Adaptive evolution of lateral plates in three-spined stickleback Gasterosteus aculeatus: A case study in functional analysis of natural variation

Journal of Fish Biology

Volumn 77, Issue 2, 2010, Pages 311-328

  Barrett, R D H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adaptation; Ectodysplasin; Evolution; Lateral plates; Natural selection; Three spined G. aculeatus

Indexed keywords

ANIMAL; EVOLUTION; GENETIC FITNESS; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HISTOLOGY; PHENOTYPE; REVIEW; SMEGMAMORPHA; ANATOMY AND HISTOLOGY; REPRODUCTIVE FITNESS;

ANIMALS; EVOLUTION; GENETIC FITNESS; GENETIC VARIATION; GENOTYPE; PHENOTYPE; SELECTION, GENETIC; SMEGMAMORPHA; BIOLOGICAL EVOLUTION;

GASTEROSTEUS ACULEATUS; PISCES;

EID: 77955020172     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2010.02640.x     Document Type: Review

References (90)

1. Abzhanov A, Extavour C G, Groover A, Hodges S A, Hoekstra H E, Kramer E M, Moneiro A. Are we there yet? Tracking the development of new model systems. Trends in Genetics 2008, 24:353-360.
2. Arnold S J. Morphology, performance and fitness. American Zoology 1983, 23:347-361.
3. Avise J C. Genetics of plate morphology in an unusual population of threespine sticklebacks (Gasterosteus aculeatus). Genetics Research 1976, 27:33-46.
4. Baack E J, Sapir Y, Chapman M A, Burke J M, Rieseberg L H. Selection on domestication traits and quantitative trait loci in crop-wild sunflower hybrids. Molecular Ecology 2008, 17:666-677.
5. Baird N A, Etter P D, Atwood T S, Currey M C, Shiver A L, Lewis Z A, Selker E U, Cresko W A, Johnson E A. Rapid SNP discovery and genetic mapping using sequenced RAD markers. Public Library of Science One 2008, 3:e3376.
6. Banbura J, Bakker T C M. Lateral plate morph genetics revisited: evidence for a fourth morph in three-spined sticklebacks. Behaviour 1995, 132:1152-1171.
7. Barrett R D H, Rogers S M, Schluter D. Natural selection on a major armor gene in threespine stickleback. Science 2008, 322:255-257.
8. Barrett R D H, Rogers S M, Schluter D. Environment specific pleiotropy facilitates divergence at the ectodysplasin locus in threespine stickleback. Evolution 2009a, 63:2831-2837.
9. Barrett R D H, Vines T H, Bystriansky J S, Schulte P M. Should I stay or should I go? The ectodysplasin locus is associated with behavioural differences in threespine stickleback. Biology Letters 2009b, 5:788-791.
10. Bell M A. Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterostedae). Biological Journal of the Linnean Society 1987, 31:347-382.
11. Bell M A. Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica 2001, 112:445-461.
12. Bell M A, Foster S A. The Evolutionary Biology of the Threespine Stickleback 1994, Oxford, Oxford University Press
13. Bell M A, Haglund T R. Selective predation of threespine sticklebacks (Gasterosteus aculeatus) by garter snakes. Evolution 1978, 32:304-319.
14. Bell M A, Orti G, Walker J A, Koenings J P. Evolution of pelvic reduction in threespine stickleback fish - a test of competing hypotheses. Evolution 1993, 47:906-914.
15. Bell M A, Aguirre W E, Buck N J. Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 2004, 58:814-824.
16. Bergstrom C A. Fast-start swimming performance and reduction in lateral plate number in threespine stickleback. Canadian Journal of Zoology-Revue Canadienne De Zoologie 2002, 80:207-213.
17. Bernatchez L, Renaut S, Whiteley A R, Derome N, Jeukens J, Landry L, Lu G, Nolte A W, Østbye K, Rogers S M, St-Cyr J. On the origin of species: insights from the ecological genomics of lake whitefish. Philsophical Transactions of the Royal Society B 2010, 365:1783-1800. doi: 10.1098/rstb.2009.0274
18. Bertin L. Recherches bionomique, biométriques et systé-matiques sur les epinoches (Gasterosteidae). Annals of the Institute of Oceanography Monaco 1925, 2:1-204.
19. Bourgeois J F, Blouw D M, Koenings J P, Bell M A. Multivariate-analysis of geographic covariance between phenotypes and environments in the threespine stickleback, Gasterosteus aculeatus, from the Cook Inlet Area, Alaska. Canadian Journal of Zoology 1994, 72:1497-1509.
20. Bradshaw H D, Schemske D W. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 2003, 426:176-178.
21. Cano J M, Matsuba C, Makinen H, Merila J. The utility of QTL-linked markers to detect selective sweeps in natural populations - a case study of the EDA gene and a linked marker in threespine stickleback. Molecular Ecology 2006, 15:4613-4621.
22. Colosimo P F, Peichel C L, Nereng K, Blackman B K, Shapiro M D, Schluter D, Kingsley D M. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. Public Library of Science Biology 2004, 2:635-641.
23. Colosimo P F, Hosemann K E, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers R M, Schluter D, Kingsley D M. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 2005, 307:1928-1933.
24. Cossins A R, Crawford D L. Fish as models for environmental genomics. Nature Reviews Genetics 2005, 6:324-333.
25. Cresko W A. Armor development and fitness. Science 2008, 322:204-206.
26. Cresko W A, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell M A, Kimmel C B, Postlethwait J H. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:6050-6055.
27. Cresko W A, McGuigan K L, Phillips P C, Postlethwait J H. Studies of threespine stickleback developmental evolution: progress and promise. Genetica 2007, 129:105-126.
28. Curry R A, Currie S L, Arndt S K, Bielak A T. Winter survival of age-0 smallmouth bass, Micropterus dolomieu, in north eastern lakes. Environmental Biology of Fishes 2005, 72:111-122.
29. Dalziel A, Rogers S M, Schulte P M. Linking genotypes to phenotypes and fitness: how mechanistic biology can inform molecular ecology. Molecular Ecology 2009, 18:4997-5017.
30. Endler J A. Natural Selection in the Wild 1986, Princeton, NJ, Princeton University Press
31. Evans D H, Piermarini P M, Choe K P. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 2005, 85:97-177.
32. Fangue N A, Hofmeister M, Schulte P M. Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus. Journal of Experimental Biology 2006, 209:2859-2872.
33. Foster S A, Garcia V B, Town M Y. Cannibalism as the cause of an ontogenetic niche shift in habitat use by fry of the threespine stickleback. Oecologia 1988, 74:577-585.
34. Giles N. The possible role of environmental calcium levels during the evolution of phenotypic diversity in the outer Hebridean populations of the three-spined stickleback, Gasterosteus aculeatus. Journal of Zoology London 1983, 199:535-544.
35. Hagen D W, Gilbertson L G. Selective predation and intensity of selection acting upon lateral plates of threespine sticklebacks. Heredity 1973, 30:273-287.
36. Hagen D W, McPhail J D. The species problem within Gasterosteus aculeatus on the Pacific coast of North America. Journal of the Fisheries Research Board Canada 1970, 27:147-155.
37. Harris M P, Rohner N, Schwarz H, Perathoner S, Konstantinidis P, Nusslein-Volhard C. Zebrafish eda and edar mutants reveal conserved and ancestral roles of ectodysplasin signaling in vertebrates. Public Library of Science Genetics 2008, 4:e1000206.
38. Heuts M J. Experimental studies on adaptive evolution in Gasterosteus aculeatus L. Evolution 1947, 1:89-102.
39. Hoekstra H E, Hirschmann R J, Bundey R A, Insel P A, Crossland J P. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 2006, 313:101-104.
40. Hoffmann A A, Willi Y. Detecting genetic responses to environmental change. Nature Reviews Genetics 2008, 9:421-432.
41. Kim Y, Stephan W. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 2002, 160:765-777.
42. Kingsley D M, Peichel C L. The molecular genetics of evolutionary change in sticklebacks. Biology of the Three-Spined Stickleback 2007, 41-82. Östlund-Nilsson S, Mayer IHuntingford F A. eds), pp., Boca Raton, FL, CRC Press
43. Kingsley D M, Baoli Z, Osoegawa K, De Jong P J, Schein J, Marra M, Peichel C, Amemiya C, Schluter D, Balabhadra S, Friedlander B, Yee Man C, Dickson M, Grimwood J, Schmutz J, Talbot W S, Myers R. New genomic tools for molecular studies of evolutionary change in threespine sticklebacks. Behaviour 2004, 141:1331-1344.
44. Kingsolver J G, Huey R B. The evolution of morphology, performance, and fitness. Integrative and Comparative Biology 2003, 43:361-366.
45. Kitano J, Bolnick D I, Beauchamp D A, Mazur M M, Mori S, Nakano T, Peichel C L. Reverse evolution of armor plates in the threespine stickleback. Current Biology 2008, 18:769-774.
46. Klepaker T. Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Canadian Journal of Zoology 1993, 71:1251-1258.
47. Knecht A K, Hosemann K E, Kingsley D M. Constraints on utilization of the EDA-signaling pathway in threespine stickleback evolution. Evolution & Development 2007, 9:141-154.
48. Kondo S, Kuwahara Y, Kondo M, Naruse K, Mitani H, Wakamatsu Y, Ozato K, Asakawa S, Shimizu N, Shima A. The medaka rs-3 locus required for scale development encodes ectodysplasin-A receptor. Current Biology 2001, 11:1202-1206.
49. Kristjansson B K. Rapid morphological changes in threespine stickleback, Gasterosteus aculeatus, in freshwater. Environmental Biology of Fishes 2005, 74:357-363.
50. Kristjansson B K, Skulason S, Noakes D L G. Rapid divergence in a recently isolated population of threespine stickleback (Gasterosteus aculeatus L.). Evolutionary Ecology Research 2002, 4:659-672.
51. Lexer C, Welch M E, Durphy J L, Rieseberg L H. Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology 2003, 12:1225-1235.
52. Makinen H S, Cano J M, Merila J. Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Molecular Ecology 2008, 17:3565-3582.
53. Marchinko K. Predation's role in repeated phenotypic and genetic divergence of armor in threespine stickleback. Evolution 2009, 63:127-138.
54. Marchinko K B, Schluter D. Parallel evolution by correlated response: lateral plate reduction in threespine stickleback. Evolution 2007, 61:1084-1090.
55. Marshall W S. Transport by fish gills: retrospective review and prospective synthesis. Journal of Experimental Zoology 2002, 293:264-283.
56. McKinnon J S, Rundle H D. Speciation in nature: the threespine stickleback model systems. Trends in Ecology & Evolution 2002, 17:480-488.
57. McPhail J D. Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. The Evolutionary Biology of the Threespine Stickleback 1994, 399-437. Bell M AFoster S A. eds), pp., London, Oxford University Press
58. Mikkola M L, Thesleff I. Ectodysplasin signaling in development. Cytokine & Growth Factor Reviews 2003, 14:211-224.
59. Miller M R, Dunham J P, Amores A. Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Research 2007, 17:240-248.
60. Moodie G E E, McPhail J D, Hagen D W. Experimental demonstration of selective predation on Gasterosteus aculeatus. Behaviour 1973, 47:95-105.
61. Muniz I P. Freshwater acidification: its effects on species and communities of freshwater microbes, plants, and animals. Proceedings of the Royal Society of Edinburgh B 1991, 97:227-254.
62. Nielsen R. Statistical tests of selective neutrality in the age of genomics. Heredity 2001, 86:641-647.
63. Oleksiak M F, Roach J L, Crawford D L. Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nature Genetics 2005, 37:67-72.
64. Peichel C L. Fishing for the secrets of vertebrate evolution in threespine sticklebacks. Developmental Dynamics 2005, 234:815-823.
65. Peichel C L, Nereng K S, Ohgi K A, Cole B L E, Colosimo P F, Buerkle C A, Schluter D, Kingsley D M. The genetic architecture of divergence between threespine stickleback species. Nature 2001, 414:901-905.
66. Peterson R D, Martin-Robichaud D J. Growth and major inorganic cation budgets of Atlantic salmon alevins at three ambient acidities. Transactions of the American Fisheries Society 1986, 115:220-226.
67. Raeymaekers J A M, Maes G E, Audenaert E, Volckaert F A M. Detecting Holocene divergence in the anadromous-freshwater three-spined stickleback (Gasterosteus aculeatus) system. Molecular Ecology 2005, 14:1001-1014.
68. Raeymaekers J A M, Van Houdt J K J, Larmuseau M H D, Geldof S, Volckaert F A M. Divergent selection as revealed by P-ST and QTL-based F-ST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Molecular Ecology 2007, 16:891-905.
69. Rafinski J, Bangbura J, Przybylski M. Genetic differentiation of freshwater and marine sticklebacks, (Gasterosteus aculeatus) of Eastern Europe. Journal of Zoological Systematics & Evolutionary Research 1989, 27:33-43.
70. Reimchen T E. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus- an adaptation to predators. Canadian Journal of Zoology-Revue Canadienne de Zoologie 1980, 58:1232-1244.
71. Reimchen T E. Structural relationships between spines and lateral plates in threespine stickleback (Gasterosteus aculeatus). Evolution 1983, 37:931-946.
72. Reimchen T E. Trout foraging failures and the evolution of body size in stickleback. Copeia 1991, 1991:1098-1104.
73. Reimchen T E. Injuries on stickleback from attacks by a toothed predator (Oncorhynchus) and implications for the evolution of lateral plates. Evolution 1992, 46:1224-1230.
74. Reimchen T E. Predators and morphological evolution in threespine stickleback. The Evolutionary Biology of the Threespine Stickleback 1994, 240-273. Bell M AFoster S A. eds), pp., Oxford, Oxford University Press
75. Reimchen T E. Predator handling failures of lateral plate morphs in Gasterosteus aculeatus: functional implications for the ancestral plate condition. Behaviour 2000, 137:1081-1096.
76. Reusch T B H, Wegner K M, Kalbe M. Rapid genetic divergence in postglacial populations of threespine stickleback (Gasterosteus aculeatus): the role of habitat type, drainage and geographical proximity. Molecular Ecology 2001, 10:2435-2445.
77. Rogers S M, Bernatchez L. 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 2007, 24:1423-1438.
78. Santiago E, Caballero A. Variation after a selective sweep in a subdivided population. Genetics 2005, 169:475-483.
79. Schluter D. Adaptive radiation in sticklebacks - trade-offs in feeding performance and growth. Ecology 1995, 76:82-90.
80. Schluter D, Nagel L M. Parallel speciation by natural-selection. American Naturalist 1995, 146:292-301.
81. Schluter D, Clifford E A, Nemethy M, McKinnon J S. Parallel evolution and inheritance of quantitative traits. American Naturalist 2004, 163:809-822.
82. Schultz E T, Clifton L M, Warner R R. Energetic constraints and size-based tactics: the adaptive significance of breeding-schedule variation in a marine fish (Embiotocidae: Micrometrus minimus). American Naturalist 1991, 138:1408-1430.
83. Scott W B, Crossman E J. Freshwater Fishes of Canada 1973, Ottawa, Fisheries Board of Canada
84. Simpson G G. The Major Features of Evolution 1953, New York, NY, Columbia University Press
85. Slatkin M, Wiehe T. Genetic hitch-hiking in a subdivided population. Genetical Research 1998, 71:155-160.
86. Taylor E B, McPhail J D. Prolonged and burst swimming in anadromous and freshwater threespine stickleback, Gasterosteus aculeatus. Canadian Journal of Zoology 1986, 64:416-420.
87. Taylor E B, McPhail J D. Evolutionary history of an adaptive radiation in species pairs of threespine sticklebacks (Gasterosteus): insights from mitochondrial DNA. Biological Journal of the Linnean Society 1999, 66:271-291.
88. Vamosi S M. Predation sharpens the adaptive peaks: survival trade-offs in sympatric sticklebacks. Annales Zoologici Fennici 2002, 39:237-248.
89. Waples R S, Naish K A. Genetic and evolutionary considerations in fishery management: research needs for the future. The Future of Fisheries Science in North America 2008, 427-451. Beamish R, Rothschild B. eds), pp., New York, NY, Springer
90. Wegner K M, Kalbe M, Milinski M, Reusch T B H. Mortality selection during the 2003 European heat wave in three-spined sticklebacks: effects of parasites and MHC genotype. BMC Evolutionary Biology 2008, 8:124.