Pleistocene desiccation in East Africa bottlenecked but did not extirpate the adaptive radiation of Lake Victoria haplochromine cichlid fishes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 32, 2009, Pages 13404-13409

  Elmer, Kathryn R ^a   Reggio, Chiara ^a   Wirth, Thierry ^a,c   Verheyen, Erik ^b   Salzburger, Walter ^a,d   Meyer, Axel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^c Sorbonne Universités   (France)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Bayesian statistics; Haplochromine cichlids; Lake Victoria region superflock; Microsatellites; Population genetic structure

Indexed keywords

ADAPTIVE RADIATION; AFRICA; ARTICLE; BOTTLENECK POPULATION; CICHLID; CLIMATE CHANGE; DESICCATION; GENE LOCUS; GENETIC ANALYSIS; GENETIC POLYMORPHISM; GEOLOGY; LAKE; MORPHOLOGY; NONHUMAN; PERCIFORMES; PLEISTOCENE; POPULATION GENETICS; PRIORITY JOURNAL; RIVER;

ADAPTATION, BIOLOGICAL; AFRICA, EASTERN; ANIMALS; CICHLIDS; CLUSTER ANALYSIS; DESICCATION; EVOLUTION; FRESH WATER; GEOGRAPHY; PHYLOGENY; POPULATION DYNAMICS; TIME FACTORS;

CICHLIDAE; PERCIFORMES; PISCES; TELEOSTEI;

EID: 69449090756     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902299106     Document Type: Article

References (74)

1. Takimoto G, Higashi M, Yamamura N (2000) A deterministic genetic model for sympatric speciation by sexual selection. Evolution 54:1870-1881. (Pubitemid 32113819)
2. Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808-1811. (Pubitemid 27449190)
3. Liem KF (1973) Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws. Syst Zool 22:425-441.
4. Seehausen O, et al. (2008) Speciation through sensory drive in cichlid fish. Nature 455:620-626.
5. Abila R, Barluenga M, Engelken J, Meyer A, Salzburger W (2004) Population-structure and genetic diversity in a haplochromine fish cichlid of a satellite lake of Lake Victoria. Mol Ecol 13:2589-2602. (Pubitemid 39151618)
6. Verheyen E, Salzburger W, Snoeks J, Meyer A (2003) Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:325-329. (Pubitemid 36433723)
7. Genner MJ, et al. (2007) Age of cichlids: New dates for ancient lake fish radiations. Mol Biol Evol 24:1269-1282.
8. Stager JC, Day JJ, Santini S (2004) Comment on "Origin of the Superflock of cichlid fishes from Lake Victoria, East Africa." Science 304:963.
9. Koblmuller S, et al. (2008) Age and spread of the haplochromine cichlid fishes in Africa. Mol Phylogen Evol 49:153-169.
10. Schluter D (2000) in The Ecology of Adaptive Radiations (Oxford Univ Press Inc, New York).
11. Kocher TD (2004) Adaptive evolution and explosive speciation: The cichlid fish model. Nat Rev Genet 5:288-298.
12. Seehausen O (2006) African cichlid fish: A model system in adaptive radiation research. Proc R Soc Lond B 273:1987-1998. (Pubitemid 44214911)
13. Salzburger W, Meyer A (2004) The species flocks of East African cichlid fishes: Recent advances in molecular genetics and population genetics. Naturwissenschaften 91:277-290. (Pubitemid 38916482)
14. Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18:169-185.
15. Gavrilets S, Losos JB (2009) Adaptive radiation: Contrasting theory with data. Science 323:732-738.
16. Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Mol Ecol 10:793-806. (Pubitemid 32406361)
17. Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa. Proc Natl Acad Sci USA 96(9):5107-5110. (Pubitemid 129657925)
18. Kocher TD, Conroy JA, McKaye KR, Stauffer JR (1993) Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol Phylogen Evol 2:158-165.
19. Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 8:279-285.
20. Kornfield I, Smith PF (2000) African cichlid fishes: Model systems for evolutionary biology. Annu Rev Ecol Syst 31:163-196. (Pubitemid 32122399)
21. Nishida M (1991) Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: Inferences from allozyme data. Cellul Molec Life Sci 47:974-979.
22. Salzburger W, Meyer A, Baric S, Verheyen E, Sturmbauer C (2002) Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Syst Biol 51:113-135. (Pubitemid 35169410)
23. Greenwood PH (1980) Towards a phyletic classification of the "genus" Haplochromis (Pisces, Cichlidae) and related taxa. Part II: The species from Lakes Victoria, Nabugabo, Edward, George and Kivu. Bull Br Mus Nat Hist (Zool) 39:1-101.
24. Greenwood PH (1973) A revision of the Haplochromis and related species (Pisces, Cichlidae) from Lake George, Uganda. Bull Br Mus Nat Hist (Zool) 25:139-242.
25. Johnson TC, et al. (1996) Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091.
26. Bishop WW, Trendall AF (1966) Erosion-surfaces, tectonics and volcanic activity in Uganda. Q J Geol Soc 122:385-420.
27. Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550-553. (Pubitemid 20341543)
28. Nagl S, et al. (2000) The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc R Soc Lond B 267:1049-1061. (Pubitemid 30326405)
29. McCune AR, Lovejoy NR (1998) in Endless Forms: Species and Speciation, eds Howard DJ, Berlocher SH (Oxford Univ Press, New York), pp 172-185.
30. Stager JC, Reinthal PN, Livingstone DA (1986) A 25,000-year history for Lake Victoria, East Africa, and some comments on its significance for the evolution of cichlid fishes. Freshwater Biol 16:15-19.
31. Stager JC, Johnson TC (2008) The late Pleistocene desiccation of Lake Victoria and the origin of its endemic biota. Hydrobiologia 596:5-16.
32. Booton GC, et al. (1999) Evolution of the ribosomal RNA internal transcribed spacer one (ITS-1) in cichlid fishes of the Lake Victoria Region. Mol Phylogen Evol 11:273-282.
33. Fryer G (2001) On the age and origin of the species flock of haplochromine cichlid fishes of Lake Victoria. Proc R Soc Lond B 268:1147-1152.
34. Fryer G (2004) Speciation rates in lakes and the enigma of Lake Victoria. Hydrobiologia 519:167-183.
35. Kocher TD (2003) Fractious phylogenies. Nature 423:489-490.
36. Salzburger W, Mack T, Verheyen E, Meyer A (2005) Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol 5:17. (Pubitemid 40548671)
37. Seehausen O (2002) Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14,600 year history for its cichlid species flock. Proc R Soc Lond B 269:491.
38. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013-2029.
39. Nagl S, Tichy H, Mayer WE, Takahata N, Klein J (1998) Persistence of neutral polymorphism in Lake Victoria cichlid fish. Proc Natl Acad Sci USA 95:14238-14243. (Pubitemid 28549351)
40. Seehausen O, et al. (2003) Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock. Proc R Soc Lond B 270:129-137. (Pubitemid 36143363)
41. Moeyersons J (1979) Mus. R. Afr. Centr. Tervuren (Belgium) Dépt. Géol. Min. Rapp. Ann. 1978:127.
42. Kendall RL (1969) An ecological history of the Lake Victoria Basin. Ecological Monographs 39:121-176.
43. Snoeks J (1994) The haplochromines (Teleostei, Cichlidae) of Lake Kivu (East Africa). Ann Mus R Afr Centr Sci Zool 270:1-221.
44. Moran P, Kornfield I (1995) Were population bottlenecks associated with the radiation of the mbuna species flock (Teleostei: Cichlidae) of Lake Malawi? Mol Biol Evol 12:1085-1093.
45. Avise JC (1994) in Molecular Markers, Natural History, and Evolution (Chapman & Hall, New York).
46. Ballard JWO, Rand DM (2005) The population biology of mitochondrial DNA and its phylogenetic implications. Annu Rev Ecol Evol Syst 36:621-642. (Pubitemid 43068873)
47. Hudson RR, Turelli M (2003) Stochasticity overrules the "three-times rule": Genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA. Evolution 57:182-190.
48. Templeton AR (1993) The "Eve" Hypotheses: A genetic critique and reanalysis. Am Anthropol 95:51-72.
49. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198-207.
50. Gasse F, Talling JF, Kilham P (1983) Diatom assemblages in East Africa: Classification, distribution and ecology. Rev Hydrobiol Trop 16:3-34.
51. Livingstone DA, Kendall R (1969) Stratigraphic studies of East African lakes. Mitt Internat Verein Limnol 17:147-153.
52. Cohen AS, Dussinger R, Richardson J (1983) Lacustrine paleochemical interpretations based on Eastern and Southern African ostracodes. Palaeogeogr Palaeocl 43:129-151. (Pubitemid 14276315)
53. Stager JC, Cumming B, Meeker L (1997) A high-resolution 11,400-yr diatom record from Lake Victoria, East Africa. Quat Res 47:81-89. (Pubitemid 127424038)
54. Nicholson SE (1998) in Environmental Change and Response in East African Lakes, ed Lehman JT (Kluwer Academic Publishers, Dortrecht), pp 7-35.
55. Seehausen O, et al. (2003) Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock. Proc R Soc Lond B 270:129. (Pubitemid 36143363)
56. Barel CDN, et al. (1985) Destruction of fisheries in Africa's lakes. Nature 315:19-20.
57. Lippitsch E (1993) A phyletic study on lacustrine haplochromine fishes (Perciformes, Cichlidae) of East Africa, based on scale and squamation characters. J Fish Biol 42:903-946.
58. Klein D, et al. (1993) Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 364:330-334. (Pubitemid 23265272)
59. Terai Y, et al. (2006) Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biol 4:e433.
60. Clabaut C, Bunje PME, Salzburger W, Meyer A (2007) Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations. Evolution 61:560-578. (Pubitemid 46657684)
61. Hey J, Won Y-J, Sivasundar A, Nielsen R, Markert J (2004) Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol 13:909-919. (Pubitemid 38390596)
62. Won Y-J, Sivasundar A, Wang Y, Hey J (2005) On the origin of Lake Malawi cichlid species: A population genetic analysis of divergence. Proc Natl Acad Sci USA 102:6581-6586. (Pubitemid 40628307)
63. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: Lessons from Lake Malawi. Mol Ecol 10:1075-1086.
64. Wu L, Kaufman L, Fuerst PA (1999) Isolation of microsatellite markers in Astatoreochromis alluaudi and their cross-specific amplifications in other African cichlids. Mol Ecol 8:895-906. (Pubitemid 29266898)
65. Zardoya R, et al. (1996) Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proc R Soc Lond B 263:1589-1598. (Pubitemid 26400231)
66. Kellogg KA, Markert JA, Stauffer JR, Jr, Kocher TD (1995) Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa. Proc R Soc Lond B 260:79-84.
67. Sanetra M, Henning F, Fukamachi S, Meyer A (2009) A microsatellite-based genetic linkage map of the cichlid fish, Astatotilapia burtoni (Teleostei): A comparison of genomic architectures among rapidly speciating cichlids Genetics 182:387-397.
68. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of populations structure. Evolution 38:1358-1370.
69. Schneider S, Roessli D, Excoffier L (2000) in Arlequin ver. 2.000: A software for population genetics data analysis (Genetics and Biometry Laboratory, University of Geneva, Switzerland).
70. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics. Brief Bioinform 5:150-163.
71. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945-959. (Pubitemid 30397141)
72. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567-1587. (Pubitemid 37102217)
73. Streelman JT, et al. (2004) Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park. Mol Ecol 13:2471-2479.
74. Wirth T, Bernatchez L (2003) Decline of North Atlantic eels: A fatal synergy? Proc R Soc Lond B 270:681-688. (Pubitemid 36433919)