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Population genetic variation in the New Zealand greenshell mussel: locus-dependent conflicting signals of weak structure and high gene flow balanced against pronounced structure and high self-recruitment

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Abstract

A pronounced north–south multitaxon genetic discontinuity occurs in central New Zealand (NZ). Polymorphic microsatellite markers have been used to test the location and structure of this discontinuity in the endemic greenshell mussel, Perna canaliculus. Nine neutral loci revealed limited evidence of genetic structure, but one outlier locus (Pcan1-27) which may be under selection provided evidence of the discontinuity in central NZ. Whilst the limited multilocus evidence of structure is assumed to result from high levels of gene flow among populations of this continuously distributed species, assignment tests indicated high to very high mean levels of self-recruitment within the 14 populations and the north and south regions. The nine neutral loci were unable to provide further clarification as to the geographic location of the discontinuity, whereas the Pcan1-27 locus was particularly informative. These results highlight a tension between limited evidence of genetic structure and presumptive high gene flow among populations versus high levels of self-recruitment and pronounced structure depending on microsatellite loci and analyses in question. Evidence from all 10 loci indicates that the genetic discontinuity is maintained by high levels of self-recruitment, and evidence from Pcan1-27 suggests that selection may also be important in explaining the existence of the discontinuity.

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References

  • Addison JA, Hart MW (2005) Spawning, copulation and inbreeding coefficients in marine invertebrates. Biol Lett 1:450–453

    Article  CAS  Google Scholar 

  • Addison JA, Ort BS, Mesa KA, Pogson GH (2008) Range-wide genetic homogeneity in the California sea mussel (Mytilus californianus): a comparison of allozymes, nuclear DNA markers, and mitochondrial DNA sequences. Mol Ecol 17:4222–4232

    Article  CAS  Google Scholar 

  • Almany GR, Berumen ML, Thorrold SR, Planes S, Jones GP (2007) Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744

    Article  CAS  Google Scholar 

  • Apte S, Gardner JPA (2001) Absence of population genetic differentiation in the New Zealand greenshell mussel, Perna canaliculus, as assessed by allozyme variation. J Exp Mar Biol Ecol 258:173–194

    Article  Google Scholar 

  • Apte S, Gardner JPA (2002) Population genetic variation in the New Zealand greenshell mussel, Perna canaliculus: SSCP and RFLP analyses of mitochondrial DNA. Mol Ecol 11:1617–1628

    Article  CAS  Google Scholar 

  • Apte S, Star B, Gardner JPA (2003) A comparison of genetic diversity between cultured and wild populations, and a test of genetic introgression in the New Zealand greenshell mussel, Perna canaliculus (Gmelin 1791). Aquaculture 219:193–220

    Article  Google Scholar 

  • Ayers KL, Waters JM (2005) Marine biogeographic disjunction in central New Zealand. Mar Biol 147:1045–1052

    Article  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) A marine Wallace’s line? Nature 406:692–693

    Article  CAS  Google Scholar 

  • Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2002) Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences. Mol Ecol 11:659–674

    Article  CAS  Google Scholar 

  • Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561

    Article  Google Scholar 

  • Bester-van der Merwe AE, Roodt-Wilding R, Volckaert FAM, D’Amato ME (2011) Historical isolation and hydrodynamically constrained gene flow in declining populations of the South African abalone, Haliotis midae. Conserv Genet 12:543–555

    Article  Google Scholar 

  • Carreras-Carbonell J, Macpherson E, Pascual M (2007) High self-recruitment levels in a Mediterranean littoral fish population revealed by microsatellite markers. Mar Biol 151:719–727

    Article  Google Scholar 

  • Chambers GK, MacAvoy ES (2000) Microsatellites: consensus and controversy. Comp Biochem Physiol B: Biochem Mol Biol 126:455–476

    Article  CAS  Google Scholar 

  • Cornuet J, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  Google Scholar 

  • Diz AP, Presa P (2009) The genetic diversity pattern of Mytilus galloprovincialis in Galician Rías (NW Iberian estuaries). Aquaculture 287:278–285

    Article  CAS  Google Scholar 

  • 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 131:479–491

    CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Foster NL, Paris CB, Kool JT, Baums IB, Stevens JR, Sanchez JA, Bastidas C, Agudelo C, Bush P, Day O, Ferrari R, Gonzalez P, Gore S, Guppy R, McCartney MA, McCoy C, Mendes J, Srinivasan A, Steiner S, Vermeij MJA, Weil E, Mumby PJ (2012) Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow. Mol Ecol 21:1143–1157

    Article  Google Scholar 

  • Galindo HM, Olson DB, Palumbi SR (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Curr Biol 16:1622–1626

    Article  CAS  Google Scholar 

  • Galindo HM, Pfeiffer-Herbert AS, McManus MA, Chao Y, Chai F, Palumbi SR (2010) Seascape genetics along a steep cline: using genetic patterns to test predictions of marine larval dispersal. Mol Ecol 19:3692–3707

    Article  Google Scholar 

  • Gao X, Starmer JD (2008) AWclust: point-and-click software for non-parametric population structure analysis. BMC Bioinformatics 9:77. doi:10.1186/1471-2105-9-77

    Article  Google Scholar 

  • Gardner JPA (1992) Null alleles and heterozygote deficiencies among mussels (Mytilus edulis and M. galloprovincialis) of two sympatric populations. Malacologia 34:99–106

    Google Scholar 

  • Gardner JPA, Palmer NL (1998) Size-dependent, spatial and temporal genetic variation at a leucine aminopeptidase (LAP) locus among blue mussel (Mytilus galloprovincialis) populations along a salinity gradient. Mar Biol 132:275–281

    Article  CAS  Google Scholar 

  • Gardner JPA, Thompson RJ (1999) High levels of shared allozyme polymorphism among strongly differentiated congeneric clams of the genus Astarte (Bivalvia: Mollusca). Heredity 82:89–99

    Article  CAS  Google Scholar 

  • Gardner JPA, Bell JJ, Constable HB, Hannan D, Ritchie PA, Zuccarello GC (2010) Multi-species coastal marine connectivity: a literature review with recommendations for further research. New Zealand aquatic environment and biodiversity report no. 58, p 47. ISSN 1176-9440

  • Goldstien SJ, Schiel DR, Gemmell NJ (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268

    Article  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (version. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (2000) FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.1. Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)

  • Gruber MAM, Hoffman BD, Ritchie PA, Lester PJ (2012) The conundrum of the yellow crazy ant (Anoplolepis gracilipes) reproductive mode: no evidence for dependent lineage genetic caste determination. Insects Soc. doi:10.1007/s00040-012-0277-z

  • Harris TFW (1990) Greater cook strait. DSIR (Department of Scientific and Industrial Research) Marine and Freshwater, Wellington, p 212

  • Hayden BJ (1994) What do we know about greenshell mussel spat? Part I. Seafood New Zealand 2:45–47

    Google Scholar 

  • Hedgecock D, Li G, Hubert S, Bucklin K, Ribes V (2004) Widespread null alleles and poor cross-species amplification of microsatellite DNA loci from the Pacific oyster, Crassostrea gigas. J Shellfish Res 23:379–385

    Google Scholar 

  • Hellberg ME, Burton RS, Hedgecock D, Neigel JE, Palumbi SR (2002) The use of genetic data to assess connectivity among marine populations. Bull Mar Sci 70:273–290

    Google Scholar 

  • Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207

    Article  Google Scholar 

  • Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804

    Article  CAS  Google Scholar 

  • Kelly RP, Eernisse DJ (2007) Southern hospitality: a latitudinal gradient in gene flow in the marine environment. Evolution 61:700–707

    Article  CAS  Google Scholar 

  • Koehn RK, Diehl WJ, Scott TM (1988) The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth rate in the coot clam, Mulinia lateralis. Genetics 118:121–130

    CAS  Google Scholar 

  • Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc R Soc Lond B 265:583–588

    Article  Google Scholar 

  • MacAvoy ES, Wood AR, Gardner JPA (2008) Development and evaluation of microsatellite markers for individual identification of greenshell mussels (Perna canaliculus) in aquaculture. Aquaculture 274:41–48

    Article  CAS  Google Scholar 

  • Manel S, Gaggioti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142

    Article  Google Scholar 

  • Meirmans PG (2006) Using the AMOVA framework to estimate a standardised genetic differentiation measure. Evolution 60:2399–2402

    Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Evol 11:5–18

    Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Miller MP (2005) Alleles In Space (AIS): computer software for the joint analysis of interindividual spatial and genetic information. J Hered 96:722–724

    Article  CAS  Google Scholar 

  • Miller MP, Bellinger MR, Forsman ED, Haig SM (2006) Effects of historical climate change, habitat connectivity, and vicariance on genetic structure and diversity across the range of the red tree vole (Phenacomys longicaudus) in the Pacific Northwestern United States. Mol Ecol 15:145–159

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • Ong CC, Yusoff K, Yap CK, Tan SG (2009) Genetic characterization of Perna viridis L. in peninsular Malaysia using microsatellite markers. J Genet 88:153–163

    Article  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrant detection. J Hered 95:536–539

    Article  CAS  Google Scholar 

  • Poulsen NA, Hemmer-Hansen J, Loeschcke V, Carvalho GR, Nielsen EE (2011) Microgeographical population structure and adaptation in Atlantic cod Gadus morhua: spatio-temporal insights from gene-associated DNA markers. Mar Ecol Prog Ser 436:231–243

    Article  Google Scholar 

  • Prakoon W, Tunkijjanuki SJ, Nguyen TTT, Na-Nakorn U (2010) Spatial and temporal genetic variation of green mussel, Perna viridis in the Gulf of Thailand and implication for aquaculture. Mar Biotechnol 12:506–515

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Raymond M, Rousset F (2004) GENEPOP, version 3.4: population genetics software for exact tests and ecumenicism. Laboratoire de Genetique et Environment, Montpellier, France. http://genepop.curtin.edu.au/

  • Ross PM, Hogg ID, Pilditch CA, Lundquist CJ (2009) Phylogeography of New Zealand’s coastal benthos. NZ J Mar Freshw Res 43:1009–1027

    Article  Google Scholar 

  • Saenz-Agudelo P, Jones GP, Thorrold SR, Planes S (2011) Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc R Soc Lond B. doi: 10.1098/rspb.2010.2780

  • Silva EP, Russo CAM (2000) Techniques and statistical data analysis in molecular population genetics. Hydrobiologia 420:119–135

    Google Scholar 

  • Sponer R (2002) Phylogeography and evolutionary history of the cosmopolitan brooding brittle star Amphipholis squamata (Delle Chiaje, 1828; Echinodermata: Ophiuroidea). PhD thesis, University of Otago, Dunedin, New Zealand

  • Star B, Apte S, Gardner JPA (2003) Genetic structuring among populations of the greenshell mussel Perna canaliculus (Gmelin 1791) revealed by analysis of Randomly Amplified Polymorphic DNA. Mar Ecol Prog Ser 249:171–182

    Article  CAS  Google Scholar 

  • Stevens GR, McClone M, McCulloch B (1995) Prehistoric New Zealand. Reed Publishing (NZ) Ltd., Auckland

    Google Scholar 

  • Subirana JA, Messeguer X (2008) Structural families of genomic microsatellites. Gene 408:124–132

    Article  CAS  Google Scholar 

  • Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  • Takezaki N, Nei M, Tamura K (2010) POPTREE2: Software for constructing population trees from allele frequency data and computing other population statistics with Windows-interface. Mol Biol Evol 27:747–752

    Article  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109

    Article  CAS  Google Scholar 

  • Teske PR, Papadopoulos I, Newman BK, Dworschak PC, McQuaid CD, Barker NP (2008) Oceanographic dispersal barriers, adaptation and larval retention: an interdisciplinary assessment of potential factors maintaining a phylogeographic break between sister lineages of an African prawn. BMC Evol Biol 8:341. doi:10.1186/1471-2148-8-341

    Article  Google Scholar 

  • Tiexeira de Sousa J, Joaquim S, Matias D, Ben-Hamadou R, Leitão A (2012) Evidence of non-random chromosome loss in bivalves: differential chromosomal susceptibility in aneuploidy metaphases of Crassostrea angulata (Ostreidae) and Ruditapes decussatus (Veneridae). Aquaculture 344:239–241

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784

    Article  CAS  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley PF (2004) Microchecker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Verhoeven KJF, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Article  Google Scholar 

  • Waters JM, Roy MS (2004) Phylogeography of a high-dispersal New Zealand sea-star: does upwelling block gene-flow? Mol Ecol 13:2797–2806

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Westfall KM (2010) Molecular ecology and systematics of blue mussels (genus Mytilus) (Mytilidae; Bivalvia; Mollusca) in the Southern Hemisphere. PhD thesis, Victoria University of Wellington, New Zealand (submitted to)

  • Will M, Hale ML, Schiel DR, Gemmell NJ (2011) Low to moderate levels of genetic differentiation detected across the distribution of the New Zealand abalone, Haliotis iris. Mar Biol 158:1417–1429

    Article  Google Scholar 

  • Wood AR, Gardner JPA (2007) Small spatial scale population genetic structure in two limpets (Scutellastra kermadecensis and Siphonaria raoulensis) endemic to the Kermadec Islands, New Zealand. Mar Ecol Prog Ser 349:159–170

    Article  Google Scholar 

  • Yeh FC, Yang R-C, Boyle T (1999) POPGENE, version 1.32: microsoft window-based freeware for population genetic analysis. The Centre for International Forestry Research, University of Alberta, Alberta, Canada. Available from http://www.ualberta.ca/~fyeh/

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

    Google Scholar 

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Acknowledgments

We thank the following: Smita Apte for sample collection; Smita Apte, Liz MacAvoy and Rose McColl for help in the laboratory; and Smita Apte and Liz MacAvoy for comments on an earlier version of the manuscript. We thank the journal editor and two anonymous reviewers for their insightful comments on the paper. This research was supported by funding from the New Zealand Foundation for Research, Science and Technology (contract CAWX0303 to JPAG) and by the China Scholarship Council (to KW).

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  1. Kaijian Wei

    Present address: College of Fisheries, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

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  1. Centre for Marine Environmental and Economic Research, School of Biological Sciences, Victoria University of Wellington, P O Box 600, Wellington, 6140, New Zealand

    Kaijian Wei, Ann R. Wood & Jonathan P. A. Gardner

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  1. Kaijian Wei
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Wei, K., Wood, A.R. & Gardner, J.P.A. Population genetic variation in the New Zealand greenshell mussel: locus-dependent conflicting signals of weak structure and high gene flow balanced against pronounced structure and high self-recruitment. Mar Biol 160, 931–949 (2013). https://doi.org/10.1007/s00227-012-2145-9

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