Environmental gradients predict the genetic population structure of a coral reef fish in the Red Sea

Molecular Ecology

Volumn 23, Issue 3, 2014, Pages 591-602

  Nanninga, Gerrit B ^a   Saenz Agudelo, Pablo ^a   Manica, Andrea ^b   Berumen, Michael L ^a,c  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

connectivity; coral reef fish; genetic structure; isolation by distance; isolation by environment; microsatellites

Indexed keywords

AMPHIPRION BICINCTUS; ANTHOZOA;

MICROSATELLITE DNA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CONNECTIVITY; CORAL REEF; CORAL REEF FISH; GENE FLOW; GENETIC ISOLATION BY DISTANCE; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; INDIAN OCEAN; ISOLATION BY ENVIRONMENT; MICROSATELLITES; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PERCIFORMES; POPULATION GENETICS; SAUDI ARABIA;

CONNECTIVITY; CORAL REEF FISH; GENETIC STRUCTURE; ISOLATION BY DISTANCE; ISOLATION BY ENVIRONMENT; MICROSATELLITES;

ANIMALS; CORAL REEFS; GENE FLOW; GENETICS, POPULATION; GEOGRAPHY; INDIAN OCEAN; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PERCIFORMES; SAUDI ARABIA;

EID: 84892988231     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12623     Document Type: Article

References (63)

1. Alberto F, Raimondi PT, Reed DC, et al,. (2010) Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology, 91, 49-56.
2. Alberto F, Raimondi PT, Reed DC, et al,. (2011) Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel. Molecular Ecology, 20, 2543-2554.
3. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B, Statistical Methodology, 57, 289-300.
4. Berumen ML, Hoey AS, Bass WH, et al,. (2013) The status of coral reef ecology research in the Red Sea. Coral Reefs, 32, 1-12.
5. Bohonak AJ, (2002) IBD (isolation by distance): a program for analyses of isolation by distance. Journal of Heredity, 93, 153-154.
6. Bonte D, Van Dyck H, Bullock JM, et al,. (2012) Costs of dispersal. Biological reviews of the Cambridge Philosophical Society, 87, 290-312.
7. Botsford LW, White JW, Coffroth M, et al,. (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs, 28, 327-337.
8. Bower A, Abualnaja Y, (2012) New observations of the Gulf of Aden intermediate water intrusion into the Red Sea. EGU General Assembly Conference Abstracts, 14, 3481.
9. Bradbury IR, Bentzen P, (2007) Non-linear genetic isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Marine Ecology Progress Series, 340, 245-257.
10. Burgess SC, Treml E, Marshall DJ, (2012) How do dispersal costs and habitat selection influence realized population connectivity? Ecology, 93, 1378-1387.
11. Carassou L, Ponton D, Mellin C, Galzin R, (2008) Predicting the structure of larval fish assemblages by a hierarchical classification of meteorological and water column forcing factors. Coral Reefs, 27, 867-880.
12. Crispo E, Bentzen P, Reznick DN, Kinnison MT, Hendry AP, (2006) The relative influence of natural selection and geography on gene flow in guppies. Molecular Ecology, 15, 49-62.
13. DiBattista JD, Berumen ML, Gaither MR, et al,. (2013) After continents divide: comparative phylogeography of reef fishes from the Red Sea and Indian Ocean. Journal of Biogeography, 40, 1170-1181.
14. Doherty PJ, Planes S, Mather P, (1995) Gene flow and larval duration in seven species of fish from the Great Barrier Reef. Ecology, 76, 2373-2391.
15. Dyer RJ, Nason JD, (2004) Population Graphs: the graph theoretic shape of genetic structure. Molecular Ecology, 13, 1713-1727.
16. Earl DA, (2012) structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
17. Eshel G, Naik NH, (1997) Climatological coastal jet collision, intermediate water formation, and the general circulation of the Red Sea. Journal of Physical Oceanography, 27, 1233-1257.
18. Fine M, Gildor H, Genin A, (2013) A coral reef refuge in the Red Sea. Global Change Biology, 19, 3640-3647.
19. Froukh T, Kochzius M, (2007) Genetic population structure of the endemic fourline wrasse (Larabicus quadrilineatus) suggests limited larval dispersal distances in the Red Sea. Molecular Ecology, 16, 1359-1367.
20. Gaines SD, Lester SE, Grorud-Colvert K, Costello C, Pollnac R, (2010) Evolving science of marine reserves: new developments and emerging research frontiers. Proceedings of the National Academy of Sciences of the United States of America, 107, 18251-18255.
21. Galindo HM, Olson DB, Palumbi SR, (2006) Seascape genetics: a coupled oceanographic-genetic model predicts population structure of Caribbean corals. Current Biology, 16, 1622-1626.
22. Hellberg ME, Burton RS, Neigel JE, Palumbi SR, (2002) Genetic assessment of connectivity among marine populations. Bulletin of Marine Science, 70, 273-290.
23. Jenkins DG, Carey M, Czerniewska J, et al,. (2010) A meta-analysis of isolation by distance: relic or reference standard for landscape genetics? Ecography, 33, 315-320.
24. Jensen JL, Bohonak AJ, Kelley ST, (2005) Isolation by distance, web service. BMC genetics, 6, 13.
25. Johns WE, Jacobs GA, Kindle JC, Murray SP, Carron M, (1999) Arabian marginal seas and gulfs. DTIC Document. oai accession number: ADA379285
26. Johnson MS, Black R, (1982) Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Marine Biology, 70, 157-164.
27. Legendre P, Fortin M, (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Molecular Ecology Resources, 10, 831-844.
28. Liggins L, Treml EA, Riginos C, (2013) Taking the plunge: an introduction to undertaking seascape genetic studies and using biophysical models. Geography Compass, 7, 173-196.
29. Lo-Yat A, Simpson SD, Meekan M, et al,. (2011) Extreme climatic events reduce ocean productivity and larval supply in a tropical reef ecosystem. Global Change Biology, 17, 1695-1702.
30. Marshall DJ, Morgan SG, (2011) Ecological and evolutionary consequences of linked life-history stages in the sea. Current Biology, 21, 718-725.
31. Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S, (2010) Phenotype-environment mismatches reduce connectivity in the sea. Ecology letters, 13, 128-140.
32. Mendez M, Rosenbaum HC, Subramaniam A, Yackulic C, Bordino P, (2010) Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range. Molecular Ecology, 19, 2212-2228.
33. Nanninga G, Mughal M, Saenz-Agudelo P, Bayer T, Berumen M, (2012) Development of 35 novel microsatellite markers for the two-band anemonefish Amphiprion bicinctus. Conservation Genetics Resources, 4, 1-4.
34. Nosil P, Vines TH, Funk DJ, (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution, 59, 705-719.
35. van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P, (2004) microchecker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
36. Peakall R, Smouse PE, (2012) genalex 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics, 28, 2537-2539.
37. Pinsky ML, Montes HR Jr, Palumbi SR, (2010) Using isolation by distance and effective density to estimate dispersal scales in anemonefish. Evolution, 64, 2688-2700.
38. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
39. Raitsos DE, Hoteit I, Prihartato PK, et al,. (2011) Abrupt warming of the Red Sea. Geophysical Research Letters, 38, L14601.
40. Raitsos DE, Pradhan Y, Brewin RJW, Stenchikov G, Hoteit I, (2013) Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS ONE, 8, e64909.
41. Raymond M, Rousset F, (1995) genepop (version 1.2): population genetics software for exact tests and ecumenicism. Journal of heredity, 86, 248-249.
42. Riginos C, Liggins L, (2013) Seascape genetics: populations, individuals, and genes marooned and adrift. Geography Compass, 7, 197-216.
43. Roberts CM, Shepherd ARD, Ormond RFG, (1992) Large-scale variation in assemblage structure of Red Sea butterflyfishes and angelfishes. Journal of Biogeography, 19, 239-250.
44. Rousset F, (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228.
45. Schmidt PS, Serrão EA, Pearson GA, et al,. (2008) Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci. Ecology, 89, 91-107.
46. Selkoe KA, Toonen RJ, (2011) Marine connectivity: a new look at pelagic larval duration and genetic metrics of dispersal. Marine Ecology Progress Series, 436, 291-305.
47. Selkoe KA, Gaines SD, Caselle JE, Warner RR, (2006) Current shifts and kin aggregation explain genetic patchiness in fish recruits. Ecology, 87, 3082-3094.
48. Selkoe KA, Henzler CM, Gaines SD, (2008) Seascape genetics and the spatial ecology of marine populations. Fish and Fisheries, 9, 363-377.
49. Selkoe KA, Watson JR, White C, et al,. (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Molecular Ecology, 19, 3708-3726.
50. Shima JS, Swearer SE, (2010) The legacy of dispersal: larval experience shapes persistence later in the life of a reef fish. The Journal of Animal Ecology, 79, 1308-1314.
51. Sexton JP, Hangartner SB, Hoffmann AA, (2013) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution, doi: 10.1111/evo.12258
52. Slatkin M, (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution, 47, 264-279.
53. Smouse PE, Long JC, Sokal RR, (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology, 35, 627-632.
54. Sofianos SS, Johns WE, (2002) An oceanic general circulation model (OGCM) investigation of the Red Sea circulation, 1. Exchange between the Red Sea and the Indian Ocean. Journal of Geophysical Research, 107, 3196.
55. Spaet JLY, Thorrold SR, Berumen ML, (2012) A review of elasmobranch research in the Red Sea. Journal of Fish Biology, 80, 952-965.
56. Vigliola L, Doherty PJ, Meekan MG, et al,. (2007) Genetic identity determines risk of post-settlement mortality of a marine fish. Ecology, 88, 1263-1277.
57. Wang IJ, (2013) Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67, 3403-3411.
58. Wang IJ, Summers K, (2010) Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog. Molecular Ecology, 19, 447-458.
59. Wang IJ, Glor RE, Losos JB, (2013) Quantifying the roles of ecology and geography in spatial genetic divergence. Ecology letters, 16, 175-182.
60. Wenger AS, Johansen JL, Jones GP, (2011) Suspended sediment impairs habitat choice and chemosensory discrimination in two coral reef fishes. Coral Reefs, 30, 879-887.
61. Wenger AS, Johansen JL, Jones GP, (2012) Increasing suspended sediment reduces foraging, growth and condition of a planktivorous damselfish. Journal of Experimental Marine Biology and Ecology, 428, 43-48.
62. White C, Selkoe KA, Watson J, et al,. (2010) Ocean currents help explain population genetic structure. Proceedings of the Royal Society B: Biological Sciences, 277, 1685-1694.
63. Wright S, (1943) Isolation by distance. Genetics, 28, 114-138.