Abstract
The northern Gulf of California (NGC) is one of the most dynamic and productive marine ecosystems in the world, yet knowledge about population connectivity and dispersal patterns is lacking for many of its resident species. Using nuclear and mitochondrial markers, we investigated the effects of open water, geographical distance and suitable habitat on patterns of genetic structure of Solenosteira macrospira, a benthic buccinid whelk with direct development. We collected samples in April 2004, 2005 and May 2007 from the upper NGC (31°34.39″N, 114°44.45″W). Phylogenetic analyses, hierarchical analyses of variance and Bayesian assignment tests substantiated a break between the east and west coasts. Genetic distance between population pairs increased with geographical distance, but only when assuming a U-shaped dispersal pathway over the open water of the NGC. Given S. macrospira’s association with rocky intertidal habitats, and its limited dispersal potential, we assumed that the geographical distribution of rocky habitat would play a significant role in genetic differentiation of S. macrospira. Nevertheless, populations separated by sand were more similar than populations separated by rocks. The influence of open water, geographical distance and suitable habitat (rocks vs. sand) also varied significantly across different genetic markers that presumably evolve at different rates. Specifically, the more rapidly evolving nuclear microsatellites suggested that physical transport processes strongly influence genetic differentiation on contemporary time scales, even in a species with direct benthic development. This underscores the strong, and potentially homogenizing, effect of present-day ocean circulation patterns in the NGC.
Similar content being viewed by others
References
Armour JAL, Neumann R, Gobert S, Jefferys AJ (1994) Isolation of human simple repeat loci by hybridization selection. Hum Mol Genet 3:599–605
Ayre DJ, Minchinton TE, Perrin C (2009) Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Mol Ecol 18:1887–1903
Aznar CV, Leslie H, Sievanen L (2010) Artisanal fisheries of the northern Gulf of California, Mexico: Environment and Society Project (PANGAS). Duke University/Brown University, Beaufort NC/Providence RI
Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evolution 57:1599–1609
Billot C, Engel CR, Rousvoal S, Kloareg B, Valero M (2003) Current patterns, habitat discontinuities and population genetic structure: the case of the kelp Laminaria digitata in the English Channel. Mar Ecol Prog Ser 253:111–121
Bishop JDD (1998) Fertilization in the sea: are the hazards of broadcast spawning avoided when free-spawned sperm fertilize retained eggs? Proc R Soc Lond B 265:725–731
Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45
Briggs JC (1974) Marine zoogeography. McGraw-Hill, New York
Brusca CR (2004) The Gulf of California—an overview. In: Brusca CR, Kimrey E, Moore W (eds) A seashore guide to the northern Gulf of California. Arizona-Sonora Desert Museum, Tucson
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Carrillo-Bribiezca LE, Lavín MF, Palacios-Hernández E (2002) Seasonal evolution of the geostrophic circulation in the northern Gulf of California. Estuar Coast Shelf S 54:157–173
Cisneros-Mata MA (2004) Sustainability and complexity: from fisheries management to conservation of species, communities and spaces in the Sea of Cortez. In: Brusca CR, Kimrey E, Moore W (eds) A seashore guide to the northern Gulf of California. Arizona-Sonora Desert Museum, Tucson
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Ann Rev Mar Sci 1:443–466
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Cudney-Bueno R, Lavin MF, Marinone SG, Raimondi PT, Shaw W (2009) Rapid effects of marine reserves via larval dispersal. PLoS one 4:e4140
Dawson MN, Grosberg RK, Botsford LW (2006) Connectivity in marine protected areas. Science 313:43–44
Deng QME, Hazel W (2010) 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
Doellman MM, Trussell GC, Grahame JW, Vollmer SV (2011) Phylogeographic analysis reveals a deep lineage split within North Atlantic Littorina saxatilis. Proc R Soc Lond B 278:3175–3183
Donald KM, Kennedy M, Spencer HG (2005) Cladogenesis as the result of long-distance rafting events in South Pacific topshells (Gastropoda, Trochidae). Evolution 59:1701–1711
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Ezcurra EL, Bourillio´n, Cantu A, Elena M, Robles A (2002) Ecological conservation. In: Case TJ, Cody ML, Ezcurra E (eds) A new island biogeography in the Sea of Cortez. Oxford University Press, Oxford, pp 417–444
Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record—influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642
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 3:294–299
Galindo-Becti MS, Noriega EAA, Hernandez-Ayon JM, Lavin MF, Diaz MAH, Hinojosa FD, Zavala JAS (2010) Distribution of penaeid shrimp larvae and postlarvae in the upper Gulf of California. Crustaceana 83:809–819
Garrick RC, Nason JD, Meadows CA, Dyer RJ (2009) Not just vicariance: phylogeography of a Sonoran Desert euphorb indicates a major role of range expansion along the Baja peninsula. Mol Ecol 18:1916–1931
Gautschi B, Tenzer IJP, Muller JP, Schmid B (2000a) Isolation and characterization of microsatellite loci in the bearded vulture (Gypaetus barbatus) and cross-amplification in three old world vulture species. Mol Ecol 9:2193–2195
Gautschi B, Widmer A, Koella J (2000b) Isolation and characterization of microsatellite loci in the dice snake (Natrix tessellate). Mol Ecol 9:2191–2193
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Grosberg RK (1991) Sperm-mediated gene flow and the genetic structure of a population of the colonial ascidian Botryllus schlosseri. Evolution 45:130–142
Grosberg RK, Levitan DR, Cameron BB (1996) Evolutionary genetics of allorecognition in the colonial hydroid Hydractinia symbiolongicarpus. Evolution 50:2221–2240
Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48:1829–1854
Hellberg ME (1995) Stepping stone gene flow in the solitary coral Balanophyllia elegans—equilibrium and nonequilibrium at different spatial scales. Mar Biol 123:573–581
Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50:1167–1175
Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Ann Rev Ecol Evol Syst 40:291–310
Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848
Helmuth B, Veit RR, Holberton R (1994) Long-distance dispersal of a sub-Antarctic brooding bivalve (Gaimardia trapesina) by kelp rafting. Mar Biol 120:421–426
Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790
Houston RS (1978) Notes on the spawning and egg capsules of two prosobranch gastropods: Nassarius tiarula (Kiener, 1841) and Solenosteira macrospira (Berry, 1957). Veliger 20: 367–368
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
Hurtado LA, Mateos M, Santamaria CA (2010) Phylogeography of supralittoral rocky intertidal Ligia isopods in the pacific region from central California to central Mexico. PLoS ONE 5:e11633
IUCN (2005) Islands and protected areas of the Gulf of California (Mexico). IUCN, Gland
Johannesson K (1988) The paradox of Rockall: why is a brooding gastropod (Littorina saxatilis) more widespread than one having a planktonic larval dispersal stage (L. littorea)? Mar Biol 99:507–513
Johannesson K, Warmoes T (1990) Rapid colonization of Belgian breakwaters by the direct developer, Littorina saxatilis (Olivi) (Prosobranchia, Mollusca). Hydrobiologia 193: 99–108
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13
Johansson ML, Banks MA, Glunt KD, Hassel-Finnegan HM, Buonaccorsi VP (2008) Influence of habitat discontinuity, geographical distance, and oceanography on fine-scale population genetic structure of copper rockfish (Sebastes caurinus). Mol Ecol Notes 17:3051–3061
Kamel SJ, Grosberg RK (2012) Exclusive male care despite extreme female promiscuity and low paternity in a marine snail. Ecol Lett 15:1167–1173
Kinlan BP, Gaines SD (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020
Knowlton N, Weigt LA, Solorzano LA, Mills DK, Bermingham E (1993) Divergence in proteins, mitochondrial DNA, and reproductive compatibility across the Isthmus of Panama. Science 260:1629–1632
Kyle CJ, Boulding EG (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845
Lester SE, Ruttenberg BI, Gaines SD, Kinlan BP (2007) The relationship between dispersal ability and geographic range size. Ecol Lett 10:745–758
Lourie SA, Green DM, Vincent ACJ (2005) Dispersal, habitat differences, and comparative phylogeography of Southeast Asian seahorses (Syngnathidae hippocampus). Mol Ecol 14:1073–1094
Manly BFJ (1997) RT, A program for Randomization Testing V 2.1. Western EcoSystems Technology Inc, Cheyenne
Marinone SG, Ulloa MJ, Pares-Sierra A, Lavin MF, Cudney-Bueno R (2008) Connectivity in the northern Gulf of California from particle tracking in a three-dimensional numerical model. J Mar Syst 71:149–158
Marinone SG, Lavin MF, Pares-Sierra A (2011) A quantitative characterization of the seasonal Lagrangian circulation of the Gulf of California from a three-dimensional numerical model. Cont Shelf Res 31:1420–1426
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
Marko PB, Hart MW (2011) The complex analytical landscape of gene flow inference. Trends Ecol Evol 26:448–456
Martel A (1993) Dispersal and recruitment of zebra mussels (Dreissena polymorpha) in a near-shore area in west central Lake Erie: the significance of post-metamorphic drifting. Can J Fish Aquat Sci 50:3–12
Miranda L, Thiel M (2008) Active and passive migration in boring isopods Limnoria spp. (Crustacea, Peracarida) from kelp holdfasts. J Sea Res 60:176–183
Morgan SG, Fisher JL, Miller SH, McAfee ST, Largier JL (2009) Nearshore larval retention in a region of strong upwelling and recruitment limitation. Ecology 90:3489–3502
Ortlieb L (1981) Pleistocene interglacial high stands of sea level in the Gulf of California area: Geological Society of America Abstracts with Programs 13:99
Ortlieb L (1984) Pleistocene high stand of sea level and vertical movements in the Gulf of California area. In: Malpica-Cruz V, Celis-Gutierrez S, Guerrero-Garcfa J, Ortlieb L (eds) Neotectonic and sea level variations in the Gulf of California Area, a symposium. Universidad Nacional Autónoma de Mexico, Instituto de Geologia, Hermosillo, Mexico, pp 131–132
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
Panova M, Blakeslee AMH, Miller AW, Mäkinen T, Ruiz GM, Johannesson K, André C (2011) Glacial history of the North Atlantic marine snail, Littorina saxatilis, inferred from distribution of mitochondrial DNA Lineages. PLoS one 6:e17511
Perrin C, Borsa P (2001) Mitochondrial DNA analysis of the geographic structure of Indian scad mackerel in the Indo-Malay archipelago. J Fish Biol 59:1421–1426
Pinsky ML, Palumbi SR, Andrefouet S, Purkis SJ (2012) Open and closed seascapes: where does habitat patchiness create populations with high fractions of self-recruitment? Ecol Appl 22:1257–1267
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (Version 1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Riginos C (2005) Cryptic vicariance in Gulf of California fishes parallels vicariant patterns found in Baja California mammals and reptiles. Evolution 59:2678–2690
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
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Schulze SR, Rice S, Simon JL, Karl SA (2000) Evolution of poecilogony and the biogeography of North American populations of the polychaete Streblospio. Evolution 54:1247–1259
Selkoe KA, Watson JR, White C, Horin TB, Iacchei M, Mitarai S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol 19:3708–3726
Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385
Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47:264–279
Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Thiel M, Haye PA (2006) The ecology of rafting in the marine environment. III. Biogeographical and evolutionary consequences. Oceanography and Marine Biology—an annual review. CRC Press, Taylor and Francis Group, Boca Raton, pp 323–429
Thorrold SR, Jones GP, Hellberg ME, Burton RS, Swearer SE, Neigel JE, Morgan SG, Warner RR (2002) Quantifying larval retention and connectivity in marine populations with artificial and natural markers. Bull Mar Sci 70:291–308
Toonen RJ, Hughes S (2001) Increased throughput for fragment analysis on an ABI 377 automated sequencer using a 100-lane RapidLoad membrane comb and STRand software. Biotechniques 31(31):1320–1324
Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469
Waters JM, Roy MS (2004) Out of Africa: the slow train to Australasia. Syst Biol 53:18–24
Weaver AJ, Saenko OA, Clark PU, Mitrovica JX (2003) Meltwater pulse 1A from Antarctica as a trigger of the Bølling-Allerød warm interval. Science 299:1709–1713
Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12
Winston JE (2012) Dispersal in marine organisms without a pelagic larval phase. Integr Comp Biol 52:447–457
Worcester SE (1994) Adult rafting versus larval swimming—dispersal and recruitment of a Botryllid ascidian on eelgrass. Mar Biol 121:309–317
Wright S (1943) Isolation by distance. Genetics 28:114
Yund PO (1995) Gene flow via the dispersal of fertilizing sperm in a colonial ascidian (Botryllus schlosseri)—the effect of male density. Mar Biol 122:649–654
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Uthicke.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kamel, S.J., Grosberg, R.K. & Addison, J.A. Multiscale patterns of genetic structure in a marine snail (Solenosteira macrospira) without pelagic dispersal. Mar Biol 161, 1603–1614 (2014). https://doi.org/10.1007/s00227-014-2444-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2444-4