Genetic architecture of skeletal evolution in european lake and stream stickleback

Evolution

Volumn 68, Issue 6, 2014, Pages 1792-1805

  Berner, Daniel ^a   Moser, Dario ^a   Roesti, Marius ^a   Buescher, Heinz ^a   Salzburger, Walter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Effect size; Gasterosteus aculeatus; Lateral plate; QTL mapping; RAD sequencing; Vertebral number

Indexed keywords

ADAPTIVE RADIATION; BONE; DIVERGENCE; EVOLUTIONARY BIOLOGY; FRESHWATER ENVIRONMENT; FUNCTIONAL ROLE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC STRUCTURE; GENOMICS; PHENOTYPE; POLYMORPHISM; SKELETON; TELEOST;

EUROPE;

GASTEROSTEUS ACULEATUS;

FISH PROTEIN;

ANATOMY AND HISTOLOGY; ANIMAL; BONE; FEMALE; GENE FREQUENCY; GENETICS; LAKE; MALE; MOLECULAR EVOLUTION; QUANTITATIVE TRAIT LOCUS; RIVER; SINGLE NUCLEOTIDE POLYMORPHISM; SMEGMAMORPHA; SPECIES DIFFERENTIATION;

ANIMALS; BONE AND BONES; EVOLUTION, MOLECULAR; FEMALE; FISH PROTEINS; GENE FREQUENCY; GENETIC SPECIATION; LAKES; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RIVERS; SMEGMAMORPHA;

EID: 84901693332     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12390     Document Type: Article

References (131)

1. Aguirre, W. E. 2009. Microgeographical diversification of threespine stickleback: body shape-habitat correlations in a small, ecologically diverse Alaskan drainage. Biol. J. Linn. Soc. 98:139-151.
2. Aguirre, W. E., and O. Akinpelu. 2010. Sexual dimorphism of head morphology in threespine stickleback (Gasterosteus aculeatus). J. Fish Biol. 77:802-821.
3. Akey, J. M., G. Zhang, K. Zhang, L. Jin, and M. D. Shriver. 2002. Interrogating a high-density SNP map for signatures of natural selection. Genome Res. 12:1805-1814.
4. Albert, A. Y. K., S. Sawaya, T. H. Vines, A. K. Knecht, C. T. Miller, B. R. Summers, S. Balabhadra, D. M. Kingsley, and D. Schluter. 2008. The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution 62:76-85.
5. Alho, J. S., T. Leinonen, and J. Merilä. 2011. Inheritance of vertebral number in the three-spined stickleback (Gasterosteus aculeatus). PLoS One 6:e19579.
6. Arendt, J., and D. Reznick. 2008. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23:26-32.
7. Baird, N. A., P. D. Etter, T. S. Atwood, M. C. Currey, A. L. Shiver, Z. A. Lewis, E. U. Selker, W. A. Cresko, and E. A. Johnson. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376.
8. Barrett, R. D. H., S. M. Rogers, and D. Schluter. 2009. Environment specific pleiotropy facilitates divergence at the ectodysplasin locus in threespine stickleback. Evolution 63:2831-2837.
9. Barton, N. H., and P. D. Keightley. 2002. Understanding quantitative genetic variation. Nat. Rev. Genet. 3:11-21.
10. Bayes, M., A. J. Hartung, S. Ezer, J. Pispa, I. Thesleff, A. K. Srivastava, and J. Kere. 1998. The anhidrotic ectodermal dysplasia gene (EDA) undergoes alternative splicing and encodes ectodysplasin-A with deletion mutations in collagenous repeats. Hum. Mol. Genet. 7:1661-1669.
11. Beavis, W. D. 1994. The power and deceit of QTL experiments: lessons from comparative QTL studies. Pp. 250-266 in Proceedings of the 49th annual corn and sorghum industry research conference. American Seed Trade Association, Washington, DC.
12. Bell, M. A., and S. A. Foster. 1994. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford, U.K.
13. Bentzen, P., and J. D. McPhail. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Can. J. Zool. 62:2280-2286.
14. Bentzen, P., M. S. Ridgway, and J. D. McPhail. 1984. Ecology and evolution of sympatric sticklebacks (Gasterosteus)-spatial segregation and seasonal habitat shifts in the Enos Lake species pair. Can. J. Zool. 62:2436-2439.
15. Bergendal, B., J. Klar, C. Stecksen-Blicks, J. Norderyd, and N. Dahl. 2011. Isolated oligodontia associated with mutations in EDARADD, AXIN2, MSX1, and PAX9 genes. Am. J. Med. Genet. Part A 155A:1616-1622.
16. Bergstrom, C. A. 2002. Fast-start swimming performance and reduction in lateral plate number in threespine stickleback. Can. J. Zool. 80:207-213.
17. Berner, D. 2011. Size correction in biology: how reliable are approaches based on (common) principal component analysis? Oecologia 166:961-971.
18. Berner, D., D. C. Adams, A.-C. Grandchamp, and A. P. Hendry. 2008. Natural selection drives patterns of lake-stream divergence in stickleback foraging morphology. J. Evol. Biol. 21:1653-1665.
19. Berner, D., A.-C. Grandchamp, and A. P. Hendry. 2009. Variable progress toward ecological speciation in parapatry: stickleback across eight lake-stream transitions. Evolution 63:1740-1753.
20. Berner, D., M. Roesti, A. P. Hendry, and W. Salzburger. 2010a. Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents. Mol. Ecol. 19:4963-4978.
21. Berner, D., W. E. Stutz, and D. I. Bolnick. 2010b. Foraging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution 64:2265-2277.
22. Berner, D., R. Kaeuffer, A.-C. Grandchamp, J. A. M. Raeymaekers, K. Räsänen, and A. P. Hendry. 2011. Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation. J. Evol. Biol. 24:1975-1983.
23. Boden, S. D., Y. S. Liu, G. A. Hair, J. A. Helms, D. Hu, M. Racine, M. S. Nanes, and L. Titus. 1998. LMP-1, a LIM-domain protein, mediates BMP-6 effects on bone formation. Endocrinology 139:5125-5134.
24. Bolnick, D. I. 2004. Can intraspecific competition drive disruptive selection? An experimental test in natural populations of sticklebacks. Evolution 58:608-618.
25. Bolnick, D. I., L. K. Snowberg, C. Patenia, W. E. Stutz, T. Ingram, and O. L. Lau. 2009. Phenotype-dependent native habitat preference facilitates divergence between parapatric lake and stream stickleback. Evolution 63:2004-2016.
26. Broman, K. W., and S. Sen. 2009. A guide to QTL mapping with R/qtl. Springer, New York.
27. Caldecutt, W. J., and D. C. Adams. 1998. Morphometrics of trophic osteology in the threespine stickleback, Gasterosteus aculeatus. Copeia 1998:827-838.
28. Callahan, N., A. Modesto, R. Meira, F. Seymen, A. Patir, and A. R. Vieira. 2009. Axis inhibition protein 2 (AXIN2) polymorphisms and tooth agenesis. Arch. Oral Biol. 54:45-49.
29. Chassaing, N., S. Bourthoumieu, M. Cosse, P. Calvas, and M. C. Vincent. 2006. Mutations in EDAR account for one-quarter of non-ED1-related hypohidrotic ectodermal dysplasia. Hum. Mutat. 27:255-259.
30. Colosimo, P. F., C. L. Peichel, K. Nereng, B. K. Blackman, M. D. Shapiro, D. Schluter, and D. M. Kingsley. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2:635-641.
31. Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Villareal Jr., M. Dickson, J. Grimwood, J. Schmutz, R. M. Myers, D. Schluter, and D. M. Kingsley. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928-1933.
32. Cresko, W. A., A. Amores, C. Wilson, J. Murphy, M. Currey, P. Phillips, M. A. Bell, C. B. Kimmel, and J. H. Postlethwait. 2004. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc. Natl. Acad. Sci. USA 101:6050-6055.
33. Day, T., J. Pritchard, and D. Schluter. 1994. Ecology and genetics of phenotypic plasticity: a comparison of two sticklebacks. Evolution 48:1723-1734.
34. Deagle, B. E., F. C. Jones, Y. F. Chan, D. M. Absher, D. M. Kingsley, and T. E. Reimchen. 2012. Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions. Proc. R. Soc. Lond. B 279:1277-1286.
35. Gerking, S. D. 1994. Feeding ecology of fish. Academic, San Diego, CA.
36. Giles, N. 1983. The possible role of environmental calcium levels during the evolution of phenotypic diversity in Outer Hebridean populations of the three-spined stickleback, Gasterosteus aculeatus. J. Zool. 199:535-544.
37. Göring, H. H. H., J. D. Terwilliger, and J. Blangero. 2001. Large upward bias in estimation of locus-specific effects from genomewide scans. Am. J. Hum. Genet. 69:1357-1369.
38. Gross, H. P., and J. M. Anderson. 1984. Geographic variation in the gillrakers and diet of European sticklebacks, Gasterosteus aculeatus. Copeia 1984:87-97.
39. Hagen, D. W., and L. G. Gilbertson. 1972. Geographic variation and environmental selection in Gasterosteus aculeatus L. in the pacific northwest, America. Evolution 26:32-51.
40. Harris, M. P., N. Rohner, H. Schwarz, S. Perathoner, P. Konstantinidis, and C. Nüsslein-Volhard. 2008. Zebrafish eda and edar mutants reveal conserved and ancestral roles of ectodysplasin signaling in vertebrates. PLoS Genet. 4:e1000206.
41. Headon, D. J., S. A. Emmal, B. M. Ferguson, A. S. Tucker, M. J. Justice, P. T. Sharpe, J. Zonana, and P. A. Overbeek. 2001. Gene defect in ectodermal dysplasia implicates a death domain adapter in development. Nature 414:913-916.
42. Hendry, A. P., and E. B. Taylor. 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.
43. Henthorn, P. S., M. Raducha, K. N. Fedde, M. A. Lafferty, and M. P. Whyte. 1992. Different missense mutations at the tissue-nonspecific alkaline-phosphatase gene locus in autosomal recessively inherited forms of mild and severe hypophosphatasia. Proc. Natl. Acad. Sci. USA 89:9924-9928.
44. Heuts, M. J. 1947. Experimental studies on adaptive evolution in Gasterosteus aculeatus L. Evolution 1:89-102.
45. Hoekstra, H. E., and J. A. Coyne. 2007. The locus of evolution: evo devo and the genetics of adaptation. Evolution 61:995-1016.
46. Hohenlohe, P. A., S. Bassham, P. D. Etter, N. Stiffler, E. A. Johnson, and W. A. Cresko. 2010. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6:e1000862.
47. Houston, B., E. Seawright, D. Jefferies, E. Hoogland, D. Lester, C. Whitehead, and C. Farquharson. 1999. Identification and cloning of a novel phosphatase expressed at high levels in differentiating growth plate chondrocytes. Biochim. Biophys. Acta 1448:500-506.
48. Houston, B., A. J. Stewart, and C. Farquharson. 2004. PHOSPHO1-a novel phosphatase specifically expressed at sites of mineralisation in bone and cartilage. Bone 34:629-637.
49. Jones, F. C., M. G. Grabherr, Y. F. Chan, P. Russell, E. Mauceli, J. Johnson, R. Swofford, M. Pirun, M. C. Zody, S. White, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
50. Kaeuffer, R., C. Peichel, D. I. Bolnick, and A. P. Hendry. 2012. Convergence and non-convergence in ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66:402-418.
51. Kahilainen, K., and K. Ostbye. 2006. Morphological differentiation and resource polymorphism in three sympatric whitefish Coregonus lavaretus (L.) forms in a subarctic lake. J. Fish Biol. 68:63-79.
52. Kalamajski, S., A. Aspberg, K. Lindblom, D. Heinegard, and A. Oldberg. 2009. Asporin competes with decorin for collagen binding, binds calcium and promotes osteoblast collagen mineralization. Biochem. J. 423:53-59.
53. Kere, J., A. K. Srivastava, O. Montonen, J. Zonana, N. Thomas, B. Ferguson, F. Munoz, D. Morgan, A. Clarke, P. Baybayan, et al. 1996. X-linked anhidrotic (hypohidrotic) ectodermal dysplasia is caused by mutation in a novel transmembrane protein. Nat. Genet. 13:409-416.
54. Kimura, T., M. Shinya, and K. Naruse. 2012. Genetic analysis of vertebral regionalization and number in Medaka (Oryzias latipes) inbred lines. G3 2:1317-1323.
55. Kirsch, T., G. Harrison, E. E. Golub, and H. D. Nah. 2000. The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J. Biol. Chem. 275:35577-35583.
56. Kitano, J., S. Mori, and C. L. Peichel. 2007. Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus). Copeia 2007:336-349.
57. Kizawa, H., I. Kou, A. Iida, A. Sudo, Y. Miyamoto, A. Fukuda, A. Mabuchi, A. Kotani, A. Kawakami, S. Yamamoto, et al. 2005. An aspartic acid repeat polymorphism in asporin inhibits chondrogenesis and increases susceptibility to osteoarthritis. Nat. Genet. 37:138-144.
58. Koyama, K., K. Nakazato, S. K. Min, K. Gushiken, Y. Hatakeda, K. Seo, and K. Hiranuma. 2012. COL11A1 gene is associated with limbus vertebra in gymnasts. Int. J. Sports Med. 33:586-590.
59. Lammi, L., S. Arte, M. Somer, H. Jarvinen, P. Lahermo, I. Thesleff, S. Pirinen, and P. Nieminen. 2004. Mutations in AXIN2 cause familial tooth agenesis and predispose to colorectal cancer. Am. J. Hum. Genet. 74:1043-1050.
60. Lande, R., and R. Thompson. 1990. Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743-756.
61. Lavin, P. A., and J. D. McPhail. 1993. Parapatric lake and stream sticklebacks on northern Vancouver Island: disjunct distribution or parallel evolution? Can. J. Zool. 71:11-17.
62. Lawniczak, M. K. N., S. J. Emrich, A. K. Holloway, A. P. Regier, M. Olson, B. White, S. Redmond, L. Fulton, E. Appelbaum, J. Godfrey, et al. 2010. Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330:512-514.
63. Leinonen, T., G. Herczeg, J. M. Cano, and J. Merilä. 2011a. Predation-imposed selection on threespine stickleback (Gasterosteus aculeatus) morphology: a test of the refuge use hypothesis. Evolution 65:2916-2926.
64. Leinonen, T., J. M. Cano, and J. Merilä. 2011b. Genetics of body shape and armour variation in threespine sticklebacks. J. Evol. Biol. 24:206-218.
65. Leinonen, T., R. J. S. McCairns, G. Herczeg, and J. Merilä. 2012. Multiple evolutionary pathways to decreased lateral plate coverage in freshwater threespine sticklebacks. Evolution 66:3866-3875.
66. Lessells, C. M., and P. T. Boag. 1987. Unrepeatable repeatabilities-a common mistake. Auk 104:116-121.
67. Li, Y., D. A. Lacerda, M. L. Warman, D. R. Beier, H. Yoshioka, Y. Ninomiya, J. T. Oxford, N. P. Morris, K. Andrikopoulos, F. Ramirez, et al. 1995. A fibrillar collagen gene, COL11A1, is essential for skeletal morphogenesis. Cell 80:423-430.
68. Liu, Y. H., G. A. Hair, S. D. Boden, M. Viggeswarapu, and L. Titus. 2002. Overexpressed LIM mineralization proteins do not require LIM domains to induce bone. J. Bone Miner. Res. 17:406-414.
69. Lucek, K., A. Sivasundar, and O. Seehausen. 2012. Evidence of adaptive evolutionary divergence during biological invasion. PLoS One 7:e49377.
70. Lucek, K., A. Sivasundar, D. Roy, and O. Seehausen. 2013. Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake-stream divergence in parapatric Swiss stickleback. J. Evol. Biol. 26:2691-2709.
71. Mackay, T. F. C., E. A. Stone, and J. F. Ayroles. 2009. The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10:565-577.
72. Madisen, L., M. Neubauer, G. Plowman, D. Rosen, P. Segarini, J. Dasch, A. Thompson, J. Ziman, H. Bentz, and A. F. Purchio. 1990. Molecular cloning of a novel bone-forming compound-osteoinductive factor. DNA Cell Biol. 9:303-309.
73. Manly, B. F. J. 2007. Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall, Boca Raton, FL.
74. Mateus, C. S., M. Stange, D. Berner, M. Roesti, B. R. Quintella, M. J. Alves, P. R. Almeida, and W. Salzburger. 2013. Strong genome-wide divergence between sympatric European river and brook lampreys. Curr. Biol. 23:R649-R650.
75. Matthews, B., K. B. Marchinko, D. I. Bolnick, and A. Mazumder. 2010. Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation. Ecology 91:1025-1034.
76. McDowall, R. M. 2008. Jordan's and other ecogeographical rules, and the vertebral number in fishes. J. Biogeogr. 35:501-508.
77. McPhail, J. D. 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.
78. Mikawa, S., T. Morozumi, S.-I. Shimanuki, T. Hayashi, H. Uenishi, M. Domukai, N. Okumura, and T. Awata. 2007. Fine mapping of a swine quantitative trait locus for number of vertebrae and analysis of an orphan nuclear receptor, germ cell nuclear factor (NR6A1). Genome Res. 17:586-593.
79. Mikawa, S., S. Sato, M. Nii, T. Morozumi, G. Yoshioka, N. Imaeda, T. Yamaguchi, T. Hayashi, and T. Awata. 2011. Identification of a second gene associated with variation in vertebral number in domestic pigs. BMC Genet. 12:5.
80. Miller, C. T., D. Yelon, D. Y. R. Stainier, and C. B. Kimmel. 2003. Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130:1353-1365.
81. Mitchell-Olds, T., J. H. Willis, and D. B. Goldstein. 2007. Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat. Rev. Genet. 8:845-856.
82. Monreal, A. W., B. M. Ferguson, D. J. Headon, S. L. Street, P. A. Overbeek, and J. Zonana. 1999. Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat. Genet. 22:366-369.
83. Moodie, G. E. E., and T. E. Reimchen. 1976. Phenetic variation and habitat differences in Gasterosteus populations of Queen Charlotte Islands. Syst. Zool. 25:49-61.
84. Moser, D., M. Roesti, and D. Berner. 2012. Repeated lake-stream divergence in stickleback life history within a Central European lake basin. PLoS One 7:e50620.
85. Mostowska, A., B. Biedziak, and P. P. Jagodzinski. 2006. Axis inhibition protein 2 (AXIN2) polymorphisms may be a risk factor for selective tooth agenesis. J. Hum. Genet. 51:262-266.
86. Myhre, F., and T. Klepaker. 2009. Body armour and lateral-plate reduction in freshwater three-spined stickleback Gasterosteus aculeatus: adaptations to a different buoyancy regime? J. Fish Biol. 75:2062-2074.
87. Nadeau, N. J., A. Whibley, R. T. Jones, J. W. Davey, K. K. Dasmahapatra, S. W. Baxter, M. A. Quail, M. Joron, R. H. Ffrench-Constant, M. L. Blaxter, et al. 2012. Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philos. Trans. R. Soc. Lond. B 367:343-353.
88. Nei, M., and F. Tajima. 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97:145-163.
89. Nichols, K. M., P. A. Wheeler, and G. H. Thorgaard. 2004. Quantitative trait loci analyses for meristic traits in Oncorhynchus mykiss. Environ. Biol. Fish. 69:317-331.
90. Nielsen, R. 2005. Molecular signatures of natural selection. Annu. Rev. Genet. 39:197-218.
91. Oleksyk, T. K., M. W. Smith, and S. J. O'Brien. 2010. Genome-wide scans for footprints of natural selection. Philos. Trans. R. Soc. Lond. B 365:185-205.
92. Orr, H. A. 1998. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52:935-949.
93. Pfaender, J., F. W. Miesen, R. K. Hadiaty, and F. Herder. 2011. Adaptive speciation and sexual dimorphism contribute to diversity in form and function in the adaptive radiation of Lake Matano's sympatric roundfin sailfin silversides. J. Evol. Biol. 24:2329-2345.
94. Phillips, P. C. 2005. Testing hypotheses regarding the genetics of adaptation. Genetica 123:15-24.
95. R Development Core Team 2013. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Austria, Vienna.
96. Ravinet, M., P. A. Prodoehl, and C. Harrod. 2013. Parallel and nonparallel ecological, morphological and genetic divergence in lake-stream stickleback from a single catchment. J. Evol. Biol. 26:186-204.
97. Reimchen, T. E. 1994. Predators and morphological evolution in threespine stickleback. Pp. 240-273 in M. A. Bell and S. A. Foster, eds. The evolutionary biology of the threespine stickleback. Oxford Univ. Press, Oxford, U.K.
98. Reimchen, T. E., E. M. Stinson, and J. S. Nelson. 1985. Multivariate differentiation of parapatric and allopatric populations of threespine stickleback in the Sangan River watershed, Queen Charlotte Islands. Can. J. Zool. 63:2944-2951.
99. Reist, J. D. 1985. An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Can. J. Zool. 63:1429-1439.
100. Ren, D. R., J. Ren, G. F. Ruan, Y. M. Guo, L. H. Wu, G. C. Yang, L. H. Zhou, L. Li, Z. Y. Zhang, and L. S. Huang. 2012. Mapping and fine mapping of quantitative trait loci for the number of vertebrae in a White Duroc x Chinese Erhualian intercross resource population. Anim. Genet. 43:545-551.
101. Roberts, S., S. Narisawa, D. Harmey, J. L. Millan, and C. Farquharson. 2007. Functional involvement of PHOSPHO1 in matrix vesicle-mediated skeletal mineralization. J. Bone Miner. Res. 22:617-627.
102. Rockman, M. V. 2011. The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66:1-17.
103. Roesti, M., A. P. Hendry, W. Salzburger, and D. Berner. 2012a. Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs. Mol. Ecol. 21:2852-2862.
104. Roesti, M., W. Salzburger, and D. Berner. 2012b. Uninformative polymorphisms bias genome scans for signatures of selection. BMC Evol. Biol. 12:94.
105. Roesti, M., D. Moser, and D. Berner. 2013. Recombination in the threespine stickleback genome-patterns and consequences. Mol. Ecol. 22:3014-3027.
106. Roesti, M., S. Gavrilets, A. P. Hendry, W. Salzburger, and D. Berner. 2014. The genomic signature of parallel adaptation from shared genetic variation. Mol. Ecol. In press.
107. Rohlf, F. J. 2001. tpsDig, tpsRelw, tpsRegr. Distributed by the author. Department of Ecology and Evolution, State University of New York, Stony Brook, NY.
108. Sanderson, S. L., A. Y. Cheer, J. S. Goodrich, J. D. Graziano, and W. T. Callan. 2001. Crossflow filtration in suspension-feeding fishes. Nature 412:439-441.
109. Schluter, D., and J. D. McPhail. 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140:85-108.
110. Sharpe, D. M. T., K. Räsänen, D. Berner, and A. P. Hendry. 2008. Genetic and environmental contributions to the morphology of lake and stream stickleback: implications for gene flow and reproductive isolation. Evol. Ecol. Res. 10:849-866.
111. Song, Y.-Q., K. M. C. Cheung, D. W. H. Ho, S. C. S. Poon, K. Chiba, Y. Kawaguchi, Y. Hirose, M. Alini, S. Grad, A. F. Y. Yee, et al. 2008. Association of the asporin D14 allele with lumbar-disc degeneration in Asians. Am. J. Hum. Genet. 82:744-747.
112. Stern, D. L., and V. Orgogozo. 2008. The loci of evolution: how predictable is genetic evolution? Evolution 62:2155-2177.
113. Stinchcombe, J. R., and H. E. Hoekstra. 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158-170.
114. Stölting, K. N., R. Nipper, D. Lindtke, C. Caseys, S. Waeber, S. Castiglione, and C. Lexer. 2013. Genomic scan for single nucleotide polymorphisms reveals patterns of divergence and gene flow between ecologically divergent species. Mol. Ecol. 22:842-855.
115. Storz, J. F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol. Ecol. 14:671-688.
116. Storz, J. F., and C. W. Wheat. 2010. Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution 64:2489-2509.
117. Swain, D. P. 1992. The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution 46:987-997.
118. The UniProt Consortium. 2013. Update on activities at the Universal Protein Resource (UniProt) in 2013. Nucleic Acids Res. 41:D43-D47.
119. Thompson, C. E., E. B. Taylor, and J. D. McPhail. 1997. Parallel evolution of lake-stream pairs of threespine sticklebacks (Gasterosteus) inferred from mitochondrial DNA variation. Evolution 51:1955-1965.
120. Thouverey, C., A. Strzelecka-Kiliszek, M. Balcerzak, R. Buchet, and S. Pikula. 2009. Matrix vesicles originate from apical membrane microvilli of mineralizing osteoblast-like saos-2 cells. J. Cell. Biochem. 106:127-138.
121. Tompson, S. W., C. A. Bacino, N. P. Safina, M. B. Bober, V. K. Proud, T. Funari, M. F. Wangler, L. Nevarez, L. Ala-Kokko, W. R. Wilcox, et al. 2010. Fibrochondrogenesis results from mutations in the COL11A1 type XI collagen gene. Am. J. Hum. Genet. 87:708-712.
122. Van Wesenbeeck, L., P. R. Odgren, F. P. Coxon, A. Frattini, P. Moens, B. Perdu, C. A. MacKay, E. Van Hul, J.-P. Timmermans, F. Vanhoenacker, et al. 2007. Involvement of PLEKHM1 in osteoclastic vesicular transport and osteopetrosis in incisors absent rats and humans. J. Clin. Invest. 117:919-930.
123. Voight, B. F., S. Kudaravalli, X. Wen, and J. K. Pritchard. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
124. Wake, D. B., M. H. Wake, and C. D. Specht. 2011. Homoplasy: from detecting pattern to determining process and mechanism of evolution. Science 331:1032-1035.
125. Wang, W., and T. Kirsch. 2002. Retinoic acid stimulates annexin-mediated growth plate chondrocyte mineralization. J. Cell Biol. 157:1061-1069.
126. Ward, A. B., and E. L. Brainerd. 2007. Evolution of axial patterning in elongate fishes. Biol. J. Linn. Soc. 90:97-116.
127. Weiss, M. J., D. E. C. Cole, K. Ray, M. P. Whyte, M. A. Lafferty, R. A. Mulivor, and H. Harris. 1988. A missense mutation in the human liver/bone/kidney alkaline-phosphatase gene causing a lethal form of hypophosphatasia. Proc. Natl. Acad. Sci. USA 85:7666-7669.
128. Wray, G. A. 2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206-216.
129. Wund, M. A., J. A. Baker, B. Clancy, J. L. Golub, and S. A. Foster. 2008. A test of the "Flexible stem" model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am. Nat. 172:449-462.
130. Xu, S. Z. 2003. Theoretical basis of the Beavis effect. Genetics 165:2259-2268.
131. Yeaman, S., and M. C. Whitlock. 2011. The genetic architecture of adaptation under migration-selection balance. Evolution 65:1897-1911.