Population genomic tests of models of adaptive radiation in Lake Victoria region cichlid fish

Evolution

Volumn 65, Issue 12, 2011, Pages 3381-3397

  Bezault, Etienne ^a,b   Mwaiko, Salome ^b   Seehausen, Ole ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

AFLP; AMOVA; Gene flow; Genetic diversity; Speciation

Indexed keywords

FRESH WATER;

ADAPTIVE RADIATION; FRAGMENTATION; GENE FLOW; GENETIC DIFFERENTIATION; GENOMICS; MOLECULAR ANALYSIS; NUMERICAL MODEL; PERCIFORM; POLYMORPHISM; POPULATION STRUCTURE; SPECIATION (BIOLOGY); TAXONOMY; TIMESCALE;

ADAPTATION; AFRICA; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ARTICLE; CICHLID; GENE FLOW; GENETIC POLYMORPHISM; GENETICS; GENOME; GENOMICS; GENOTYPE; POPULATION DYNAMICS; SPECIES DIFFERENTIATION;

ADAPTATION, PHYSIOLOGICAL; AFRICA, EASTERN; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; CICHLIDS; FRESH WATER; GENE FLOW; GENETIC SPECIATION; GENOME; GENOMICS; GENOTYPE; POLYMORPHISM, GENETIC; POPULATION DYNAMICS;

EAST AFRICAN LAKES; LAKE VICTORIA;

CICHLIDAE;

EID: 82755182710     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2011.01417.x     Document Type: Article

References (75)

1. Barrett, R. D. H., and D. Schluter 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23:38-44.
2. Barrier, M., B. G. Baldwin, R. H. Robichaux, and M. D. Purugganan 1999. Interspecific hybrid ancestry of a plant adaptive radiation: allopolyploidy of the Hawaiian silversword alliance (Asteraceae) inferred from floral homeotic gene duplications. Mol. Biol. Evol. 16:1105-1113.
3. Basasibwaki, P. 1975. Comparative electrophoretic patterns of lactase dehydrogenase and malate dehydrogenase in five Lake Victoria cichlid species African. J. Trop. Hydrobiol. Fish. 4:21-26.
4. Beadle, L. G. 1981. The inland waters of tropical Africa. An introduction to tropical limnology. Langman Inc., New York
5. Beuning, K. R. M., M. R. Talbot, and K. Kelts 1997. A revised 30000-year paleoclimatic and paleohydrologic history of Lake Albert, East Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 136:259-279.
6. Bonin, A., D. Ehrich, and S. Manel 2007. Statistical analysis of amplified fragment length polymorphism data: a toolbox for molecular ecologists and evolutionists. Mol. Ecol. 16:3737-3758.
7. Dieckmann, U., and M. Doebeli 1999. On the origin of species by sympatric speciation. Nature 400:354-357.
8. Elmer, K. R., C. Reggio, T. Wirth, E. Verheyen, W. Salzburger, and A. Meyer 2009. Pleistocene desiccation in East Africa bottlenecked but did not extirpate the adaptive radiation of Lake Victoria haplochromine cichlid fishes. Proc. Natl. Acad. Sci. U.S.A. 106:13404-13409.
9. Excoffier, L., G. Laval, and S. Schneider 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
10. Excoffier, L., P. E. Smouse, and J. M. Quattro 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes-application to human mitochondrial-DNA restriction data. Genetics 131:479-491.
11. Gavrilets, S., and J. B. Losos 2009. Adaptive radiation: contrasting theory with data. Science 323:732-737.
12. Givnish, T. J. 1997. Adaptive radiation and molecular systematics: issues and approaches. Pp. 1-54 in T. J. Givnish and K. J. Sytsma, eds. Molecular evolution and adaptive radiation. Cambridge Univ. Press, Cambridge
13. Goudet, J. 2005. HIERFSTAT, a package for R to compute and test hierarchicalF-statistics. Mol. Ecol. Notes 5:184-186.
14. Grant, P. R., and B. R. Grant 2008. How and why species multiply: the radiation of Darwin's finches. Princeton Univ. Press, Princeton, NJ
15. Greenwood, P. H. 1980. Towards a phyletic classification of the 'genus'Haplochromis(Pisces, Cichlidae) and related taxa. Part 2; the species from Lakes Victoria Nabugabo, Edward, George and Kivu Bulletin of the British Museum (Natural History). Zool. Ser. 39:1-101.
16. Haberyan, K. A., and R. E. Hecky 1987. The late pleistocene and holocene stratigraphy and paleolimnology of Lakes Kivu and Tanganyika. Palaeogeogr. Palaeoclimatol. Palaeoecol. 61:169-197.
17. Harmon, L. J., J. A. Schulte, A. Larson, and J. B. Losos 2003. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301:961-964.
18. Herder, F., J. Pfaender, and U. K. Schliewen 2008. Adaptive sympatric speciation of polychromatic "roundfin" sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62:2178-2195.
19. Hudson, A. G., P. Vonlanthen, and O. Seehausen 2011. Rapid parallel adaptive radiations from a single hybridogenic ancestral population. Proc. R. Soc. Lond. Ser. B 278:58-66.
20. Huff, D. R., R. Peakall, and P. E. Smouse 1993. RAPD variation within and among natural-populations of outcrossing Buffalograss [Buchloe-Dactyloides (Nutt) Engelm]. Theor. Appl. Genet. 86:927-934.
21. Johnson, T. C., K. Kelts, and E. Odada 2000. The holocene history of Lake Victoria. Ambio 29:2-11.
22. Johnson, T. C., C. A. Scholz, M. R. Talbot, K. Kelts, R. D. Ricketts, G. Ngobi, K. Beuning, I. Ssemmanda, and J. W. McGill 1996. Late pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091-1093.
23. Joyce, D. A., D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills, and O. Seehausen 2011. Repeated colonization and hybridization in Lake Malawi cichlids. Curr. Biol. 21:R108-R109.
24. Kimura, M., and T. Ohta 1969. Average number of generations until fixation of a mutant gene in a finite population. Genetics 61:763-771.
25. Klein, J., A. Sato, and N. Nikolaidis 2007. MHC, TSP, and the origin of species: from immunogenetics to evolutionary genetics. Ann. Rev. Genet. 41:281-304.
26. Kondrashov, A. S., and F. A. Kondrashov 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351-354.
27. Laerdal, T., and M. R. Talbot 2002. Basin neotectonics of Lakes Edward and George, East African Rift. Palaeogeogr. Palaeoclimatol. Palaeoecol. 187:213-232.
28. Magalhaes, I. S., S. Mwaiko, M. V. Schneider, and O. Seehausen 2009. Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish. J. Evol. Biol. 22:260-274.
29. Magalhaes, I. S., S. Mwaiko, and O. Seehausen 2010. Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria. Mol. Ecol. 19:3285-300.
30. Mallet, J. 2007. Hybrid speciation. Nature 446:279-283.
31. Mallet, J., A. Meyer, P. Nosil, and J. L. Feder 2009. Space, sympatry and speciation. J. Evol. Biol. 22:2332-2341.
32. Mayr, E. 1984. Evolution of fish species flocks: a commentary. Pp. 3-12 in A. A. Echelle and I. Kornfield, eds. Evolution of fish species flocks. Univ. of Maine at Orono Press, Orono, ME
33. Meyer, A., T. D. Kocher, P. Basasibwaki, and A. C. Wilson 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550-553.
34. Moran, P., and I. Kornfield 1993. Retention of an ancestral polymorphism in the Mbuna species flock (Teleostei, Cichlidae) of Lake Malawi. Mol. Biol. Evol. 10:1015-1029.
35. Mzighani, S. I., M. Nikaido, M. Takeda, O. Seehausen, Y. L. Budeba, B. P. Ngatunga, E. F. B. Katunzi, M. Aibara, S. Mizoiri, T. Sato et al. 2010. Genetic variation and demographic history of the Haplochromis laparogramma group of Lake Victoria-an analysis based on SINEs and mitochondrial DNA. Gene 450:39-47.
36. Nagl, S., H. Tichy, W. E. Mayer, N. Takahata, and J. Klein 1998. Persistence of neutral polymorphisms in Lake Victoria cichlid fish. Proc. Natl. Acad. Sci. U.S.A. 95:14238-14243.
37. Nagl, S., H. Tichy, W. E. Mayer, N. Takezaki, N. Takahata, and J. Klein 2000. The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 267:1049-1061.
38. Nosil, P., D. J. Funk, and D. Ortiz-Barrientos 2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18:375-402.
39. Parker, A., and I. Kornfield 1997. Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of Lake Malawi, East Africa. J. Mol. Evol. 45:70-83.
40. Rabosky, D. L. 2009. Heritability of extinction rates links diversification patterns in molecular phylogenies and fossils. Syst. Biol. 58:629-640.
41. Rabosky, D. L., and I. J. Lovette 2008. Explosive evolutionary radiations: decreasing speciation or increasing extinction through time Evolution 62:1866-1875.
42. Rieseberg, L. H., M. A. Archer, and R. K. Wayne 1999. Transgressive segregation, adaptation and speciation. Heredity 83:363-372.
43. Russell, J. M., T. C. Johnson, K. R. Kelts, T. Laerdal, and M. R. Talbot 2003. An 11 000-year lithostratigraphic and paleohydrologic record from Equatorial Africa: Lake Edward, Uganda-Congo. Palaeogeogr. Palaeoclimatol. Palaeoecol. 193:25-49.
44. Russell, J. M., D. Verschuren, and H. Eggermont 2007. Spatial complexity of 'Little Ice Age' climate in East Africa: sedimentary records from two crater lake bassins in western Uganda. Holocene 17:183-193.
45. Sage, R. D., and R. K. Selander 1975. Trophic radiation through polymorphism in Cichlid fishes. Proc. Natl. Acad. Sci. U.S.A. 72:4669-4673.
46. Salzburger, W., S. Baric, and C. Sturmbauer 2002. Speciation via introgressive hybridization in East African cichlids Mol. Ecol. 11:619-625.
47. Salzburger, W., and A. Meyer 2004. The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 91:277-290.
48. Samonte, I. E., Y. Satta, A. Sato, H. Tichy, N. Takahata, and J. Klein 2007. Gene flow between species of Lake Victoria haplochromine fishes. Mol. Biol. Evol. 24:2069-2080.
49. Schliewen, U. K., and B. Klee 2004. Reticulate sympatric speciation in Cameroonian crater Lake Cichlids. Front. Zool. 1:5.
50. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, Oxford
51. Schluter, P. M., and S. A. Harris 2006. Analysis of multilocus fingerprinting data sets containing missing data. Mol. Ecol. Notes 6:569-572.
52. Seehausen, O. 2004. Hybridization and adaptive radiation. Trends Ecol. Evol. 19:198-207.
53. Seehausen, O. 2006. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 273:1987-1998.
54. Seehausen, O. 2009. Progressive levels of trait divergence along a "speciation transect" in the Lake Victoria cichlid fish Pundamilia in R. K. Butlin, D. Schluter and J. Bridle, eds. Speciation and patterns of diversity. Cambridge Univ. Press, Cambridge.
55. Seehausen, O., and I. S. Magalhaes 2010. Geographical mode and evolutionary mechanism of ecological speciation in cichlid fish in P. Grant and R. Grant, eds. From field observations to mechanisms: a program in evolutionary biology. Princeton Univ. Press, Princeton, NJ
56. Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. van der Sluijs, M. V. Schneider, M. E. Maan, H. Tachida, et al.. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620-U23.
57. Seehausen, O., F. Witte, E. F. Katunzi, J. Smits, and N. Bouton 1997. Patterns of the remnant cichlid fauna in southern Lake Victoria. Conserv. Biol. 11:890-904.
58. Simpson, G. G. 1944. Tempo and mode in evolution. Columbia Univ. Press, New York
59. Smadja, C., J. Galindo, and R. Butlin 2008. Hitching a lift on the road to speciation. Mol. Ecology 17:4177-4180.
60. Snoeks, J. 1994. The Haplochromines (Teleostei, Cichlidae) of Lake Kivu: a taxonomic revision with notes on their ecology. Musée Royal de l'Afrique Centrale, Tervuren (Belgique), Belgium
61. Stager, J. C., and T. C. Johnson 2008. The late Pleistocene desiccation of Lake Victoria and the origin of its endemic biota. Hydrobiologia 596:5-16.
62. Stewart, C. N., and L. Excoffier 1996. Assessing population genetic structure and variability with RAPD data: application toVaccinium macrocarpon(American Cranberry). J. Evol. Biol. 9:153-171.
63. Van Rompaey, J., S. Z. Ahmadyar, and E. Verheyen 1988. General protein patterns of muscle homogenates of some Lake Victoria haplochromines (Pisces: Cichlidae). J. Zool. 214:505-518.
64. Vekemans, X. 2002. AFLP-SURV version 1.0. Distributed by the author, Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium
65. Verheyen, E., W. Salzburger, J. Snoeks, and A. Meyer 2003. Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:325-329.
66. Verheyen, E., J. Van Rompaey, and M. Selens 1984. Enzyme variations in haplochromine cichlid fishes from Lake Victoria. Neth. J. Zool. 35:469-478.
67. Via, S. 2009. Natural selection in action during speciation. Proc. Natl. Acad. Sci. U.S.A. 106:9939-9946.
68. Via, S., and J. West 2008. The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Mol. Ecol. 17:4334-4345.
69. Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. Vandelee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kuiper, et al. 1995. AFLP-a new technique for DNA-fingerprinting. Nucl. Acids Res. 23:4407-4414.
70. Witte, F., T. Goldschmidt, J. Wanink, M. Vanoijen, K. Goudswaard, E. Wittemaas, and N. Bouton 1992. The destruction of an endemic species flock-quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ. Biol. Fishes 34:1-28.
71. Wood, H. M., J. W. Grahame, S. Humphray, J. Rogers, and R. K. Butlin 2008. Sequence differentiation in regions identified by a genome scan for local adaptation. Mol. Ecol. 17:3123-3135.
72. Wright, S. 1951. The genetical structure of populations. Ann. Eugenics 15:323-354.
73. Wu, C. I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14:851-865.
74. Yang, R. C. 1998. Estimating hierarchical F-statistics. Evolution 52:950-956.
75. Yatabe, Y., N. C. Kane, C. Scotti-Saintagne, and L. H. Rieseberg 2007. Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuusandH. petiolaris. Genetics 175:1883-1893.