Greater genetic diversity in spatially restricted coral reef fishes suggests secondary contact among differentiated lineages

Diversity

Volumn 3, Issue 3, 2011, Pages 483-502

  Bay, Line K ^a   Julian Caley, M ^a  

^a AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

Author keywords

Central; Coral reef fishes; Genetic diversity; Genetic structure; Geographical range; Peripheral; Pomacentridae; Spatially restricted; Widespread

Indexed keywords

CONSERVATION GENETICS; CORAL REEF; EXTINCTION; FISH; GENETIC STRUCTURE; GENETIC VARIATION; GEOGRAPHICAL DISTRIBUTION; HYBRIDIZATION; MITOCHONDRIAL DNA; PERIPHERAL REGION; POPULATION GENETICS; SPATIAL DISTRIBUTION;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; PACIFIC OCEAN; QUEENSLAND;

ANTHOZOA; PISCES; POMACENTRIDAE;

EID: 84859393045     PISSN: None     EISSN: 14242818     Source Type: Journal    
DOI: 10.3390/d3030483     Document Type: Article

References (89)

1. McNeely, J.A.; Miller, K.R.; Reid, W.V.; Mittermeier, R.A.; Werner, T.B. Conserving the World's Biological Diversity; World Conservation Union, World Resources Institute, Conservation International, World Wildlife Fund-US, and the World Bank: Washington, DC, USA, 1990; pp. 1-93.
2. Reed, D.H.; Frankham, R. Correlation between fitness and genetic diversity. Conservat. Biol. 2003, 17, 230-237.
3. Hedrick, P.W. Genetics of Populations; Jones and Bartlett Publishers: Sudbury, MA, USA, 2005; Volume 3, pp.1-737.
4. Frankham, R. Inbreeding and extinction: Island populations. Conservat. Biol. 1998, 12, 665-675.
5. Reed, D.H.; Briscoe, D.A.; Frankham, R. Inbreeding and extinction: The effect of environmental stress and lineage. Conservat. Genet. 2002, 3, 301-307.
6. Eckert, C.G.; Samis, K.E.; Lougheed, S.C. Genetic variation across species' geographical ranges: The central-marginal hypothesis and beyond. Mol. Ecol. 2008, 17, 1170-1188.
7. Rogers, A.R.; Harpending, H. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 1992, 9, 552-569.
8. Hartl, D.L.; Clark, A.G. Principles of Population Genetics; Sinauer Associates, Inc.: Sunderland, MA, USA, 1989; pp. 1-565.
9. Darwin, C. On the Origin of Species by Means of Natural Selection; John Murray: London, UK, 1859; pp.1-516.
10. Mayr, E. Animal Species and Evolution; Belknap Press: Cambridge, MA, USA, 1963; pp. 1-797.
11. Holt, R.D.; Keitt, T.H. Species' borders: A unifying theme in ecology. Oikos 2005, 108, 3-6.
12. Holt, R.D.; Keitt, T.H.; Lewis, M.A.; Maurer, B.A.; Taper, M.L. Theoretical models of species' borders: Single species approaches. Oikos 2005, 108, 18-27.
13. Brown, J.H.; Stevens, G.C.; Kaufman, D.M. The geographic range: Size, shape, boundaries and internal structure. Annu. Rev. Ecol. Systemat. 1996, 27, 597-563.
14. Symonds, M.R.E.; Johnson, C.N. Range size-abundance relationships in Australian passerines. Glob. Ecol. Biogeogr. 2006, 15, 143-152.
15. Gaston, K.J. The Structure and Dynamics of Geographical Ranges; Oxford University Press: Oxford, UK, 2003; pp. 1-266.
16. Holt, R.D.; Keitt, T.H. Alternative causes for range limits: A metapopulation perspective. Ecol. Lett. 2000, 3, 41-47.
17. Lennon, J.J.; Turner, J.R.G.; Connell, D. A metapopulation model of species boundaries. Oikos 1997, 78, 486-502.
18. Hoffmann, A.A.; Parsons, P.P. Evolutionary Genetics and Environmental Stress; Oxford University Press: Oxford, UK, 1991; pp. 1-276.
19. Brown, J.H. On the relationship between abundance and distribution of species. Am. Nat. 1984, 124, 255-279.
20. Vucetich, J.A.; Waite, T.A. Spatial patterns of demography and genetic processes across the species' range: Null hypotheses for landscape conservation genetics. Conservat. Genet. 2003, 4, 639-645.
21. Holt, R.D. Population dynamics and evolutionary processes: The manifold roles of habitat selection. Evol. Ecol. 1987, 1, 331-347.
22. Frankham, R. Relationship of genetic variation to population size in wildlife. Conservat. Biol. 1996, 10, 1500-1508.
23. Nevo, E. Genetic variation in natural populations: patterns and theory. Theor. Popul. Biol. 1978, 13, 121-177.
24. Ayre, D.J.; Hughes, T.P. Climate change, genotypic diversity and gene flow in reef-building corals. Ecol. Lett. 2004, 7, 273-278.
25. Gapare, W.A.; Aitken, S.N. Strong spatial genetic structure in peripheral but not core populations of sitka spruce [Picea sitchensis (Bong.) Carr.]. Mol. Ecol. 2005, 14, 2659-2667.
26. Grant, M.C.; Antonovics, J. Biology of ecologically marginal populations of Anthoxanthum odoratum. I. Phenetics and dynamics. Evolution 1978, 32, 822-838.
27. Durka, W. Genetic diversity in peripheral and subcentral populations of Corrigiola litoralis L. (Illecebraceae). Heredity 1999, 83, 476-484.
28. Bowen, B.W.; Clark, A.M.; Abreu-Grobois, F.A.; Chaves, A.; Reichart, H.A.; Ferl, R.J. Global phylogeography of the ridley sea turtles (Lepidochelys spp.) as inferred from mitochondrial DNA sequences. Genetica 1997, 101, 179-189.
29. Palumbi, S.R.; Grabowsky, G.; Duda, T.F.; Geyer, L.; Tachino, N. Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 1997, 51, 1506-1517.
30. Lecomte, F.; Grant, W.S.; Dodson, J.J.; Rodriguez-Sanchez, R.; Bowen, B.W. Living with uncertainty: Genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Mol. Ecol. 2004, 13, 2169-2182.
31. Hoffman, E.A.; Blouin, M.S. Historical data refute recent range contraction as cause of low genetic diversity in isolated frog populations. Mol. Ecol. 2004, 13, 271-276.
32. McCauley, R.A.; Ballard, H.E. Inferring nativity and biogeographic affinities of central and marginal populations of Froelichia floridana (Amaranthaceae) from Inter-Simple Sequence Repeat (ISSR) markers. J. Torrey Botanic. Soc. 2002, 129, 311-325.
33. Pedersen, A.A.; Loeschcke, V. Conservation genetics of peripheral populations of the mygalomorph spider Atypus affinis (Atypidae) in northern Europe. Mol. Ecol. 2001, 10, 1133-1142.
34. 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.
35. Betancourt, J.L.; Schluser, W.S.; Mitton, J.B.; Anderson, R.S. Fossil and genetic history of a pinyon pine (Pinus edilus) isolate. Ecology 1991, 72, 1685-1697.
36. Tigerstedt, P.M.A. Studies on isozyme variation in marginal and central populations of Picea abies. Hereditas 1973, 75, 47-60.
37. Gapare, W.J.; Aitken, S.N.; Ritland, C.E. Genetic diversity of core and peripheral Sitka spruce (Picea sitchensis (Bong.) Carr) populations: Implications for conservation of widespread species. Biol. Conserv. 2005, 123, 113-123.
38. Garner, T.W.J.; Pearman, P.B.; Angelone, S. Genetic diversity across a vertebrate species' range: A test of the central-peripheral hypothesis. Mol. Ecol. 2004, 13, 1047-1053.
39. Planes, S.; Fauvelot, C. Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 2002, 56, 378-399.
40. Harvey, P.H.; Pagel, M.D. The Comparative Method in Evolutionary Biology; Oxford University Press: Oxford, UK, 1991; pp. 1-239.
41. Lawton, R.; Messmer, V.; Pratchett, M.; Bay, L.K. High gene flow across large geographic scales reduces extinction risk for a highly specialized coral feeding butterflyfish. Mol. Ecol. 2011, 20, 3584-3598.
42. Smith, P.J.; Fujio, Y. Genetic variation in marine teleosts: high variability in habitat specialists and low variability in habitat generalists. Mar. Biol. 1982, 69, 7-20.
43. Rocha, L.A.; Robertson, D.R.; Roman, J.; Bowen, B.W. Ecological speciation in tropical reef fishes. Proc. Roy. Soc. Lond. B 2005, 272, 573-579.
44. Mitton, J.B.; Lewis, W.M.J. Relationships between genetic variability and life-history features of bony fishes. Evolution 1989, 43, 1712-1723.
45. Selander, R.K.; Kaufman, D.W. Genetic variability and strategies of adaptation in animals. Proc. Natl. Acad. Sci. USA 1973, 70, 1875-1877.
46. Kuiter, R.H. Coastal Fishes of South-Eastern Australia; University of Hawaii Press: Honolulu, HI, USA, 1993; pp. 1-437
47. Randall, J.E.; Allen, G.R.; Steene, R.C. Fishes of the Great Barrier Reef and Coral Sea; Crawford House Publishing: Bathurst, Australia, 1997; pp. 1-557.
48. Fishbase. Avaliable on line: http://www.fishbase.org (accessed on 1 June 2011).
49. Ocean Biogeographic Information System. Avaliable on line: http://www.iobis.org (accessed on 1 June 2011).
50. Fautin, D.G.; Allen, G.R. Anemone Fishes and Their Host Sea Anemones: A Guide for Aquarists and Divers; Western Australian Museum: Perth, Australia, 1997; pp. 1-170.
51. Bay, L.K.; Buechler, K.; Gagliano, M.; Caley, M.J. Intraspecific variation in the pelagic larval duration of tropical reef fishes. J. Fish Biol. 2006, 68, 1206-1214.
52. Doherty, P.J.; Planes, S.; Mather, P. Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology 1995, 76, 2373-2391.
53. Thorrold, S.R.; Milicich, M.J. Comparison of larval duration and pre-and post-settlement growth in two species of damselfish, Chromis atripectoralis and Pomacentrus coelestis (Pisces: Pomacentridae), from the Great Barrier Reef. Mar. Biol. 1990, 105, 375-384.
54. Sambrook, J.; Russell, D. Molecular cloning. A laboratory manual, 3rd Edition; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 2001.
55. Bay, L.K.; Crozier, R.H.; Caley, M.J. The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar. Biol. 2006, 149, 1247-1256.
56. Bornet, B.; Branchard, M. Nonanchored inter simple sequence repeat (ISSR) markers: Reproducible and specific tools for genome fingerprinting. Plant Mol. Biol. Rep. 2001, 19, 209-215.
57. Zietkiewicz, E.; Rafalski, A.; Labuda, D. Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 1994, 20, 176-183.
58. Swofford, D.L. Phylogenetic Analysis Using Parsimony (*and other methods), Version 4; Sinauers Associates: Sunderland, MA, USA, 1998.
59. Posada, D.; Crandall, K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14, 817-818.
60. Nei, M. Molecular Evolutionary Genetics; Colombia University Press: New York, NY, USA, 1987; pp. 1-512.
61. Nei, M.N.; Graur, D. Extent of protein polymorphism and the neutral mutation theory. Evol. Biol. 1984, 17, 73-118.
62. Schneider, S.; Roessli, D.; Excoffier, L. Arlequin: A software for population genetics data analysis, Version 2.000; Genetics and Biometry Laboratory, Department of Anthropology: University of Geneva, Geneva, Switzerland, 2000.
63. Sokal, R.R.; Rohlf, F.J. Biometry. The Principles and Practice of Statistics in Biological Research; W. H. Freeman and Company: New York, NY, USA, 1995; pp. 1-887.
64. Rozas, J.; Sanchez-Delbarrio, J.C.; Messeguer, X.; Rozas, R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19, 2496-2497.
65. Burnham, K.P.; Anderson, D.R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach; Springer: New York, NY, USA, 2002; pp. 1-488.
66. Lynch, M.; Milligan, B.G. Analysis of population genetic structure with RAPD markers. Mol. Ecol. 1994, 3, 91-99.
67. Vekemans, X.; Beauwens, T.; Lemaire, M.; Roldan-Ruiz, I. Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol. Ecol. 2002, 11, 139-151.
68. Peakall, R.; Smouse, P.E. GenALEx V5: Genetic Analysis in Excel. Population Genetic Software for Teaching and Research. Australian National University: Canberra, Australia, 2001; Avaliable online: http://www.anu.au/BoZo/GenALEx/.
69. Fauvelot, C.; Bernardi, G.; Planes, S. Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 2003, 57, 1571-1583.
70. Grant, W.S.; Bowen, B.W. Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. Heredity 1998, 89, 415-426.
71. Messmer, V.; van Herwerden, L.; Munday, P.; Jones, G. Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef. Coral Reefs 2005, 24, 392-402.
72. Klanten, O.S.; Choat, J.H.; Hva Herwerden, L. Extreme genetic diversity and temporal rather than spatialpartitioning in a widely distributed coral reef. Mar. Biol. 2007, 150, 659-670.
73. Avise, J.C. Phylogeography. The History and Formation of Species; Harvard University Press: Cambridge, MA, USA, 2000; pp. 1-447.
74. McMillan, W.O.; Weigt, L.A.; Palumbi, S.R. Color pattern evolution, assortative mating, and genetic differentiation in brightly colored butterflyfishes (Chaetodontidae). Evolution 1999, 53, 247-260.
75. Van Herwerden, L.; Doherty, P.J. Contrasting genetic structures across two hybrid zones of a tropical reef fish, Acanthochromis polyacanthus (Bleeker 1855). J. Evol. Biol. 2006, 19, 239-252.
76. Yaakub, S.M.; Bellwood, D.R.; van Herwerden, L.; Walsh, F.M. Hybridization in coral reef fishes: Introgression and bi-directional gene exchange in Thalassoma (family Labridae). Mol. Phylogenet. Evol. 2006, 40, 84-100.
77. Marie, A.D.; van Herwerden, L.; Choat, J.H.; Hobbs, J.P. Hybridisation of reef fish at the Indo-Pacific biogeographic barrier: A case study. Coral Reefs 2007, 26, 841-850.
78. Davies, P.J. Evolution of the Great Barrier Reef-Reductionist dream or expansionist vision. In Proceedings of the 6th International Coral Reef Symposium; Townsville, Australia, 1989; Choat, J.H., Barnes, D., Borowitzka, M.A., Coll, J.C., Davies, P.J., Flood, P., Hatcher, B.G., Hopley, D., Hutchings, P.A., Kinsey, D., et al. Eds.; Reefbase: Townsville, Australia; Volume 1, pp. 9-17.
79. Hopley, D.; Thom, B.G. Australian Sea levels in the last 15000 years: An introductory review. In Australian Sea Levels in the Last 15000 Years: A Review; Hopley, D., Ed.; Department of Geography, James Cook University: Townsville, Australia, 1983; pp. 29-36.
80. Larcombe, P. Holocene Great Barrier Reef: Sedimentary controls and implications for environmental management. In Gondwana to Greenhouse. Australian Environmental Geoscience; Gostin, V.A., Ed.; Southwood Press: Sydney, Australia, 2001; Volume 21, pp. 281-294.
81. Planes, S.; Doherty, P.J.; Bernardi, G. Strong genetic divergence among populations of a marine fish with limited dispersal, Acanthochromis polyacanthus, within the Great Barrier Reef and the Coral Sea. Evolution 2001, 55, 2263-2273.
82. Bay, L.K.; Caley, M.J.; Crozier, R.H. Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation. BMC Evol. Biol. 2008, 8, 248.
83. Briggs, J.C. Centrifugal speciation and centres of origin. J. Biogeogr. 2000, 27, 1183-1188.
84. Brown, W.L.J. Centrifugal speciation. Q. Rev. Biol. 1957, 32, 247-277.
85. Briggs, J.C. Marine Zoogeography; McGraw-Hill Book Company: New York, NY, USA, 1974.
86. Quenouille, B.; Bermingham, E.; Planes, S. Molecular systematics of the damselfishes (Teleosti: Pomacentridae): Bayesian phylogenetic analyses of mitochondrial and nuclear DNA sequences. Mol. Phylogenet. Evol. 2004, 31, 66-88.
87. Frankham, R. Genetics and extinction. Biol. Conservat. 2005, 126, 131-140.
88. Dudgeon, C.L.; Gust, N.; Blair, D. No apparent genetic basis to demographic differences in scarid fishes across the continental shelf of the Great Barrier Reef. Mar. Biol. 2000, 137, 1059-1066.
89. Jones, D.B.; Jerry, D.R.; McCormick, M.I.; Bay, L.K. The population genetic structure of a common tropical damselfish on the Great Barrier Reef and eastern Papua New Guinea. Coral Reefs 2010, 29, 455-467.