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Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California

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Abstract

Using sequence variation in the mitochondrial cytochrome oxidase I locus, we estimated the population structure and phylogeography of the intertidal acorn barnacle, Chthamalus anisopoma, and its gastropod predator, Mexacanthina lugubris angelica. Both are endemic to the Gulf of California, being derived from taxa on the Pacific coast of the Baja peninsula, and both exhibit phenotypic plasticity for traits affecting their coevolutionary interactions. Consistent with expectations based on differences in dispersal, C. anisopoma populations generally lack geographic structure, while those of M. l. angelica are more strongly structured. However, the variable degree of differentiation in both species suggests that the extent of reciprocal selection and local adaptation in the species will vary geographically, a result consistent with the concept of a geographic mosaic of coevolution. The pattern of variation in C. anisopoma shows clear evidence of recent spatial expansion, possibly due to increased habitat availability following the last glacial maximum. Phylogeographic analyses suggest that M. l. angelica diversified into three distinct clades after the colonization of the Gulf. Overall, our results illustrate how dispersal potential, geological and climatic events, and recent population growth have impacted the pattern of sequence variation in the two species.

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References

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Avise J (2004) Molecular markers, natural history, and evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Barragán RRM, Birkle P, Portugal ME, Arellano GVM, Alvarez RJ (2001) Geochemical survey of medium temperature geothermal resources from the Baja California Peninsula and Sonora, México. J Volcanol Geotherm Res 110:101–119

    Article  Google Scholar 

  • Brusca RC (1980) Common intertidal invertebrates of the Gulf of California. University of Arizona Press, Tucson

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864

    Article  CAS  PubMed  Google Scholar 

  • Excoffier LLG, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinform Online 1:47–50

    CAS  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 5:294–299

    Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  Google Scholar 

  • Hairston NG, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127

    Article  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial-DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Hazel WN, Smock R, Johnson MD (1990) A polygenic model for the evolution and maintenance of conditional strategies. Proc R Soc Lond Ser B-Biol Sci 242:181–187

    Article  CAS  Google Scholar 

  • Hazel W, Smock R, Lively CM (2004) The ecological genetics of conditional strategies. Am Nat 163:888–900

    Article  PubMed  Google Scholar 

  • Hoekstra HE, Drumm KE, Nachman MW (2004) Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 58:1329–1341

    CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:554–555

    Article  Google Scholar 

  • Hurtado LA, Frey M, Gaube P, Pfeiler E, Markow TA (2007) Geographical subdivision, demographic history and gene flow in two sympatric species of intertidal snails, Nerita scabricosta and Nerita funiculata, from the tropical eastern Pacific. Mar Biol 151:1863–1873

    Article  Google Scholar 

  • Lin HC, Sanchez-Ortiz C, Hastings PA (2009) Colour variation is incongruent with mitochondrial lineages: cryptic speciation and subsequent diversification in a Gulf of California reef fish (Teleostei: Blennioidei). Mol Ecol 18:2476–2488

    Article  CAS  PubMed  Google Scholar 

  • Lively CM (1986a) Canalization versus developmental conversion in a spatially-variable environment. Am Nat 128:561–572

    Article  Google Scholar 

  • Lively CM (1986b) Competition, comparative life histories, and maintenance of shell dimorphism in a barnacle. Ecology 67:858–864

    Article  Google Scholar 

  • Lively CM (1986c) Predator-induced shell dimorphism in the acorn barnacle Chthamalus anisopoma. Evolution 40:232–242

    Article  Google Scholar 

  • Lively CM, Hazel WN, Schellenberger MJ, Michelson KS (2000) Predator-induced defense: variation for inducibility in an intertidal barnacle. Ecology 81:1240–1247

    Article  Google Scholar 

  • Marinone SG (2003) A three-dimensional model of the mean and seasonal circulation of the Gulf of California. J Geophys Res Oceans 108

  • Marko PB (2004) ‘What’s larvae got to do with it?’ Disparate patterns of post-glacial population structure in two benthic marine gastropods with identical dispersal potential. Mol Ecol 13:597–611

    Article  CAS  PubMed  Google Scholar 

  • Marko PB, Vermeij GJ (1999) Molecular phylogenetics and the evolution of labral spines among eastern Pacific Ocenebrine gastropods. Mol Phylogenet Evol 13:275–288

    Article  CAS  PubMed  Google Scholar 

  • Marko PB, Palmer AR, Vermeij GJ (2003) Resurrection of Nucella ostrina (Gould, 1852), lectotype designation for N. emarginata (Deshayes, 1839), and molecular genetic evidence of Pleistocene speciation. Veliger 46:77–85

    Google Scholar 

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

    Google Scholar 

  • Oskin M, Stock J (2003a) Marine incursion synchronous with plate-boundary localization in the Gulf of California. Geology 31:23–26

    Article  Google Scholar 

  • Oskin M, Stock J (2003b) Pacific-north America plate motion and opening of the Upper Delfin Basin, northern Gulf of California, Mexico. Geol Soc Am Bull 115:1173–1190

    Article  Google Scholar 

  • Oskin M, Stock J, Martin-Barajas A (2001) Rapid localization of Pacific-North America plate motion in the Gulf of California. Geology 29:459–462

    Article  Google Scholar 

  • Pelc R, Warner R, Gaines S (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J Biogeogr 36:1881–1890

    Article  Google Scholar 

  • Pfeiler E, Hurtado LA, Knowles LL, Torre-Cosio J, Bourillon-Moreno L, Marquez-Farias JF, Montemayor-Lopez G (2005) Population genetics of the swimming crab Callinectes bellicosus (Brachyura : Portunidae) from the eastern Pacific Ocean. Mar Biol 146:559–569

    Article  Google Scholar 

  • Pitombo FB, Burton R (2007) Systematics and biogeography of Tropical Eastern Pacific Chthamalus with descriptions of two new species (Cirripedia, Thoracica). Zootaxa 1–30

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:2

    Article  Google Scholar 

  • Raimondi PT, Forde SE, Delph LF, Lively CM (2000) Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms. Oikos 91:353–361

    Article  Google Scholar 

  • Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86

    Article  CAS  PubMed  Google Scholar 

  • Ridenhour BJ, Brodie ED (2007) Patterns of genetic differentiation in Thamnophis and Taricha from the Pacific Northwest. J Biogeogr 34:724–735

    Article  Google Scholar 

  • Riginos C, Nachman MW (2001) Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus. Mol Ecol 10:1439–1453

    Article  CAS  PubMed  Google Scholar 

  • 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 Ser B-Biol Sci 268:1931–1936

    Article  CAS  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 

  • Sanford E, Roth MS, Johns GC, Wares JP, Somero GN (2003) Local selection and latitudinal variation in a marine predator-prey interaction. Science 300:1135–1137

    Article  CAS  PubMed  Google Scholar 

  • Siddall M, Rohling EJ, Almogi-Labin A, Hemleben C, Meischner D, Schmelzer I, Smeed DA (2003) Sea-level fluctuations during the last glacial cycle. Nature 423:853–858

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Slatkin M (1987) Gene flow and selection in a cline. Genetics 75:733–756

    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 

  • Slobodkin LB (1961) Growth and regulation of animal populations. Holt, Rinhart and WInston, New York

    Google Scholar 

  • Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecol Lett 8:448–459

    Article  Google Scholar 

  • Stock JM (2000) Relation of Puertocitos Volcanic Province, Baja California, Mexico, to development of the plate boundary in the Gulf of California. In: Delgado-Granados H, Aguirre-Ciaz G, Stock JM (eds) Cenozoic tectonics and volcanism of Mexico. Geological Society of America Special Paper 334, Boulder

    Google Scholar 

  • Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283

    Article  PubMed  Google Scholar 

  • Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, Robertson DR, Morgan SG, Selkoe KA, Ruiz GM, Warner RR (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer & Associates, Sunderland

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460

    CAS  PubMed  Google Scholar 

  • Tajima F (1989a) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tajima F (1996) The amount of DNA polymorphism maintained in a finite population when the neutral mutation rate varies among sites. Genetics 143:1457–1465

    CAS  PubMed  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Thompson JN (2009) The coevolving web of life. Am Nat 173:125–140

    Article  PubMed  Google Scholar 

  • Wares JP (2001) Patterns of speciation inferred from mitochondrial DNA in North American Chthamalus (Cirripedia : Balanomorpha : Chthamaloidea). Mol Phylogenet Evol 18:104–116

    Article  CAS  PubMed  Google Scholar 

  • Warner RR (1997) Evolutionary ecology: how to reconcile pelagic dispersal with local adaptation. Coral Reefs 16:S115–S120

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST[ne]1/(4Nm+1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Yensen NP (1979) The function of the labial spine and the effect of prey size on “switching” polymorphs and Acanthina angelica (Gastropoda: Thaididae). Ecol Evol Biol, Tucson

    Google Scholar 

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Acknowledgments

The research was supported by NSF grant DEB-0223089 and the DePauw University Faculty Development Program. M. Reeves, S. Timm, T. Pfister and M. Ziebell assisted with the collecting. Housing during the collection trips was provided by R. and T. Warren and the Kino Bay Center for Cultural and Ecological Studies. P. Evans and C. Fornari provided invaluable advice and assistance during the sequencing. J. Stock and M. Oskin assisted with the interpretation of the geology of the Gulf of California. Undergraduates in Hazel’s Bio 320 Genetics classes at DePauw University assisted in the some of the DNA extraction, sequencing and restriction digests. F. Pitombo and J. Wares verified our identification of C. southwardorum specimens. P. Marko provided advice on primers. B. Wilkerson, DePauw GIS coordinator constructed Figure 1. C. Riginos, J. Tomkins, M. Johnson and three anonymous reviewers provided comments that improved the manuscript. We thank them all.

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  1. Qiming E. Deng

    Present address: Department of Biological Chemistry, University of California, Los Angeles, 615 Charles E. Young Drive South, BSRB 547, Los Angeles, CA, 90095, USA

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  1. Department of Biology, Depauw University, Greencastle, IN, 46135, USA

    Qiming E. Deng & Wade Hazel

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  1. Qiming E. Deng
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Correspondence to Wade Hazel.

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Communicated by C. Riginos.

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Deng, Q.E., Hazel, W. Population structure and phylogeography of an acorn barnacle with induced defense and its gastropod predator in the Gulf of California. Mar Biol 157, 1989–2000 (2010). https://doi.org/10.1007/s00227-010-1468-7

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