Abstract
Analysis of genetic data can reveal past and ongoing demographic connections between reef populations. The history, extent, and geography of isolation and exchange help to determine which populations are evolutionarily distinct and how to manage threatened reefs. Here the genetic approaches undertaken to understand connectivity among reefs are reviewed, ranging from early allozyme studies on genetic subdivision, through the use of sequence data to infer population histories, to emerging analyses that pull the influences of the past connections away from the effects of ongoing dispersal. Critically, some of these new approaches can infer migration and isolation over recent generations, thus offering the opportunity to answer many questions about reef connectivity and to better collaborate with ecologists and oceanographers to address problems that remain.
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Arbogast BS, Edwards SV, Wakeley J, Beerli P, Slowinski JB (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annu Rev Ecol Syst 33:707–740
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
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
Ayre DJ, Hughes TP (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Ecol Lett 7:273–278
Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Syst 36:621–642
Barber PH, Palumbi SR, Erdmann MV, Moosa MK (2000) Biogeography—a marine Wallace’s line? Nature 406:692–693
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
Baums IB, Miller MW, Hellberg ME (2005a) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390
Baums IB, Hughes CR, Hellberg ME (2005b) Highly polymorphic microsatellite markers for the Caribbean hard coral Acropora palmata. Mar Ecol Prog Ser 288:115–127
Baums IB, Paris CB, Cherubin LM (2006a) A bio-oceanographic filter to larval dispersal in a reef-building coral. Limnol Oceanogr 51:1969–1981
Baums IB, Miller MW, Hellberg ME (2006b) Geographic variation in clonal structure in a reef building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519
Bay LK, Crozier RH, Caley MJ (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
Bazin E, Glemin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572
Beerli P (2006) Comparison of Bayesian and maximum-likelihood inference of population genetic parameters. Bioinformatics 22:341–345
Beerli P, Felsenstein J (2001) Maximum likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568
Benzie JAH (1999) Genetic structure of coral reef organisms: ghosts of dispersal past? Am Zool 39:131–145
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
Berry OF (2006) Mitochondrial DNA and population size. Science 314:1388–1388
Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Mol Ecol 13:551–561
Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol (in press)
Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift—equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121:613–627
Block BA, Teo SLH, Walli A, Boustany A, Stokesbury MJW, Farwell CJ, Weng KC, Dewar H, Williams TD (2005) Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434:1121–1127
Bowen BW (1999) Preserving genes, species, or ecosystems? Healing the fractured foundations of conservation policy. Mol Ecol 8:S5–S10
Bowen BW, Bass AL, Muss A, Carlin J, Robertson DR (2006) Phylogeography of two Atlantic squirrelfishes (Family Holocentridae): exploring links between pelagic larval duration and population connectivity. Mar Biol 149:899–913
Buroker NE (1983) Population genetics of the American oyster Crassostrea virginica along the Atlantic coast and the Gulf of Mexico. Mar Biol 75:99–112
Carlon DB, Olson RR (1993) Larval dispersal distance as an explanation for adult spatial pattern in 2 Caribbean reef corals. J Exp Mar Biol Ecol 173:247–263
Colin PL (1975) Neon gobies. TFH Publications, Neptune City
Cornuet J-M, 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
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527
Crow JF, Aoki K (1984) Group selection for a polygenic trait: estimating the degree of population subdivision. Proc Natl Acad Sci USA 81:6073–6077
Darwin C (1859) On the origin of species by means of natural selection. Or the preservation of favoured races in the struggle for life. John Murray, London
Doherty PJ, Planes S, Mather P (1995) Gene flow and larval duration in 7 species of fish from the great-barrier-reef. Ecology 76:2373–2391
Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea level change. Evolution 57:1571–1583
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2751
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
Gutierrez-Rodriguez C, Lasker HR (2004) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Mol Ecol 13:2211–2221
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
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 (2006a) Genetic approaches to understanding marine metapopulation dynamics. In: Kritzer J, Sale PF (eds) Marine metapopulations. Academic, San Diego, pp 431–455
Hellberg ME (2006b) No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol Biol 6:24
Hellberg ME, Balch DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1710
Hellberg ME, Burton RS, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290
Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates, and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760
Hoffman EA, Kolm N, Berglund A, Arguello JR, Jones AG (2005) Genetic structure in the coral reef associated Banggai cardinalfish, Pterapogon kauderni. Mol Ecol 14:1367–1375
Hudson RR, Turelli MT (2003) Sochasticity overrules the “three times rule”: genetic drift, genetic draft, and coalescent times for nuclear loci versus mitochondrial DNA. Evolution 57:182–190
Hutchinson DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914
Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evolution 56:2383–2394
James MK, Armsworth PR, Mason LB, Bode L (2002) The structure of reef fish metapopulations: modelling larval dispersal and retention patterns. Proc R Soc Lond B Biol Sci 269:2079–2086
Jones GP, Planes S, Thorrold SR (2005) Coral reef fish larvae settle close to home. Curr Biol 15:1314–1318
Karl SA, Avise JC (1992) Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256:100–102
Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434
Lacson JM, Riccardi VM, Calhoun SW, Morizot DC (1989) Genetic differentiation of bicolor damselfish (Eupomacentrus partitus) populations in the Florida Keys. Mar Biol 103:445–451
Launey S, Hedgecock D (2001) High genetic load in the Pacific oyster Crassostrea gigas. Genetics 159:255–265
Lavery S, Moritz C, Fielder DR (1995) Changing patterns of population structure and gene flow at different spatial scales in the coconut crab (Birgus latro). Heredity 74:531–541
Lavery S, Moritz C, Fielder DR (1996) Indo-Pacific population structure and evolutionary history of the coconut crab Birgus latro. Mol Ecol 5:557–570
Lee T, O’Foighil D (2005) Placing the Floridian marine genetic disjunction into a regional evolutionary context using the scorched mussel, Brachidontes exustus, species complex. Evolution 59:2139–2158
Lessios HA, Robertson DR (2006) Crossing the impassible: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proc R Soc Lond B Biol Sci 273:2201–2208
Lessios HA, Kessing BD, Robertson DR (1998) Massive gene flow across the world’s most potent marine biogeographic barrier. Proc R Soc Lond B Biol Sci 265:583–588
Lessios HA, Garrido MJ, Kessing BD (2001) Demographic history of Diadema antillarum, a keystone herbivore on Caribbean reefs. Proc R Soc Lond B Biol Sci 268:2347–2353
Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036
Lourie SA, Vincent ACJ (2004) A marine fish follows Wallace’s Line: the phylogeography of the three-spot seahorse (Hippocampus trimaculatus, Syngnathidae, Teleostei) in Southeast Asia. J Biogeogr 31:1975–1985
Mackenzie JB, Munday PL, Willis BL, Miller DJ, van Oppen MJH (2004) Unexpected patterns of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Mol Ecol 13:9–20
Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868
Maier E, Tollrian R, Rinkevich B, Nurnberger B (2005) Isolation by distance in the scleractinian coral Seriatopora hystrix from the Red Sea. Mar Biol 147:1109–1120
Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142
Marko PB (1998) Historical allopatry and the biogeography of speciation in the prosobranch snail genus Nucella. Evolution 52:757–774
Márquez LM, van Oppen MJH, Willis BL, Miller DJ (2002) Sympatric populations of the highly cross-fertile coral species Acropora hyacinthus and Acropora cytherea are genetically distinct. Proc R Soc Lond B Biol Sci 269:1289–1294
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution 59:113–125
Neigel JE (1997) A comparison of alternative strategies for estimating gene flow from genetic markers. Annu Rev Ecol Syst 28:105–128
Nichols WJ, Resendiz A, Seminoff JA, Resendiz B (2000) Trans-Pacific migration of a loggerhead turtle monitored by satellite telemetry. Bull Mar Sci 67:937–947
Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–897
Nishida M, Lucas JS (1988) Genetic differences between geographic populations of the crown-of-thorns starfish throughout the Pacific region. Mar Biol 98:359–368
Ovenden JR, Salini J, O’Connor S, Street R (2004) Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei:Perciformes:Lutjanidae) from the East Indies triangle. Mol Ecol 13:1991–1999
Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158
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
Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56:378–399
Planes S, Galzin R, Bonhomme F (1996) A genetic metapopulation model for reef fishes in oceanic islands: the case of the surgeonfish, Acanthurus triostegus. J Evol Biol 9:103–117
Planes S, Doherty PJ, Bernardi G (2001) Strong genetic divergence among populations of a marine fish with limited dispersal, Acanthochromis polyacanthus, within the Great Barrier Reef and the Coral Sea. Evolution 55:2263–2273
Planes S, Lecaillon G, Lenfant P, Meekan M (2002) Genetic and demographic variation in new recruits of Neso unicornis. J Fish Biol 61:1033–1049
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Purcell JFH, Cowen RK, Hughes CR, Williams DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proc R Soc Lond B Biol Sci 273:1483–1490
Rannala B, Mountain JL (1997) Detecting immigration using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201
Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics 124:397–406
Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006
Rhodes KL, Lewis RI, Chapman RW, Sadovy Y (2003) Genetic structure of camouflage grouper, Epinephelus polyphekadion (Pisces:Serranidae), in the western central Pacific. Mar Biol 142:771–776
Richards VP, Thomas JD, Stanhope MJ, Shivji MS (2007) Genetic connectivity in the Florida reef system: comparative phylogeography of commensal invertebrates with contrasting reproductive strategies. Mol Ecol 16:139–157
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
Rocha LA, Bass AL, Robertson DR, Bowen BW (2002) Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei:Acanthuridae). Mol Ecol 11:243–252
Rocha LA, Robertson DR, Rocha CR, Van Tassell JL, Craig MT, Bowen BW (2005a) Recent invasion of the tropical Atlantic by an Indo-Pacific coral reef fish. Mol Ecol 14:3921–3928
Rocha LA, Robertson DR, Roman J, Bowen BW (2005b) Ecological speciation in tropical reef fishes. Proc R Soc Lond B Biol Sci 272:573–579
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Rosenberg NA (2003) The shapes of neutral gene genealogies in two species: probabilities of monophyly, paraphyly, and polyphyly in a coalescent model. Evolution 57:1465–1477
Rosenberg NA, Burke T, Elo K, Feldmann MW, Freidlin PJ, Groenen MAM, Hillel J, Maki-Tanila A, Tixier-Boichard M, Vignal A, Wimmers K, Weigend S (2001) Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics 159:699–713
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Ruzzante DE (1998) A comparison of several measures of genetic distance and population structure with microsatellite data: bias and sampling variances. Can J Fish Aquat Sci 55:1–14
Ryman N, Palm S, Andre C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palme A, Ruzzante DE (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045
Sale PF (1980) The ecology of fishes on coral reefs. Oceanogr Mar Biol Annu Rev 18:367–421
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
Severance EG, Karl SA (2006) Contrasting population genetic structures of sympatric, mass-spawning Caribbean corals. Mar Biol 150:57–68
Shearer TL, Coffroth MA (2004) Isolation of microsatellite loci from the scleractinain corals Montastrea cavernosa and Porites astreoides. Mol Ecol Notes 4:11–19
Shearer TL, van Oppen MJH, Romano SL, Wörheide G (2002) Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol Ecol 11:2475–2487
Shulman MJ, Bermingham E (1995) Early-life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910
Silberman JD, Sarver SK, Walsh PJ (1994) Mitochondrial DNA variation and population-structure in the spiny lobster Panulirus argus. Mar Biol 120:601–608
Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279
Slatkin M (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73
Starck WA, Colin PL (1978) Gramma linki—new species of grammid fish from tropical Western Atlantic. Bull Mar Sci 28:146–152
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Taylor MS, Hellberg ME (2006) Comparative phylogeography of a genus of coral reef fishes: biogeographical and genetical concordance in the Caribbean. Mol Ecol 15:695–707
Thacker CE (2004) Population structure in two species of the reef goby Gnatholepis (Teleostei:Perciformes) among four South Pacific island groups. Coral Reefs 23:357–366
Thompson AR, Thacker CE, Shaw EY (2005) Phylogeography of marine mutualists: parallel patterns of genetic structure between obligate goby and shrimp partners. Mol Ecol 14:3557–3572
Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45
Van Oppen MJH, Gates RD (2006) Conservation genetics and the resilience of reef-building corals. Mol Ecol 15:3863–3883
Van Oppen MJH, Willis BL, van Vugt HWJA, Miller DJ (2000) Examination of species boundaries in the Acropora cervicornis group (Scleractinia, Cnidaria) using nuclear DNA sequence analyses. Mol Ecol 9:1363–1373
Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenies. Mol Ecol 13:2763–2772
Wang Z, Baker AJ, Hill GE, Edwards SV (2003) Reconciling actual and inferred population histories in the house finch (Carpodacus mexicanus) by AFLP analysis. Evolution 57:2852–2864
Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Heredity 89:438–450
Waples RS, 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
Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469
Wares JP, Barber PH, Ross-Ibarra J, Sotka EE, Toonen RJ (2006) Mitochondrial DNA and population size. Science 314:1388–1389
Wei N-WV, Wallace CC, Dai C-F, Moothien Pillay KR, Chen CA (2006) Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Sclertinia; Acroporidae). Zool Stud 45:404–418
Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: F-ST not equal 1/(4Nm + 1). Heredity 82:117–125
Williams ST, Benzie JAH (1997) Indo-West Pacific patterns of genetic differentiation in the high dispersal starfish Linckia laevigata. Mol Ecol 6:559–573
Wilson GA, Rannala B (2003) Baysian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191
Winans G (1980) Geographic variation in the milkfish Chanos chanos. I. Biochemical evidence. Evolution 34:558–574
Wörheide G (2006) Low variation in partial cytochrome oxidase subunit I (COI) mitochondrial sequences in the coralline demosponge Astrosclera willeyana across the Indo-Pacific. Mar Biol 148:907–912
Wörheide G, Nichols SA, Goldberg J (2004) Intragenomic variation of the rDNA internal transcribed spacers in sponges (Phylum Porifera): implications for phylogenetic studies. Mol Phylogenet Evol 33:816–830
Wright S (1943) Isolation by distance. Genetics 28:114–138
Zartman CE, McDaniel SF, Shaw AJ (2006) Experimental habitat fragmentation increases linkage disequilibrium but does not affect genetic diversity or population structure in the Amazonian liverwort Radula flaccida. Mol Ecol 15:2305–2315
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I thank Iliana Baums, Mike Taylor, Rob Toonen and an anonymous reviewer for comments on the manuscript. This work has been supported by the National Science Foundation (OCE-0550270) and the National Maine Fisheries Southeast Science Center.
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Hellberg, M.E. Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26, 463–473 (2007). https://doi.org/10.1007/s00338-007-0205-2
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DOI: https://doi.org/10.1007/s00338-007-0205-2