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Exploring Coral Reefs Using the Tools of Molecular Genetics

Chapter

Abstract

The tools of molecular genetics have been transformed over the last decades and have in turn transformed our understanding of coral reefs. Initially limited to information on single genes, we are now capable of analyzing entire genomes. These developments make it possible to do many things that were either impossible or extremely difficult before: identify cryptic species, microbes, larvae and gut contents; determine relationships among populations and species; characterize reproductive and dispersal patterns; infer mechanisms of speciation; and soon perhaps embark on genetic engineering. Notably, many aspects of coral reef conservation can and will increasingly benefit from insights derived from the application of molecular genetic tools.

Keywords

Identification Bioinformatics Barcoding Phylogenetics Speciation 

Notes

Glossary1

Barcode

is a standard short stretch of DNA that is unique to each species and therefore used to delineate species or identify unknown specimens. In animals, the most common barcode is a 658 bp segment of the mitochondrial cytochrome c oxidase subunit I gene.

Barcode of Life Data Systems (BOLD)

is an online platform for the storage, analysis and publication of DNA barcode records.

Coalescent theory

uses a mathematical model to reconstruct the genealogy of genes back to their common ancestor.

DNA microarray

analyses are most commonly used to measure the expression levels of a large number of target genes simultaneously. Microarray chips contain thousands of microscopic spots where specific DNA probes are inserted. The relative abundance of target genes is quantified via fluorescence when target DNA hybridizes to probes.

Environmental DNA

is the sum total of DNA in an environmental sample. It comprises not only the DNA from intact organisms in the sample, but also other sources of cellular or extracellular DNA released by an organism into the environment (e.g. in mucus, gametes, feces).

Expressed Sequence Tags (ESTs)

are portions of complementary DNA (cDNA) that are constructed from messenger RNA. These fragments of expressed coding genes are used for gene discovery, mapping, gene prediction, gene expression and polymorphism analysis.

GenBank

is a publicly available collection of DNA sequences hosted by the National Institute of Health (NIH).

Genome

is the entirety of the genetic information contained in an organism.

Genomic library

is the collection of DNA fragments representing the genome of an organism stored as short fragments within many individual bacteria or yeast cells. Such collections facilitated early efforts at genome sequencing.

Genomics

is the quantitative analysis of the genome.

High-throughput sequencing

technologies (i.e. pyrosequencing, semiconductor sequencing) produce millions of sequences concurrently within a few hours. These technologies have drastically lowered the cost of studies that require large amounts of sequence data.

Metabarcoding

uses DNA-based species identification and high-throughput sequencing as a cost- and time-effective way to infer the species composition of environmental samples (e.g. plankton, sediments).

Metagenomics

is the study of the genetic material collected from the environment. It provides a profile of diversity, including many small organisms that cannot be cultured, and a detailed characterization of the metabolic genes present in an environmental sample.

MicroRNA (miRNA)

are short non-coding RNA molecules (approximately 22 nucleotides in length) found in the genomes of plants, animals and some viruses that play a key role in the regulation of gene expression.

Microsatellites

are short repeating DNA sequences (two to ten base pairs in length) found across the genome of a species. Because they evolve rapidly, they are especially useful for population studies and individual fingerprinting.

Molecular clock

is a mathematical approach that uses the fossil record and rates of DNA sequence evolution to estimate the time since two species or a group of species diverged.

Molecular cloning

is a technique that uses a host organism (easy-to-grow bacteria) to replicate a single DNA molecule into multiple identical copies.

Nuclear DNA/organelle DNA/ribosomal DNA

are different types of DNA found in the nucleus and organelles (such as the mitochondria, mtDNA) of eukaryotic organisms. Ribosomal DNA (rDNA) refers to the genes that code the RNA that makes up the ribosomes.

Operational Taxonomic Units (OTUs)

are low-level taxa often equivalent to species that are defined genetically rather than being identified to species using traditional morphological methods.

Phylogeography

is the study of historical processes (i.e. vicariance, population expansion) that explain the present day distribution of populations or species using mitochondrial/nuclear gene genealogies.

Polymerase Chain Reaction (PCR)

is used to replicate a single copy of a DNA fragment into millions of copies of the same DNA fragment within a few hours, allowing the DNA to be sequenced.

Primers

are strands of nucleic acids used as a starting point for DNA replication during the polymerase chain reaction.

Protein electrophoresis

is a laboratory technique used to separate individual proteins from complex mixtures using differences in size and electric charge. This was one of the first molecular genetic tools to be used in coral reef studies.

Proteomics

is the study of the composition, structure and function of the whole set of proteins produced by the coding genes of an organism.

Restriction-site Associated DNA (or RAD)

sequencing is a method used to sample thousands of random parts of the genome of many individuals simultaneously using high-throughput sequencing. Because it analyzes a small fraction of the entire genome, it allows affordable study of many markers across the genome for population genetic studies in non-model species.

Restriction Fragment Length Polymorphism (RFLP)

analysis is a DNA profiling technique that uses restriction enzymes to cut stretches of DNA at specific genetic sequences within a gene, followed by analysis of variation in the lengths of the fragments.

Sanger Capillary Sequencing

is an automated DNA sequencing technology developed in 1977 by Fred Sanger. It uses a laser to read the position and identity of dye-labeled nucleotides on DNA fragments previously amplified via PCR.

Shotgun Sequencing

is a method used to read the sequence of very long stretches of DNA (i.e. genomes). The process involves shearing the long DNA stretch into smaller fragments (<1000 bp) that can be sequenced individually and later reassembled bioinformatically using overlapping regions.

Single Nucleotide Polymorphism (SNP)

is a genetic variant at one position in a DNA sequence shared by multiple individuals in a population. The frequency of different SNP alleles can be analyzed with respect to such factors as environment or geographic locale.

Transcriptomics

is the study of sets of genes expressed in the genome of a given organism under specific conditions.

References

  1. Almany GR, Hamilton RJ, Bode M et al (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23:626–630CrossRefPubMedGoogle Scholar
  2. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  3. Baker DM, Weigt L, Fogel M et al (2013) Ancient DNA from coral-hosted Symbiodinium reveal a static mutualism over the last 172 years. PLoS One 8:e55057PubMedCentralCrossRefPubMedGoogle Scholar
  4. Barber PH, Palumbi SR, Erdmann MV (2000) Biogeography – a marine Wallace’s line? Nature 406:692–693CrossRefPubMedGoogle Scholar
  5. Barrott KL, Rodriguez-Brito B, Janouskovec J et al (2011) Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environ Microbiol 13:1192–1204CrossRefGoogle Scholar
  6. Bascompte J, Melián CJ, Sala E (2005) Interaction strength combinations and the overfishing of a marine food web. Proc Natl Acad Sci U S A 102:5443–5447PubMedCentralCrossRefPubMedGoogle Scholar
  7. Bernardi G, Beldade R, Holbrook SJ et al (2012) Full-sibs in cohorts of newly settled coral reef fishes. PLoS One 7:e44953PubMedCentralCrossRefPubMedGoogle Scholar
  8. Betancur-R R, Hines A, Acero A et al (2011) Reconstructing the lionfish invasion: insights into Greater Caribbean biogeography. J Biogeogr 38:1281–1293CrossRefGoogle Scholar
  9. Bowen BW, Rocha LA, Toonen RJ et al (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366CrossRefPubMedGoogle Scholar
  10. Carlon DB, Lippé C (2011) Estimation of mating systems in short and tall ecomorphs of the coral Favia fragum. Mol Ecol 20:812–828CrossRefPubMedGoogle Scholar
  11. Closek CJ, Sunagawa S, DeSalvo MK et al (2014) Coral transcriptome and bacterial community profiles reveal distinct yellow band disease states in Orbicella faveolata. ISME J 8:2411–2422CrossRefPubMedGoogle Scholar
  12. Combosch DJ, Vollmer SV (2013) Mixed asexual and sexual reproduction in the Indo-Pacific reef coral Pocillopora damicornis. Ecol Evol 3:3379–3387PubMedCentralPubMedGoogle Scholar
  13. Cox CE, Jones CD, Wares JP et al (2013) Genetic testing reveals some mislabelling but general compliance with a ban on herbivorous fish harvesting in Belize. Conserv Lett 6:132–140CrossRefGoogle Scholar
  14. Delrieu-Trottin E, Maynard J, Planes S (2014) Endemic and widespread coral reef fishes have similar mitochondrial genetic diversity. Proc R Soc B 281:20141068Google Scholar
  15. Dinsdale EA, Pantos O, Smriga S et al (2008) Microbial ecology of four coral atolls in the Northern Line Islands. PLoS One 3:e1584PubMedCentralCrossRefPubMedGoogle Scholar
  16. Drake JL, Mass T, Haramaty L et al (2013) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci U S A 110:3788–3793PubMedCentralCrossRefPubMedGoogle Scholar
  17. Duffy JE (1996) Species boundaries, specialization, and the radiation of sponge-dwelling alpheid shrimp. Biol J Linn Soc 58:307–324CrossRefGoogle Scholar
  18. Duran S, Rützler K (2006) Ecological speciation in a Caribbean marine sponge. Mol Phylogenet Evol 40:292–297CrossRefPubMedGoogle Scholar
  19. Fogarty ND, Vollmer SV, Levitan DR (2012) Weak prezygotic isolating mechanisms in threatened Acropora corals. PLoS One 7:e30486PubMedCentralCrossRefPubMedGoogle Scholar
  20. Foster NL, Baums IB, Sanchez JA et al (2013) Hurricane-driven patterns of clonality in an ecosystem engineer: the Caribbean coral Montastraea annularis. PLoS One 8:e53283PubMedCentralCrossRefPubMedGoogle Scholar
  21. Fukami H, Budd AF, Levitan DR et al (2004) Geographical differences in species boundaries among members of the Montastraea anularis complex based on molecular and morphological markers. Evolution 58:324–337CrossRefPubMedGoogle Scholar
  22. Fukami H, Chen CA, Budd AF et al (2008) Mitochondrial and nuclear genes suggest that stony corals are monophyletic but most families of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum Cnidaria). PLoS One 3:e3222PubMedCentralCrossRefPubMedGoogle Scholar
  23. Hemond EM, Kaluziak ST, Vollmer SV (2014) The genetics of colony form and function in Caribbean Acropora corals. BMC Genomics 15:1133PubMedCentralCrossRefPubMedGoogle Scholar
  24. Huang D, Roy K (2015) The future of evolutionary diversity in reef corals. Philos Trans Roy Soc B 370:20140010Google Scholar
  25. Huang D, Meier R, Todd PA et al (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174CrossRefPubMedGoogle Scholar
  26. Huang D, Benzoni F, Arrigoni R et al (2014) Towards a phylogenetic classification of reef corals: the Indo-Pacific genera Merulina, Goniastrea and Scapophyllia (Scleractinia, Merulindae). Zool Scr 43:531–548CrossRefGoogle Scholar
  27. Hubert N, Espiau B, Meyer C et al (2015) Identifying the ichthyoplankton of a coral reef using DNA barcodes. Mol Ecol Resour 15:57–67CrossRefPubMedGoogle Scholar
  28. Hume BCC, D’Angelo C, Smith EG et al (2015) Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world’s hottest sea, the Persian/Arabian Gulf. Sci Rep 5:8562PubMedCentralCrossRefPubMedGoogle Scholar
  29. Jackson JBC, Cheetham AH (1990) Evolutionary significance of morphospecies: a test with cheilostome Bryozoa. Science 248:579–583CrossRefPubMedGoogle Scholar
  30. Kelly LW, Williams GJ, Barott KL et al (2014) Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc Natl Acad Sci 111:10227–10232PubMedCentralCrossRefPubMedGoogle Scholar
  31. Keshavmurthy S, Yang S-Y, Alamaru A et al (2013) DNA barcoding reveals the coral “laboratory-rat”, Stylophora pistillata encompasses multiple identities. Sci Rep 3:1520PubMedCentralCrossRefPubMedGoogle Scholar
  32. Kitahara MV, Cairns SD, Stolarski J et al (2010) A comprehensive phylogenetic analysis of the Scleractinia (Cnidaria, Anthozoa) based on mitochondrial COI sequence data. PLoS One 5:e11490PubMedCentralCrossRefPubMedGoogle Scholar
  33. Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90CrossRefGoogle Scholar
  34. Knowlton N, Jackson JBC (1994) New taxonomy and niche partitioning on coral reefs: jack of all trades or master of some? Trends Ecol Evol 9:7–9CrossRefPubMedGoogle Scholar
  35. Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc B 265:2257–2263PubMedCentralCrossRefGoogle Scholar
  36. Lasker HR, Gutierrez-Rodriguez C, Bala K et al (2008) Male reproductive success during spawning events of the octocoral Pseudopterogorgia elisabethae. Mar Ecol Prog Ser 367:153–161CrossRefGoogle Scholar
  37. Leray M, Knowlton N (2015) DNA barcoding and metabarcoding reveal patterns of diversity in cryptic benthic communities. Proc Natl Acad Sci U S A 112:2076–2081PubMedCentralCrossRefPubMedGoogle Scholar
  38. Leray M, Yang JY, Meyer CP et al (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front Zool 10:34PubMedCentralCrossRefPubMedGoogle Scholar
  39. Lessios HA (2007) Reproductive isolation between species of sea urchins. Bull Mar Sci 81:191–208Google Scholar
  40. Lessios HA (2008) The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Ann Rev Ecol Evol Syst 39:63–91CrossRefGoogle Scholar
  41. Lessios HA (2011) Speciation genes in free-spawning marine invertebrates. Integr Comp Biol 51:456–465CrossRefPubMedGoogle Scholar
  42. Lessios HA, Robertson DR (2006) Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proc R Soc B 273:2201–2208PubMedCentralCrossRefPubMedGoogle Scholar
  43. Lessios HA, Garrido MJ, Kessing BD (2001) Demographic history of Diadema antillarum, a keystone herbivore on Caribbean reefs. Proc R Soc B 268:2347–2353PubMedCentralCrossRefPubMedGoogle Scholar
  44. Levitan DR, Fogarty ND, Jara J et al (2011) Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex. Evolution 65:1254–1270CrossRefPubMedGoogle Scholar
  45. Levy O, Appelbaum L, Leggat W et al (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–470CrossRefPubMedGoogle Scholar
  46. Libro S, Kaluziak ST, Vollmer SV (2013) RNA-seq profiles of immune related genes in the staghorn coral Acropora cervicornis infected with white band disease. PLoS One 8:e81821PubMedCentralCrossRefPubMedGoogle Scholar
  47. Lim YW, Cuevas DA, Silva GGZ et al (2014) Sequencing at sea: challenges and experiences in Ion Torrent PGM sequencing during the 2013 Southern Line Islands Research Expedition. Peer J 2:e520PubMedCentralCrossRefPubMedGoogle Scholar
  48. Lundgren P, Vera JC, Peplow L et al (2013) Genotype-environment correlations in corals from the Great Barrier Reef. BMC Genet 14:9PubMedCentralCrossRefPubMedGoogle Scholar
  49. Marko PB, Lee SC, Rice AM et al (2004) Fisheries: mislabeling of a depleted reef fish. Nature 430:309–310CrossRefPubMedGoogle Scholar
  50. McFadden CS, Benayahu Y, Pante E et al (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Resour 11:19–31CrossRefPubMedGoogle Scholar
  51. Meyer CP (2003) Molecular systematics of cowries (Gastropoda: Cypraeidae) and diversification patterns in the tropics. Biol J Linn Soc 79:401–459CrossRefGoogle Scholar
  52. Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:e422PubMedCentralCrossRefPubMedGoogle Scholar
  53. Meyer CP, Geller JB, Paulay G (2005) Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 59:113–125CrossRefPubMedGoogle Scholar
  54. Moya A, Huisman L, Foret S et al (2015) Rapid acclimation of juvenile corals to CO2-mediated acidification by upregulation of heat shock and Bcl-2 genes. Mol Ecol 24:438–452CrossRefPubMedGoogle Scholar
  55. Munday PL, van Herwerden L, Dudgeon CL (2004) Evidence of sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504CrossRefPubMedGoogle Scholar
  56. Palumbi SR, Vollmer S, Romano S et al (2012) The role of genes in understanding the evolutionary ecology of reef building corals. Evol Ecol 26:317–335CrossRefGoogle Scholar
  57. Plaisance L, Caley MJ, Brainard RE et al (2011) The diversity of coral reefs: what are we missing? PLoS One 6:e325026CrossRefGoogle Scholar
  58. Pollock FJ, Morris PJ, Willis BL et al (2011) The urgent need for robust coral diagnostics. PLoS Pathog 7:e1002183PubMedCentralCrossRefPubMedGoogle Scholar
  59. Prada C, DeBiasse MB, Neigel JE et al (2014a) Genetic delineation among branching Caribbean Porites corals. Coral Reefs 33:1019–1030CrossRefGoogle Scholar
  60. Prada C, Mcilroy SE, Beltran DM et al (2014b) Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Mol Ecol 23:3330–3340CrossRefPubMedGoogle Scholar
  61. Puebla O, Bermingham E, Guichard F (2012) Pairing dynamics and the origin of species. Proc R Soc B 279:1085–1092PubMedCentralCrossRefPubMedGoogle Scholar
  62. Puillandre N, Strong EE, Bouchet P et al (2009) Identifying gastropod spawn from DNA barcodes: possible but not yet practicable. Mol Ecol Resour 9:1311–1321CrossRefPubMedGoogle Scholar
  63. Puillandre N, Bouchet P, Duda TF et al (2014) Molecular phylogeny and evolution of the cone snails (Gastropoda, Conoidea). Mol Phylogenet Evol 78:290–303CrossRefPubMedGoogle Scholar
  64. Puritz JB, Keever CC, Addison JA et al (2012) Extraordinarily rapid life-history divergence between Cryptasterina sea star species. Proc R Soc B 279:3914–3922PubMedCentralCrossRefPubMedGoogle Scholar
  65. Quenouille B, Bermingham E, Planes S (2004) Molecular systematics of the damselfishes (Teleostei: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Mol Phylogenet Evol 31:66–88CrossRefPubMedGoogle Scholar
  66. Quigley KM, Davies SW, Kenkel CD et al (2014) Deep-sequencing method for quantifying background abundances of Symbiodinium types: exploring the rare Symbiodinium biosphere in reef-building corals. PLoS One 9:e94297PubMedCentralCrossRefPubMedGoogle Scholar
  67. Richards ZT, van Oppen MJH (2012) Rarity and genetic diversity in Indo-Pacific Acropora corals. Ecol Evol 2:1867–1888PubMedCentralCrossRefPubMedGoogle Scholar
  68. Roberts CM, McClean CJ, Veron JE et al (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284CrossRefPubMedGoogle Scholar
  69. Rocha LA, Robertson DR, Roman J et al (2005) Ecological speciation in tropical reef fishes. Proc R Soc B 272:573–579PubMedCentralCrossRefPubMedGoogle Scholar
  70. Rocha LA, Craig MT, Bowen BW (2007) Phylogeography and the conservation of coral reef fishes. Coral Reefs 26:501–512CrossRefGoogle Scholar
  71. Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642CrossRefGoogle Scholar
  72. Rosic N, Kaniewska P, Chan C-KK et al (2014) Early transcriptional changes in the reef-building coral Acropora aspera in response to thermal and nutrient stress. BMC Genom 15:1052CrossRefGoogle Scholar
  73. Saenz-Agudelo P, Jones GP, Thorrold SR et al (2011) Connectivity dominates larval replenishment in a coastal reef fish metapopulation. Proc R Soc B 278:2954–2961PubMedCentralCrossRefPubMedGoogle Scholar
  74. Schweinsberg M, Gonzalez Pech RA, Tollrian R et al (2014) Transfer of intracolonial genetic variability through gametes in Acropora hyacinthus corals. Coral Reefs 33:77–87CrossRefGoogle Scholar
  75. Shearer TL, Coffroth MA (2008) Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Resourc 8:247–255CrossRefGoogle Scholar
  76. Shearer TL, Snell TW, Hay ME (2014) Gene expression of corals in response to macroalgal competitors. PLoS One 9:e114525PubMedCentralCrossRefPubMedGoogle Scholar
  77. Shinzato C, Mungpakdee S, Satoh N et al (2014) A genomic approach to coral-dinoflagellate symbiosis: studies of Acropora digitifera and Symbiodinium minutum. Front Microbiol 5:00336Google Scholar
  78. Thurber RV, Willner-Hall D, Rodriguez-Mueller B et al (2009) Metagenomic analysis of stressed coral holobionts. Environ Microbiol 11:2148–2163CrossRefGoogle Scholar
  79. Timmers MA, Bird CE, Skillings DJ et al (2012) There’s no place like home: crown-of-thorn outbreaks in the central Pacific are regionally derived and independent events. PLoS One 7:e31159PubMedCentralCrossRefPubMedGoogle Scholar
  80. Tonk L, Sampayo EM, LaJeunesse TC et al (2014) Symbiodinium (Dinophyceae) diversity in reef-invertebrates along an offshore to inshore reef gradient near Lizard Island, Great Barrier Reef. J Phycol 50:552–563CrossRefGoogle Scholar
  81. Valdez-Moreno M, Quintal-Lizama C, Gómez-Lozano R et al (2012) Monitoring an alien invasion: DNA barcoding and the identification of lionfish and their prey on coral reefs of the Mexican Caribbean. PLoS One 7:e36636PubMedCentralCrossRefPubMedGoogle Scholar
  82. van der Meer MH, Hobbs J-PA, Jones GP et al (2012) Genetic connectivity among and self-replenishment within island populations of a restricted range subtropical reef fish. PLoS One 7:e49660PubMedCentralCrossRefPubMedGoogle Scholar
  83. van Oppen MJH, Oliver JK, Putnam HM et al (2015) Building coral reef resilience through assisted evolution. Proc Natl Acad Sci U S A 112:2307–2313PubMedCentralCrossRefPubMedGoogle Scholar
  84. Vieira C, D’hondt S, de Clerck O et al (2014) Towards an inordinate fondness for stars, beetles and Lobophora? Species diversity of the genus Lobophora (Dictyotales, Phaeophyceae) in New Caledonia. J Phycol 50:1101–1119CrossRefGoogle Scholar
  85. Vogler C, Benzie J, Lessios H et al (2008) A threat to coral reefs multiplied? Four species of crown-of-thorns starfish. Biol Lett 4:696–699PubMedCentralCrossRefPubMedGoogle Scholar
  86. Vollmer SV, Palumbi SR (2002) Hybridization and the evolution of reef coral diversity. Science 296:2023–2025CrossRefPubMedGoogle Scholar
  87. Westneat MW, Alfaro ME (2005) Phylogenetic relationships and evolutionary history of the reef fish family Labridae. Mol Phylogenet Evol 36:370–390CrossRefPubMedGoogle Scholar
  88. Williams ST, Knowlton N, Jara J et al (2003) The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr Comp Biol 42:941–952CrossRefGoogle Scholar
  89. Wooninck LM, Warner RR, Fleischer RC (2000) Relative fitness components measured with competitive PCR. Mol Ecol 9:1409–1414CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Department of Invertebrate ZoologyNational Museum of Natural History, Smithsonian InstitutionWashington, DCUSA

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