Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids

Molecular Ecology

Volumn 19, Issue 5, 2010, Pages 940-951

  Mims, Meryl C ^a,b   Hulsey, C Darrin ^c   Fitzpatrick, Benjamin M ^c   Streelman, J Tod ^b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Evolutionary radiation; Hybridization; Mitochondrial introgression; Reproductive isolation; Single nucleotide polymorphism; Sympatry

Indexed keywords

CICHLIDAE; LABEOTROPHEUS FUELLEBORNI; METRIACLIMA ZEBRA;

MITOCHONDRIAL DNA;

AFRICA; ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CELL NUCLEUS; CICHLID; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENE FLOW; GENETICS; GEOGRAPHY; HAPLOTYPE; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENCE;

AFRICA; ANIMALS; BAYES THEOREM; CELL NUCLEUS; CICHLIDS; CLUSTER ANALYSIS; DNA, MITOCHONDRIAL; GENE FLOW; GENETICS, POPULATION; GEOGRAPHY; HAPLOTYPES; MODELS, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 77953637839     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04529.x     Document Type: Article

References (64)

1. Albertson RC, Kocher TD (2005) Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution, 59, 686-690.
2. Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences of the United States of America, 96, 5107-5110.
3. Albertson RC, Streelman JT, Kocher TD (2003) Genetic basis of adaptive shape differences in the cichlid head. Journal of Heredity, 94, 291-301.
4. Albertson RC, Streelman JT, Kocher TD, Yelick PC (2005) Integration and evolution of the cichlid mandible: the molecular basis of alternative feeding strategies. Proceedings of the National Academy of Sciences of the United States of America, 102, 16287-16292.
5. Arnegard ME, Markert JA, Danley PD, Stauffer JR, Ambali AJ, Kocher TD (1999) Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proceedings of the Royal Society of London Series B Biological Sciences, 226, 119-130.
6. Avise JC (1994) Molecular Markers, Natural History and Evolution. Chapman & Hall, New York, NY.
7. Bachtrog D, Thornton K, Clark A, Andolfatto P (2006) Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution, 60, 292-302.
8. Barrett RD, Schluter D (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38-44.
9. Beaumont MA (2005) Adaptation and speciation: what can F)st tell us? Trends in Ecology & Evolution, 20, 435-440.
10. Bossu CM, Near TJ (2009) Gene trees reveal repeated instances of mitochondrial introgression in Orangethroat darters (Percidae: Etheostoma). Systematic Biology, 58, 114-129.
11. Campbell D, Bernatchez L (2004) Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Molecular Biology & Evolution, 21, 945-956.
12. Chan KMA, Levin SA (2005) Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution, 59, 720-729.
13. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1660.
14. Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution, 54, 7125-1737.
15. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology, 10, 1075-1086.
16. Dowling T, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics, 28, 593-619.
17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
18. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47-50.
19. 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.
20. Fraser GJ, Hulsey CD, Bloomquist R, Uyesugi K, Manley NR, Streelman JT (2009) An ancient gene network is co-opted for teeth on old and new jaws. PLoS Biology, 7, e1000031.
21. Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics, 180, 977-993.
22. Gerber AS, Tibbets CA, Dowling TE (2001) The role of introgressive hybridization in the evolution of the Gila robusta complex (Teliostei: Cyprinidae). Evolution, 55, 2028-2039.
23. Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR, Turner GF (2007) Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution, 24, 1269-1282.
24. Genner MJ, Turner GF (2005) The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish and Fisheries, 6, 1-34.
25. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006) Homoploid hybrid speciation in an extreme habitat. Science, 314, 1923-1925.
26. Gow JL, Peichel CL, Taylor EB (2006) Contrasting hybridization rates between sympatric three-spined sticklebacks highlights the fragility of reproductive barriers between evolutionarily young species. Molecular Ecology, 15, 739-752.
27. Grant PR, Grant BR, Petren K (2005) Hybridization in the recent past. American Naturalist, 166, 56-67.
28. Hert E (1992) Homing and home-site fidelity in rock-dwelling cichlids of Lake Malawi, Africa. Environmental Biology of Fishes, 33, 229-237.
29. Hulsey CD, Garcia de Leon FJ, Rodiles-Hernandez R (2006) Micro- and macroevolutionary decoupling of cichlid jaws: a test of Liem's Key Innovation Hypothesis. Evolution, 60, 2096-2109.
30. Hulsey CD, Mims MC, Streelman JT (2007) Do constructional constraints influence cichlid craniofacial diversification? Proceedings of the Royal Society of London Series B Biological Sciences, 274, 1867-1875.
31. Kidd MR, Kidd CE, Kocher TD (2006) Axes of differentiation in the bower-building cichlids of Lake Malawi. Molecular Ecology, 15, 459-478.
32. Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF (1995) Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Molecular Phylogenetics and Evolution, 4, 420-432.
33. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics, 5, 288-298.
34. Kornfield I, Smith PF (2000) African cichlid fishes: Model systems for evolutionary biology. Annual Review of Ecology and Systematics, 31, 163-196.
35. Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to a new environment. Evolution, 20, 315-336.
36. Loh YHE, Katz LS, Mims MC, Kocher TD, Yi SV, Streelman JT (2008) Comparative analysis reveals signatures of differentiation amid genomic polymorphism in Lake Malawi cichlids. Genome Biology, 9, R113.
37. Maddison DR, Maddison WP (2000) MacClade 4.0. Sinauer, Sunderland, MA.
38. McElroy DM, Kornfield I (1993) Novel jaw morphology in hybrids between Pseudotropheus zebra and Labeotropheus feulleborni (Teleostei, Cichlidae) from Lake Malawi, Africa. Copeia, 1993, 933-945.
39. Moran P, Kornfield I (1993) Retention of an ancestral polymorphism in the mbuna species flock (Teleostei, Cichlidae) of Lake Malawi. Molecular Biology and Evolution, 10, 1015-1029.
40. Munthali SM, Ribbink AJ (1998) Condition and fecundity of translocated rock-dwelling cichlid fish in Lake Malawi. Journal of Zoology (London), 244, 347-355.
41. Nolte AW, Freyhof J, Stemshorn KC, Tautz D (2005) An invasive lineage of sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat adaptations has originated from hybridization between old phylogeographic groups. Proceedings of the Royal Society of London Series B Biological Sciences, 272, 2379-2387.
42. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375-402.
43. Owen RB, Crossley R, Johnson TC, Tweddle D, Kornfield I, Davison S, Eccles DH, Engstrom D (1990) Major low levels of Lake Malawi Africa and their implications for speciation rates in cichlid fishes. Proceedings of the Royal Society of London Series B Biological Sciences, 240, 519-553.
44. Parnell NF, Hulsey CD, Streelman JT (2008) Hybridization produces novelty when the mapping of form to function is many to one. BMC Evolutionary Biology, 8, 122.
45. Powell JR (1983) Interspecific cytoplasmic gene flow in the absence of nuclear gene flow-evidence from Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 80, 492-495.
46. Panganiban G, Rubenstein JLR (2002) Developmental functions of the Distal)less? Dlx homeobox genes. Development, 129, 4371-4386.
47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of Population Structure Using Multilocus Genotype Data. Genetics, 155, 945-959.
48. Reinthal PN (1990) The feeding habits of a group of herbivourous rock-dwelling cichlid fishes cichlidae perciformes from Lake Malawi Africa. Environmental Biology of Fishes, 27, 215-233.
49. Ribbink AJ, Marsh BA, Marsh AC, Ribbink AC, Sharp BJ (1983) A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi Africa. South African Journal of Zoology, 188, 149-310.
50. Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiation of cichlid fishes. Molecular Ecology, 18, 169-185.
51. Schluter D, Conte GL (2009) Genetics and ecological speciation. Proceedings of the National Academy of Sciences of the United States of America, 106(Suppl 1), 9955-9962.
52. Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198-207.
53. Shaw PW, Turner GF, Idid MR, Robinson RL, Carvalho GR (2000) Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proceedings of the Royal Society Biological Sciences Series B, 267, 2273-2280.
54. 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.
55. Stauffer Jr JR, Bowers NJ, Kocher TD, McKaye KR (1996) Evidence of hybridization between Cynotilapia afra and Pseudotropheus zebra (Teleostei: Cichlidae) following an intralacustrine translocation in Lake Malawi. Copeia, 1996, 203-208.
56. Stelkens R, Seehausen O (2009) Genetic distance between species predicts novel trait expression in their hybrids. Evolution, 63, 884-897.
57. Streelman JT, Albertson RC, Kocher TD (2007a) Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology, 52, 525-538.
58. Streelman JT, Peichel CL, Parichy DM (2007b) Developmental genetics of adaptation in fishes: the case for novelty. Annual Review of Ecology, Evolution and Systematics, 38, 655-681.
59. Streelman JT, Gmyrek SL, Kidd MR, Kidd C, Robinson RL, Hert E, Ambali AJ, Kocher TD (2004) Hybridization and contemporary evolution in an introduced cichlid fish from Lake Malawi National Park. Molecular Ecology, 13, 2471-2479.
60. Thompson JD, Plewniak F, Poch O (1999) A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Research, 27, 2682-2690.
61. Via S (2009) Natural selection in action during speciation. Proceedings of the National Academy of Sciences of the United States of America, 106(Suppl 1), 9939-9946.
62. Via S, West J (2008) The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Molecular Ecology, 17, 4334-4345.
63. Won YJ, Sivasundar A, Wang Y, Hey J (2005) On the origin of Lake Malawi cichlid species: A population genetic analysis of divergence. Proceedings of the National Academy of Sciences of the United States of America, 102, 6581-6586.
64. Won YJ, Wang Y, Sivasundar A, Raincrow J, Hey J (2006) Nuclear gene variation and molecular dating of the cichlid species flock of Lake Malawi. Molecular Biology and Evolution, 23, 828-837.