Parallel evolution in Ugandan crater lakes: repeated evolution of limnetic body shapes in haplochromine cichlid fish
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  • 作者:Gonzalo Machado-Schiaffino (1)
    Andreas F Kautt (1) (2)
    Henrik Kusche (1) (2)
    Axel Meyer (1) (2)

    1. Department of Biology
    ; Chair of Zoology and Evolutionary Biology ; University of Konstanz ; Universit盲tsstrasse 10 ; 78457 ; Konstanz ; Germany
    2. International Max Planck Research School for Organismal Biology
    ; University of Konstanz ; Universit盲tsstrasse 10 ; 78457 ; Konstanz ; Germany
  • 关键词:Parallel evolution ; Benthic ; limnetic ; Speciation
  • 刊名:BMC Evolutionary Biology
  • 出版年:2015
  • 出版时间:December 2015
  • 年:2015
  • 卷:15
  • 期:1
  • 全文大小:1,042 KB
  • 参考文献:1. Meyer A. Phylogenetic-relationships and evolutionary processes in East-African cichlid fishes. Trends Ecol Evol. 1993;8(8):279鈥?4. CrossRef
    2. Kocher TD. Adaptive evolution and explosive speciation: The cichlid fish model. Nat Rev Genet. 2004;5(4):288鈥?8. CrossRef
    3. Henning F, Meyer A. The evolutionary genomics of cichlid fishes: explosive speciation and adaptation in the postgenomic era. Annual Rev Genomics Human Genetics. 2014;15:417鈥?1. CrossRef
    4. Salzburger W, Mack T, Verheyen E, Meyer A. Out of Tanganyika: Genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol. 2005;5:17. CrossRef
    5. Meyer A, Kocher TD, Basasibwaki P, Wilson AC. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial-DNA sequences. Nature. 1990;347(6293):550鈥?. CrossRef
    6. Verheyen E, Salzburger W, Snoeks J, Meyer A. Origin of the superflock of cichlid fishes from Lake Victoria. East Africa Sci. 2003;300(5617):325鈥?.
    7. Elmer KR, Reggio C, Wirth T, Verheyen E, Salzburger W, Meyer A. 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. 2009;106(32):13404鈥?. CrossRef
    8. Seehausen O. Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14 600聽year history for its cichlid species flock. Proc R Soc B-Biol Sci. 2002;269(1490):491鈥?. CrossRef
    9. Stiassny MLJ, Meyer A. Cichlids of the Rift lakes. SciAm. 1999;280(2):64鈥?.
    10. McCune AR, Lovejoy NR. The relative rate of sympatric and allopatric speciation in fishes: tests using DNA sequence divergence between sister species among clades. In: Howard DJ, Berlocher SH, editors. Endless Forms : Species and Speciation. New York: Oxford University Press; 1998. p. 172鈥?5.
    11. Kocher TD, Conroy JA, McKaye KR, Stauffer JR. Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence. Mol Phylogenet Evol. 1993;2(2):158鈥?5. CrossRef
    12. Ruber L, Verheyen E, Meyer A. Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proc Natl Acad Sci U S A. 1999;96(18):10230鈥?. CrossRef
    13. Schluter D, Nagel LM. Parallel speciation by natural-selection. Am Nat. 1995;146(2):292鈥?01. CrossRef
    14. Losos JB. Convergence, adaptation and constraint. Evolution. 2011;65(7):1827鈥?0. CrossRef
    15. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, Johnson J, et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484(7392):55鈥?1. CrossRef
    16. Mahler DL, Ingram T, Revell LJ, Losos JB. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science. 2013;341(6143):292鈥?. CrossRef
    17. Elmer KR, Kusche H, Lehtonen TK, Meyer A. Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Philos Trans R Soc B-Biol Sci. 2010;365(1547):1763鈥?2. CrossRef
    18. Elmer KR, Meyer A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol Evol. 2011;26(6):298鈥?06. CrossRef
    19. Boven A, Pasteels P, Punzalan LE, Yamba TK, Musisi JH. Quaternary perpotassic magmatism in Uganda (Toro-Ankole Volcanic Province): age assessment and significance for magmatic evolution along the East African Rift. J Afr Earth Sci. 1998;26(3):463鈥?6. CrossRef
    20. Sato A, Takezaki N, Tichy H, Figueroa F, Mayer WE, Klein J. Origin and speciation of haplochromine fishes in east african crater lakes investigated by the analysis of their mtDNA, Mhc genes, and SINEs. Mol Biol Evol. 2003;20(9):1448鈥?2. CrossRef
    21. Samonte IE, Satta Y, Sato A, Tichy H, Takahata N, Klein J. Gene flow between species of Lake Victoria haplochromine fishes. Mol Biol Evol. 2007;24(9):2069鈥?0. CrossRef
    22. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611鈥?0. CrossRef
    23. Coyne JA, Orr HA. Speciation. Sunderland, Massachusetts: Sinauer; 2004.
    24. Mayr E. Systematics and the Origin of Species from the Viewpoint of a Zoologist. Cambridge, MA: Harvard University Press; 1942.
    25. Mayr E. Animal Species and Evolution. Cambridge: Belknap Press of Harvard University Press; 1963. CrossRef
    26. Wootton RJ. Ecology of Teleost Fishes. London: Chapman and Hall; 1990.
    27. Landry L, Bernatchez L. Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs (Coregonus sp.). J Evol Biol. 2010;23(12):2602鈥?3. CrossRef
    28. Gow JL, Rogers SM, Jackson M, Schluter D. Ecological predictions lead to the discovery of a benthic-limnetic sympatric species pair of threespine stickleback in little quarry lake, British Columbia. Can J Zool-Rev Can Zool. 2008;86(6):564鈥?1. CrossRef
    29. Schluter D. The Ecology of Adaptive Radiation. Oxford: Oxford University Press; 2000.
    30. Barrett RDH, Rogers SM, Schluter D. Natural selection on a major armor gene in threespine stickleback. Science. 2008;322(5899):255鈥?. CrossRef
    31. Alberch P. Ontogenesis and morphological diversification. Am Zool. 1980;20(4):653鈥?7.
    32. Meyer A. Phenotypic plasticity and heterochrony in Cichlasoma-managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution. 1987;41(6):1357鈥?9. CrossRef
    33. Schluter D, McPhail JD. Ecological character displacement and speciation in sticklebacks. Am Nat. 1992;140(1):85鈥?08. CrossRef
    34. Ostbye K, Amundsen PA, Bernatchez L, Klemetsen A, Knudsen R, Kristoffersen R, et al. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Mol Ecol. 2006;15(13):3983鈥?001. CrossRef
    35. Malmquist HJ, Snorrason SS, Skulason S, Jonsson B, Sandlund OT, Jonasson PM. Diet differentiation in polymorphic arctic charr in Thingvallavatn. Iceland J Anim Ecol. 1992;61(1):21鈥?5. CrossRef
    36. Robinson BW, Wilson DS. Character release and displacement in fishes - a neglected literature. Am Nat. 1994;144(4):596鈥?27. CrossRef
    37. Kautt AF, Elmer KR, Meyer A. Genomic signatures of divergent selection and speciation patterns in a natural experiment', the young parallel radiations of Nicaraguan crater lake cichlid fishes. Mol Ecol. 2012;21(19):4770鈥?6. CrossRef
    38. Meyer A. Ecological and evolutionary consequences of the trophic polymorphism in / Cichlasoma-citrinellum (pisces, cichlidae). Biol J Linnean Soc. 1990;39(3):279鈥?9. CrossRef
    39. Hulsey CD, Roberts RJ, Loh YHE, Rupp MF, Streelman JT. Lake Malawi cichlid evolution along a benthic/limnetic axis. Ecol Evol. 2013;3(7):2262鈥?2. CrossRef
    40. Kusche H, Recknagel H, Elmer KR, Meyer A. Crater lake cichlids individually specialize along the benthic- limnetic axis. Ecol Evol. 2014;4(7):1127鈥?9. CrossRef
    41. Franchini P, Fruciano C, Spreitzer ML, Jones JC, Elmer KR, Henning F, et al. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Mol Ecol. 2014;23(7):1828鈥?5. CrossRef
    42. Seehausen O. African cichlid fish: a model system in adaptive radiation research. Proc R Soc B-Biol Sci. 2006;273(1597):1987鈥?8. CrossRef
    43. Martin CH. Strong assortative mating by diet, color, size, and morphology but limited progress toward sympatric speciation in a classic example: Cameroon crater lake cichlids. Evolution. 2013;67(7):2114鈥?3. CrossRef
    44. Wagner CE, Harmon LJ, Seehausen O. Ecological opportunity and sexual selection together predict adaptive radiation. Nature. 2012;487(7407):366鈥揢124. CrossRef
    45. Schliewen UK, Tautz D, Paabo S. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature. 1994;368(6472):629鈥?2. CrossRef
    46. Barluenga M, Meyer A. Phylogeography, colonization and population history of the Midas cichlid species complex (Amphilophus spp.) in the Nicaraguan crater lakes. BMC Evol Biol. 2010;10:326. CrossRef
    47. Recknagel H, Elmer KR, Meyer A. Crater lake habitat predicts morphological diversity in adaptive radiations of cichlid fishes. Evolution. 2014;68:2145鈥?5. CrossRef
    48. Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature. 2006;439(7077):719鈥?3. CrossRef
    49. Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T, Tautz D. Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol. 2001;10(6):1471鈥?8. CrossRef
    50. Bruford MW, Hanotte O, Brookfield JFY, Burke T. Multilocus and single locus DNA fingerprinting. In: Hoelzel AR, editor. Molecular Genetics Analysis of Populations: A Practical Approach. Oxford: Oxford University Press; 1998. p. 287鈥?36.
    51. Sanetra M, Henning F, Fukamachi S, Meyer A. A microsatellite-based genetic linkage Map of the cichlid fish, astatotilapia burtoni (teleostei): a comparison of genomic architectures among rapidly speciating cichlids. Genetics. 2009;182(1):387鈥?7. CrossRef
    52. Wu L, Kaufman L, Fuerst PA. Isolation of microsatellite markers in Astatoreochromis alluaudi and their cross-species amplifications in other African cichlids. Mol Ecol. 1999;8(5):895鈥?. CrossRef
    53. Zardoya R, Vollmer DM, Craddock C, Streelman JT, Karl S, Meyer A. Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proc R Soc B-Biol Sci. 1996;263(1376):1589鈥?8. CrossRef
    54. Kellogg KA, Markert JA, Stauffer JR, Kocher TD. Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from lake Malawi, africa. Proc R Soc B-Biol Sci. 1995;260(1357):79鈥?4. CrossRef
    55. Meyer A, Morrissey JM, Schartl M. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature. 1994;368(6471):539鈥?2. CrossRef
    56. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95鈥?.
    57. Rozas J, S谩nchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19:2496鈥?. CrossRef
    58. Posada D, Crandall K. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817鈥?. CrossRef
    59. Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online. 2005;1:47鈥?0.
    60. Nei M. Molecular Evolutionary Genetics. New York: Columbia University Press; 1987.
    61. Teacher AGF, Griffiths DJ. HapStar: automated haplotype network layout and visualization. Mol Ecol Resour. 2011;11(1):151鈥?. CrossRef
    62. Schneider S, Roessli D, Excoffier L. Arlequin ver. 2000: A Software for Population Genetics Data Analysis. University of Geneva, Switzerland: Genetics and Biometry Laboratory; 2000.
    63. Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147(2):915鈥?5.
    64. Schneider S, Excoffier L. Estimation of demographic parameters from the distribution of pairwise differenced when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics. 1999;152:1079鈥?9.
    65. Nielsen R, Wakeley JW. Distinguishing migration from isolation: an MCMC approach. Genetics. 2001;158:885鈥?6.
    66. Koblmuller S, Duftner N, Sefc KM, Aigner U, Rogetzer M, Sturmbauer C. Phylogeographic structure and gene flow in the scale-eating cichlid Perissodus microlepis (Teleostei, Perciformes, Cichlidae) in southern Lake Tanganyika. Zool Scr. 2009;38(3):257鈥?8. CrossRef
    67. Van Oosterhout C, William F, Hutchinson DP, Wills M, Shipley P. Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535鈥?. CrossRef
    68. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G. LOSITAN: A workbench to detect molecular adaptation based on a F(st)-outlier method. BMC Bioinformatics. 2008;9:5. CrossRef
    69. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. Genetix 4.02, Logiciel Sous Windows TM Pour la G茅n茅tique des Populations. Montpellier (France): Laboratoire G茅nome, Populations, Universit茅 de Montpellier II; 2004.
    70. Rice WR. Analyzing tables of statistical tests. Evolution. 1989;43:223鈥?. CrossRef
    71. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945鈥?9.
    72. Earl DA, Vonholdt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4(2):359鈥?1. CrossRef
    73. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics. 2012;28(19):2537鈥?. CrossRef
    74. Beerli P, Felsenstein J. Maximum likelihood estimation of migration rates and population numbers of two populations using a coalescent approach. Genetics. 1999;152(2):763鈥?3.
    75. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.6a2. Seattle: Department of Genetics, University of Washington; 1993.
    76. Rohlf FJ. TPSDIG2.17. A program for landmark development and analysis. 2001. Available online: http://life.bio.sunysb.edu/morph/soft-dataacq.html.
    77. Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11(2):353鈥?. CrossRef
    78. Dryden I, Mardia K. Statistical Shape Analysis. New York: Wiley; 1998.
    79. Zelditch M, Swiderski D, Sheets HD, Fink WL. Geometric Morphometrics for Biologists. San Diego, California: Elsevier Academic Press; 2004.
  • 刊物主题:Evolutionary Biology; Animal Systematics/Taxonomy/Biogeography; Entomology; Genetics and Population Dynamics; Life Sciences, general;
  • 出版者:BioMed Central
  • ISSN:1471-2148
文摘
Background The enormous diversity found in East African cichlid fishes in terms of morphology, coloration, and behavior have made them a model for the study of speciation and adaptive evolution. In particular, haplochromine cichlids, by far the most species-rich lineage of cichlids, are a well-known textbook example for parallel evolution. Southwestern Uganda is an area of high tectonic activity, and is home to numerous crater lakes. Many Ugandan crater lakes were colonized, apparently independently, by a single lineage of haplochromine cichlids. Thereby, this system could be considered a natural experiment in which one can study the interaction between geographical isolation and natural selection promoting phenotypic diversification. Results We sampled 13 crater lakes and six potentially-ancestral older lakes and, using both mitochondrial and microsatellite markers, discovered strong genetic and morphological differentiation whereby (a) geographically close lakes tend to be genetically more similar and (b) three different geographic areas seem to have been colonized by three independent waves of colonization from the same source population. Using a geometric morphometric approach, we found that body shape elongation (i.e. a limnetic morphology) evolved repeatedly from the ancestral deeper-bodied benthic morphology in the clear and deep crater lake habitats. Conclusions A pattern of strong genetic and morphological differentiation was observed in the Ugandan crater lakes. Our data suggest that body shape changes have repeatedly evolved into a more limnetic-like form in several Ugandan crater lakes after independent waves of colonization from the same source population. The observed morphological changes in crater lake cichlids are likely to result from a common selective regime.
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