Phylogenetic evidence for recent diversification of obligate coral-dwelling gobies compared with their host corals

Molecular Phylogenetics and Evolution

Volumn 69, Issue 1, 2013, Pages 123-132

  Duchene, David ^a   Klanten, Selma O ^a,b   Munday, Philip L ^a   Herler, Jürgen ^c   van Herwerden, Lynne ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

Acropora; Coral reef; Cospeciation; Gobiodon; Molecular dating; Mutualism

Indexed keywords

MITOCHONDRIAL DNA;

ACROPORA; ANIMAL; ANTHOZOA; ARTICLE; CELL NUCLEUS; CLASSIFICATION; CORAL REEF; COSPECIATION; DNA SEQUENCE; ECOSYSTEM; EVOLUTION; GENETICS; GOBIODON; HISTOLOGY; INDIAN OCEAN; MOLECULAR DATING; PACIFIC OCEAN; PERCIFORMES; PHENOTYPE; PHYLOGENY; PHYLOGEOGRAPHY; PHYSIOLOGY; SYMBIOSIS; TIME;

ACROPORA; CORAL REEF; COSPECIATION; GOBIODON; MOLECULAR DATING; MUTUALISM;

ANIMALS; ANTHOZOA; BIOLOGICAL EVOLUTION; CELL NUCLEUS; CORAL REEFS; DNA, MITOCHONDRIAL; ECOSYSTEM; INDIAN OCEAN; PACIFIC OCEAN; PERCIFORMES; PHENOTYPE; PHYLOGENY; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA; SYMBIOSIS; TIME FACTORS;

ACROPORA; ANTHOZOA; GOBIIDAE; GOBIODON; PISCES;

EID: 84880320624     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.04.033     Document Type: Article

References (93)

1. Abbott R., Albach D., Ansell S., Arntzen J.W., Baird S.J.E., Bierne N., Boughman J., Brelsford A., Buerkle C.A., Buggs R., Butlin R.K., Diekmann U., Eroukhmanoff F., Grill A., Cahan S.H., Hermansen J.S., Hewitt G., Hudson A.G., Jiggins C., Jones J., Keller B., Marczewski T., Mallett J., Martinez-Rodriguez P., Most M., Mullen S., Nichols R., Nolte A.W., Parisod C., Pfennig K., Rice A.M., Ritchie M.G., Seifert B., Smadja C.M., Stelkens R., Szymura J.M., Vainola R., Wolf J.B.W., Zinner D. Hybridization and speciation. J. Evol. Biol. 2013, 26:229-246.
2. Allen G.R. Conservation hotspots of biodiversity and endemism for Indo-Pacific coral reef fishes. Aquat. Conserv.: Marine Freshwater Ecosyst. 2008, 18:541-556.
3. Althoff D.M., Segraves K.A., Smith C.I., Leebens-Mack J., Pellmyr O. Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification. Mol. Phylogenet. Evol. 2011, 62:898-906.
4. Bannikov A.F. Revision of some Eocene fishes from Bolca, norther Italy, previously classified with the Apogonidae and Enoplosiadae (Perciformes). Studi ric. giacim. terz. Bolca 2008, 9:65-76.
5. Barrier M., Robichaux R.H., Purugganan M.D. Accelerated regulatory gene evolution in an adaptive radiation. Proc. Natl Acad. Sci. 2001, 98:10208-10213.
6. Bellwood D.R., Wainwright P.C. The history and biogeography of fishes on coral reefs. Coral reef fishes dynamics and diversity in a complex ecosystem 2002, 5-32. Academic Press.
7. Bellwood D.R., Klanten S., Cowman P.F., Pratchett M.S., Konow N., Van Herwerden L. Evolutionary history of the butterfly fishes (f: Chaetodontidae) and the rise of coral feeding fishes. J. Evol. Biol. 2010, 23:335-349.
8. Brandley M.C., Schmitz A., Reeder T.W. Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of scincid lizards. Syst. Biol. 2005, 54:373-390.
9. Brooker R.M., Munday P.L., Ainsworth T.D. Diets of coral-dwelling fishes of the genus Gobiodon with evidence of corallivory. J. Fish Biol. 2010, 76:2578-2583.
10. Brown J.M., Lemmon A.R. The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics. Syst. Biol. 2007, 56:643-655.
11. Budd A.F., Pandolfi J.M. Overlapping species boundaries and hybridization within the Montastraea "annularis" reef coral complex in the Pleistocene of the Bahama Islands. Paleobiology 2004, 30:396-425.
12. Caley M.J., Munday P.L. Growth trades off with habitat specialization. Proc. Roy. Soc. B Biol. 2003, 270:175-177.
13. Carbone F., Mateuccf R., Pignatti J. Facies analysis and biostratigraphy of the Aradu limestone formation in the Berbera-Sheikh area. Northwestern Somalia. Geologia Romana. 1993, 29:213-235.
14. Carnevale G., Bannikov A.F., Landini W., Sorbini C. Volhynian (Early Samartian sensu lato) fishes from Tsurevsky, North Caucasus. Russia. J. Paleontol. 2006, 80:684-699.
15. Charlesworth B. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 2009, 10:195-205.
16. Choat J.H., Klanten O.S., Van Herwerden L., Robertson D.R., Clements K.D. Patterns and processes in the evolutionary history of parrotfishes (Family Labridae). Biol. J. Linn. Soc. 2012, 107:529-557.
17. Chow S., Hazama K. Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol. Ecol. 1998, 7:1255-1256.
18. Combosch D.J., Guzman H.M., Schumacher H., Vollmer S.V. Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Mol. Ecol. 2008, 17:1304-1312.
19. Cowman P., Bellwood D. Coral reefs as drivers of cladogenesis. J. Evol. Biol. 2011, 1-20.
20. Coyne J.A., Orr H.A. The evolutionary genetics of speciation. Phil. Trans. Roy. Soc. B Biol. 1998, 353:287-305.
21. Depczynski M., Fulton C.J., Marnane M.J., Bellwood D.R. Life history patterns shape energy allocation among fishes on coral reefs. Oecologia 2007, 153:111-120.
22. DiBattista J.D., Berumen M.L., Gaither M.R., Rocha L.A., Eble J.A., Choat J.H., Craig M.T., Skillings D.J., Bowen B.W. After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. J. Biogeogr. 2013, 10.1111/jbi.12068.
23. Dickson D.L., Hay M.E. Corals chemically cue mutualistic fishes to remove competing seaweeds. Science 2012, 338:804-807.
24. Dirnwoeber M., Herler J. Microhabitat specialisation and ecological consequences for coral gobies of the genus Gobiodon in the Gulf of Aqaba, northern Red Sea. Mar. Ecol-Prog. Ser. 2007, 342:265-275.
25. Dirnwoeber M., Herler J. Toxic coral gobies reduce the feeding rate of a corallivorous butterfly fish on Acropora corals. Coral Reefs 2012, 10.1007/s00338-012-0947-3.
26. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
27. Drummond A.J., Ho S.Y., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4:e88.
28. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 2004, 32:1792-1797.
29. Gouy M., Guindon S., Gascuel O. SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 2010, 27:221-224.
30. Graham N.A., Wilson S.K., Jennings S., Polunin N.V., Bijoux J.P., Robinson J. Dynamic fragility of oceanic coral reef ecosystems. Proc. Natl. Acad. Sci. 2006, 103:8425-8429.
31. Graur D., Martin W. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet. 2004, 20:80-86.
32. Harold A.S., Winterbottom R., Munday P.L., Chapman R.W. Phylogenetic relationships of Indo-Pacific coral gobies of the genus Gobiodon (Teleostei: Gobiidae), based on morphological and molecular data. Bull. Mar. Sci. 2008, 82:119-136.
33. Hellberg M. No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation. BMC Evol. Biol. 2006, 6:24.
34. Herler J., Koblmüller S., Sturmbauer C. Phylogenetic relationships of coral-associated gobies (Teleostei, Gobiidae) from the Red Sea based on mitochondrial DNA data. Mar. Biol. 2009, 156:725-739.
35. Herler J., Munday P.L., Hernaman V. Gobies on coral reefs. Biology of Gobies 2011, Science Publishers, Inc. R.A. Patzner, J.L. Van Tassell, M. Kovacic, B.G. Kapoor (Eds.).
36. Ho S.Y.W., Phillips M.J. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 2009, 58:367-380.
37. Hobbs J., Munday P.L. Intraspecific competition controls spatial distribution and social organisation of the coral-dwelling goby Gobiodon histrio. Mar. Ecol-Prog. Ser. 2004, 278:253-259.
38. Hodge J.R., Read C.I., van Herwerden L., Bellwood D.R. The role of peripheral endemism in species diversification: evidence from the coral reef fish genus Anampses (Family: Labridae). Mol. Phylogenet. Evol. 2011, 62:653-663.
39. Huelsenbeck J., Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
40. Huyse T., Volckaert F.A.M. Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Syst. Biol. 2005, 54:710-718.
41. Jones G.P., McCormick M.I., Srinivasan M., Eagle J.V. Coral decline threatens fish biodiversity in marine reserves. Proc. Natl. Acad. Sci. 2004, 101:8251-8253.
42. Kassen R. Toward a general theory of adaptive radiation. Ann. NY Acad. Sci. 2009, 1168:3-22.
43. Kenyon J.C. Models of reticulate evolution in the coral genus Acropora based on chromosome numbers: parallels with plants. Evolution 1997, 51:756-767.
44. Kiessling W., Simpson C., Foote M. Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 2010, 327:196-198.
45. Kocher T.D., Thomas W.K., Meyer A., Edwards S.V., Paabo S., Villablanca F.X., Wilson C. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 1989, 86:6196-6200.
46. Lanterbecq D., Rouse G.W., Eeckhaut I. Evidence for cospeciation events in the host-symbiont system involving crinoids (Echinodermata) and their obligate associates, the myzostomids (Myzostomida, Annelida). Mol. Phylogenet. Evol. 2010, 54:357-371.
47. Maguire B.A., Zimmermann R.A. The ribosome in focus. Cell 2001, 104:813-816.
48. Márquez L.M., Van Oppen M.J.H., Willis B.L., Reyes A., Miller D.J. The highly cross-fertile coral species, Acropora hyacinthus and Acropora cytherea, constitute statistically distinguishable lineages. Mol. Ecol. 2002, 11:1339-1349.
49. Miller D.J., van Oppen M.J.H. A "fair go" for coral hybridization. Mol. Ecol. 2003, 12:805-807.
50. Miller, M.A., Holder, M.T., Vos, R., Midford, P.E., Liebowitz, T., Chan, L., Hoover, P., Warnow, T., 2009. The CIPRES Portals.
51. Munday P.L. Interactions between habitat use and patterns of abundance in coral-dwelling fishes of the genus Gobiodon. Environ. Biol. Fish. 2000, 58:355-369.
52. Munday P.L. Fitness consequences of habitat use and competition among coral-dwelling fishes. Oecologia 2001, 128:585-593.
53. Munday P.L. Does habitat availability determine geographical-scale abundances of coral-dwelling fishes?. Coral Reefs 2002, 21:105-116.
54. Munday P.L. Habitat loss, resource specialization, and extinction on coral reefs. Glob. Change Biol. 2004, 10:1642-1647.
55. Munday P.L. Competitive coexistence of coral-dwelling fishes: the lottery hypothesis revisited. Ecology 2004, 85:623-628.
56. Munday P.L., Wilson S.K. Comparative efficacy of clove oil and other chemicals in anaesthetization of Pomacentrus amboinensis, a coral reef fish. J. Fish Biol. 1997, 51:931-938.
57. Munday P.L., Jones G.P., Caley M.J. Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar. Ecol. Prog. Ser. 1997, 152:227-239.
58. Munday P.L., Harold A.S., Winterbottom R. Guide to coral-dwelling gobies (genus Gobiodon) of Papua New Guinea and the Great Barrier Reef. Rev. Fr. Aquar. 1999, 26:49-54.
59. Munday P.L., Jones G.P., Caley M.J. Interspecific competition and coexistence in a guild of coral-dwelling fishes. Ecology 2001, 82:2177-2189.
60. Munday P.L., van Herwerden L., Dudgeon C.L. Evidence for sympatric speciation by host shift in the sea. Curr. Biol. 2004, 14:1498-1504.
61. Nylander, J.A.A., 2004. MrModeltest v. 2. Evolutionary Biology Centre, Uppsala University.
62. Nylander J.A.A., Ronquist F., Huelsenbeck J.P., Nieves-Aldrey J.L. Bayesian phylogenetic analysis of combined data. Syst. Biol. 2004, 53:47-67.
63. Paterson A.M., Banks J. Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. Int. J. Parasitol. 2001, 31:1012-1022.
64. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
65. Rambaut, A., 1996. Se-Al: Sequence Alignment Editor. <>. http://evolve.zoo.ox.ac.uk.
66. Rambaut, A., Drummond, A.J., 2007. Tracer, a MCMC Trace Analysis Tool. Institute of Evolutionary Biology, University of Edinburgh. <>. http://beast.bio.ed.ac.uk/.
67. Richards Z.T., van Oppen M.J.H., Wallace C.C., Willis B.L., Miller D.J. Some rare Indo-Pacific coral species are probable hybrids. PLoS ONE 2008, 3:e3240.
68. Richards Z.T., Wallace C.C., Miller D.J. Archetypal "elkhorn" coral discovered in the Pacific Ocean. Syst. Biodivers. 2010, 8:281-288.
69. Rocha L.A., Bowen B.W. Speciation in coral-reef fishes. J. Fish Biol. 2008, 72:1101-1121.
70. Sambrook J., Russell D.W. Molecular cloning, a laboratory manual 2001, Cold Spring Harbour Laboratory Press, USA, New York.
71. Schliep K.P. Phangorn: phylogenetic analysis in R. Bioinformatics 2011, 27:592-593.
72. Shearer T., van Oppen M., Romano S., Wörheide G. Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria). Mol. Ecol. 2002, 11:2475-2487.
73. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection 2001, Bioinformatics.
74. Simpson C., Kiessling W., Mewis H., Baron-Szabo R.C., Müller J. Evolutionary diversification of reef corals: a comparison of the molecular and fossil records. Evolution 2011, 65:3274-3284.
75. Storfer A., Alfaro M.E., Ridenhour B.J., Jancovich J.K., Mech S.G., Parris M.J., Collins J.P. Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecol. Lett. 2007, 10:1075-1083.
76. Swofford, D., 1998. PAUP 4.0: Phylogenetic analysis using parsimony. Sunderland, Sinauer Associates, Massachusetts.
77. Thacker C. Phylogeny of Gobioidei and placement within Acanthomorpha, with a new classification and investigation of diversification and character evolution. Copeia 2009, 2009:93-104.
78. Thompson J.N. The coevolving web of life. Am. Nat. 2009, 173:125-140.
79. Thompson J.D., Gibson T.J., Plewniak F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 24:4876-4882.
80. Van Oppen M.J.H., Willis B.L., Miller D.J. Atypically low rate of cytochrome b evolution in the scleractinian coral genus Acropora. Proc. Roy. Soc. Lond. B. Biol. 1999, 266:179-183.
81. Van Oppen M., McDonald B., Willis B., Miller D.J. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence?. Biol. Evol. 2001, 18:1315-1329.
82. Van Oppen M.J.H., Koolmees E.M., Veron J.E.N. Patterns of evolution in the scleractinian coral genus Montipora (Acroporidae). Mar. Biol. 2004, 144:9-18.
83. Veron J.E.N. New species described in Corals of the World 2002, Australian Institute of Marine Science, Townsville, QLD, Australia.
84. Vollmer S.V., Palumbi S.R. Hybridization and the evolution of reef coral diversity. Science 2002, 296:2023-2025.
85. Wallace C. Staghorn corals of the world: a revision of the genus Acropora 1999, CSIRO Publishing, Collingwood, VIC, Australia.
86. Wallace C.C. New species and records from the Eocene of England and France support early diversification of the coral genus Acropora. J. Paleontol. 2008, 82:313-328.
87. Wallace C.C., Rosen B.R. Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals. Proc. Roy. Soc. Lond. B. Biol. 2006, 273:975-982.
88. Weiblen G.D., Bush G.L. Speciation in fig pollinators and parasites. Mol. Ecol. 2002, 11:1573-1578.
89. Willis B.L., van Oppen M.J.H., Miller D.J., Vollmer S.V., Ayre D.J. The role of hybridization in the evolution of reef corals. Annu. Rev. Ecol. Evol. Syst. 2006, 37:489-517.
90. Winters K.L., van Herwerden L., Choat J.H., Robertson D.R. Phylogeography of the Indo-Pacific parrotfish Scarus psittacus: isolation generates distinctive peripheral populations in two oceans. Mar. Biol. 2010, 157:1679-1691.
91. Wolstenholme J.K. Temporal reproductive isolation and gametic compatability are evolutionary mechanisms in the Acropora humilis group (Cindaria; Scleractinia). Mar. Biol. 2004, 144:567-582.
92. Woolfit M. Effective population size and the rate and pattern of nucleotide substitutions. Biol. Lett. 2009, 5:417-420.
93. Zwickl D. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion Ph.D. dissertation 2006, The University of Texas, Austin.