Skip to main content

Advertisement

Log in

The population genetic structure of a common tropical damselfish on the Great Barrier Reef and eastern Papua New Guinea

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Understanding patterns of connectivity in marine species is vital for the management and conservation of marine biodiversity. Here, the population genetic structure of a common and abundant tropical reef damselfish, Pomacentrus amboinensis, is reported. Using nine polymorphic microsatellite loci, the genetic structure at both small (i.e., around Lizard Island, Great Barrier Reef [GBR]) and large (GBR and Papua New Guinea [PNG]) spatial and temporal scales (2–1,600 km; 28 days– 6 years; n = 1,119) was analyzed. Temporal analyses found no evidence of genetic differentiation within or between Lizard Island recruitment pulses (R ST = −0.001, P = 0.788), or corresponding established adult populations separated by 6 years of sampling (R ST = 0.003, P = 0.116). The spatial analysis revealed that P. amboinensis populations are largely panmictic on the GBR and eastern PNG (R ST = 0.001, P = 0.913), the only genetic discontinuity being between Kimbe Bay to the north of PNG and all populations south of PNG (R ST = 0.077, P < 0.0001). Despite assumed high levels of self-recruitment based on previous tagging studies (15–60%), data presented here indicate that enough recruits are dispersing to impede the evolution of genetic structure over distances as great as 1,600 kms in this species. Data therefore indicate that the temporal genetic stability recorded here is maintained by high levels of gene flow.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allen GR (1991) Damselfishes of the world. Mergus Publishers, Melle, Germany

    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  PubMed  Google Scholar 

  • Almany G, Connolly S, Heath D, Hogan J, Jones G, McCook L, Mills M, Pressey R, Williamson D (2009) Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28:339–351

    Article  Google Scholar 

  • Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76

    Article  CAS  Google Scholar 

  • Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54:1590–1605

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bay L, Crozier R, Caley M (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc: Series B 57:289–300

    Google Scholar 

  • Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past. Am Zool 39:131–145

    Google Scholar 

  • Benzie JAH, Stoddart JA (1992) Genetic structure of outbreaking and non-outbreaking crown-of-thorns starfish (Acanthaster planci) populations on the Great Barrier Reef. Mar Biol 112:119–130

    Article  Google Scholar 

  • Benzie JAH, Williams ST (1997) Genetic structure of giant clam (Tridacna maxima) populations in the West Pacific is not consistent with dispersal by present-day ocean currents. Evolution 51:768–783

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Botsford L, White J, Coffroth M, Paris C, Planes S, Shearer T, Thorrold S, Jones G (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs 28:327–337

    Article  Google Scholar 

  • Caley JM, Carr MH, Hixon MA, Hughes TP, Jones GP, Menge BA (1996) Recruitment and the local dynamics of open populations. Annu Rev Ecol Syst 27:477–500

    Article  Google Scholar 

  • Callen DF, Thompson AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR (1993) Incidence and origin of “null” alleles in the (AC)n microsatellite markers. Am J Hum Genet 52:922–927

    CAS  PubMed  Google Scholar 

  • Castle PHJ (1984) Notacanthiformes and Anguilliformes: development. In, Ontogeny and systematics of fishes. American Society of Ichthyologists and Herpetologists. Lawrence, KS, pp 62–93

    Google Scholar 

  • Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Charnock H (1967) The encyclopedia of oceanography. In: Fairbridge RW, Reinhold E (eds) Encyclopedia of earth sciences, vol 1. Science: New York, pp 1162

  • Church JA (1987) East Australian Current adjacent to the Great Barrier Reef Australia. Aust J Mar Freshw Res 38:671–684

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner FE (2007) Population connectivity in marine systems: an overview. Oceanography 20:14–21

    Google Scholar 

  • Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64

    Google Scholar 

  • 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

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  • Fisher R (2005) Swimming speeds of larval coral reef fishes: impacts on self-recruitment and dispersal. Mar Ecol Prog Ser 285:223–232

    Article  Google Scholar 

  • Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Gaines SD, Gaylord B, Gerber LR, Hastings A, Kinlan BP (2007) Connecting places: the ecological consequences of dispersal in the sea. Oceanography 20:90–99

    Google Scholar 

  • Gell FR, Roberts CM (2003) Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol Evol 18:448–455

    Article  Google Scholar 

  • Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863

    Article  CAS  PubMed  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 (1999) PCA-GEN, a computer package which performs principal component analysis (PCA) on gene frequency data. Available from http://www2unilch/izea/softwares/pcagenhtml

  • Guillot G, Mortier F, Estoup A (2005a) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005b) A spatial statistical model for landscape genetics. Genetics 170:1261–1280

    Article  CAS  PubMed  Google Scholar 

  • Halpern BS, Warner RR (2002) Marine reserves have rapid and lasting effects. Ecol Lett 5:361–366

    Article  Google Scholar 

  • Hare MP, Karl SA, Avise JC (1996) Anonymous nuclear DNA markers in the American oyster and their implications for the heterozygote deficiency phenomenon in marine bivalves. Mol Biol Evol 13:334–345

    CAS  PubMed  Google Scholar 

  • Hedrick PW (2005a) Genetics of populations. Jones and Bartlett Publishers, London

    Google Scholar 

  • Hedrick PW (2005b) A standardized genetic differentiation measure. Evolution 59:1633–1638

    CAS  PubMed  Google Scholar 

  • Hellberg M (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473

    Article  Google Scholar 

  • Hixon MA, Boersma PD, Malcolm L, Hunter J, Micheli F, Norse EA, Possingham HP, Snelgrove PVR (2001) Oceans at risk: research priorities in marine conservation biology. Island Press, Washington

    Google Scholar 

  • Hopley D, Thom BG (1983) Australian sea levels in the last 15000 years: an introductory review. In: Hopley D (ed) Australian sea levels in the last 15000 years: a review. Department of Geography, James Cook University, Townsville, pp 29–36

    Google Scholar 

  • Horne JB, van Herwerden L, Choat JH, Robertson DR (2008) High population connectivity across the Indo-Pacific: congruent lack of phylogeographic structure in three reef fish congeners. Mol Phylogenet Evol 49:629–638

    Article  PubMed  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Hutchings JA, Reynolds JD (2004) Marine fish population collapses: consequences for recovery and extinction risk. Bioscience 54:297–309

    Article  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    Article  Google Scholar 

  • Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214

    Article  Google Scholar 

  • Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–637

    Article  CAS  PubMed  Google Scholar 

  • James MK, Armsworth PR, Mason LB, Bode L (2002) The structure of reef fish metapopulations: modelling larval dispersal and retention patterns. Proc R Soc Biol Sci Ser B 269:2079–2086

    Article  Google Scholar 

  • Jones GP (1987) Competitive interactions among adults and juveniles in a coral reef fish. Ecology 68:1534–1547

    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 

  • Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318

    Article  CAS  PubMed  Google Scholar 

  • Jones GP, Srinivasan M, Almany GR (2007) Population connectivity and conservation of marine biodiversity. Oceanography 20:100–111

    Google Scholar 

  • Jones DB, Jerry DR, McCormick MI, Bay LK (2008) Development of nine microsatellite markers for Pomacentrus amboinensis. Mol Ecol Resources 8:1332–1334

    Article  CAS  Google Scholar 

  • Jones G, Almany G, Russ G, Sale P, Steneck R, van Oppen M, Willis B (2009) Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325

    Article  Google Scholar 

  • Kerrigan BA (1996) Temporal patterns in the size and condition of settlement in two tropical reef fishes (Pomacentridae: Pomacentrus amboinensis and P. nagasakiensis). Mar Ecol Prog Ser 135:27–41

    Article  Google Scholar 

  • Kingsford MJ, Leis JM, Shanks A, Lindeman KC, Morgan SG, Pineda J (2002) Sensory environments, larval abilities and local self-recruitment. Mar Sci 70:309–340

    Google Scholar 

  • Larcombe P (2001) Holocene Great Barrier Reef: sedimentary controls and implications for environmental management. In: Gostin VA (ed) Gondwana to greenhouse. Australian environmental geoscience. Southwood Press, Sydney, pp 281–294

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Second english edition. Elsevier Science BV, Amsterdam, The Netherlands

    Google Scholar 

  • Leis JM, McCormick MI (2002) The biology, behavior, and ecology of the pelagic larval stage of coral reef fishes. In: Sale PF (ed) coral reef fishes. Dynamics and diversity in a complex ecosystem. Academic Press, London, pp 171–199

    Chapter  Google Scholar 

  • Lindstrom E, Lukas R, Fine R, Firing E, Godfrey S, Meyers G, Tsuchiya M (1987) The western equatorial Pacific Ocean circulation study. Nature 330:533–537

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  • Macaranas JM, Ablan CA, Pante MJR, Benzie JAH, Williams ST (1992) Genetic structure of giant clam (Tridacna derasa) populations from reefs in the Indo-Pacific. Mar Biol 113:231–238

    Google Scholar 

  • Meekan MG, Milicich MJ, Doherty PJ (1993) Larval production drives temporal patterns of larval supply and recruitment of a coral reef damselfish. Mar Ecol Prog Ser 93:217–225

    Article  Google Scholar 

  • Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar Biol 139:373–381

    Article  Google Scholar 

  • Messmer V, van Herwerden L, Munday P, Jones G (2005) Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef. Coral Reefs 24:392–402

    Article  Google Scholar 

  • Millar R (1971) The biology of ascidians. Adv Mar Biol 9:1–100

    Article  Google Scholar 

  • Mora C, Sale PF (2002) Are populations of coral reef fish open or closed? Trends Ecol Evol 17:422–428

    Article  Google Scholar 

  • Munday P, Leis J, Lough J, Paris C, Kingsford M, Berumen M, Lambrechts J (2009) Climate change and coral reef connectivity. Coral Reefs 28:379–395

    Article  Google Scholar 

  • Munkres KP, Bay LK, Jerry DR, McCormick MI, Van Herwerden L (2007) Development and characterization of microsatellite markers for parentage analyses of the coral reef damselfish (Pomacentrus amboinensis: Pomacentridae). Conserv Genet 8:987–990

    Article  CAS  Google Scholar 

  • Nash WJ, Goddard M, Lucas JS (1988) Population genetic studies of the crown-of-thorns starfish, Acanthaster planci, in the Great Barrier Reef region. Coral Reefs 7:11–18

    Article  Google Scholar 

  • Neigel JE (2002) Is FST obsolete? Conserv Genet 3:167–173

    Article  CAS  Google Scholar 

  • O’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363

    Article  Google Scholar 

  • 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 

  • Paris CB, Cowen RK (2004) Direct evidence of a biophysical retention mechanism for coral reef fish larvae. Limnol Oceanogr 49:1964–1979

    Article  Google Scholar 

  • Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peres-Neto PR, Jackson DA, Somers KM (2003) Giving meaningful interpretation to ordination axes: assessing loading significance in principal component analysis. Ecology 84:2347–2363

    Article  Google Scholar 

  • Powles H, Bradford MJ, Bradford RG, Doubleday WG, Innes S, Levings CD (2000) Assessing and protecting endangered marine species. J Mar Sci 57:669–676

    Google Scholar 

  • Pritchard JK, Wen W (2004) Documentation for Structure software: version 2. Available at http://pritch.bsd.uchicago.edu/software/readme_structure2_1.pdf

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Reynolds JD, Dulvy NK, Goodwin NB, Hutchings JA (2005) Biology of extinction risk in marine fishes. Proc R Soc Biol Sci Ser B 272:2337–2344

    Article  Google Scholar 

  • Roberts CM, Polunin NVC (1991) Are marine reserves effective in management of reef fisheries? Rev Fish Biol Fish 1:65–91

    Article  Google Scholar 

  • Rocha LA, Craig MT, Bowen BW (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs 26:501–512

    Article  Google Scholar 

  • Roughgarden J, Iwasa Y, Baxter C (1985) Demographic theory for an open marine population with space-limited recruitment. Ecology 66:54–67

    Article  Google Scholar 

  • Sale PF (1991) Reef fish communities: open nonequilibrial systems. In: Sale PF (ed) The ecology of fishes on coral reefs. Academic Press, San Diego, pp 564–598

    Google Scholar 

  • Shulman MJ (1998) What can population genetics tell us about dispersal and biogeographic history of coral-reef fishes? Aust J Ecol 23:216–255

    Article  Google Scholar 

  • Spieth P (1974) Gene flow and genetic differentiation. Genetics 78:961–965

    CAS  PubMed  Google Scholar 

  • Steneck R, Paris C, Arnold S, Ablan-Lagman M, Alcala A, Butler M, McCook L, Russ G, Sale P (2009) Thinking and managing outside the box: coalescing connectivity networks to build region-wide resilience in coral reef ecosystems. Coral Reefs 28:367–378

    Article  Google Scholar 

  • Swearer S, Caselle J, Lea D, Warner R (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802

    Article  CAS  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 

  • Swearer SE, Forrester GE, Steele MA, Brooks AJ, Lea DW (2003) Spatio-temporal and interspecific variation in otolith trace-elemental fingerprints in a temperate estuarine fish assemblage. Estuar Coast Shelf Sci 56:1111–1123

    Article  CAS  Google Scholar 

  • Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–108

    Article  CAS  PubMed  Google Scholar 

  • Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385

    PubMed  Google Scholar 

  • Tomczak M, Godfrey JS (1994) Regional oceanography: an introduction. Pergamon Press, Oxford

    Google Scholar 

  • Treml E, Halpin P, Urban D, Pratson L (2008) Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landsc Ecol 23:19–36

    Article  Google Scholar 

  • van Herwerden L, Benzie JAH, Davies C (2003) Microsatellite variation and population genetic structure of the red throat emperor on the Great Barrier Reef. J Fish Biol 62:987–999

    Article  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Waples R, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Williams ST, Benzie JAH (1993) Genetic consequences of long larval life in the starfish Linckia laevigata (Echinodermata: Asteroidea) on the Great Barrier Reef. Mar Biol 117:71–77

    Article  Google Scholar 

  • Williams DM, Wolanski E, Andrews JC (1984) Transport mechanisms and the potential movement of planktonic larvae in the central region of the Great Barrier Reef. Coral Reefs 3:229–236

    Article  Google Scholar 

  • Wolanski E, Pickard GL (1985) Long-term observations of currents on the central Great Barrier Reef continental shelf. Coral Reefs 4:47–57

    Article  Google Scholar 

  • Wood L, Fish L, Laughren J, Pauly D (2008) Assessing progress towards global marine protection targets: shortfalls in information and action. Oryx 42:340–351

    Article  Google Scholar 

Download references

Acknowledgments

Our gratitude goes to Monica Galliano, James Moore, and Vanessa Messner for sample collection across the GBR and PNG; Jessica Hopf, Adrian Lutz, Rhianna Willis, Raechel Littman, Bette Willis, David Abrego, Eneour Puill-Stephan, and the Orpheus Island Research Station staff for help with the collection of samples. Genotyping was conducted at the Genetic Analysis Facility at James Cook University. This work was funded through the ARC Centre of Excellence for Coral Reef Studies and the AIMS@JCU joint venture. We also would like to thank Rolf Bak, Ruth Gates, and the Coral Reefs reviewers for their hard work and contributions to this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D. B. Jones.

Additional information

Communicated by Biology Editor Dr. Ruth Gates

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, D.B., Jerry, D.R., McCormick, M.I. et al. The population genetic structure of a common tropical damselfish on the Great Barrier Reef and eastern Papua New Guinea. Coral Reefs 29, 455–467 (2010). https://doi.org/10.1007/s00338-010-0591-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-010-0591-8

Keywords

Navigation