Studies of threespine stickleback developmental evolution: Progress and promise

Genetica

Volumn 129, Issue 1, 2007, Pages 105-126

  Cresko, William A ^a   McGuigan, Katrina L ^a,b   Phillips, Patrick C ^a   Postlethwait, John H ^a  

^a UNIVERSITY OF OREGON   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adaptive radiation; Development; Gasterosteus; Micro evo devo; Population divergence; Speciation; Stickleback

Indexed keywords

ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR EVOLUTION; PHENOTYPE; POPULATION GENETICS; PRENATAL DEVELOPMENT; REVIEW; SMEGMAMORPHA;

ANIMALS; EVOLUTION, MOLECULAR; GENETICS, POPULATION; MODELS, ANIMAL; MODELS, GENETIC; PHENOTYPE; SMEGMAMORPHA; VARIATION (GENETICS);

GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 33845638631     PISSN: 00166707     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10709-006-0036-z     Document Type: Review

References (227)

1. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321-326
2. Aguirre WE, Doherty PK, Bell MA (2004) Genetics of lateral plate and gillraker phenotypes in a rapidly evolving population of threespine stickleback. Behaviour 141:1465-1483
3. Ahn DG, Gibson. G, (1999a) Axial variation in the three-spine stickleback: genetic and environmental factors. Evol Dev 1:100-112
4. Ahn DG, Gibson G (1999b) Axial variation in the threespine stickleback: relationship to Hox gene expression. Dev Genes Evol 209:473-481
5. Ahn DG, Gibson G (1999c) Expression patterns of threespine stickleback Hox genes and insights into the evolution of the vertebrate body axis. Develop Genes Evol 209:482-494
6. Albertson RC, Streelman JT, Kocher TD (2003) Genetic basis of adaptive shape differences in the cichlid head. J Hered 94:291-301
7. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH (1998) Zebrafish hox clusters and vertebrate genome evolution. Science 282:1711-1714
8. Amores A, Suzuki T, Yan YL, Pomeroy J, Singer A, Amemiya C, Postlethwait JH (2004) Developmental roles of pufferfish Hox clusters and genome evolution in ray-fin fish. Gen Res 14:1-10
9. Andersson E, Borg B, Goos HJT (1992) Temperature, but not photoperiod, influences gonadotropin-releasing hormone binding in the pituitary of the three-spined stickleback, Gasterosteus aculeatus. Gen Comp Endocrinol 88:111-116
10. Arnold SJ, Pfrender M, Jones AG (2001) The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112/113: 112-123
11. Avise JC (1976) Genetics of plate morphology in an unusual population of threespine sticklebacks (Gasterosteus aculeatus). Genet Res 27:33-46
12. Banbura J (1994) A new model of lateral plate morph inheritance in the threespine stickleback, Gasterosteus aculeatus. Theor App Gen 88:871-876
13. Banbura J, Bakker TCM (1995) Lateral plate morph genetics revisited: evidence for a fourth morph in three-spined sticklebacks. Behaviour 132:15-16
14. Baguna J, Garcia-Fernandez J (2003) Evo-Devo: the long and winding road. Int J Dev Biol 47:705-713
15. Baker JA, Foster SA, Bell MA (1995) Armor morphology and reproductive output in threespine stickleback, Gasterosteus aculeatus. Environ Biol Fishes 44:1-3
16. Baker JA, Foster SA (2002) Phenotypic plasticity for life history traits in a stream population of the threespine stickleback, Gasterosteus aculeatus L. Ecol Fresh Fish 11:20-29
17. Baker JA, Cresko WA, Foster SA, Heins DC (2005) Life-history differentiation of benthic and limnetic ecotypes in a polytypic population of threespine stickleback (Gasterosteus aculeatus). Evol Ecol Res 7:121-131
18. Bakker TCM (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255-257
19. Bakker TCM, Mundwiler B (1999) Pectoral fin size in a fish species with paternal care: a condition-dependent sexual trait revealing infection status. Freshwater Biol 41:543-551
20. Baumgartner JV (1994) Phenotypic, genetic and environmental integration of morphology in a stream population of the threespine stickleback, Gasterosteus aculeatus. Can J Fish Aquat Sci 52:1307-1317
21. Barber I, Svensson PA (2003) Effects of experimental Schistocephalus solidus infections on growth, morphology and sexual development of female three-spined sticklebacks, Gasterosteus aculeatus. Parasitology 126:359-367
22. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc Royal Soc Lond B 268:71-76
23. Barber I, Arnott SA, Braithwaite VA, Andrew J, Mullen W, Huntingford FA (2000) Carotenoid-based sexual coloration and body condition in nesting male sticklebacks. J Fish Biol 57:777-790
24. Baumgartner JV, Bell MA (1984) Lateral plate morph variation in California populations of the threespine stickleback, Gasterosteus aculeatus. Evolution 38:665-674
25. Bell MA (1985) Developmental osteology of the pelvic complex of Gasterosteus aculeatus. Copeia 1985:789-792
26. Bell MA (1987) Interacting evolutionary constraints on pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae). Biol J Linn Soc 31:347-382
27. Bell MA (2001) Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica 112:445-461
28. Bell MA, Orti G (1994) Pelvic reduction in threespine stickleback from Cook Inlet lakes: geographical distribution and intrapopulation variation. Copeia 1994:314-325
29. Bell MA, Foster SA (1994) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, New York. 21 pp
30. Bell MA, Orti G, Walker JA, Koenings JP (1993) Evolution of pelvic reduction in threespine stickleback fish - a test of competing hypotheses. Evolution 47:906-914
31. Bell MA, Francis RC, Havens AC (1985) Pelvic reduction and its directional asymmetry in threespine sticklebacks from the Cook Inlet Region, Alaska. Copeia 2:437-444
32. Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814-824
33. Bergstrom CA, Reimchen TE (2000) Functional implications of fluctuating asymmetry among endemic populations of Gasterosteus aculeatus. Behaviour 137:1097-1112
34. Bergstrom CA, Reimchen TE (2002) Geographical variation in asymmetry in Gasterosteus aculeatus. Biol J Linn Soc 77:9-22
35. Bergstrom CA, Reimchen TE (2003) Asymmetry in structural defenses: insights into selective predation in the wild. Evolution 57:2128-2138
36. Bernatchez L, Chouinard A, Lu GQ (1999) Integrating molecular genetics and ecology in studies of adaptive radiation: whitefish, Coregonus sp., as a case study. Biol J Linn Soc 68:173-194
37. Blows MW (2004) Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am Nat 163:329-340
38. Bolker JA (2000) Modularity in development and why it matters to evo-devo. Am Zool 40:770-776
39. Bolnick DI (2004) Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 58:608-618
40. Borg B, Mayer I (1995) Androgens and behaviour in the three-spined stickleback. Behaviour 132:13-14
41. Borg B, Bornestaf C, Hellqvist A, Schmitz M, Mayer I (2004) Mechanisms in the photoperiodic control of reproduction in the stickleback. Behaviour 141:1521-1530
42. Borg B, Goos HJ, Terlou M (1982) LHRH-immunoreactive cells in the brain of the three-spined stickleback, Gasterosteus aculeatus L. (Gasterosteidae). Cell Tiss Res 226(3): 695-699
43. Borg B, Mayer I, Lambert J, Granneman J, Schulz R (1992) Metabolism of androstenedione and 11-ketotestosterone in the kidney of the three-spined stickleback, Gasterosteus aculeatus. Gen Comp Endocrinol 86:248-256
44. Borg B, Timmers RJ, Lambert JG (1987) Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. I. Distribution and effects of season and photoperiod. Exp Biol 47(2):22
45. Bornestaf C, Borg B (2000) Endogenous breeding cycles in male threespine sticklebacks, Gasterosteus aculeatus. Behaviour 137:921-932
46. Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944-948
47. Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384:236-242
48. Campbell D, Bernatchez L (2004) Genomic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol Biol Evol 21:945-956
49. Candolin U (1999) Male-male competition facilitates female choice in sticklebacks. Proc Roy Soc Lond B 266:785-789
50. Candolin U (2000) Changes in expression and honesty of sexual signaling over the reproductive lifetime of sticklebacks. Proc Roy Soc Lond B 267:2425-2430
51. Carroll SB (2001) Homeobox genes. Am Nat 158:21-21
52. Clauss MJ, Mitchell-Olds T (2003) Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history. Mol Ecol 12:1287-99
53. Cole NJ, Tanaka M, Prescott A, Tickle C (2003) Expression of limb initiation genes and clues to the morphological diversification of threespine stickleback. Curr Biol 13:R951-R952
54. Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD, Schluter D, Kingsley DM (2004) The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PloS Biol 2:635-641
55. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928-1933
56. Cresko WA, Baker JA (1996) Two morphotypes of lacustrine threespine stickleback, Gasterosteus aculeatus, in Benka Lake, Alaska. Environ Biol Fish 45:343-350
57. Cresko WA, Yan YL, Baltrus DA, Amores A, Singer A, Rodriguez-Mari A, Postlethwait JH (2003) Genome duplication, subfunction partitioning, and lineage divergence: Sox9 in stickleback and zebrafish. Develop Dyn 228(3):480-489
58. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell MA, Kimmel CB, Postlethwait JH (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan three-spine stickleback populations. Proc Natl Acad Sci USA 101:6050-6055
59. Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54:1725-1737
60. Davidson EH (2001) Genomic regulatory systems: development and evolution. Academic Press, San Diego
61. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, Yuh CH, Minokawa T, Amore G, Hinman V, Arenas-Mena C, Otim O, Brown CT, Livi CB, Lee PY, Revilla R, Rust AG, Pan ZJ, Schilstra MJ, Clarke PJC, Arnone MI, Rowen L, Cameron RA, McClay DR, Hood L, Bolouri H (2002) A genomic regulatory network for development. Science 295:1669-1678
62. Day T, Pritchard J, Schluter D (1994) Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks. Evolution 48:1723
63. Deagle BE, Reimchen TE, Levin DB (1996) Origins of endemic stickleback from the Queen Charlotte Islands: mitochondrial and morphological evidence. Can J Zool 74:1045-1056
64. Draper BW, Morcos PA, Kimmel CB (2001) Inhibition of zebrafish fgf8 pre-mRNA splicing with Morpholino oligos: a quantifiable method for gene knockdown. Genesis 30(3):154-156
65. Ekstreöm P, Nyberg L, van Veen T (1985) Ontogenetic development of serotoninergic neurons in the brain of a teleost, the three-spined stickleback. An immunohistochemical analysis. Brain Res 349(1-2):209-224
66. Ekstreöm P, Honkanen T, Borg B (1992) Development of tyrosine hydroxylase-, dopamine- and dopamine beta-hydroxylase-immunoreactive neurons in a teleost, the three-spined stickleback. J Chem Neuro 5(6):481-501
67. Ekstreöm P, Borg B, van Veen T (1983) Ontogenetic development of the pineal organ, parapineal organ, and retina of the three-spined stickleback, Gasterosteus aculeatus L. (Teleostei). Development of photoreceptors. Cell Tissue Res 233(3): 593-609
68. Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton
69. Etges WJ, Jackson LL (2001) Epicuticular hydrocarbon variation in Drosophila mojavensis cluster species. J Chem Ecol 27:2125-2149
70. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Essex, UK
71. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
72. Foote CJ, Brown GS, Hawryshyn CW (2004) Female colour and male choice in sockeye salmon: implications for the phenotypic convergence of anadromous and nonanadromous morphs. Anim Behav 67:69-83
73. Force A, Cresko WA, Pickett FB (2004) Informational accrestion, gene duplication and the mechanisms of genetic module parcellation. In: Schlossser G, Wagner G (eds) Modularity in development and evolution, Chicago
74. Force A, Cresko WA, Pickett FB, Proulx SR, Amemiya C, Lynch M (2005) The origin of gene subfunctions and modular gene regulation. Genetics 170:433-446
75. Foster SA (1988) Diversionary displays of paternal stickleback. Defenses against cannibalistic groups. Behav Ecol Sociobiol 22:335-340
76. Foster SA (1994a) Evolution of the reproductive behavior of the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford Science Publications, Oxford
77. Foster SA (1994b) Inference of evolutionary pattern: diversionary displays of three-spined sticklebacks. Behav Ecol 5:114-121
78. Foster SA, Baker JA (2004) Evolution in parallel: new insights from a classic system. Trends Ecol Evol 19:456-459
79. Foster SA, Scott RJ, Cresko WA (1998) Nested biological variation and speciation. Phil Roy Soc Lond B 353:207-218
80. Furutani-Seiki M, Wittbrodt J (2004) Medaka and Zebrafish, an evolutionary twin study. Mech Dev 121:629-637
81. Garcia-Dorado A, Marin JM (1998) Minimum distance estimation of mutational parameters for quantitative traits. Biometrics 54:1097-1114
82. Garenc C, Silversides F, Guderley H (1998) Burst swimming and its enzymatic correlates in 25 the threespine stickleback (Gasterosteus aculeatus): full-sib heritabilities. Can J Zool 76:9
83. Gibson G (2002) Microarrays in ecology and evolution: a preview. Mol Ecol 11:17-24
84. Gibson G, Wagner G (2000) Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22:372-380
85. Gibson G, Mackay TFC (2002) Enabling population and quantitative genomics. Gen Res 80:1-6
86. Gibson G, Dworkin IM (2004) Uncovering cryptic genetic variation. Nat Rev Genet 5:681-691
87. Gilbert SF (2003) The morphogenesis of evolutionary developmental biology. Int J Dev Biol 47:467-477
88. Griffiths R, Orr K, Adam A, Barber I (2000) DNA sex identification in the three-spined stickleback. J Fish Biol 57:4
89. Hagen DW (1973) Inheritance of numbers of lateral plates and gill rakers in Gasterosteus aculeatus. Heredity 30:303-312
90. Hagen DW, Moodie GEE (1979) Polymorphism for breeding colors in Gasterosteus aculeatus. I. Their genetics and geographic distribution. Evolution 33:641-648
91. Hagen DW, Gilbertson LG (1973a) Selective predation and the intensity of selection acting on the lateral plates of threespine sticklebacks. Heredity 30:273-287
92. Hagen DW, Gilbertson LG (1973b) The genetics of plate morphs in freshwater threespine sticklebacks. Heredity 31:75-84
93. Haglund TR, Buth DG, Blouw DM (1990) Allozyme variation and the recognition of the "white stickleback". Biochem Syst Ecol 18:7-8
94. Haglund TR, Buth DG, Lawson R (1992) Allozyme variation and phylogenetic relationships of Asian, North American, and European populations of the threespine stickleback, Gasterosteus aculeatus. Copeia 1992:432-433
95. Hall BK (2003) Evo-Devo: evolutionary developmental mechanisms. Int J Dev Biol 47:491-495
96. Hatfield T (1997) Genetic divergence in adaptive characters between sympatric species of stickleback. Am Nat 149:1009-1029
97. Heins DC, Baker JA (2003) Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite. J Parasit 89:1-6
98. Heins DC, Baker JA, Martin HC (2002) The "crowding effect" in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. J Parasit 88:302-307
99. Hellqvist A, Schmitz M, Lindberg C, Olsson PE, Borg B (2001) LH-beta and FSH-beta mRNA expression in nesting and post-breeding three-spined stickleback, Gasterosteus aculeatus, and effects of castration on expression of LH-beta, FSH-beta and spiggin mRNA. Fish Phys Biochem 25:311-317
100. Hendry AP, Taylor EB, McPhail JD (2002) Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the misty system. Evolution 56:1199-1216
101. Hendry AP, Wenburg JK, Bentzen P, Volk EC, Quinn TP (2000) Rapid evolution of re-productive isolation in the wild: evidence from introduced salmon. Science 290:516-518
102. Hermida M, Fernandez C, Amaro R, San Miguel E (2002) Heritability and "evolvability" of meristic characters in a natural population of Gasterosteus aculeatus. Can J Zool 80:532-541
103. Heuts MJ (1947) Experimental studies on adaptive evolution in Gasterosteus aculeatus L. Evolution 1:89-102
104. Higuchi M, Goto A (1996) Genetic evidence supporting the existence of two distinct species in the genus Gasterosteus around Japan. Environ Biol Fishes 47:1-16
105. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of pocket mice. Mol Ecol 12:1185-1194
106. Honkanen T, Ekstrom P (1992) Comparative study of the olfactory epithelium of the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius). Cell Tiss Res 269:267-273
107. Hosemann KE, Colosimo PE, Summers BR, Kingsley DM (2004) A simple and efficient microinjection protocol for making transgenic sticklebacks. Behaviour 141:1345-1355
108. Igarashi K (1964) Observations on the development of the scutes in the landlocked form of three-spined stickleback, Gasterosteus aculeatus. Bull Jap Soc Sci Fish 30:95-103
109. Igarashi K (1970) Formation of the scutes in the marine form of the three-spined stickleback, Gasterosteus aculeatus aculeatus (Linnaeus) from Nasu Area, tochigi-Ken. Annat Zool Jap 43:34-42
110. Ikeda K (1934) On the variation and inheritance of lateral shields in the three-spined stickleback. Jap J Genetics 9:104-106
111. Johnson NA, Porter AH (2001) Toward a new synthesis: population genetics and evolutionary developmental biology. Genetica 112-113:45-58
112. Jones AG, Arnold SJ, Bèurger R (2003) Stability of the G-matrix in a population experiencing pleiotropic mutation, stabilizing selection, and genetic drift. Evolution 57:1747-1760
113. Jones AG, Arnold SJ, Burger R (2004) Evolution and stability of the G-matrix on a landscape with a moving optimum. Evolution 58:1639-1654
114. Jonsson B, Skulason S (2000) Polymorphic segregation in Arctic charr Salvelinus alpinus (L.) from Vatnshlidarvatn, a shallow Icelandic lake. Biol J Linn Soc 69:55-74
115. Jowett T, Yan Y-L (1996) Double fluorescent in situ hybridization to zebrafish embryo. Trends Genet 12:387-389
116. Katsiadaki I, Scott AP, Hurst MR, Matthiessen P, Mayer I (2002) Detection of environmental androgens: a novel method based on enzyme-linked immunosorbent assay of spiggin, the stickleback (Gasterosteus aculeatus) glue protein. Env Tox Chem 21(9):1946-1954
117. Kimmel CB, Ullmann B, Walker C, Wilson C, Currey M, Phillips PC, Bell MA, Postlethwait JH, Cresko WA (2005) Evolution and development of facial bone morphology in threespine sticklebacks. Proc Natl Acad Sci USA 102:5791-5796
118. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253-310
119. Kingsley DM, Zhu BL, Osoegawa K, De Jong PJ, Schein J, Marra M, Peichel C, Amamiya C, Schluter D, Balabhadra S, Friedlander B, Cha YM, Dickson M, Grimwood J, Schmutz J, Talbot WS, Myers R (2004) New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour 141:1331-1344
120. Klepaker T (1993) Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can J Zool 71:1251-1258
121. Klepaker T (1995) Postglacial evolution in lateral plate morphs in Norwegian freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Can J Zool 73:898-906
122. Klepaker T (1996) Lateral plate polymorphism in marine and estuarine populations of the threespine stickleback (Gasterosteus aculeatus) along the coast of Norway. Copeia 1996(4):832-838
123. Kocher T (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288-298
124. Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution 33:402-416
125. Largiader CR, Fries V, Kobler B, Bakker TCM (1999) Isolation and characterization of microsatellite loci from the three-spined stickleback (Gasterosteus aculeatus L.). Mol Ecol 8:342-344
126. Larson G (1976) Social behaviour and feeding ability of two phenotypies of Gasterosteus aculeatus in realtion to their spatial and trophic segregation in a temperate lake. Can J Zool 54:107-121
127. Lavin PA, McPhail JD (1985) The evolution of freshwater diversity in the threespine stickleback (Gasterosteus aculeatus): site-specific differentiation of trophic morphology. Can J Zool 63:2632-2638
128. Lavin PA, McPhail JD (1986) Adaptive divergence of trophic phenotype among freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Can J Fish Aquat Sci 43:2455-2463
129. Lavin PA, McPhail JD (1987) Morphological divergence and the organization of trophic characters among lacustrine populations of the threespine stickleback (Gasterosteus aculeatus). Can J Fish Aquat Sci 44:1820-1829
130. Lenski RE, Ofria C, Pennock RT, Adami C (2003) The evolutionary origin of complex features. Nature 423:139-145
131. Lindsey CC (1962a) Experimental study of meristic variation in a population of threespine stickleback, Gasterosteus aculeatus. Can J Zool 40:271-312
132. Lindsey CC (1962b) Observation on meristic variation in nine-spine stickleback, Pungitius pungitius, reared at different temperatures. Can J Zool 40:1237-1247
133. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981-994
134. Lynch M, Walsh JB (1998) Genetics and analysis of quantitative traits. Sinauer Assocs., Inc., Sunderland, MA
135. Mackay TFC (2001) The genetic architecture of quantitative traits. Anu Rev Genet 35:303-339
136. Mayer I, Borg B, Pall M (2004) Hormonal control of male reproductive behaviour in fishes: a stickleback perspective. Behaviour 141:1499-1510
137. Mayer I, Bornestaf C, Wetterberg L, Borg B (1997) Melatonin does not prevent long photoperiod stimulation of secondary sexual characters in the male three-spined stickleback Gasterosteus aculeatus. Gen Comp End 108(3):386-394
138. McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology's role in speciation. Nature 429:294-298
139. McKinnon J, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. TREE 17:1-9
140. McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can J Zool 62:1402-1408
141. Mezey JG, Cheverud JM, Wagner GP (2000) Is the genotype-phenotype map modular?: A statistical approach using mouse quantitative trait loci data. Genetics 156:305-311
142. Munzig J (1959) Genetic von Gasterosteus aculeatus L. (Pisces). Untersuchungen im Elbegebiet. Int Revue ges Hydrobiol 44:317-382
143. Nachman MW, Hoekstra HE, D'Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci 100(9):5268-5273
144. Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209-218
145. Naruse K, Hori H, Shimizu N, Kohara Y, Takeda H (2004) Medaka genomics: a bridge between mutant phenotype and gene function. Mech Dev 121:619-628
146. Nijhout HF (2002) The nature of robustness in development. Bioessays 24:553-563
147. O'-Reilly P, Reimchen TE, Beech R, Strobeck C (1993) Mitochondrial DNA in Gasterosteus and Pleistocene glacial refugium on the Queen Charlotte Islands, British Columbia. Evolution 47:678-684
148. Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nat Genet 32:261-266
149. Olsson PE, Berg H, von Hofsten J, Lindberg C, Grahn B, Hellqvist A, Borg B, Thomas P (2003) Cloning and characterization of the three spined stickleback kidney androgen receptor suggests that 11-ketotestosterone regulation of spiggin is mediated through a dihydrotestosterone receptor. Biol Rep 68:364-365
150. Orti G, Bell MA, Reimchen TE, Meyer A (1994) Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent migrations. Evolution 48:608-622
151. Overli O, Pall M, Borg B, Jobling M, Winberg S (2001) Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proc Roy Soc Lond B 268:1411-1415
152. Palsson A, Gibson G (2004) Association between nucleotide variation in Egfr and wing shape in Drosophila melanogaster. Genetics 167:1187-1198
153. Peichel CL, Nereng KS, Ohgi KA, Cole BL, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414:901-905
154. Peichel CL, Ross JA, Matson CK, Dickson M, Grimwood J, Schmutz J, Myers RM, Mori S, Schluter D, Kingsley DM (2004) The master sex-determination locus in threespine stickleback is on a nascent Y chromosome. Curr Biol 14:1416-1424
155. Phillips PC (1999) From complex traits to complex alleles. Trends Genet 15:6-8
156. Phillips PC (2005) Testing hypotheses regarding the genetics of adaptation. Genetica 123:15-24
157. Phillips PC, McGuigan KL (2006) Evolution of genetic variance-covariance structure. In: Fox C, Wolf J (eds) Evolutionary genetics: concepts and case studies. Oxford University Press, Oxford, England. 310-325
158. Porter AH, Johnson NA (2002) Speciation despite gene flow when developmental pathways evolve. Evolution 56:2103-2111
159. Postlethwait JH, Amores A, Cresko WA, Yan Y (2004) Evolutionary and developmental consequences of teleost genome duplication. Trends Genet 20(10):481-490
160. Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan YL, Kelly PD, Chu F, Huang H, Hill-Force A, Talbot WS (2000) Zebrafish comparative genomics and the origins of vertebrate chromosomes. Gen Res 10:1890-1902
161. Postlethwait JH, Yan YL, Gates MA, Horne S, Amores A, Brownlie A, Donovan A, Egan ES, Force A, Gong Z, Goutel C, Fritz A, Kelsh R, Knapik E, Liao E, Paw B, Ransom D, Singer A, Thomson M, Abduljabbar TS, Yelick P, Beier D, Joly JS, Larhammar D, Talbot WS (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Gen 18:345-349
162. Price T, Qvarnstrom A, Irwin D (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270:1433-1440
163. Raff RA (2000) Evo-devo: the evolution of a new discipline. Nat Rev Genet 1:74-79
164. Reimchen TE (1980) Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can J Zool 37:931-946
165. Reimchen TE (1995) Predator-induced cyclical changes in lateral plate frequencies of Gasterosteus aculeatus. Behaviour 132:13-14
166. Reimchen TE (2000) Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: functional implications for the ancestral plate condition. Behaviour 137:1081-1096
167. Reimchen TE, Nosil P (2002) Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56(12):2472-2483
168. Reusch TB, Wegner KM, Kalbe M (2001) Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity. Mol Ecol 10(10):2435-2445
169. Raeymaekers JA, Maes GE, Audenaert E, Volckaert FA (2005) Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system. Mol Ecol 14:1001-1014
170. Rico C, Zadworny D, Kuhnlein U, Fitzgerald GJ (1993) Characterization of hypervariable microsatellite loci in the threespine stickleback Gasterosteus aculeatus. Mol Ecol 2:271-272
171. Robinson BW (2000) Trade offs in habitat-specific foraging efficiency and the nascent adaptive divergence of sticklebacks in lakes. Behaviour 137:865-888
172. Robinson BW, Wilson DS (1994) Character release and displacement in fishes: a neglected literature. Am Nat 144:596-627
173. Robinson BW, Wilson DS (1996) Genetic variation and phenotypic plasticity in a trophically polymorphic population of pumpkinseed sunfish (Lepomis gibbosus). Evol Ecol 10:631-652
174. Robinson BW, Parsons KJ (2002) Changing times, spaces and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can J Fish Aquat Sci 59:1819-1831
175. Rudel D, Sommer RJ (2003) The evolution of developmental mechanisms. Dev Biol 264:15-37
176. Rundle HD, Nagel L, Boughman JW, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306-308
177. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer, Sunderland, MA USA
178. Schliewen UK, Tautz D, Paabo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368:629-632
179. Schluter D (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology 74:699-709
180. Schluter D (1995) Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76:82-90
181. Schluter D (1996b) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774
182. Schluter D (1996a) Ecological causes of adaptive radiation. Am Nat 148:S40-S64
183. Schluter D (2000) The ecology of adaptive radiations. Oxford University Press, Oxford
184. Schluter D, Clifford EA, Nemethy M, McKinnon JS (2004) Parallel evolution and inheritance of quantitative traits. Am Nat 163:809-822
185. Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85-108
186. Scott RJ (2004) Assortative mating between adjacent populations of threespine stickleback (Gasterosteus aculeatus). Ecol Fresh Fish 13:1-7
187. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jonsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717-723
188. Steppan SJ, Phillips PC, Houle D (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol 17:320-327
189. Stern DL (2000) Evolutionary developmental biology and the problem of variation. Evolution 54:1079-1091
190. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671-688
191. Streelman JT, Albertson RC, Kocher TD (2003) Genome mapping of the orange blotch colour pattern in cichlid fishes. Mol Ecol 12:2465-2471
192. Swarup H (1958) Stages in the development of the stickleback Gasterosteus aculeatus (L.). J Embryol Exp Morphol 6:373-383
193. Tanaka M, Hale LA, Amores A, Yan YL, Cresko WA, Suzuki T, Postlethwait JH (2005) Developmental genetic basis for the evolution of pelvic fin loss in the pufferfish Takifugu rubripes. Develop Biol 281:227-239
194. Taylor EB (1998) Microsatellites isolated from the threespine stickleback Gasterosteus aculeatus. Mol Ecol 7:930-931
195. Taylor EB, McPhail JD (1999) Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): insights from mitochondrial DNA. Biol J Linn Soc 66:271-291
196. Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc Roy Soc Lond B 267:2375-2384
197. Taylor J., Braasch I, Frickey T, Meyer A, Van De Peer Y (2003) Genome duplication, a trait shared by 22,000 species of ray-finned fish. Genome Res 13:382-390
198. Thompson CE, Taylor EB, McPhail JD (1997) Parallel evolution of lake-stream pairs of threespine sticklebacks (Gasterosteus) inferred from mitochondrial DNA variation. Evolution 51:1955-1965
199. Vamosi SM, Schluter D (2004) Character shifts in the defensive armor of
200. Van de Peer Y, Taylor JS, Meyer A (2003) Are all fishes ancient polyploids? J Struct Funct Genomics 3:65-73
201. van Veen T, Ekstrom P, Nyberg L, Borg B, Vigh-Teichmann I, Vigh B (1984) Serotonin and opsin immunoreactivities in the developing pineal organ of the three-spined stickleback, Gasterosteus aculeatus L. Cell Riss Res 237(3):559-564
202. van Veen T, Ekstrom P, Borg B, Moller M (1980) The pineal complex of the three-spined stickleback, Gasterosteus aculeatus L.: a light-, electron microscopic and fluorescence histochemical investigation. Cell Riss Res 209:11-28
203. Via S, Conner J (1995) Evolution in heterogeneous environments: genetic variability within and across different grains in Tribolium castaneum. Heredity 74:80-90
204. Waddington CH (1942) The canalization of development and the inheritance of acquired characters. Nature 150:563-565
205. Waddington CH (1952) Selection of the genetic basis for an acquired character. Nature 169:278
206. Waddington CH (1953) Genetic assimilation of an acquired character. Evolution 7:118-126
207. Wagner GP (2000) What is the promise of developmental evolution? Part I: Why is developmental biology necessary to explain evolutionary innovations? J Exp Zool 288:95-98
208. Wagner GP (2001) What is the promise of developmental evolution? Part II: a causal explanation of evolutionary innovations may be impossible. J Exp Zool 291:305-309
209. Wagner GP (2003) Evolutionary genetics: the nature of hidden genetic variation unveiled. Curr Biol 13:R958-R960
210. Wagner GP, Altenberg L (1996) Complex adaptations and the evolution of evolvability. Evolution 50:967-976
211. Wagner GP, Booth G, Bagheri-Chaichian H (1997) A population genetic theory of canalization. Evolution 51:329-347
212. Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L (Gasterosteidae) body shape. Biol J Linn Soc 61:3-50
213. Walker JA, Bell MA (2000) Net evolutionary trajectories of body shape evolution within a microgeographic radiation of threespine sticklebacks (Gasterosteus aculeatus). J Zool 252:293-302
214. Watanabe K, Mori S, Nishida M (2003) Genetic relationships and origin of two geographic groups of the freshwater threespine stickleback, 'hariyo'. Zool Sci 20(2):265-274
215. Weinig C, Schmitt J (2004) Environmental effects on the expression of quantitative trait loci and implications for phenotypic evolution. BioScience 54:627-635
216. Weinig C, Stinchcombe JR, Schmitt J (2003a) Evolutionary genetics of resistance and tolerance to natural herbivory in Arabidopsis thaliana. Evolution 57(6):1270-1280
217. Weinig C, Stinchcombe JR, Schmitt J (2003b) QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments. Mol Ecol 12(5):1153-1163
218. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
219. Wilke CO (2003) Probability of fixation of an advantageous mutant in a viral quasispecies. Genetics 163:467-474
220. Withler RE, McPhal JD (1985) Genetic variability in freshwater and anadromous sticklebacks (Gasterosteus aculeatus) of southern British Columbia. Can J Zool 63:528-533
221. Withler RE, McPhail JD, Devlin RH (1986) Electrophoretic polymorphism and sexual dimorphism in the freshwater and anadromous threespine sticklebak (Gasterosteus aculeatus) of the Little Campbell River, British Columbia. Biochem Genet 24:701-713
222. Wittbrodt J, Meyer A, Schartl M (2002) Medaka - a model organism from the far East. Nat Rev Genet 3:53-64
223. Wootton RJ (1976) The biology of the sticklebacks. Academic Press, London
224. Wray GA (2003) Transcriptional regulation and the evolution of development. Int J Develop Biol 47:675-684
225. Wright HA, Wootton RJ, Barber I (2004) Interpopulation variation in early growth of threespine sticklebacks (Gasterosteus aculeatus) under laboratory conditions. Can J Fish Aquat Sci 61:1832-1838
226. Yamada M, Higuchi M, Goto A (2001) Extensive introgression of mitochondrial DNA found between two genetically divergent forms of threespine stickleback, Gasterosteus aculeatus, around Japan. Env Biol Fishes 61:16
227. Ziuganov VV (1983) Genetics of osteal plate polymorphism and microevolution of threespine stickleback (Gasterosteus aculeatus L.). Theor Appl Genet 65:239-246