) from the Gulf of California, as revealed by allozyme variation. Fish Bull (Wash DC) 98: 674–683Google Scholar
  17. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185–1192CrossRefGoogle Scholar
  18. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50CrossRefGoogle Scholar
  20. 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 Biotech 3:294–299Google Scholar
  21. Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925PubMedPubMedCentralGoogle Scholar
  22. Garrity SD, Levings SC (1981) A predator–prey interaction between two physically and biologically constrained tropical rocky shore gastropods: direct, indirect and community effects. Ecol Monogr 51:267–286CrossRefGoogle Scholar
  23. Grosberg RK, Cunningham CW (2001) Genetic structure in the sea: from populations to communities. In: Bertness MD, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 61–84Google Scholar
  24. Gutiérrez OQ, Marinone SG, Parés-Sierra A (2004) Lagrangian surface circulation in the Gulf of California from a 3D numerical model. Deep Sea Res Part II- Top Stud Oceanogr 51:659–672CrossRefGoogle Scholar
  25. Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedPubMedCentralGoogle Scholar
  26. Hastings PA (2000) Biogeography of the tropical eastern Pacific: distribution and phylogeny of chaenopsid fishes. Zool J Linnean Soc 128:319–335CrossRefGoogle Scholar
  27. Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysine cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848CrossRefGoogle Scholar
  28. Helenes J, Carreño AL (1999) Neogene sedimentary evolution of Baja California in relation to regional tectonics. J South Am Earth Sci 12:589–605CrossRefGoogle Scholar
  29. Houston RS (1980) Mollusca. In: Brusca RC (ed) Common intertidal invertebrates of the Gulf of California, 2nd edn. The University of Arizona Press, Tucson, pp 130–204Google Scholar
  30. Houston RS (1990) Reproductive systems of neritimorph archeogastropods from the eastern Pacific, with special reference to Nerita funiculata Menke, 1851. The Veliger 33:103–110Google Scholar
  31. Huang D, Bernardi G (2001) Disjunct Sea of Cortez-Pacific Ocean Gillichthys mirabilis populations and the evolutionary origin of their Sea of Cortez endemic relative, Gillichthys seta. Mar Biol 138:421–428CrossRefGoogle Scholar
  32. Hurtado LA, Mateos M, Lutz RA, Vrijenhoek RC (2003) Coupling of bacterial endosymbiont and mitochondrial genes in the hydrothermal vent clam Calyptogena magnifica. Appl Environ Microbiol 69: 2058–2064CrossRefGoogle Scholar
  33. Hurtado LA, Lutz RA, Vrijenhoek RC (2004) Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents. Mol Ecol 13: 2603–2615CrossRefGoogle Scholar
  34. Keen AM (1971) Sea shells of tropical west America; marine mollusks from Baja California to Peru. Stanford University Press, StanfordGoogle Scholar
  35. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  36. Knowlton N, Weigt LA, Solórzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260:1629–1632CrossRefGoogle Scholar
  37. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163CrossRefGoogle Scholar
  38. Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57: 2026–2036CrossRefGoogle Scholar
  39. Levings SC, Garrity SD (1983) Diel and tidal movement of two co-occurring neritid snails: differences in grazing patterns on a tropical rocky shore. J Exp Mar Biol Ecol 67:261–278CrossRefGoogle Scholar
  40. Lewis JB (1960) The fauna of rocky shores of Barbados, West Indies. Can J Zool 38:391–435CrossRefGoogle Scholar
  41. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  42. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  43. Passamonti M, Scali V (2001) Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca Bivalvia). Curr Genet 39:117–124CrossRefGoogle Scholar
  44. Pfeiler E, Hurtado LA, Knowles LL, Torre-Cosío J, Bourillón-Moreno L, Márquez-Farías JF, Montemayor-López G (2005) Population genetics of the swimming crab Callinectes bellicosus (Brachyura: Portunidae) from the eastern Pacific Ocean. Mar Biol 146:559–569CrossRefGoogle Scholar
  45. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  46. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86CrossRefGoogle Scholar
  47. Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contribution of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453CrossRefGoogle Scholar
  48. Riginos C, Victor BC (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proc R Soc Lond B 268:1931–1936CrossRefGoogle Scholar
  49. Sandoval-Castillo J, Rocha-Olivares A, Villavicencio-Garayzar C, Balart E (2004) Cryptic isolation of Gulf of California shovelnose guitarfish evidenced by mitochondrial DNA. Mar Biol 145:983–988CrossRefGoogle Scholar
  50. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152: 1079–1089PubMedPubMedCentralGoogle Scholar
  51. Soulé JD (1960) The distributions and affinities of the littoral marine Bryozoa (Ectoprocta). Symposium on the biogeography of Baja California and adjacent seas. Part II. Mar Biotas Syst Zool 9:100–104CrossRefGoogle Scholar
  52. Stepien CA, Rosenblatt RH, Bargmeyer BA (2001) Phylogeography of the spotted sand bass, Paralabrax maculatofasciatus: divergence of Gulf of California and Pacific Coast populations. Evolution 55: 1852–1862CrossRefGoogle Scholar
  53. Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
  54. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  55. Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465PubMedPubMedCentralGoogle Scholar
  56. Terry A, Bucciarelli G, Bernardi G (2000) Restricted gene flow and incipient speciation in disjunct Pacific Ocean and Sea of Cortez populations of a reef fish species, Girella nigricans. Evolution 54:652–659CrossRefGoogle Scholar
  57. Thomson DA, Findley LT, Kerstitch AN (2000) Reef fishes of the Sea of Cortez. The University of Texas Press, AustinGoogle Scholar
  58. Vermeij GJ (2001) Distribution, history, and taxonomy of the Thais clade (Gastropoda: Muricidae) in the Neogene of tropical America. J Paleontol 75:697–705CrossRefGoogle Scholar
  59. Walker BW (1960) The distributions and affinities of the marine fish fauna of the Gulf of California. Symposium on the biogeography of Baja California and adjacent seas. Part II. Mar Biotas Syst Zool 9:123–133CrossRefGoogle Scholar
  60. Waters JM, King TM, O’Loughlin PM, Spencer HG (2005) Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Mol Ecol 14:2789–2802CrossRefGoogle Scholar
  61. Zouros E, Ball AO, Saavedra C, Freeman KR (1994) An unusual mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • L. A. Hurtado
    • 1
    • 4
  • M. Frey
    • 2
  • P. Gaube
    • 1
  • E. Pfeiler
    • 3
  • T. A. Markow
    • 1
    Email author
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Center for Population Biology, Section of Evolution and EcologyUniversity of California DavisDavisUSA
  3. 3.Centro de Investigación en Alimentación y Desarrollo, A.C.Unidad GuaymasSonoraMexico
  4. 4.Department of Wildlife and Fisheries SciencesTexas A&M UniversityCollege StationUSA

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