Positive Darwinian selection drives the evolution of the morphology-related gene, EPCAM, in particularly species-rich lineages of African cichlid fishes

Journal of Molecular Evolution

Volumn 73, Issue 1-2, 2011, Pages 1-9

  Fan, Shaohua ^a   Elmer, Kathryn R ^a   Meyer, Axel ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Adaptive radiation; Epithelial cell adhesion molecule; Positive Darwinian selection

Indexed keywords

CELL ADHESION MOLECULE; TUMOR ANTIGEN; TUMOR ASSOCIATED ANTIGEN GA733; TUMOR-ASSOCIATED ANTIGEN GA733;

ANIMAL; ARTICLE; CICHLID; CLASSIFICATION; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; SPECIES DIFFERENCE;

ANIMALS; ANTIGENS, NEOPLASM; CELL ADHESION MOLECULES; CICHLIDS; EVOLUTION, MOLECULAR; PHYLOGENY; SELECTION, GENETIC; SPECIES SPECIFICITY;

AFRICAN CICHLIDS; AMPHILOPHUS; AMPHILOPHUS CITRINELLUS; CICHLIDAE; OREOCHROMIS NILOTICUS; PISCES; TILAPIA;

EID: 79960879029     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-011-9452-5     Document Type: Article

References (77)

1. R Abila M Barluenga J Engelken A Meyer W Salzburger 2004 Population-structure and genetic diversity in a haplochromine fish cichlid of a satellite lake of Lake Victoria Mol Ecol 13 2589 2602 15315673 10.1111/j.1365-294X.2004.02270.x 1:CAS:528:DC%2BD2cXotlemtL4%3D (Pubitemid 39151618)
2. RC Albertson TD Kocher 2006 Genetic and developmental basis of cichlid trophic diversity Heredity 97 211 221 16835594 10.1038/sj.hdy.6800864 1:CAS:528:DC%2BD28XosVOmt7Y%3D (Pubitemid 44289681)
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
4. M Anisimova JP Bielawski Z Yang 2001 Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution Mol Biol Evol 18 1585 1592 11470850 1:CAS:528:DC%2BD3MXlslOisLw%3D (Pubitemid 32735106)
5. PA Baeuerle O Gires 2007 EpCAM (CD326) finding its role in cancer Br J Cancer 96 417 423 17211480 10.1038/sj.bjc.6603494 1:CAS:528:DC%2BD2sXhtlKjtrg%3D (Pubitemid 46215211)
6. M Barrier RH Robichaux MD Purugganan 2001 Accelerated regulatory gene evolution in an adaptive radiation Proc Natl Acad Sci USA 98 10208 10213 11517318 10.1073/pnas.181257698 1:CAS:528:DC%2BD3MXmvFWitLc%3D (Pubitemid 32802999)
7. HM Berman J Westbrook Z Feng G Gilliland TN Bhat H Weissig IN Shindyalov PE Bourne 2000 The protein data bank Nucleic Acids Res 28 235 242 10592235 10.1093/nar/28.1.235 1:CAS:528:DC%2BD3cXhvVKjt7w%3D (Pubitemid 30047768)
8. Boguski MS, Lowe TMJ, Tolstoshev CM (1993) Dbest - database for expressed sequence tags. Nat Genet 4:332-333 (Pubitemid 23231478)
9. Dann SG, Allison WT, Levin DB, Taylor JS, Hawryshyn CW (2004) Salmonid opsin sequences undergo positive selection and indicate an alternate evolutionary relationship in Oncorhynchus. J Mol Evol 58:400-412 (Pubitemid 38501414)
10. N Eldredge JN Thompson PM Brakefield S Gavrilets D Jablonski JBC Jackson RE Lenski BS Lieberman MA McPeek W Miller 2005 The dynamics of evolutionary stasis Paleobiology 31 133 145 10.1666/0094-8373(2005)031[0133:TDOES]2.0.CO;2 (Pubitemid 40906548)
11. KR Elmer C Reggio T Wirth E Verheyen W Salzburger 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 USA 106 13404 13409 19651614 10.1073/pnas.0902299106 1:CAS:528: DC%2BD1MXhtVOitr3I
12. KR Elmer S Fan HM Gunter JC Jones S Boekhoff S Kuraku A Meyer 2010 Rapid evolution and selection inferred from the transcriptomes of sympatric crater lake cichlid fishes Mol Ecol 19 197 211 20331780 10.1111/j.1365-294X.2009.04488. x 1:CAS:528:DC%2BC3cXksVyrtbw%3D
13. KR Elmer H Kusche TK Lehtonen A Meyer 2010 Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes Philos Trans R Soc Lond B Biol Sci 365 1763 1782 20439280 10.1098/rstb.2009.0271
14. IP Farias G Orti I Sampaio H Schneider A Meyer 1999 Mitochondrial DNA phylogeny of the family Cichlidae: monophyly and fast molecular evolution of the neotropical assemblage J Mol Evol 48 703 711 10229574 10.1007/PL00006514 1:CAS:528:DyaK1MXkt1yntbk%3D (Pubitemid 29287960)
15. JV Forrester HP Xu L Kuffova AD Dick PG McMenamin 2010 Dendritic cell physiology and function in the eye Immunol Rev 234 282 304 20193026 10.1111/j.0105-2896.2009.00873.x 1:CAS:528:DC%2BC3cXjslartLk%3D
16. S Gavrilets JB Losos 2009 Adaptive radiation: contrasting theory with data Science 323 732 737 19197052 10.1126/science.1157966 1:CAS:528: DC%2BD1MXhtlertrc%3D
17. MJ Genner O Seehausen DH Lunt DA Joyce PW Shaw GR Carvalho GF Turner 2007 Age of cichlids: new dates for ancient lake fish radiations Mol Biol Evol 24 1269 1282 17369195 10.1093/molbev/msm050 1:CAS:528:DC%2BD2sXmtVOisLs%3D (Pubitemid 47343652)
18. DT Gerrard A Meyer 2007 Positive selection and gene conversion in SPP120, a fertilization-related gene, during the East African cichlid fish radiation Mol Biol Evol 24 2286 2297 17675335 10.1093/molbev/msm159 1:CAS:528: DC%2BD2sXht1ejsLnL (Pubitemid 47574729)
19. GB Golding AM Dean 1998 The structural basis of molecular adaptation Mol Biol Evol 15 355 369 9549087 1:CAS:528:DyaK1cXitlKiurs%3D (Pubitemid 28153146)
20. S Guindon F Delsuc JF Dufayard O Gascuel 2009 Estimating maximum likelihood phylogenies with PhyML Methods Mol Biol 537 113 137 19378142 10.1007/978-1-59745-251-9-6 1:CAS:528:DC%2BD1MXmvVSqtbw%3D
21. M Hasegawa H Kishino T Yano 1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA J Mol Evol 22 160 174 3934395 10.1007/BF02101694 1:CAS:528:DyaL2MXmtFSns7g%3D (Pubitemid 16227864)
22. HE Hoekstra RJ Hirschmann RA Bundey PA Insel JP Crossland 2006 A single amino acid mutation contributes to adaptive beach mouse color pattern Science 313 101 104 16825572 10.1126/science.1126121 1:CAS:528:DC%2BD28XmsFWjurg%3D (Pubitemid 44051263)
23. Hofmann CM, O'Quin KE, Marshall NJ, Cronin TW, Seehausen O, Carleton KL (2009) The eyes have it: regulatory and structural changes both underlie cichlid visual pigment diversity. PLoS Biol 7:e1000266
24. X Huang A Madan 1999 CAP3: a DNA sequence assembly program Genome Res 9 868 877 10508846 10.1101/gr.9.9.868 1:CAS:528:DyaK1MXmslKgs7Y%3D (Pubitemid 29488446)
25. T Hubbard D Barker E Birney G Cameron Y Chen L Clark T Cox J Cuff V Curwen T Down R Durbin E Eyras J Gilbert M Hammond L Huminiecki A Kasprzyk H Lehvaslaiho P Lijnzaad C Melsopp E Mongin R Pettett M Pocock S Potter A Rust E Schmidt S Searle G Slater J Smith W Spooner A Stabenau J Stalker E Stupka A Ureta-Vidal I Vastrik M Clamp 2002 The Ensembl genome database project Nucleic Acids Res 30 38 41 11752248 10.1093/nar/30.1.38 1:CAS:528:DC%2BD38Xht12ksbY%3D (Pubitemid 34679498)
26. AL Hughes 2007 Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level Heredity 99 364 373 17622265 10.1038/sj.hdy.6801031 1:CAS:528:DC%2BD2sXhtVyjt7%2FE (Pubitemid 47482647)
27. CD Hulsey RJ Roberts AS Lin R Guldberg JT Streelman 2008 Convergence in a mechanically complex phenotype: detecting structural adaptations for crushing in cichlid fish Evolution 62 1587 1599 18373629 10.1111/j.1558-5646.2008.00384.x (Pubitemid 352000087)
28. J Jeukens D Bittner R Knudsen L Bernatchez 2009 Candidate genes and adaptive radiation: insights from transcriptional adaptation to the limnetic niche among coregonine fishes (Coregonus spp., Salmonidae) Mol Biol Evol 26 155 166 18927090 10.1093/molbev/msn235 1:CAS:528:DC%2BD1MXlsVKhtw%3D%3D
29. MV Kapralov DA Filatov 2006 Molecular adaptation during adaptive radiation in the Hawaiian endemic genus Schiedea PLoS One 1 e8 17183712 10.1371/journal.pone.0000008
30. T Kijimoto M Watanabe K Fujimura M Nakazawa Y Murakami S Kuratani Y Kohara T Gojobori N Okada 2005 cimp1, a novel astacin family metalloproteinase gene from East African cichlids, is differentially expressed between species during growth Mol Biol Evol 22 1649 1660 15858202 10.1093/molbev/msi159 1:CAS:528:DC%2BD2MXmslCqu7c%3D (Pubitemid 41373576)
31. N Kobayashi M Watanabe T Horiike Y Kohara N Okada 2009 Extensive analysis of EST sequences reveals that all cichlid species in Lake Victoria share almost identical transcript sets Gene 441 187 191 19101614 10.1016/j.gene.2008.11.023 1:CAS:528:DC%2BD1MXmsFGrtrk%3D
32. S Koblmuller W Salzburger C Sturmbauer 2004 Evolutionary relationships in the sand-dwelling cichlid lineage of Lake Tanganyika suggest multiple colonization of rocky habitats and convergent origin of biparental mouthbrooding J Mol Evol 58 79 96 14743316 10.1007/s00239-003-2527-1 (Pubitemid 38117600)
33. TD Kocher 2004 Adaptive evolution and explosive speciation: the cichlid fish model Nat Rev Genet 5 288 298 15131652 10.1038/nrg1316 1:CAS:528: DC%2BD2cXjtVartLs%3D (Pubitemid 38435624)
34. TD Kocher JA Conroy KR McKaye JR Stauffer 1993 Similar morphologies of cichlid fish in Lakes Tanganyika and Malawi are due to convergence Mol Phylogenet Evol 2 158 165 8025722 10.1006/mpev.1993.1016 1:CAS:528: DyaK2cXhvVOmu7Y%3D
35. S Kuraku A Meyer 2008 Genomic analysis of cichlid fish 'natural mutants' Curr Opin Genet Dev 18 551 558 19095433 10.1016/j.gde.2008.11.002 1:CAS:528:DC%2BD1MXhtFCjsr0%3D
36. BY Lee AE Howe MA Conte H D'Cotta E Pepey JF Baroiller F di Palma KL Carleton TD Kocher 2010 An EST resource for tilapia based on 17 normalized libraries and assembly of 116,899 sequence tags BMC Genomics 11 278 20433739 10.1186/1471-2164-11-278
37. W Messier CB Stewart 1997 Episodic adaptive evolution of primate lysozymes Nature 385 151 8990116 10.1038/385151a0 1:CAS:528:DyaK2sXks1Sjug%3D%3D (Pubitemid 27034214)
38. A Meyer 1993 Phylogenetic-relationships and evolutionary processes in East-African cichlid fishes Trends Ecol Evol 8 279 284 21236169 10.1016/0169-5347(93)90255-N 1:STN:280:DC%2BC3M7itVyqug%3D%3D (Pubitemid 24410252)
39. A Meyer TD Kocher P Basasibwaki AC Wilson 1990 Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences Nature 347 550 553 2215680 10.1038/347550a0 1:CAS:528:DyaK3cXmt1yhs7w%3D (Pubitemid 20341543)
40. A Meyer CH Biermann G Orti 1993 The phylogenetic position of the zebrafish (Danio-Rerio), a model system in developmental biology-an invitation to the comparative method Proc R Soc Lond B Biol Sci 252 231 236 10.1098/rspb.1993.0070 1:CAS:528:DyaK2cXktVGnur0%3D (Pubitemid 23210754)
41. T Ohta 1995 Synonymous and nonsynonymous substitutions in mammalian genes and the nearly neutral theory J Mol Evol 40 56 63 7714912 10.1007/BF00166595 1:CAS:528:DyaK2MXjtVektLk%3D
42. GI Peterson J Masel 2009 Quantitative prediction of molecular clock and Ka/Ks at short timescales Mol Biol Evol 26 2595 2603 19661199 10.1093/molbev/msp175 1:CAS:528:DC%2BD1MXht1OqsL3I
43. D Posada KA Crandall 1998 MODELTEST: testing the model of DNA substitution Bioinformatics 14 817 818 9918953 10.1093/bioinformatics/14.9.817 1:CAS:528:DyaK1MXktlCltw%3D%3D (Pubitemid 28552116)
44. E Quevillon V Silventoinen S Pillai N Harte N Mulder R Apweiler R Lopez 2005 InterProScan: protein domains identifier Nucleic Acids Res 33 W116 W120 15980438 10.1093/nar/gki442 1:CAS:528:DC%2BD2MXlslyqsbs%3D (Pubitemid 44529891)
45. SM Rogers L Bernatchez 2007 The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonas sp. Salmonidae) species pairs Mol Biol Evol 24 1423 1438 17404398 10.1093/molbev/msm066 1:CAS:528:DC%2BD2sXmsl2jtLk%3D (Pubitemid 47343948)
46. L Ruber E Verheyen A Meyer 1999 Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika Proc Natl Acad Sci USA 96 10230 10235 10468591 10.1073/pnas.96.18.10230 1:CAS:528:DyaK1MXlvFegu70%3D (Pubitemid 29422541)
47. W Salzburger A Meyer 2004 The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics Naturwissenschaften 91 277 290 15241604 10.1007/s00114-004-0528-6 1:CAS:528:DC%2BD2cXlsVCrsr0%3D (Pubitemid 38916482)
48. W Salzburger A Meyer S Baric E Verheyen C Sturmbauer 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 11943095 10.1080/106351502753475907 (Pubitemid 35169410)
49. W Salzburger T Mack E Verheyen A Meyer 2005 Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes BMC Evol Biol 5 17 15723698 10.1186/1471-2148-5-17 (Pubitemid 40548671)
50. W Salzburger I Braasch A Meyer 2007 Adaptive sequence evolution in a color gene involved in the formation of the characteristic egg-dummies of male haplochromine cichlid fishes BMC Biol 5 51 18005399 10.1186/1741-7007-5-51 (Pubitemid 351757068)
51. W Salzburger SC Renn D Steinke I Braasch HA Hofmann A Meyer 2008 Annotation of expressed sequence tags for the East African cichlid fish Astatotilapia burtoni and evolutionary analyses of cichlid ORFs BMC Genomics 9 96 18298844 10.1186/1471-2164-9-96 (Pubitemid 351472498)
52. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford
53. D Schluter 2001 Ecology and the origin of species Trends Ecol Evol 16 372 380 11403870 10.1016/S0169-5347(01)02198-X (Pubitemid 32525778)
54. D Schluter 2009 Evidence for ecological speciation and its alternative Science 323 737 741 19197053 10.1126/science.1160006 1:CAS:528: DC%2BD1MXhtlert78%3D
55. O Seehausen 2006 African cichlid fish: a model system in adaptive radiation research Proc R Soc Lond B Biol Sci 273 1987 1998 10.1098/rspb.2006. 3539 (Pubitemid 44214911)
56. O Seehausen Y Terai IS Magalhaes KL Carleton HD Mrosso R Miyagi I van der Sluijs MV Schneider ME Maan H Tachida H Imai N Okada 2008 Speciation through sensory drive in cichlid fish Nature 455 620 626 18833272 10.1038/nature07285 1:CAS:528:DC%2BD1cXhtF2hsbrL
57. K Slanchev TJ Carney MP Stemmler B Koschorz A Amsterdam H Schwarz M Hammerschmidt 2009 The epithelial cell adhesion molecule EPCAM is required for epithelial morphogenesis and integrity during zebrafish epiboly and skin development PLoS Genet 5 e1000563 19609345 10.1371/journal.pgen.1000563
58. TC Spady O Seehausen ER Loew RC Jordan TD Kocher KL Carleton 2005 Adaptive molecular evolution in the opsin genes of rapidly speciating cichlid species Mol Biol Evol 22 1412 1422 15772376 10.1093/molbev/msi137 1:CAS:528:DC%2BD2MXksFGktb8%3D (Pubitemid 40734192)
59. D Steinke W Salzburger A Meyer 2006 Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs J Mol Evol 62 772 784 16752215 10.1007/s00239-005-0170-8 1:CAS:528:DC%2BD28Xlt1Ois7w%3D (Pubitemid 43847227)
60. C Sturmbauer A Meyer 1992 Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes Nature 358 578 581 1501712 10.1038/358578a0 1:STN:280:DyaK38zmsFyiug%3D%3D (Pubitemid 23395472)
61. T Sugawara Y Terai N Okada 2002 Natural selection of the rhodopsin gene during the adaptive radiation of East African Great Lakes Cichlid fishes Mol Biol Evol 19 1807 1811 12270908 1:CAS:528:DC%2BD38XnvFSlu7c%3D
62. Sugie A, Terai Y, Ota R, Okada N (2004) The evolution of genes for pigmentation in African cichlid fishes. Gene 343:337-346 (Pubitemid 39593443)
63. Summers K, Zhu Y (2008) Positive selection on a prolactin paralog following gene duplication in cichlids: adaptive evolution in the context of parental care? Copeia 4:872-876
64. Y Terai N Morikawa K Kawakami N Okada 2002 Accelerated evolution of the surface amino acids in the WD-repeat domain encoded by the hagoromo gene in an explosively speciated lineage of East African cichlid fishes Mol Biol Evol 19 574 578 11919300 1:CAS:528:DC%2BD38XivV2gurw%3D (Pubitemid 34289434)
65. Terai Y, Morikawa N, Kawakami K, Okada N (2003) The complexity of alternative splicing of hagoromo mRNAs is increased in an explosively speciated lineage in East African cichlids. Proc Natl Acad Sci USA 100:12798-12803 (Pubitemid 37339979)
66. Y Terai N Morikawa N Okada 2002 The evolution of the pro-domain of bone morphogenetic protein 4 (Bmp4) in an explosively speciated lineage of East African cichlid fishes Mol Biol Evol 19 1628 1632 12200490 (Pubitemid 36752787)
67. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2:Unit 2.3
68. M Trzpis PM McLaughlin LM de Leij MC Harmsen 2007 Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule Am J Pathol 171 386 395 17600130 10.2353/ajpath.2007.070152 1:CAS:528: DC%2BD2sXpsFaitLg%3D (Pubitemid 47344671)
69. M Trzpis E Bremer PM McLaughlin LF de Leij MC Harmsen 2008 EpCAM in morphogenesis Front Biosci 13 5050 5055 18508569 10.2741/3063 1:CAS:528:DC%2BD1cXnsVOjt7k%3D (Pubitemid 351611593)
70. M Trzpis PM McLaughlin ER Popa P Terpstra TG Van Kooten LM De Leij MC Harmsen 2008 EpCAM homologues exhibit epithelial-specific but different expression patterns in the kidney Transgenic Res 17 229 238 17940847 10.1007/s11248-007-9141-8 1:CAS:528:DC%2BD1cXjsVSksrY%3D (Pubitemid 351421976)
71. E Verheyen W Salzburger J Snoeks A Meyer 2003 Origin of the superflock of cichlid fishes from Lake Victoria, East Africa Science 300 325 329 12649486 10.1126/science.1080699 1:CAS:528:DC%2BD3sXislyqtLg%3D (Pubitemid 36433723)
72. M Watanabe N Kobayashi T Shin-i T Horiike Y Tateno Y Kohara N Okada 2004 Extensive analysis of ORF sequences from two different cichlid species in Lake Victoria provides molecular evidence for a recent radiation event of the Victoria species flock: identity of EST sequences between Haplochromis chilotes and Haplochromis sp. "Redtailsheller" Gene 343 263 269 15588581 10.1016/j.gene.2004.09.013 1:CAS:528:DC%2BD2cXhtVGit7zM (Pubitemid 39610454)
73. Z Yang 2007 PAML 4: phylogenetic analysis by maximum likelihood Mol Biol Evol 24 1586 1591 17483113 10.1093/molbev/msm088 1:CAS:528:DC%2BD2sXpsVGrs7c%3D (Pubitemid 47236688)
74. Z Yang R Nielsen 2002 Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages Mol Biol Evol 19 908 917 12032247 1:CAS:528:DC%2BD38Xks1Ojtbk%3D (Pubitemid 34602960)
75. ZH Yang WSW Wong R Nielsen 2005 Bayes empirical Bayes inference of amino acid sites under positive selection Mol Biol Evol 22 1107 1118 15689528 10.1093/molbev/msi097 1:CAS:528:DC%2BD2MXjtFaisbk%3D (Pubitemid 40471423)
76. R Zardoya DM Vollmer C Craddock JT Streelman S Karl A Meyer 1996 Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes) Proc Biol Sci 263 1589 1598 8952095 10.1098/rspb.1996.0233 1:CAS:528:DyaK2sXivVentA%3D%3D (Pubitemid 26400231)
77. J Zhang R Nielsen Z Yang 2005 Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level Mol Biol Evol 22 2472 2479 16107592 10.1093/molbev/msi237 1:CAS:528: DC%2BD2MXht1KgtLbM (Pubitemid 41661383)