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Thinking outside the barrier: neutral and adaptive divergence in Indo-Pacific coral reef faunas

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Abstract

Population divergence in marine species frequently occurs where there is no conspicuous geographic feature to mark a population boundary. In the absence of a discernible barrier to gene flow, strong conclusions about the processes that drive population divergence in the ocean are often elusive. Because our knowledge of patterns far outpaces our understanding of processes, there is a need to expand hypotheses regarding population divergence in marine species. Here, I posit that certain population-level processes (range expansion, spatial diffusion constraints and metapopulation dynamics) are primary causes of spatial structuring in marine populations rather than auxiliary factors that aid divergence across an incomplete physical barrier to gene flow. In particular, I use examples from Indo-Pacific coral reef organisms to illustrate this point. In connection, spatial patterns of adaptive divergence are unlikely to be correlated with patterns of selectively neutral divergence in many cases, as the processes affecting adaptive and neutral genetic markers are different.

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References

  • Avise JC (1994) Molecular markers, natural history and evolution. Chapman & Hall, New York

    Book  Google Scholar 

  • Banks SC, Cary GJ, Smith AL, Davies ID, Driscoll DA, Gill AM, Lindenmayer DB, Peakall R (2013) How does ecological disturbance influence genetic diversity? Trends Ecol Evol 28:670–679

    Article  PubMed  Google Scholar 

  • Belanger CL, Jablonski D, Roy K, Berke SK, Krug AZ, Valentine JW (2012) Global environmental predictors of benthic marine biogeographic structure. Proc Natl Acad Sci USA 109:14046–14051

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20

    Article  PubMed  CAS  Google Scholar 

  • Boström-Einarsson L, Bonin MC, Monday PL, Jones GP (2013) Strong intraspecific competition and habitat selectivity influence abundance of a coral dwelling damselfish. J Exp Mar Biol Ecol 448:85–92

    Article  Google Scholar 

  • Bowen BW, Rocha LA, Toonen RJ, Karl SA, Lab T (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366

    Article  PubMed  Google Scholar 

  • Bowen BW, Shanker K, Yasuda N (2014) Phylogeography unplugged: comparative surveys in the genomic era. Bull Mar Sci 90:13–46

    Article  Google Scholar 

  • Carpenter KE, Barber PH, Crandall ED, Manjaji-Matsumoto BM, Juinio-Me-ez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the coral triangle and implications for marine management. J Mar Biol 2011. Article ID 396982

  • Conover DO, Clarke LM, Munch SB, Wagner GN (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J Fish Biol 69:21–47

    Article  Google Scholar 

  • Corander J, Majander KK, Cheng L, Merila J (2013) High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Mol Ecol 22:2931–2940

    Article  PubMed  CAS  Google Scholar 

  • Cowman PF, Bellwood DR (2013) Vicariance across major marine biogeographic barriers: temporal concordance and the relative importance of soft vs. hard barriers. P R Soc B 280:20131541

  • Craig MT (2008) The goldrim surgeonfish (Acanthurus nigricans; Acanthuridae) from Diego Garcia, Chagos Archipelago: first record for the central Indian Ocean. Zootaxa 1850:65–68

    Google Scholar 

  • Craig MT, Eble JA, Bowen BW, Robertson DR (2007) High genetic connectivity across the Indian and Pacific Oceans in the reef fish Myripristis berndti (Holocentridae). Mar Ecol Prog Ser 334:245–254

    Article  CAS  Google Scholar 

  • Crandall ED, Jones ME, Munoz MM, Akinronbi B, Erdmann MV, Barber PH (2008) Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle. Mol Ecol 17:5276–5290

    Article  PubMed  Google Scholar 

  • Crandall ED, Taffel JR, Barber PH (2010) High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae). Heredity 104:563–572

    Article  PubMed  CAS  Google Scholar 

  • Crandall ED, Treml EA, Barber PH (2012a) Coalescent and biophysical models of stepping-stone gene flow in neritid snails. Mol Ecol 21:5579–5598

    Article  PubMed  Google Scholar 

  • Crandall ED, Sbrocco EJ, DeBoer TS, Barber PH, Carpenter KE (2012b) Expansion dating: calibrating molecular clocks in marine species from expansions onto the Sunda Shelf Following the Last Glacial Maximum. Mol Biol Evol 29:707–719

    Article  PubMed  CAS  Google Scholar 

  • Crandall ED, Treml EA, Liggins L, Gleeson L, Yasuda N, Barber PH, Wörheid G, Riginos C (2014) Return of the ghosts of dispersal past: historical spread and contemporary gene flow in the blue sea star Linkia laevigata. Bull Mar Sci 90:399–425

    Article  Google Scholar 

  • de Aguiar MA, Baranger M, Baptestini EM, Kaufman L, Bar-Yam Y (2009) Global patterns of speciation and diversity. Nature 460:384–387

    Article  PubMed  Google Scholar 

  • DiBattista JD, Rocha LA, Craig MT, Feldheim KA, Bowen BW (2012a) Phylogeography of two closely related Indo-Pacific butterflyfishes reveals divergent evolutionary histories and discordant results from mtDNA and microsatellites. J Hered 103:617–629

    Article  PubMed  CAS  Google Scholar 

  • DiBattista JD, Waldrop E, Bowen BW, Schultz JK, Gaither MR, Pyle RL, Rocha LA (2012b) Twisted sister species of pygmy angelfishes: discordance between taxonomy, coloration, and phylogenetics. Coral Reefs 31:839–851

    Article  Google Scholar 

  • Drew J, Barber PH (2009) Sequential cladogenesis of the reef fish Pomacentrus moluccensis (Pomacentridae) supports the peripheral origin of marine biodiversity in the Indo-Australian archipelago. Mol Phylogenet Evol 53:335–339

    Article  PubMed  CAS  Google Scholar 

  • Ekman S (1953) Zoogeography of the sea. Sidgwick and Jackson, London

    Google Scholar 

  • Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351

    Article  PubMed  Google Scholar 

  • Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol S 40:481–501

    Article  Google Scholar 

  • Fayard J, Klein EK, Lefevre F (2009) Long distance dispersal and the fate of a gene from the colonization front. J Evol Biol 22:2171–2182

    Article  PubMed  CAS  Google Scholar 

  • Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648

    Article  Google Scholar 

  • Gaither MR, Jones SA, Kelley C, Newman SJ, Sorenson L, Bowen BW (2011) High connectivity in the deepwater snapper Pristipomoides filamentosus (Lutjanidae) across the Indo-Pacific with Isolation of the Hawaiian Archipelago. PLoS ONE 6:e28913. doi:10.1371/journal.pone.0028913

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hanebuth T, Stattegger K, Grootes PM (2000) Rapid flooding of the Sunda Shelf: a late-glacial sea-level record. Science 288:1033–1035

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hellberg ME (2009) Gene flow and isolation among populations of marine animals. Annu Rev Ecol Evol Syst 40:291–310

    Article  Google Scholar 

  • Hemmer-Hansen J, Nielsen EE, Therkildsen NO, Taylor MI, Ogden R, Geffen AJ, Bekkevold D, Helyar S, Pampoulie C, Johansen T, Carvalho GR, Consortium F (2013) A genomic island linked to ecotype divergence in Atlantic cod. Mol Ecol 22:2653–2667

    Article  PubMed  Google Scholar 

  • Hixon MA, Jones GP (2005) Competition predation and density-dependent mortality in demersal marine fishes. Ecology 86:2847–2859

    Article  Google Scholar 

  • Hobbs JPA, Frisch AJ, Allen GR, Van Herwerden L (2009) Marine hybrid hotspot at Indo-Pacific biogeographic border. Biol Lett 5:258–261

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobbs JPA, Ayling AM, Choat JH, Gilligan JJ, Mcdonald CA, Neilson J, Newman SJ (2010) New records of marine fishes illustrate the biogeographic importance of Christmas Island, Indian Ocean. Zootaxa 2422:63–68

    Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21:797–807

    Article  Google Scholar 

  • Horne JB, van Herwerden L (2013) Long-term panmixia in a cosmopolitan Indo-Pacific coral reef fish and a nebulous genetic boundary with its broadly sympatric sister species. J Evol Biol 26:783–799

    Article  PubMed  CAS  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 

  • Horne JB, Momigliano P, Welch DJ, Newman SJ, van Herwerden L (2012) Searching for common threads in threadfins: comparative phylogeography of Australian polynemids in space and time. Mar Ecol Prog Ser 449:263–276

    Article  Google Scholar 

  • Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

    Article  Google Scholar 

  • Jones GP, Almany GR, Russ GR, Sale PF, Steneck RS, van Oppen MJH, Willis BL (2009) Larval retention and connectivity among populations of corals and coral reef fishes. Coral Reefs 28:307–325

    Article  Google Scholar 

  • Karl SA, Toonen RJ, Grant WS, Bowen BW (2012) Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 21:4171–4189

    Article  PubMed  CAS  Google Scholar 

  • Keith SA, Baird AH, Hughes TP, Madin JS, Connolly SR (2013) Faunal breaks and species composition of Indo-Pacific corals: the role of plate tectonics, environment and habitat distribution. Proc R Soc B 280:20130818

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Keyse J, Crandall ED, Toonen RJ, Meyer CP, Treml EA, Riginos C (2014) The scope of published population genetic data for Indo-Pacific marine fauna and future research opportunities in the region. Bull Mar Sci 90:47–78

    Article  Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kokko H, López-Sepulcre A (2006) From individual dispersal to species ranges: perspectives for a changing world. Science 313:789–791

    Article  PubMed  CAS  Google Scholar 

  • Kritzer JP, Sale PF (2006) Marine metapopulations. Academic Press, London

    Google Scholar 

  • Krug AZ, Jablonski D, Valentine JW (2008) Species-genus ratios reflect a global history of diversification and range expansion in marine bivalves. Proc R Soc B 275:1117–1123

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuo CH, Avise JC (2005) Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica 124:179–186

    Article  PubMed  Google Scholar 

  • Lessios HA (2008) The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu Rev Ecol Evol S 39:63–91

    Article  Google Scholar 

  • Lessios HA, Robertson DR (2006) Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proc R Soc B 273:2201–2208

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marie AD, van Herwerden L, Choat JH, Hobbs JPA (2007) Hybridization of reef fishes at the Indo-Pacific biogeographic barrier: a case study. Coral Reefs 26:841–850

    Article  Google Scholar 

  • Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

    Article  PubMed  CAS  Google Scholar 

  • Mayr E (1954) Geographic speciation in tropical echinoids. Evolution 8:1–18

    Article  Google Scholar 

  • Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59:113–125

    Article  PubMed  Google Scholar 

  • Montanari SR, van Herwerden L, Pratchett MS, Hobbs JPA, Fugedi A (2012) Reef fish hybridization: lessons learnt from butterflyfishes (genus Chaetodon). Ecol Evol 2:310–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Mora C, Treml EA, Roberts J, Crosby K, Roy D, Tittensor DP (2012) High connectivity among habitats precludes the relationship between dispersal and range size in tropical reef fishes. Ecography 35:89–96

    Article  Google Scholar 

  • Nichols RA, Hewitt GM (1994) The genetic consequences of long-distance dispersal during colonization. Heredity 72:312–317

    Article  Google Scholar 

  • Nielsen EE, Hemmer-Hansen J, Larsen PF, Bekkevold D (2009) Population genomics of marine fishes: identifying adaptive variation in space and time. Mol Ecol 18:3128–3150

    Article  PubMed  Google Scholar 

  • Norris RD, Hull PM (2012) The temporal dimension of marine speciation. Evol Ecol 26:393–415

    Article  Google Scholar 

  • Nuryanto A, Kochzius M (2009) Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima. Coral Reefs 28:607–619

    Article  Google Scholar 

  • Oleksyk TK, Smith MW, O’Brien SJ (2010) Genome-wide scans for footprints of natural selection. Philos Trans R Soc B 365:185–205

    Article  CAS  Google Scholar 

  • Oppo DW, Rosenthal Y (2010) The great Indo-Pacific communicator. Science 328:1492–1494

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Pannell JR, Charlesworth B (2000) Effects of metapopulation processes on measures of genetic diversity. Philos Trans R Soc B 355:1851–1864

    Article  CAS  Google Scholar 

  • Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L (2013) On the accumulation of deleterious mutations during range expansions. Mol Ecol 22:5972–5982

    Article  PubMed  CAS  Google Scholar 

  • Pespeni MH, Palumbi SR (2010) The purple sea urchin genome suggests local adaptation along a latitudinal gradient despite high gene flow. Integr Comp Biol 50:E136–E136

    Google Scholar 

  • Potts DC (1983) Evolutionary disequilibrium among Indo-Pacific corals. Bull Mar Sci 33:619–632

    Google Scholar 

  • Quenouille B, Hubert N, Bermingham E, Planes S (2011) Speciation in tropical seas: allopatry followed by range change. Mol Phylogenet Evol 58:546–552

    Article  PubMed  Google Scholar 

  • Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37:227–268

    Google Scholar 

  • Raynal JM, Crandall ED, Barber PH, Mahardika GM, Lagman MC, Carpenter KE (2014) Basin isolation and oceanographic features influencing lineage divergence in the humbug damselfish (Dascyllus aruanus) in the Coral Triangle. Bull Mar Sci 90:513–532

    Article  Google Scholar 

  • Reece JS, Bowen BW, Joshi K, Goz V, Larson A (2010) Phylogeography of two moray eels indicates high dispersal throughout the Indo-Pacific. J Hered 101:391–402

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rocha LA, Bowen BW (2008) Speciation in coral-reef fishes. J Fish Biol 72:1101–1121

    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 

  • Selkoe KA, Gaggiotti OE, Tobo Laboratory, Bowen BW, Toonen RJ (2014) Emergent patterns of population genetic structure for a coral reef community. Mol Ecol. doi:10.1111/mec.12804

    PubMed  Google Scholar 

  • Slatkin M (1977) Gene flow and genetic drift in a species subject to frequent local extinctions. Theor Popul Biol 12:253–262

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural-populations. Science 236:787–792

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M, Excoffier L (2012) Serial founder effects during range expansion: a spatial analog of genetic drift. Genetics 191:171–181

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Springer VG, Williams JT (1990) Widely distributed pacific plate endemics and lowered sea-level. Bull Mar Sci 47:631–640

    Google Scholar 

  • Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343

    Article  PubMed  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Wakeley J (2004) Metapopulation models for historical inference. Mol Ecol 13:865–875

    Article  PubMed  Google Scholar 

  • Wakeley J, Aliacar N (2001) Gene genealogies in a metapopulation. Genetics 159:893–905

    PubMed  CAS  PubMed Central  Google Scholar 

  • Waters JM (2011) Competitive exclusion: phylogeography’s ‘elephant in the room’? Mol Ecol 20:4388–4394

    Article  PubMed  Google Scholar 

  • Wolanski E, Lambrechts J, Thomas C, Deleersnijder E (2013) The net water circulation through Torres strait. Cont Shelf Res 64:66–74

    Article  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wright JD, Sheridan RE, Miller KG, Uptegrove J, Cramer BS, Browning JV (2009) Late Pleistocene sea level on the New Jersey Margin: implications to eustasy and deep-sea temperature. Glob Planet Chang 66:93–99

    Article  Google Scholar 

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Acknowledgments

I’d like to extend thanks to Howard Choat, Kendall Clements and two reviewers for helpful comments.

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Correspondence to John B. Horne.

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Horne, J.B. Thinking outside the barrier: neutral and adaptive divergence in Indo-Pacific coral reef faunas. Evol Ecol 28, 991–1002 (2014). https://doi.org/10.1007/s10682-014-9724-9

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