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Population genetics of Collisella subrugosa (Patellogastropoda: Acmaeidae): evidence of two scales of population structure

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Abstract

Marine invertebrate populations usually show high levels of genetic variability that has frequently been associated with spatial and temporal environmental heterogeneity. One of the most heterogeneous marine environments is the intertidal zone, the habitat of Collisella subrugosa, the most widespread and abundant Brazilian limpet. C. subrugosa has planktonic larvae that can disperse over long distances, what can promote gene flow among shores, working against interpopulational differentiation. In this study we investigated the genetic variability and populational substructure of C. subrugosa through analysis of 24 allozyme loci in 14 samples (590 individuals) collected along 2,700 km of the Brazilian coast. The genetic variability was high (\( \bar {H}_{{\text{e}}} = 0.199 \) and \( \bar {H}_{{\text{o}}} {\text{ = 0}}{\text{.087}} \)), as expected for intertidal species. Genetic differentiation among samples was low (F ST = 0.03) what may reflect intensive gene flow associated with larval dispersal. However, we detected an isolation-by-distance pattern of population substructure in one sampled region. High levels of heterozygote deficiency were also observed for many loci in each sample. Alternative hypothesis are discussed, and the “breeding groups” is suggested to explain these pattern, indicating the main cause as environmental heterogeneity.

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References

  • Andrade SCS, Magalhães CA, Solferini VN (2003) Patterns of genetic variability in Brazilian Littorinids (Mollusca): a macrogeographic approach. J Zool Syst Evol Res 41: 249–255

    Article  Google Scholar 

  • Andrade SCS, Medeiros HF, Solferini VN (2005) Homogeneity test of Hardy-Weinberg deviations in Brazilian Littorinids: evidence for selection? J Molluscan Stud 71:167–174

    Article  Google Scholar 

  • Badino G, Sella G (1980) Phosphoglucose isomerase variability in sympatric populations of Mediterranean species of Patella (Gastropoda, Prosobranchiata). Mar Ecol-Prog Ser 2:315–320

    CAS  Google Scholar 

  • Beaumont AR, Wei JHC (1991) Morphological and genetic variation in the antarctic limpet Nacella concinna (Strebel, 1908). J Molluscan Stud 57:443–450

    Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2003) GENETIX, logiciel sous Windows TM pour la génétique des populations. Version 4.02. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • Berger EM (1983) Population genetics of marine gastropods and bivalves. In: edited by Academic Press, London

  • Black W, Krafsur E (1985) A FORTRAN program for analysis of genotypic frequencies and description of the breeding structure of populations. Theor Appl Genet 70:484–490

    Article  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45

    Article  PubMed  CAS  Google Scholar 

  • Boxshall AJ (2000) The importance of flow and settlement cues to larvae of the abalone, Haliotis rufescens Swainson. J Exp Mar Biol Ecol 254:143–167

    Article  PubMed  CAS  Google Scholar 

  • Bryant EH (1976) A comment on the role of environmental variation in maintaining polymorphisms in natural populations. Evolution 30:188–190

    Article  Google Scholar 

  • Byers BA (1989) Habitat choice polymorphism associated with cryptic shell color polymorphism in the limpet Lottia digitalis. Veliger 32:394–402

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Corrias B, Rossi N, Arduina P, Cianchi R, Bullini L (1991) Orchis longicornu Poiret in Sardinia: genetic, morfological and chorological data. Webbia 45:75–101

    Google Scholar 

  • Côrte-Real HBSM, Hawkins SJ, Thorpe JP (1996a) An interpretation of the taxonomic relationship between the limpets Patella rustica and P. piperata. J Mar Biol Assoc UK 76:717–732

    Article  Google Scholar 

  • Côrte-Real HBSM, Hawkins SJ, Thorpe JP (1996b) Population differentiation and taxonomic status of the exploited limpet Patella candei in the Macaronesian islands (Azores, Madeira, Canaries). Mar Biol 125:141–152

    Article  Google Scholar 

  • Cretella M, Scillitani G, Toscano F, Turella P, Picariello O, Cataudo A (1994) Relationships between Patella ferruginea Gmelin, 1791 and the other Tyrrhenian species of Patella (Gastropoda, Patellidae). J Molluscan Stud 60:9–17

    Article  Google Scholar 

  • Crow J, Kimura M, (1970) An introduction to population genetics theory. Burgess Publishing Company, Minneapolis

    Google Scholar 

  • Dixon J (1981) Evidence of gregarious settlement in the larvae of the marine snail Collisella strigatella (Carpenter). Veliger 24:181–184

    Google Scholar 

  • Eanes WF (1999) Analysis of selection on enzme polymorphisms. Ann Rev Ecol Syst 30:301–326

    Article  Google Scholar 

  • Gaffney PM, Scott TM, Koehn RK, Diehl WJ (1990) Interrelationships of heterozygosity, growth rate and heterozygote deficiencies in the coot clam, Mulinia lateralis. Genetics 124:687–699

    PubMed  CAS  Google Scholar 

  • Goudet J (2002) FSTAT(version 2.9): A computer program to calculate F-statistics. The J Heredity 86:485–486

    Google Scholar 

  • Gresham ML, Tracey ML, (1975) Genetic variation in an intertidal gastropod, Collisella digitalis. Genetics 80:S37–S37

    Google Scholar 

  • Guo SW, Thompson EA (1992) A Monte-Carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111–1126

    PubMed  CAS  Google Scholar 

  • Hamm DE, Burton RS (2000) Population genetics of black abalone, Haliotis cracherodii, along the central California coast. J Exp Mar Biol Ecol 254:235–247

    Article  PubMed  CAS  Google Scholar 

  • Hancock B, (2000) Genetic subdivision on Roe’s abalone, Haliotis roei Greay (Mollusca: Gastropoda), in south-western Australia. Mar Freshwater Res 51:679–687

    Article  Google Scholar 

  • Hawkins AJS (1995) Effects of temperature change on ectotherm metabolism and evolution: metabolic and phisiological interrelations underlying the superiority of multi-locus heterozyotes in heterogneous environments. J Thermal Biol 20:23–33

    Article  Google Scholar 

  • Hedrick PW (1986) Genetic polymorphism in heterogeneous environments: a decade later. Ann Rev Ecol Syst 17:535–566

    Article  Google Scholar 

  • Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral Balanophyllia elegans. Evolution 48:1829–1854

    Article  Google Scholar 

  • Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Hilbish TJ (1996) Population genetics of marine species: the interaction of natural selection and historically differentiated populations. J Exp Mar Biol Ecol 200:67–83

    Article  Google Scholar 

  • Huang BX, R Peakall PJ Hanna (2000) Analysis of genetic structure of blacklip abalone (Haliotis rubra) populations using RAPD, minisatellite and microsatellite markers. Mar Biol 136:207–216

    Article  CAS  Google Scholar 

  • Johannesson K, Johannesson B, Lundgren U (1995) Strong natural selection causes microscale allozyme variation in a marine snail. Proc Natl Acad Sci USA 92:2602–2606

    Article  PubMed  CAS  Google Scholar 

  • Johannesson K, Lundberg J, Andre C, Nilsson PG (2004) Island isolation and habitat heterogeneity correlate with DNA variation in a marine snail (Littorina saxatilis). Biol J Linnean Soc 82:377–384

    Article  Google Scholar 

  • Johannesson K, Tatarenkov A (1997) Allozyme variation in a snail (Littorina saxatilis) – Deconfounding the effects of microhabitat and gene flow. Evolution 51:402–409

    Article  CAS  Google Scholar 

  • Johnson MS, Bentley SL, Ford SS, Ladyman MT, Lambert GJ (2001) Effects of a complex archipelago on genetic subdivision of the intertidal limpet Siphonaria kurracheensis. Mar Biol 139:1087–1094

    Article  Google Scholar 

  • Johnson MS, Black R (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol 70:157–164

    Article  Google Scholar 

  • Johnson MS, Black R (1984) Pattern beneath the chaos: the effect of recruitment on genetic patchiness in an intertidal limpet. Evolution 38:1371–1383

    Article  Google Scholar 

  • Johnson MS Black R (1998) Increased genetic divergence and reduced genetic variation in populations of the snail Bembicium vittatum in isolated tidal ponds. Heredity 80:163–172

    Article  Google Scholar 

  • Johnson MS, Black R (2005) Effects of a larval stage on isolation of populations of the trochid Austrocochlea constricta in tidal ponds. Mar Biol 147:189–195

    Article  Google Scholar 

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

    Google Scholar 

  • Lambert WJ, Todd CD, Thorpe JP (2003) Genetic population structure of two intertidal nudibranch molluscs with contrasting larval types: temporal variation and transplant experiments. Mar Biol 142:461–471

    Google Scholar 

  • Lavie B, Noy R, Nevo E, (1987) Genetic variability in the marine gastropods Patella coerulea and Patella aspera – patterns and problems. Mar Biol 96:367–370

    Article  Google Scholar 

  • Lehmann T, Hawley W, Grebert H, Collins F, (1998) The effective population size of Anopheles gambiae in Kenya: implications for population structure. Mol Biol Evol 15: 264–276

    PubMed  CAS  Google Scholar 

  • Levinton J, (1973) Genetic variation in a gradient of environmental variability – marine Bivalvia (Mollusca). Science 180:75–76

    Article  PubMed  CAS  Google Scholar 

  • Levinton JS, Suchanek TH, (1978) Geographic variation, niche breadth and genetic differentiation at different geographic scales in the mussels Mytilus californianus and M. edulis. Mar Biol 49:363–375

    Article  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic Data Analysis: Computer program for the analysis of allelic data. Version 1.0. Free program distributed by the authors over the internet from http://lewis.eeb.uconn.edu/lewishome/software.html

  • Lewontin RC, Krakauer J (1975) Testing heterogeneity of F-values. Genetics 80:397–398

    PubMed  CAS  Google Scholar 

  • Lindberg DR (1981) Acmaeidae: Gastropoda, Mollusca. The Boxwood Press, Pacific Grove

    Google Scholar 

  • Mallet AL, Zouros E, Gartnerkepkay KE, Freeman KR, Dickie LM, (1985) Larval viability and heterozygote deficiency in populations of marine bivalves: evidence from pair matings of mussels. Mar Biol 87:165–172

    Article  Google Scholar 

  • Manly B, (1997) Randomization, bootstrap and Monte–Carlo methods in biology. Chapman Hall, London

    Google Scholar 

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

    PubMed  Google Scholar 

  • Nevo E (1978) Genetic variation in natural populations: patterns and theory. Theor Popul Biol 13:121–177

    Article  PubMed  CAS  Google Scholar 

  • Noy R, Lavie B, Nevo E (1987) The niche-width variation hypothesis revisited: genetic diversity in the marine gastropods Littorina punctata (Gmelin) and Littorina neritoides (L). J Exp Mar Biol Ecol 109:109–116

    Article  Google Scholar 

  • Palmer AR, Strathmann RR (1981) Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia 48:308–318

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic-divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Google Scholar 

  • Palumbi, S.R., (1995) Using genetics as an indirect estimator of larval dispersal. CRC press (eds) New York

  • Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific Sea urchins. Evolution 51:1506–1517

    Article  Google Scholar 

  • Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:146–158

    Google Scholar 

  • Parsons KE (1996) The genetic effects of larval dispersal depend on spatial scale and habitat characteristics. Mar Biol 126:403–414

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F, (1995) Genepop (Version-1.2): Population genetics software for exact tests and ecumenicism. J␣Heredity 86:248–249

    Google Scholar 

  • Raymond M, Väänto RL, Thomas F, Rousset F, de Meeüs T, Renaud F (1997) Heterozygote deficiency in the mussel Mytilus edulis species complex revisited. Mar Ecol-Prog Ser 156:225–237

    Google Scholar 

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

    Article  Google Scholar 

  • Rice WR (1990) A consensus combined p-value test and the family-wide significance of component tests. Biometrics 46:303–308

    Article  Google Scholar 

  • Ridgway TM, Stewart BA, Branch GM, (1999) Limited population differentiation in the bearded limpet Patella barbara (Gastropoda: Patellidae) along the coast of South Africa. J␣Mar Biol Assoc UK 79:639–651

    Article  Google Scholar 

  • Ridgway TM, Stewart BA, Branch GM, Hodgson AN, (1998) Morphological and genetic differentiation of Patella guanularis (Gastropoda: Patellidae): recognition of two sibling species along the coast of southern Africa. J Zool 245:317–333

    Article  Google Scholar 

  • Righi G, (1966) On the Brazilian species in the Acmaea subrugosa complex (Gastropoda: Prosobranchia: Patellacea). Malacologia 4:269–295

    Google Scholar 

  • Rios C, Canales J, Pena JB, (1996) Genotype dependent spawning: Evidence from a wild population of Pecten jacobaeus (L) (Bivalvia: Pectinidae). J Shellfish Res 15: 645–651

    Google Scholar 

  • Rios E, (1994) Seashells of Brazil. UFRG, Rio Grande do Sul

    Google Scholar 

  • Rocha-Barreira CA, (2002) Gonad characterization and reproductive cycle of Collisella subrugosa (Orbigny, 1946) (Gastropoda: Acmaeidae) in the northwestern Brazil. Braz J Biol 62:885–895

    Article  PubMed  CAS  Google Scholar 

  • Sella G, Robotti CA, Biglione V, (1993) Genetic divergence among 3 sympatric species of Mediterranean Patella (Archaeogastropoda). Mar Biol 115:401–405

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Singh SM, Green RH (1984) Excess of allozyme homozygosity in marine molluscs and its possible biological significance. Malacologia 25:569–581

    Google Scholar 

  • Slatkin M, (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research. WH Freemam Company, New York

    Google Scholar 

  • Solecava AM, Thorpe JP (1991) High levels of genetic variation in natural populations of marine lower invertebrates. Biol J Linnean Soc 44:65–80

    Google Scholar 

  • Swofford D, Selander R, (1981) BIOSYS-1: a FORTRAM program for the comprehensive analysis of eletrophoretic data in population genetics and systematics. J Heredity 72:281–283

    Google Scholar 

  • Tanaka MO, Duque-Estrada TEM, Magalhães CA (2002) Dynamics of the acmaeid limpet Collisella subrugosa and vertical distribution of size and abundance along wave exposure gradient. J Molluscan Stud 68:55–64

    Article  Google Scholar 

  • Tatarenkov A, Johannesson K (1999) Micro and macrogeographic allozyme variation in Littorina fabalis: do sheltered and exposed forms hybridize? Biol J Linnean Soc 67:199–212

    Article  Google Scholar 

  • Todd CD, Lambert WJ, Thorpe JP (1998) The genetic structure of intertidal populations of two species of nudibranch molluscs with planktotrophic and pelagic lecithotrophic larval stages: are pelagic larvae “for” dispersal? J Exp Mar Biol Ecol 228:1–28

    Article  CAS  Google Scholar 

  • Tracey ML, Bellet NF, Gravem CD (1975) Excess allozyme homozygosity and breeding population structure in mussel Mytilus californianus. Mar Biol 32:303–311

    Article  CAS  Google Scholar 

  • Waples RS (1998) Seperating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Google Scholar 

  • Ward RD (1990) Biochemical genetic variation in the genus Littorina (Prosobranchia: Mollusca). Hydrobiologia 193

  • Ward RD, Warwick T (1980) Genetic differentiation in the molluscan species Littorina rudis and L. arcana (Prosobranchia: Littorinidae). Biol J Linnean Soc 14:417–428

    Google Scholar 

  • Watts RJ, Johnson MS, Black R (1990) Effects of recruitment on genetic patchiness in the urchin Echinometra mathaei in Western Australia. Mar Biol 105:145–151

    Article  Google Scholar 

  • Weber LI, Thorpe JP, Santos RS, Hawkins SJ (1998) Identification of stocks of the exploited limpets Patella aspera and P. candei at Madeira Archipelago by allozyme electrophoresis. J Shellfish Res 17:945–953

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST not equal 1/(4Nm+1). Heredity 82:117–125

    Google Scholar 

  • Wilkins NP (1977) Genetic variability in littoral gastropods: phosphoglucose isomerase and phosphoglucomutase in Patella vulgata and Patella aspera. Mar Biol 40:151–155

    Article  CAS  Google Scholar 

  • Yamada SB (1989) Are direct developers more locally adapted than planktonic developers? Mar Biol 10:403–411

    Article  Google Scholar 

  • Zouros E, Foltz DW (1984) Possible explanations of heterozygote deficiency in bivalve mollusks. Malacologia 25:583–591

    Google Scholar 

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Acknowledgements

The authors thank SCS Andrade, PR Guimarães Jr. and AG Silva for valuable comments in the manuscript and S Hyslop for reviewing the English version. We are in debt with SCS Andrade, KS Yotoko, MP Quast, TEM Duque-Estrada, FS MacCord, H Montenegro, HF Medeiros and especially with MN Galvão for help in the samplings. Financial support was provided by FAPESP grant (#01/01994-2); J José received a FAPESP fellowship (# 99/07110-7). The experiments comply with the Brazilian current laws.

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José, J., Solferini, V. Population genetics of Collisella subrugosa (Patellogastropoda: Acmaeidae): evidence of two scales of population structure. Genetica 130, 73–82 (2007). https://doi.org/10.1007/s10709-006-0024-3

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