Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish

Molecular Ecology

Volumn 18, Issue 20, 2009, Pages 4240-4255

  Nevado, B ^a,f   KoblmUller S ^b   Sturmbauer, C ^b   Snoeks, J ^c,d   Usano Alemany, J ^e   Verheyen, E ^a,f  

^a ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^b UNIVERSITY OF GRAZ   (Austria)

^c ROYAL MUSEUM FOR CENTRAL AFRICA   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e Centro de Investigación Agraria de Albaladejito Consejería de Agricultura de Castilla La Mancha   (Spain)

^f UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Hybridization; Introgression; Lake level fluctuations; Lamprologus callipterus; Neolamprologus fasciatus; Phylogeography

Indexed keywords

CICHLIDAE; LAMPROLOGUS CALLIPTERUS; NEOLAMPROLOGUS FASCIATUS;

EID: 70349859861     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04348.x     Document Type: Article

References (75)

1. Akaike J (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19, 716 723.
2. Baack EJ, Rieseberg LH (2007) A genomic view of introgression and hybrid speciation. Current Opinion in Genetics & Development, 17, 513 518.
3. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729 744.
4. Baric S, Salzburger W, Sturmbauer C (2003) Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. Journal of Molecular Evolution, 56, 54 68.
5. Barton NH (2001) The role of hybridization in evolution. Molecular Ecology, 10, 551 568.
6. Beltrán M, Jiggins CD, Bull V et al. (2002) Phylogenetic discordance at the species boundary: comparative gene genealogies among rapidly radiating Heliconius butterflies. Molecular Biology and Evolution, 19, 2176 2190.
7. Britton T, Oxelman B, Vinnersten A, Bremer K (2002) Phylogenetic dating with confidence intervals using mean path lengths. Molecular Phylogenetics and Evolution, 24, 58 65.
8. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Molecular Biology and Evolution, 25, 624 633.
9. Clement M, Posada D, Crandall KA (2000) tcs: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657 1659.
10. Cohen AS, Soreghan MJ, Scholz CA (1993) Estimating the age of formation of lakes: an example from Lake Tanganyika, East African rift system. Geology, 21, 511 514.
11. Cohen AS, Lezzar KE, Tiercelin JJ, Soreghan M (1997) New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin research, 9, 107 132.
12. Day JJ, Santini S, Garcia-Moreno J (2007) Phylogenetic relationships of the Lake Tanganyika cichlid tribe Lamprologini: the story from mitochondrial DNA. Molecular Phylogenetics and Evolution, 45, 629 642.
13. Delvaux D (1995) Age of Lake Malawi (Nyasa) and water level fluctuations. Musée Royal de l'Afrique Centrale (Tervuren, Belgium), Department of Geology and Minerology, Annual Report, 1995-1996, 99 108.
14. Donaldson KA, Wilson RR (1999) Amphi-Panamic geminates of Snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA control region of fishes. Molecular Phylogenetics and Evolution, 12, 208 213.
15. Dowling TE, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593 619.
16. Egger B, Koblmüller S, Sturmbauer C, Sefc KM (2007) Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus. BMC Evolutionary Biology, 7, 137.
17. Felsenstein J, Churchill GA (1996) A Hidden Markov Model approach to variation among sites in rate of evolution. Molecular Biology and Evolution, 13, 93 104.
18. Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLOb/b/-WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics, 12, 543 548.
19. Gasse F, Ledee V, Massault M, Fontes JC (1989) Water-level fluctuations of Lake Tanganyika in phase with oceanic changes during the last glaciation and deglaciation. Nature, 342, 57 59.
20. Genner MJ, Seehausen O, Lunt DH et al. (2007) Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution, 24, 1269 1282.
21. Grant PR, Grant BR (1994) Phenotypic and genetic effects of hybridization in Darwin's finches. Evolution, 48, 297 316.
22. Grant BR, Grant PR (2008) Fission and fusion of Darwin's finches populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 363, 2821 2829.
23. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754 755.
24. Kass RE, Raftery AE (1995) Bayes factors. Journal of the American Statistical Association, 90, 773 795.
25. Kim M, Cui M, Cubas P et al. (2008) Regulatory genes control a key morphological and ecological trait transferred between species. Science, 322, 1116 1119.
26. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111 120.
27. Koblmüller S, Duftner N, Sefc KM et al. (2007) Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika -the result of repeated introgressive hybridization. BMC Evolutionary Biology, 7, 7.
28. Koblmüller S, Sefc KM, Sturmbauer C (2008a) The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia, 615, 5 20.
29. Koblmüller S, Schliewen UK, Duftner N et al. (2008b) Age and spread of the haplochromine cichlid fishes in Africa. Molecular Phylogenetics and Evolution, 49, 153 169.
30. Koblmüller S, Nord M, Wayne RK, Leonard JA (2009a) Origin and status of the Great Lakes wolf. Molecular Ecology, 18, 2313 2326.
31. Koblmüller S, Duftner N, Sefc KM et al. (2009b) Phylogeographic structure and gene flow in the scale-eating cichlid Perissodus microlepis (Teleostei, Perciformes, Cichlidae) in southern Lake Tanganyika. Zoologica Scripta, 38, 257 268.
32. Kronforst MR, Young LG, Gilbert LE (2007) Reinforcement of mate preference among hybridizing Heliconius butterflies. Journal of Evolutionary Biology, 20, 278 285.
33. Kuwamura T (1997) Fish communities in Lake Tanganyika. In : The Evolution of Parental Care and Mating Systems among Tanganyikan cichlid (ed. Kawanabe H, Hori M, Nagoshi M pp. 57 86. Kyoto University Press, Kyoto.
34. Lezzar KE, Tiercelin JJ, Batist MDE et al. (1996) New seismic stratigraphy and Late Tertiary history of the North Tanganyika Basin, East African Rift system, deduced from multichannel and high-resolution reflection seismic data and piston core evidence. Basin Research, 8, 1 28.
35. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451 1452.
36. Mallet J, Beltrán M, Neukirchen W, Linares M (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evolutionary Biology, 7, 28.
37. McDonald DB, Parchman TL, Bower MR, Hubert WA, Rahel FJ (2008) An introduced and a native vertebrate hybridize to form a genetic bridge to a second native species. Proceedings of the National Academy of Sciences of the United States of America, 105, 10837 10842.
38. McGuire JA, Linkem CW, Koo MS et al. (2007) Mitochondrial introgression and incomplete lineage sorting through space and time: phylogenetics of crotaphytid lizards. Evolution, 61, 2879 2897.
39. Moore WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear gene trees. Evolution, 49, 718 726.
40. Newton MA, Raftery AE (1994) Approximate Bayesian inference by the weighted likelihood bootstrap (with discussion). Journal of the Royal Statistical Society Series B, 56, 3 48.
41. Nyingi D, Agnèse JJ (2007) Recent introgressive hybridization revealed by exclusive mtDNA transfer from Oreochromis leucostictus (Trewavas, 1933) to Oreochromis niloticus (Linnaeus, 1758) in Lake Baringo, Kenya. Journal of Fish Biology, 70 (suppl A 148 154.
42. Panchal M (2007) The automation of Nested Clade Phylogeographic Analysis. Bioinformatics, 23, 509 510.
43. Paradis E, Claude J, Strimmer K (2004) APE: analyses of Phylogenetics and Evolution in R language. Bioinformatics, 20, 289 290.
44. Pfennig KS (2003) A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: support for the reinforcement hypothesis. Evolution, 57, 2842 2851.
45. Plötner J, Uzzell T, Beerli P et al. (2008) Widespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs. Journal of Evolutionary Biology, 21, 668 681.
46. Poll M (1986) Classification des Cichlidae du lac Tanganika, Tribus, genres et espéces. Académie Royale de Belgique, Brussels.
47. Posada D, Crandall KA (1998) modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817 818.
48. Rüber L, Verheyen E, Meyer A (1999) Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proceedings of the National Academy of Sciences of the United States of America, 96, 10230 10235.
49. Rüber L, Meyer A, Sturmbauer C, Verheyen E (2001) Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Molecular Ecology, 10, 1207 1225.
50. Rutschmann F (2005) Bayesian Molecular Dating Using PAML/multidivtime. A Step-by-Step Manual. University of Zurich, Switzerland.
51. Salzburger W, Baric S, Sturmbauer C (2002) Speciation via introgressive hybridization in East African cichlids? Molecular Ecology, 11, 619 625.
52. Sato T, Gashagaza MM (1997) Shell-brooding cichlid fishes of Lake Tanganyika: their habitats and mating systems. In : Fish Communities in Lake Tanganyika (ed Kawanabe H, Hori M, Nagoshi M). pp. 219 240, Kyoto University Press, Kyoto.
53. Schelly R, Salzburger W, Koblmüller S, Duftner N, Sturmbauer C (2006) Phylogenetic relationships of the lamprologine cichlid genus Lepidiolamprologus (Teleostei: Perciformes) based on mitochondrial and nuclear sequences, suggesting introgressive hybridization. Molecular Phylogenetics and Evolution, 38, 426 438.
54. Schliewen UK, Klee B (2004) Reticulate sympatric speciation in Cameroonian crater lake cichlids. Frontiers in Zoology, 1, 5.
55. Scholz CA, King JW, Ellis GS et al. (2003) Palaeolimnology of Lake Tanganyika, East Africa, over the past 100 kyr. Journal of Palaeolimnology, 30, 139 150.
56. Schwenk K, Brede N, Streit B (2008) Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 363, 2805 2811.
57. Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology and Evolution, 19, 198 207.
58. Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology, 17, 30 44.
59. Shaw KL (2002) Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proceedings of the National Academy of Sciences of the United States of America, 99, 16122 16127.
60. Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16, 1114 1116.
61. Smith PF, Konings A, Kornfield I (2003) Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity. Molecular Ecology, 12, 2497 2504.
62. Stelkens RB, Pierotti MER, Joyce DA et al. (2008) Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 2861 2870.
63. Sturmbauer C, Baric S, Salzburger W, Rüber L, Verheyen E (2001) Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Molecular Biology and Evolution, 18, 144 154.
64. Sturmbauer C, Koblmüller S, Sefc KM, Duftner N (2005) Phylogeographic history of the genus Tropheus, a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika. Hydrobiologia, 542, 335 366. (Pubitemid 40778306)
65. Takahashi T (2003) Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes). Ichthyological Research, 50, 367 382.
66. Tamura K, Dudley J, Nei M, Kumar S (2007) mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596 1599.
67. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Molecular Ecology, 7, 381 397.
68. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673 4680.
69. Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Molecular Biology and Evolution, 15, 1647 1657.
70. Tiercelin J, Mondeguer A (1991) The geology of the Tanganyika through. In : Lake Tanganyika and Its Life (ed. Coulter WJ pp. 7 48. Oxford University Press, Oxford.
71. Turner GF, Seehausen O, Knight KE, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Molecular Ecology, 10, 793 806.
72. Van der Sluijs I, Van Dooren TJM, Hofker KD et al. (2008) Female mating preference functions predict sexual selection against hybrids between sibling species of cichlid fish. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 363, 2871 2877.
73. 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.
74. Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics, 146, 427 441.
75. Yang Z (2007) paml 4: Phylogenetic Analysis by Maximum Likelihood. Molecular Biology and Evolution, 24, 1586 1591.