AFLP genome scans suggest divergent selection on colour patterning in allopatric colour morphs of a cichlid fish

Molecular Ecology

Volumn 21, Issue 14, 2012, Pages 3531-3544

  Mattersdorfer, Karin ^a   Koblmüller, Stephan ^a   Sefc, Kristina M ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

colouration; differentiation; diversification; drift; Lake Tanganyika; population subdivision; Tropheus

Indexed keywords

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ARTICLE; CICHLID; DNA SEQUENCE; GENE LINKAGE DISEQUILIBRIUM; GENETIC DRIFT; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; PHENOTYPE; PIGMENTATION; POPULATION GENETICS;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; CICHLIDS; GENETIC DRIFT; GENETICS, POPULATION; LINKAGE DISEQUILIBRIUM; PHENOTYPE; PIGMENTATION; POLYMORPHISM, GENETIC; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

CICHLIDAE; TROPHEUS; TROPHEUS MOORII;

EID: 84863716835     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05634.x     Document Type: Article

References (84)

1. Andrés J, Sánchez-Guillén RA, Cordero-Rivera A, (2000) Molecular evidence for selection on female color polymorphism in the damselfly Ischnura graellsii. Evolution, 54, 2156-2161.
2. Andrés J, Sánchez-Guillén RA, Cordero-Rivera A, (2002) Evolution of female colour polymorphism in damselflies: testing the hypotheses. Animal Behaviour, 63, 677-685.
3. Antao T, Beaumont MA, (2011) Mcheza: a workbench to detect selection using dominant markers. Bioinformatics, 27, 1717-1718.
4. Arnegard ME, Markert JA, Danley PD, Stauffer JRJ, 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 London Series B, 266, 119-130.
5. Barrett RDH, Hoekstra HE, (2011) Molecular spandrels: tests of adaptation at the genetic level. Nature Reviews Genetics, 12, 767-780.
6. Barrett RDH, Schluter D, (2007) Adaptation from standing genetic variation. Trends in Ecology and Evolution, 23, 38-44.
7. Barson NJ, Knight ME, Turner GF, (2007) The genetic architecture of male colour differences between a sympatric Lake Malawi cichlid species pair. Journal of Evolutionary Biology, 20, 45-53.
8. Beaumont MA, (2005) Adaptation and speciation: what can FST tell us? Trends in Ecology and Evolution, 20, 435-440.
9. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
10. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B, 57, 289-300.
11. Bierne N, (2010) The distinctive footprints of local hitchhiking in a varied environment and global hitchhiking in a subdivided population. Evolution, 64, 3254-3272.
12. Bierne N, Welch J, Loire E, Bonhomme F, David P, (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044-2072.
13. Bonin A, Taberlet P, Miaud C, Pompanon F, (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the Common frog (Rana temporaria). Molecular Biology and Evolution, 23, 773-783.
14. Brakefield PM, (1990) Genetic drift and patterns of diversity among colour-polymorphic populations of the homopteran Philaenus spumarius in an island archipelago. Biological Journal of the Linnean Society, 39, 219-237.
15. Bulmer MG, (1971) The effect of selection on genetic variability. The American Naturalist, 105, 201-211.
16. Bush SL, Schul J, (2010) Evolution of novel signal traits in the absence of female preferences in Neoconocephalus katydids (Orhtoptera, Tettigoniidae). PLoS One, 5, e12457.
17. Cohen AS, Stone JR, Beuning KRM, et al. (2007) Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proceedings of the National Academy of Sciences of the USA, 104, 16422-16427.
18. Croucher PJP, Oxford GS, Lam A, Gillespie RG, (2011) Stabilizing selection maintains exuberant colour polymorphism in the spider Theridion califormicum (Araneae, Theridiidae). Molecular Ecology, 20, 206-218.
19. Dasmahapatra KK, Blum MJ, Aiello A, et al. (2002) Inferences from a rapidly moving hybrid zone. Evolution, 56, 741-753.
20. Dijkstra PD, Groothuis TGG, (2011) Male-male competition as a force in evolutionary diversification: evidence in haplochromine cichlid fish. International Journal of Evolutionary Biology, 68925, 4.
21. Egan SP, Nosil P, Funk DJ, (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution, 62, 1162-1181.
22. 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.
23. Egger B, Mattersdorfer K, Sefc KM, (2010) Variable discrimination and asymmetric preferences in laboratory tests of reproductive isolation between cichlid colour morphs. Journal of Evolutionary Biology, 23, 433-439.
24. Egger B, Sefc KM, Makasa L, Sturmbauer C, Salzburger W, (2012) Introgressive hybridisation between colour-morphs in a population of cichlid fishes twelve years after human-induced secondary admixis. Journal of Heredity, doi: 10.1093/jhered/ess013.
25. Endler JA, (1992) Signals, signal conditions, and the direction of evolution. The American Naturalist, 139, S125-S153.
26. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierachically structured population. Heredity, 103, 285-298.
27. Faure MF, David P, Bonhomme F, Bierne N, (2008) Genetic hitchhiking in a subdivided population of Mytulis edulis. BMC Evolutionary Biology, 8, 164.
28. 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.
29. Gillespie RG, Oxford GS, (1998) Selection on the color polymorphism in Hawaiian happy-face spiders: evidence from genetic structure and temporal fluctuations. Evolution, 52, 775-783.
30. Gray SM, McKinnon JS, (2007) Linking color polymorphism maintenance and speciation. Trends in Ecology and Evolution, 22, 71-79.
31. Grether GF, Hudon J, Endler JA, (2001) Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proceedings of the Royal Society of London Series B, 268, 1245-1253.
32. Gunter HM, Clabaut C, Salzburger W, Meyer A, (2011) Identification and characterization of gene expression involved in the coloration of cichlid fish using microarray and qRT-PCR approaches. Journal of Molecular Evolution, 72, 127-137.
33. Hill WG, (1974) Estimation of linkage disequilibrium in randomly mating populations. Heredity, 33, 229-239.
34. Hoekstra HE, (2006) Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity, 97, 222-234.
35. Hofer T, Ray N, Wegmann D, Excoffier L, (2009) Large allele frequency differences between human continental groups are more likely to have occurred by drift during range expansions than by selection. Annals of Human Genetics, 73, 95-108.
36. Hoffman EA, Schueler FW, Jones AG, Blouin MS, (2006) An analysis of selection on a colour polymorphism in the northern leopard frog. Molecular Ecology, 15, 2627-2641.
37. Hofreiter M, Schöneberg T, (2010) The genetic and evolutionary basis of colour variation in vertebrates. Cellular and Molecular Life Sciences, 67, 2591-2603.
38. Holt BG, Côté IM, Emerson BC, (2011) Searching for speciation genes: molecular evidence for selection associated with colour morphotypes in the Caribbean reef fish genus Hypoplectra. PLoS One, 6, e20394.
39. King RB, Lawson R, (1995) Color-pattern variation in Lake Erie water snakes: the role of gene flow. Evolution, 49, 885-896.
40. Klopfstein S, Currat M, Excoffier L, (2006) The fate of mutations surfing on the wave of a range expansion. Molecular Biology and Evolution, 23, 482-490.
41. Koblmüller S, Salzburger W, Obermüller B, Eigner E, Sturmbauer C, Sefc KM, (2011) Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika. Molecular Ecology, 20, 2272-2290.
42. Lande R, (1980) Genetic variation and phenotypic evolution during allopatric speciation. The American Naturalist, 116, 463-479.
43. Lande R, (1981) Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Science USA, 78, 3721-3725.
44. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P, (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics, 4, 981-994.
45. Maan ME, van der Spoel M, Quesada Jimenez P, van Alphen JJM, Seehausen O, (2006) Fitness correlates of male coloration in a Lake Victoria cichlid fish. Behavioral Ecology, 17, 691-699.
46. Maderbacher M, Bauer C, Herler J, Postl L, Makasa L, Sturmbauer C, (2008) Assessment of traditional versus geometric morphometrics for discriminating populations of the Tropheus moorii species complex (Teleostei: Cichlidae), a Lake Tanganyika model for alloapatric speciation. Journal of Zoological Systematics and Evolutionary Research, 46, 153-161.
47. Magalhaes IS, Seehausen O, (2010) Genetics of male nuptial colour divergence between sympatric sister species of a Lake Victoria cichlid fish. Journal of Evolutionary Biology, 23, 914-924.
48. Mäkinen HS, Cano JM, Merilä J, (2008) Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Molecular Ecology, 17, 3565-3582.
49. Markert JA, Arnegard ME, Danley PD, Kocher TD, (1999) Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Molecular Ecology, 8, 1013-1026.
50. Matsuno T, (2001) Aquatic animal carotenoids. Fisheries Science, 67, 771-783.
51. McGlue MM, Lezzar KE, Cohen AS, et al. (2008) Seismic records of late Pleistocene aridity in Lake Tanganyika, tropical East Africa. Journal of Paleolimnology, 40, 635-653.
52. Midamegbe A, Vitalis R, Malausa T, Delava E, Cros-Arteil S, Streiff R, (2011) Scanning the European corn borer (Ostrinia spp.) genome for adaptive divergence between host-affiliated sibling species. Molecular Ecology, 20, 1414-1430.
53. Murray MC, Hare MP, (2006) A genomic scan for divergent selection in a secondary contact zone between Atlantic and Gulf of Mexico oysters, Crassostrea virginica. Molecular Ecology, 15, 4229-4242.
54. Oetjen K, Reusch TBH, (2007) Genome scans detect consistent divergent selection among subtidal vs. intertidal populations of the marine angiosperm Zostera marina. Molecular Ecology, 16, 5156-5167.
55. Parichy DM, (2006) Evolution of danio pigment pattern development. Heredity, 97, 200-210.
56. Pauers MJ, (2011) One fish, two fish, red fish, blue fish: geography, ecology, sympatry and male coloration in the Lake Malawi cichlid genus Labeotropheus (Perciformes: Cichlidae). International Journal of Evolutionary Biology, 57546, 9.
57. Pérez-Figueroa A, García-Pereira MJ, Saura M, Rolán-Alvarez E, Caballero A, (2010) Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology, 23, 2267-2276.
58. Postl L, Herler J, Bauer C, Maderbacher M, Makasa L, Sturmbauer C, (2008) Geometric morphometrics applied to viscerocranial bones in three populations of the Lake Tanganyika cichlid fish Tropheus moorii. Journal of Zoological Systematics and Evolutionary Research, 46, 240-248.
59. Pritchard JK, Di Rienzo A, (2010) Adaptation-not by sweeps alone. Nature Reviews Genetics, 11, 665-667.
60. Prunier J, Laroche J, Beaulieu J, Bousquet J, (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Molecular Ecology, 20, 1702-1716.
61. Rempeters G, Henze M, Anders F, (1981) Carotenoids and pteridines in the skin of interspecific hybrids of Xiphophorus. Comparative Biochemistry and Physiology, 69B, 91-98.
62. Robertson JM, Zamudio KR, (2009) Genetic diversification, vicariance, and selection in a polytypic frog. Journal of Heredity, 100, 715-731.
63. Rogers SM, Bernatchez L, (2005) Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Molecular Ecology, 14, 351-361.
64. Rogers SM, Bernatchez L, (2007) The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Molecular Biology and Evolution, 24, 1423-1438.
65. Saccheri IJ, Nichols RA, Brakefield PM, (2006) Morphological differentiation following experimental bottlenecks in the butterfly Bicyclus anynana (Nymphalidae). Biological Journal of the Linnean Society, 89, 107-115.
66. Salzburger W, Niederstätter H, Brandstätter A, et al. (2006) Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proceedings of the Royal Society of London Series B, 273, 257-266.
67. Santiago E, Caballero A, (2005) Variation after a selective sweep in a subdivided population. Genetics, 169, 475-483.
68. Schlötterer C, (2002) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics, 160, 753-763.
69. Scholz CA, King JW, Ellis GS, Swart PK, Stager JC, Colman SM, (2003) Paleolimnology of Lake Tanganyika, East Africa, over the past 100 k yr. Journal of Paleolimnology, 30, 139-150.
70. Schwartz AK, Hendry AP, (2007) A test fort the parallel coevolution of male colour and female preference in Trinidadian guppies (Poecilia reticulata). Evolutionary Ecology Research, 9, 71-90.
71. Sefc KM, Baric S, Salzburger W, Sturmbauer C, (2007) Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. Journal of Molecular Evolution, 64, 33-49.
72. Stinchcombe JR, Hoekstra HE, (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158-170.
73. Storz JF, (2005) Using genome scans of DNA polymorphisms to infer adaptive population divergence. Molecular Ecology, 14, 671-688.
74. Sturmbauer C, Dallinger R, (1995) Diurnal variation of spacing and foraging behaviour in Tropheus moorii (Cichlidae) in Lake Tanganyika, Eastern Africa. Netherlands Journal of Zoology, 45, 386-401.
75. Sturmbauer C, Koblmüller S, Sefc KM, Duftner N, (2005) Phlogeographic history of the genus Tropheus, a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika. Hydrobiologia, 542, 335-366.
76. Tazzyman SJ, Iwasa Y, (2010) Sexual selection can increase the effect of random genetic drift-a quantitative genetic model of polymorphism in Oophaga pumilio, the strawberry poison frog. Evolution, 64, 1719-1728.
77. Teshima KM, Coop G, Przeworski M, (2006) How reliable are empirical genomic scans for selective sweeps? Genome Research, 16, 702-712.
78. Uyeda JC, Arnold SJ, Hohenlohe PA, Mead LS, (2009) Drift promotes speciation by sexual selection. Evolution, 63, 583-594.
79. Vekemans X, (2002) AFLP-SURV. Version 1.0. Distributed by the author, Laboratoire de Génétique et Ecologie Végétal, Université Libre de Bruxelles, Belgium.
80. Vitalis R, Dawson K, Boursot P, (2001) Interpretation of variation across marker loci as evidence of selection. Genetics, 158, 1811-1823.
81. Whitlock R, Hipperson H, Mannarelli M, Butlin RK, Burke T, (2008) An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Molecular Ecology Resources, 8, 725-735.
82. Wiener P, Edriss MA, Williams JL, et al. (2011) Information content in genome-wide scans: concordance between patterns of genetic differentiation and linkage mapping associations. BMC Genomics, 12, 65.
83. Wood HM, Grahame JW, Humphray S, Rogers J, Butling RK, (2008) Sequence differentiation in regions identified by a genome scan for local adaptation. Molecular Ecology, 17, 3123-3135.
84. Zhivotovsky LA, (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Molecular Ecology, 8, 907-913.