Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species

Molecular Ecology

Volumn 15, Issue 3, 2006, Pages 739-752

  Gow, Jennifer L ^a   Peichel, Catherine L ^b   Taylor, Eric B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Ecological speciation; Gasterosteus aculeatus; Gene flow; Introgression; Microsatellites

Indexed keywords

FRESH WATER; MICROSATELLITE DNA;

ANIMAL; ARTICLE; COMPARATIVE STUDY; DNA SEQUENCE; GENE FLOW; GENETICS; HYBRIDIZATION; MOLECULAR EVOLUTION; PHYSIOLOGY; REPRODUCTION; SMEGMAMORPHA;

ANIMALS; EVOLUTION, MOLECULAR; FRESH WATER; GENE FLOW; HYBRIDIZATION, GENETIC; MICROSATELLITE REPEATS; REPRODUCTION; SEQUENCE ANALYSIS, DNA; SMEGMAMORPHA;

GASTEROSTEUS ACULEATUS; PAXTON;

EID: 33644772078     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2006.02825.x     Document Type: Article

References (78)

1. Anderson EC Thompson EA 2002 A model-based method for identifying species hybrids using multilocus genetic data Genetics 160 1217 1229
2. Arnold ML 1994 Natural hybridization and Louisiana Irises Biosciences 44 141 147
3. Arnold ML Hodges SA 1995 Are natural hybrids fit or unfit relative to their parents? Trends in Ecology & Evolution 10 67 71
4. Barton NH Hewitt GM 1985 Analysis of hybrid zones Annual Review of Ecology and Systematics 16 113 148
5. Beerli P Felsenstein J 1999 Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach Genetics 152 763 773
6. TMpour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II Montpellier, France
7. Bell MA Aguirre WE Buck NJ 2004 Twelve years of contemporary armor evolution in a threespine stickleback population Evolution 58 814 824
8. Bell MA Foster SA 1994 The Evolutionary Biology of the Threespine Stickleback Oxford University Press Oxford, UK
9. Bentzen P McPhail JD 1984 Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair Canadian Journal of Zoology 62 2280 2286
10. Bentzen P Ridgway MS McPhail JD 1984 Ecology and evolution of sympatric sticklebacks (Gasterosteus): spatial segregation and seasonal habitat shifts in the Enos Lake species pair Canadian Journal of Zoology 62 2436 2439
11. Bettles CM Docker MF Dufour B Heath DD 2005 Hybridization dynamics between sympatric species of trout: loss of reproductive isolation Journal of Evolutionary Biology 18 1220 1233
12. Boecklen WJ Howard DJ 1997 Genetic analysis of hybrid zones: numbers of markers and power of resolution Ecology 78 2611 2616
13. Boughman JW 2001 Divergent sexual selection enhances reproductive isolation in sticklebacks Nature 411 944 948
14. Colosimo PF Hosemann KE Balabhadra S et al. 2005 Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles Science 307 1928 1933
15. Colosimo PF Peichel CL Nereng K et al. 2004 The genetic architecture of parallel armor plate reduction in threespine sticklebacks PLoS Biology 2 635 641
16. Cornuet JM Piry S Luikart G Estoup A Solignac M 1999 New methods employing multilocus genotypes to select or exclude populations as origins of individuals Genetics 153 1989 2000
17. COSEWIC 2004 Canadian Species at Risk Committee on the Status of Endangered Wildlife in Canada. Available from COSEWIC Secretariat, Canadian Wildlife Service Ottawa, Ontario, Canada
18. Coyne JA Orr HA 2004 Speciation Sinauer Associates Sunderland, Massachusetts
19. Cresko WA Amores A Wilson C et al. 2004 Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations Proceedings of the National Academy of Sciences, USA 101 6050 6055
20. Day T Pritchard J Schluter D 1994 Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks Evolution 48 1723 1734
21. Feldman MS Kumm J Pritchards J 1999 Mutation and migration in models of microsatellite evolution In Microsatellites: Evolution and Applications (eds Goldstein DB Schlötterer C pp 98 115 Oxford University Press Oxford, UK
22. Goudet J 1995 fstat (Version 1.2): a computer program to calculate F-statistics Journal of Heredity 86 485 486
23. Goudet J 2001 ) fstat, A program to estimate and test gene diversities and fixation indices (Version 2.9.3). Available from. Updated from Goudet (1995)
24. Hatfield T 1997 Genetic divergence in adaptive characters between sympatric species of stickleback American Naturalist 149 1009 1029
25. Hatfield T 2001 Status of the stickleback species pair, Gasterosteus spp., in Hadley Lake, Lasqueti Island, British Columbia Canadian Field Naturalist 115 579 583
26. Hatfield T Schluter D 1999 Ecological speciation in sticklebacks: environment dependent hybrid fitness Evolution 53 866 873
27. Hendry AP Taylor EB 2004 How much of the variation in adaptive divergence can be explained by gene flow? An evaluation using lake-stream stickleback pairs Evolution 58 2319 2331
28. Kingsley DM Zhu BL Osoegawa K et al. 2004 New genomic tools for molecular studies of evolutionary change in threespine sticklebacks Behaviour 141 1331 1334
29. Kraak SBM Mundwiler B Hart PJB 2001 Increased number of hybrids between benthic and limnetic three-spined sticklebacks in Enos Lake, Canada: the collapse of a species pair? Journal of Fish Biology 58 1458 1464
30. Larson GL 1976 Social behaviour and feeding ability of two phenotypes of Gasterosteus aculeatus in relation to their spatial and trophic segregation in a temperate lake Canadian Journal of Zoology 54 107 121
31. Lavin PA McPhail JD 1985 The evolution of freshwater diversity in the threespine stickleback, Gasterosteus aculeatus: site-specific differentiation of trophic morphology Canadian Journal of Zoology 63 2632 2638
32. Maynard Smith J Haigh J 1974 The hitch-hiking effect of a favourable gene Genetical Research 23 23 35
33. McKinnon JS Mori S Blackman BK et al. 2004 Evidence for ecology's role in speciation Nature 429 294 298
34. McKinnon JS Rundle HD 2002 Speciation in nature: the threespine stickleback model systems Trends in Ecology & Evolution 17 480 488
35. McPhail JD 1984 Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia Canadian Journal of Zoology 62 1402 1408
36. McPhail JD 1992 Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species pair in Paxton Lake, Texada Island British Columbia Canadian Journal of Zoology 70 361 369
37. McPhail JD 1993 Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin and evolution of the sympatric pairs Canadian Journal of Zoology 71 515 523
38. McPhail JD 1994 Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia In The Evolutionary Biology of the Threespine Stickleback (eds Bell MA Foster SA pp 399 437 Oxford University Press Oxford, UK
39. Nagel L Schluter D 1998 Body size, natural selection, and speciation in sticklebacks Evolution 52 209 218
40. Nielsen EE Hansen MM Bach LA 2001 Looking for a needle in a haystack: discovery of indigenous Atlantic salmon (Salmo salar L.) in stocked populations Conservation Genetics 2 219 232
41. Ostberg CO Slatton SL Rodriguez RJ 2004 Spatial partitioning and asymmetric hybridization among sympatric coastal steelhead trout (Oncorhynchus mykiss irideus), coastal cutthroat trout (O. clarki clarki) and interspecific hybrids Molecular Ecology 13 2773 2788
42. Paetkau D Slade R Burden M Estoup A 2004 Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power Molecular Ecology 13 55 65
43. Peichel CL Nereng KS Ohgi KA et al. 2001 The genetic architecture of divergence between threespine stickleback species Nature 414 901 905
44. Piry S Alapetite A Cornuet J-M et al. 2004 geneclass 2: a software for genetic assignment and first-generation migrant detection Journal of Heredity 95 536 539
45. Rannala B Mountain JL 1997 Detecting immigration by using multilocus genotypes Proceedings of the National Academy of Sciences, USA 94 9197 9201
46. Raymond M Rousset F 1995 genepop (version 1.2): population genetics software for exact tests and ecumenicism Journal of Heredity 86 248 249
47. Raymond M Rousset F 2001 ) genepop (version 3.3). Available from. Updated from Raymound & Rousset (1995)
48. Redenbach Z Taylor EB 2003 Evidence for bimodal hybrid zones between two species of char (Salvelinus) in northwestern North America Journal of Evolutionary Biology 16 1135 1148
49. Reed KM Sites JW 1995 Female fecundity in a hybrid zone between two chromosome races of the Sceloporus grammicus complex (Sauria, phrynosomatidae) Evolution 49 61 69
50. Rice WR 1989 Analyzing tables of statistical tests Evolution 43 223 225
51. Rico C Zadworny D Kuhnlein U Fitzgerald GJ 1993 Characterization of hypervariable microsatellite loci in the threespine stickleback Gasterosteus aculeatus Molecular Ecology 2 271 272
52. Ridgway MS McPhail JD 1984 Ecology and evolution of sympatric sticklebacks (Gasterosteus): mate choice and reproductive isolation in the Enos Lake species pair Canadian Journal of Zoology 62 1813 1818
53. Rubridge EM Taylor EB 2004 Hybrid zone structure and the potential role of selection in hybridizing populations of native westslope cutthroat trout (Oncorhynchus clarki lewisi) and introduced rainbow trout (O. mykiss) Molecular Ecology 13 3735 3749
54. Rundle HD 2002 A test of ecologically dependent postmating isolation between sympatric sticklebacks Evolution 56 322 329
55. Rundle HD Nosil P 2005 Ecological speciation Ecology Letters 8 336 352
56. Rundle HD Schluter D 1998 Reinforcement of stickleback mate preferences: sympatry breeds contempt Evolution 52 200 208
57. Rundle HD Vamosi SM Schluter D 2003 Experimental evidence of predation's effect on divergent selection during character displacement in sticklebacks Proceedings of the National Academy of Sciences, USA 100 14943 14948
58. Sanderson SL Cech JJ Patterson MR 1991 Fluid dynamics in suspension-feeding blackfish Science 252 1346 1348
59. Schlötterer C 2003 Hitchhiking mapping - functional genomics from the population genetics perspective Trends in Genetics 19 32 38
60. Schluter D 1993 Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency Ecology 74 699 709
61. Schluter D 1994 Experimental evidence that competition promotes divergence in adaptive radiation Science 266 798 800
62. Schluter D 1995 Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth Ecology 76 82 90
63. Schluter D 2003 Frequency dependent natural selection during character displacement in sticklebacks Evolution 57 1142 1150
64. Schluter D Clifford EA Nemethy M McKinnon JS 2004 Parallel evolution and inheritance of quantitative traits American Naturalist 163 809 822
65. Schluter D McPhail JD 1992 Ecological character displacement and speciation in sticklebacks American Naturalist 140 85 108
66. Schluter D Nagel LM 1995 Parallel speciation by natural selection The American Naturalist 146 292 301
67. Seehausen O van Alphen JJM Witte F 1997 Cichlid fish diversity threatened by eutrophication that curbs sexual selection Science 277 1808 1811
68. Shapiro MD Marks ME Peichel CL et al. 2004 Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks Nature 428 717 723
69. Shimoda N Knapik EW Ziniti J et al. 1999 Zebrafish genetic map with 2000 microsatellite markers Genomics 58 219 232
70. Taylor EB 1998 Microsatellites isolated from the threespine stickleback Gasterosteus aculeatus Molecular Ecology 7 930 931
71. Taylor EB Boughman JW Groenenboom M et al. in press Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair Molecular Ecology (doi: 10.1111/j.1365-294X.2005.02794.x)
72. Taylor EB McPhail JD 1999 Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): Insights from mitochondrial DNA Biological Journal of the Linnean Society 66 271 291
73. Taylor EB McPhail JD 2000 Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus Proceedings of the Royal Society of LondonSeries B, Biological Sciences 267 2375 2384
74. Vamosi SM Schluter D 1999 Sexual selection against hybrids between sympatric sticklebacks: evidence from a field experiment Evolution 53 874 880
75. Vamosi SM Schluter D 2004 Character shifts in the defensive armor of sympatric sticklebacks Evolution 58 376 385
76. Weir BS Cockerham CC 1984 Estimating F-statistics for the analysis of population structure Evolution 38 1358 1370
77. ST≠ 1/(4Nm+ 1) Heredity 82 17 125
78. Wright S 1931 Evolution in Mendelian populations Genetics 16 97 159