Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as "Tilapia"

Molecular Phylogenetics and Evolution

Volumn 68, Issue 1, 2013, Pages 64-80

  Dunz, Andreas R ^a   Schliewen, Ulrich K ^a  

^a ZOOLOGISCHE STAATSSAMMLUNG MÜNCHEN   (Germany)

Author keywords

Africa; Cichlidae; Cytonuclear discordance; Freshwater fishes; New classification; Pseudocrenilabrinae

Indexed keywords

MITOCHONDRIAL DNA; NUCLEAR PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; RNA 16S;

AFRICA; ANIMAL; ARTICLE; CELL NUCLEUS; CHEMISTRY; CLASSIFICATION; GENETICS; MITOCHONDRION; PHYLOGENY; PHYLOGEOGRAPHY; SPECIES DIFFERENTIATION; TILAPIA;

AFRICA, EASTERN; AFRICA, WESTERN; ANIMALS; CELL NUCLEUS; DNA, MITOCHONDRIAL; GENETIC SPECIATION; MITOCHONDRIA; NADH DEHYDROGENASE; NUCLEAR PROTEINS; PHYLOGENY; PHYLOGEOGRAPHY; RNA, RIBOSOMAL, 16S; TILAPIA;

AFRICAN CICHLIDS; CICHLIDAE; ETIA; GERVAIS; PISCES; PSEUDOCRENILABRINAE; STEATOCRANUS; TILAPIA;

EID: 84876184330     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.03.015     Document Type: Article

References (95)

1. Boulenger, G.A., 1915. Catalogue of the fresh-water fishes of Africa in the British Museum (Natural History). British Museum (Natural History), London.
2. Boulenger, G.A., 1916. Catalogue of the fresh-water fishes of Africa in the British Museum (Natural History). British Museum (Natural History), London.
3. B-Rao C., Majumdar K.C. Multivariate map representation of phylogenetic relationships: application to tilapiine fish. J. Fish Biol. 1998, 52:1199-1217.
4. Chow S., Hazama K. Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol. Ecol. 1998, 7:1255-1256.
5. Coad B.W. A new genus and species of cichlid endemic to southern Iran. Copeia 1982, 1:28-37.
6. Daget, J., 1991. In: Daget, J., Gosse, J.-P., Teugels, G.G., Thys van den Audenaerde, D.F.E. (Eds.), Check-list of the freshwater fishes of Africa (CLOFFA). ISNB, Brussels; MRAC, Tervuren; and ORSTOM, Paris, vol. 4.
7. Dunz A.R., Schliewen U.K. Description of a new species of Tilapia Smith, 1840 (Teleostei: Cichlidae) from Ghana. Zootaxa 2010, 2548:1-21.
8. Dunz A.R., Schliewen U.K. Description of a Tilapia (Coptodon) species flock of Lake Ejagham (Cameroon), including a redescription of Tilapia deckerti Thys van den Audenaerde, 1967. Spixiana 2010, 33:251-280.
9. Dunz A.R., Schliewen U.K. Description of a rheophilic Tilapia species Smith, 1840 (Teleostei: Cichlidae) from Guinea with comments on Tilapia rheophila Daget, 1962. Zootaxa 2012, 3314:17-30.
10. Dunz A.R., Vreven E., Schliewen U.K. Congolapia, a new cichlid genus from the central Congo basin (Perciformes: Cichlidae). Ichthyol. Explor. Freshwat. 2012, 23:155-179.
11. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
12. Eschmeyer, W.N., Fong, J.D., 2012. Species of Fishes by family/subfamily. (07.06.12). http://research.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp.
13. Felsenstein J. Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 1978, 27:401-410.
14. Fowler H.W. Fishes Obtained by Mr. H.W. Bell-Marley Chiefly in Natal and Zululand in 1929 to 1932. Proc. Natl. Acad. Sci. Philadelphia 1934, 86:405-514.
15. Fryer G., Iles T.D. The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution 1972, Oliver & Boyd, Edinburgh.
16. Gante H.F., Collares-Pereira M.J., Coelho M.M. Introgressive hybridisation between two Iberian Chondrostoma species (Teleostei, Cyprinidae) revisited: new evidence from morphology, mitochondrial DNA, allozymes and NOR-phenotypes. Folia. Zool. 2004, 53:423-432.
17. Gardner J.P.A. The Mytilus edulis species complex in southwest England: effects of hybridization and introgression upon interlocus associations and morphometric variation. Mar. Biol. 1996, 125:385-399.
18. Greenwood P.H. A review of the pharyngeal apophysis and its significance in the classification of African cichlid fishes. Bull. Br. Mus. Nat. Hist. Zool. 1978, 33:297-323.
19. Greenwood P.H. The genera of pelmatochromine fishes (Teleostei, Cichlidae). A phylogenetic review. Bull. Br. Mus. Nat. Hist. Zool. 1987, 53:139-203.
20. Gyllensten U., Warton D., Wilson A.C. Maternal inheritance of mitochondrial DNA during backcrossing of two species of mice. J. Hered. 1985, 76:321-324.
21. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. 1999, 41:95-98.
22. Hardig T.M., Brunsfeld S.J., Fritz R.S., Morgan M., Orians C.M. Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone. Mol. Ecol. 2000, 9:9-24.
23. Hoedeman, J.J., De Jong, J.C.M., 1947. Encyclopaedie voor de Aquariumhouder. - Uitgeverij "De Regenboog", Amsterdam, Nederland.
24. Holder M.T., Anderson J.A., Holloway A.K. Difficulties in detecting hybridization. Syst. Biol. 2001, 50:978-982.
25. Huelsenbeck J.P., Ronquist F. MrBayes: bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
26. ICZN International Code of Zoological Nomenclature 1999, International Trust for Zoological Nomenclature, London. fourth ed.
27. Joly S., McLenachan P.A., Lockhart P.J. A statistical approach for distinguishing hybridization and incomplete lineage sorting. Am. Nat. 2009, 174:54-70.
28. Klett V., Meyer A. What, if anything, is a Tilapia?-Mitochondrial ND2 phylogeny of tilapiines and the evolution of parental care systems in the African cichlid fishes. Mol. Biol. Evol. 2002, 19:865-883.
29. Koblmüller S., Duftner N., Katongo C., Phiri H., Sturmbauer C. Ancient divergence in bathypelagic Lake Tanganyika deepwater cichlids: mitochondrial phylogeny of the tribe Bathybatini. J. Mol. Evol. 2005, 60:297-314.
30. Koblmüller S., Sefc K.M., Sturmbauer C. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 2008, 615:5-20.
31. Koblmüller S., Egger B., Sturmbauer C., Sefc K.M. Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini. Mol. Phylogenet. Evol. 2009, 55:318-334.
32. Kocher T.D. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 2004, 5:288-298.
33. Kocher T.D., Thomas W.K., Meyer A., Edwards S.V., Paabo S., Villablanca F.X., Wilson A.C. Dynamics of mitochondrial-Dna evolution in animals - amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 1989, 86:6196-6200.
34. Kocher T.D., Conroy J.A., Mckaye K.R., Stauffer J.R., Lockwood S.F. Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Mol. Phylogenet. Evol. 1995, 4:420-432.
35. Kornfield I., Smith P.F. African cichlid fishes: model systems for evolutionary biology. Annu. Rev. Ecol. Syst. 2000, 31:163-196.
36. Lanfear R., Calcott B., Ho S.Y.W., Guindon S. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 2012, 29:1695-1701.
37. Li C.H., Orti G., Zhang G., Lu G.Q. A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 2007, 7:44.
38. Lippitsch E. Scale and squamation character polarity and phyletic assessment in the family Cichlidae. J. Fish Biol. 1995, 47:91-106.
39. Lippitsch E., Kawanabe H., Hiro M., Nagoshi M. Phylogenetic study of cichlid fishes in Lake Tanganyika: a lepidological approach. J. Fish Biol. 1998, 53:752-766.
40. Mayer W.E., Tichy H., Klein J. Phylogeny of African cichlid fishes as revealed by molecular markers. Heredity 1998, 80:702-714.
41. Mayland H.J. Cichliden 1995, Landbuch-Verlag, Hannover.
42. McAndrew B.J., Majumdar K.C. Evolutionary relationships within three Tilapiine genera (Pisces: Cichlidae). Zool. J. Linn. Soc. 1984, 80:421-435.
43. Meyer A. Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol. Evol. 1993, 8:279-284.
44. Morando M., Avila L.J., Baker J., Sites J.W. Phylogeny and phylogeography of the Liolaemus darwinii complex (Squamata: Liolaemidae): evidence for introgression and incomplete lineage sorting. Evolution 2004, 58:842-861.
45. Nagl S., Tichy H., Mayer W.E., Samonte I.E., McAndrew B.J., Klein J. Classification and phylogenetic relationships of African Tilapiine fishes inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 2001, 20:361-374.
46. Near T.J., Bossu C.M., Bradburd G.S., Carlson R.L., Harrington R.C., Hollingsworth P.R., Keck B.P., Etnier D.A. Phylogeny and temporal diversification of darters (Percidae: Etheostomatinae). Syst. Biol. 2011, 60:565-595.
47. Nishida M. Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: Inferences from allozyme data. Experientia 1991, 47:974-979.
48. Palumbi S., Martin A., Romano S. The Simple Fool's Guide to PCR 1991, University of Hawaii Press, Honolulu.
49. Poll M. Classification des Cichlidae du lac Tanganika. Tribus, genres et espèces. Acad. R. Belg. Mém. Cl. Sci. 1986, 45:1-163.
50. Pouyard L., Agnèse J. Phylogenetic relationships beween 21 species of three tilapiine genera Tilapia, Sarotherodon and Oreochromis using allozyme data. J. Fish. Biol. 1995, 47:26-38.
51. Regan C.T. The classification of the fishes of the family Cichlidae. - I. The Tanganyika genera. Ann. Mag. nat. Hist. 1920, 5:33-53. (Series 9).
52. Regan C.T. The classification of the fishes of the family Cichlidae. - II. On African and Syrian genera not restricted to the great lakes. Ann. Mag. Nat. Hist. 1922, 10:249-264. (Series 9).
53. Ridha M.T. Evaluation of Growth Performance of Nonimproved and Improved Strains of the Nile Tilapia (L.), Oreochromis niloticus. J. World Aquacult. Soc. 2006, 37:218-223.
54. Roberts T.R., Stewart D.J. An ecological and systematic survey of fishes in the rapids of the lower Zaire or Congo River. Bull. Mus. Comp. Zool. 1976, 147:239-317.
55. Rüber L., Meyer A., Sturmbauer C., Verheyen E. Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Mol. Ecol. 2001, 10:1207-1225.
56. Rüber L., Van Tassell J.L., Zardoya R. Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 2003, 57:1584-1598.
57. Salzburger W., Meyer A. The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 2004, 91:277-290.
58. Salzburger W., Meyer A., Baric S., Verheyen E., Sturmbauer C. Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Syst. Biol. 2002, 51:113-135.
59. Schliewen U.K., Klee B. Reticulate sympatric speciation in Cameroonian crater lake cichlids. Front. Zool. 2004, 1:5.
60. Schliewen U.K., Stiassny M.L.J. Etia nguti, a new genus and species of cichlid fish from the River Mamfue, Upper Cross River basin in Cameroon, West-Central Africa. Ichthyol. Explor. Freshwat. 2003, 14:61-71.
61. Schliewen U.K., Tautz D., Pääbo S. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 1994, 368:629-632.
62. Schwarzer J., Misof B., Tautz D., Schliewen U.K. The root of the East African cichlid radiations. BMC Evol. Biol. 2009, 3:1-11.
63. Schwarzer J., Misof B., Ifuta S.N., Schliewen U.K. Time and origin of cichlid colonization of the lower congo rapids. PLoS ONE 2011, 6(7):e22380. 10.1371/journal.pone.0022380.
64. Schwarzer J., Misof B., Schliewen U.K. Speciation within genomic networks: a case study based on Steatocranus cichlids of the lower Congo rapids. J. Evol. Biol. 2012, 25:138-148. 10.1111/j.1420-9101.2011.02409.x.
65. Schwarzer, J., Swartz, E.R., Vreven, E., Snoeks, J., Cotterill, F.P.D., Misof, B., Schliewen, U.K., 2012b. Repeated trans-watershed hybridization among haplochromine cichlids (Cichlidae) was triggered by Neogene landscape evolution. Proc. R. Soc. Lond. B Biol. Sci. 279, 4389-4398.
66. Seehausen O. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. B Biol. Sci. 2006, 273:1987-1998.
67. Shaw K.L. Conflict between mitochondrial and nuclear DNA phylogenies of a recent species radiation, what mitochondrial DNA reveals and conceals about modes of speciation in Hawaian crickets. Proc. Natl. Acad. Sci. USA 2002, 99:16122-16127.
68. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114-1116.
69. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
70. Smith S.A., Dunn C.W. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 2008, 24:715-716.
71. Snoeks J. How well known is the ichthyodiversity of the large East African lakes?. Adv. Ecol. Res. 2000, 31:17-38.
72. Sodsuk P., McAndrew B.J. Molecular systematics of three tilapiine genera, Tilapia, Sarotherodon and Oreochromis using allozyme data. J. Fish Biol. 1991, 39:301-308.
73. Stamatakis A. RAxML-VI-HPC: maximum Likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
74. Stiassny M.L.J. Tylochromis, relationships and the phylogenetic status of the African Cichlidae. Am. Mus. Novit. 1990, 2993:1-14.
75. Stiassny M.L.J. Phylogenetic intrarelationships of the family Cichlidae: an overview. Cichlid Fishes: Behaviour, Ecology and Evolution 1991, 1-35. Chapman and Hall, London. M.H.A. Keenleyside (Ed.).
76. Stiassny, M.L.J., Lamboj, A., De Weirdt, D., Teugels, G.G., 2007. Cichlidae. In: Stiassny, M.L.J., Teugels, G.G., Hopkins, C.D. (Eds.), The fresh and brackish water fishes of Lower Guinea, West-Central Africa, vol. 2. Coll. faune et flore tropicales 42. Institut de recherche de développement, Paris, France, Muséum national d'histoire naturelle, Paris, France and Musée royal de l'Afrique Central, Tervuren, Belgium, pp. 269-403.
77. Stiassny M.L.J., de Marchi G., Lamboj A. A new species of Danakilia (Teleostei, Cichlidae) from Lake Abaeded in the Danakil Depression of Eritrea (East Africa). Zootaxa 2010, 2690:43-52.
78. Streelman J.T., Zardoya R., Meyer A., Karl S.A. Multi-locus phylogeny of cichlid fishes: evolutionary comparison of microsatellite and single-copy nuclear loci. Mol. Biol. Evol. 1998, 15:798-808.
79. Sturmbauer C., Salzburger W., Duftner N., Schelly R., Koblmüller S. Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Mol. Phylogenet. Evol. 2010, 57:266-284.
80. Sültmann H., Mayer W.E., Figueroa F., Tichy H., Klein J. Phylogenetic analysis of cichlid fishes using nuclear DNA markers. Mol. Biol. Evol. 1995, 12:1033-1047.
81. Swofford D.L., Waddell P.J., Huelsenbeck J.P., Foster P.G., Lewis P.O., Rogers J.S. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Syst. Biol. 2001, 50:525-539.
82. Takahashi T. Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes). Ichthyol. Res. 2003, 50:367-382.
83. Takahashi T., Koblmüller S. The adaptive radiation of cichlid fish in lake tanganyika: a morphological perspective. Int. J. Evol. Biol. 2011, 2011:1-14.
84. Takahashi K., Terai Y., Nishida M., Okada N. Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol. Biol. Evol. 2001, 18:2057-2066.
85. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
86. Teugels, G.G., Thys van den Audenaerde, D.F.E., 2003. Cichlidae. In: Paugy, D., Teugels, G.G., Leveque, C. (Eds.), The Fresh and Brackish Water Fishes of West Africa, vol. 2. Coll. Faune et Flore Tropicales 40. Institut de recherche de développement, Paris, France, Muséum national d'histoire naturelle, Paris, France and Musée royal de l'Afrique Central, Tervuren, Belgium, pp. 521-600.
87. Thorley J.L., Wilkinson M. Testing the phylogenetic stability of early tetrapods. J. Theor. Biol. 1999, 200:343-344.
88. Thys van den Audenaerde D.F.E. Revision systematique des especes congolaises du genre Tilapia (Pisces, Cichlidae). Ann. Musee Roy. Afr. Centr. Ser. 8 Sci. Zool. 1964, 124:1-155.
89. Thys van den Audenaerde, D.F.E., 1969. An annotated bibliography of Tilapia (Pisces, Cichlidae). Ann. Musee Roy. Afr. Centr. Ser. N-14, Doc. Zool., I-XL.
90. Tracer v.1.5, http://beast.bio.ed.ac.uk/tracer.
91. Trewavas E. I. On the cichlid fishes of the genus Pelmatochromis with proposal of a new genus for P. congicus; on the relationship between Pelmatochromis and Tilapia and the recognition of Sarotherodon as a distinct genus. Bull. Br. Mus. Nat. Hist. Zool. 1973, 25:1-26.
92. Trewavas E. Tilapiine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia 1983, British Museum (Natural History), London.
93. Turner G.F., Seehausen O., Knight M.E., Allender C.J., Robinson R.L. How many species of cichlid fishes are there in African lakes?. Mol. Ecol. 2001, 10:793-806.
94. Wickler W. Zur Klassifikation der Cichlidae, am Beispiel der Gattungen Tropheus, Petrochromis, Haplochromis und Hemihaplochromis n. gen. (Pisces, Perciformes). Senckenb. Biol. 1963, 44:83-96.
95. Witte, F., van Oijen M.J.P., 1990. Taxonomy, ecology and fishery of Lake Victoria haplochromine trophic groups. Zoologische Verhandelingen, National Natuurhistorisch Museum, Leiden 262, 15.