Genetic constraints predict evolutionary divergence in Dalechampia blossoms

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1649, 2014, Pages

  Bolstad, Geir H ^a   Hansen, Thomas F ^b   Pélabon, Christophe ^a   Falahati Anbaran, Mohsen ^a,c   Pérez Barrales, Rocío ^d   Armbruster, W Scott ^a,d,e  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF TEHRAN   (Iran)

^d UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^e UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Evolutionary rate; G matrix; Integration; Macroevolution; Microevolution; Power relationship

Indexed keywords

ADAPTIVE RADIATION; DIVERGENCE; EVOLUTION; FLORAL TRAIT; GENETIC STRUCTURE; LIFE HISTORY TRAIT; MORPHOLOGY; NATURAL SELECTION; NEOTROPICAL REGION; SPECIES COMPLEX; VINE;

ADAPTATION; ANATOMY AND HISTOLOGY; BAYES THEOREM; BIOLOGICAL MODEL; COMPUTER SIMULATION; EUPHORBIACEAE; EVOLUTION; FLOWER; GENETIC SELECTION; GENETICS; MEXICO; PHENOTYPE; PHYLOGENY; POPULATION GENETICS; SPECIES DIFFERENCE; SYSTEMS BIOLOGY;

ADAPTATION, BIOLOGICAL; ANATOMY AND HISTOLOGY; BAYES THEOREM; BIOLOGICAL EVOLUTION; COMPUTER SIMULATION; EUPHORBIACEAE; FLOWERS; GENETICS; GENETICS, POPULATION; MEXICO; MODELS, BIOLOGICAL; PHENOTYPE; PHYLOGENY; SELECTION, GENETIC; SPECIES SPECIFICITY; SYSTEMS BIOLOGY;

EID: 84903889839     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0255     Document Type: Article

References (116)

1. Cheverud JM. 1984 Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110, 155-171. (doi: 10. 1016/S0022-5193(84)80050-8).
2. Schluter D. 2000 Ecological character displacement in adaptive radiation. Am. Nat. 156, S4-S16. (doi: 10. 1086/303412).
3. Arnold SJ, Pfrender ME, Jones AG. 2001 The adaptive landscape as a conceptual bridge between micro-and macroevolution. Genetica 112, 9-32. (doi: 10. 1023/A: 1013373907708).
4. Estes S, Arnold SJ. 2007 Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 169, 227-244. (doi: 10. 1086/510633).
5. Hendry AP. 2013 Key questions in the genetics and genomics of eco-evolutionary dynamics. Heredity 111, 456-466. (doi: 10. 1038/hdy. 2013. 75).
6. Arnold SJ. 2014 Phenotypic evolution: the ongoing synthesis. Am. Nat. 183, 729-746. (doi: 10. 1086/675304).
7. Stanley SM. 1979 Macroevolution: pattern and process. San Francisco, CA: W. H. Freeman.
8. Eldredge N. 1989 Macroevolutionary patterns and evolutionary dynamics: species, niches and adaptive peaks. New York, NY: McGraw-Hill.
9. Gould SJ. 2002 The structure of evolutionary theory. Cambridge, MA: Belknap.
10. Monroe MJ, Bokma F. 2010 Punctuated equilibrium in a neontological context. Theory Biosci. 129, 103-111. (doi: 10. 1007/s12064-010-0087-7).
11. Futuyma DJ. 2010 Evolutionary constraint and ecological consequences. Evolution 64, 1865-1884. (doi: 10. 1111/j. 1558-5646. 2010. 00960. x).
12. Lande R. 1979 Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 33, 402-416. (doi: 10. 2307/2407630).
13. Lande R, Arnold SJ. 1983 The measurement of selection on correlated characters. Evolution 37, 1210-1226. (doi: 10. 2307/2408842).
14. Schluter D. 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
15. Svensson EI, Calsbeek R. 2012 The adaptive landscape in evolutionary biology. Oxford, UK: Oxford University Press.
16. Roff DA. 1992 Evolution of life histories: theory and analysis. New York, NY: Chapman & Hall.
17. Hansen TF, Houle D. 2008 Measuring and comparing evolvability and constraint in multivariate characters. J. Evol. Biol. 21, 1201-1219. (doi: 10. 1111/j. 1420-9101. 2008. 01573. x).
18. Walsh B, Blows MW. 2009 Abundant genetic variation {thorn} strong selection = multivariate genetic constraints: a geometric view of adaptation. Annu. Rev. Ecol. Evol. Syst. 40, 41-59. (doi: 10. 1146/annurev. ecolsys. 110308. 120232).
19. Simonsen AK, Stinchcombe JR. 2010 Quantifying evolutionary genetic constraints in the ivyleaf morning glory, Ipomoea hederacea. Int. J. Plant Sci. 171, 972-986. (doi: 10. 1086/656512).
20. Aguirre JD, Hine E, McGuigan K, Blows MW. 2014 Comparing G: multivariate analysis of genetic variation in multiple populations. Heredity 112, 21-29. (doi: 10. 1038/hdy. 2013. 12).
21. Simpson GG. 1944 Tempo and mode in evolution. New York, NY: Colombia University Press.
22. Hansen TF. 1997 Stabilizing selection and the comparative analysis of adaptation. Evolution 51, 1341-1351. (doi: 10. 2307/2411186).
23. Hansen TF. 2012 Adaptive landscapes and macroevolutionary dynamics. In The adaptive landscape in evolutionary biology (eds EI Svensson, R Calsbeek), pp. 205-226. Oxford, UK: Oxford University Press.
24. Hansen TF, Pélabon C, Armbruster WS, Carlson ML. 2003 Evolvability and genetic constraint in Dalechampia blossoms: components of variance and measures of evolvability. J. Evol. Biol. 16, 754-766. (doi: 10. 1046/j. 1420-9101. 2003. 00556. x).
25. Hansen TF, Pélabon C, Houle D. 2011 Heritability is not evolvability. Evol. Biol. 38, 258-277. (doi: 10. 1007/s11692-011-9127-6).
26. Hansen TF. 2003 Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems 69, 83-94. (doi: 10. 1016/S0303-2647(02)00132-6).
27. Hereford J, Hansen TF, Houle D. 2004 Comparing strengths of directional selection: how strong is strong? Evolution 58, 2133-2143. (doi: 10. 1111/j. 0014-3820. 2004. tb01592. x).
28. Siepielski AM, DiBattista JD, Carlson SM. 2009 It's about time: the temporal dynamics of phenotypic selection in the wild. Ecol. Lett. 12, 1261-1276. (doi: 10. 1111/j. 1461-0248. 2009. 01381. x).
29. Bell G. 2010 Fluctuating selection: the perpetual renewal of adaptation in variable environments. Phil. Trans. R. Soc. B 365, 87-97. (doi: 10. 1098/rstb. 2009. 0150).
30. Morrissey MB, Hadfield JD. 2012 Directional selection in temporally replicated studies is remarkably consistent. Evolution 66, 435-442. (doi: 10. 1111/j. 1558-5646. 2011. 01444. x).
31. Lynch M. 1990 The rate of morphological evolution in mammals from the standpoint of the neutral expectation. Am. Nat. 136, 727-741. (doi: 10. 1086/285128).
32. Hansen TF, Martins EP. 1996 Translating between microevolutionary process and macroevolutionary patterns: the correlation structure of interspecific data. Evolution 50, 1404-1417. (doi: 10. 2307/2410878).
33. Hohenlohe PA, Arnold SJ. 2008 MIPoD: a hypothesis-testing framework for microevolutionary inference from patterns of divergence. Am. Nat. 171, 366-385. (doi: 10. 1086/527498).
34. Lynch M, Lande R. 1993 Evolution and extinction in response to environmental change. In Biotic interactions and global change (eds JG Kingsolver, PM Kareiva, RB Huey), pp. 234-250. Sunderland, MA: Sinauer Associates.
35. Hansen TF, Pienaar J, Orzack SH. 2008 A comparative method for studying adaptation to a randomly evolving environment. Evolution 62, 1965-1977. (doi: 10. 1111/j. 1558-5646. 2008. 00412. x).
36. Webster GL, Webster BD. 1972 Morphology and relationships of Dalechampia scandens (Euphorbiaceae). Am. J. Bot. 59, 573-586. (doi: 10. 2307/2441021).
37. Webster GL, Armbruster WS. 1991 A synopsis of the neotropical species of Dalechampia (Euphorbiaceae). Bot. J. Linnean Soc. 105, 137-177. (doi: 10. 1111/j. 1095-8339. 1991. tb00202. x).
38. Pérez-Barrales R, Bolstad GH, Pélabon C, Hansen TF, Armbruster WS. 2013 Pollinators and seed predators generate conflicting selection on Dalechampia blossoms. Oikos 122, 1411-1428. (doi: 10. 1111/j. 1600-0706. 2013. 20780. x).
39. Armbruster WS. 1997 Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78, 1661-1672.
40. Armbruster WS. 1985 Patterns of character divergence and the evolution of reproductive ecotypes of Dalechampia scandens (Euphorbiaceae). Evolution 39, 733-752. (doi: 10. 2307/2408674).
41. Pélabon C, Thone P, Hansen TF, Armbruster WS. 2012 Signal honesty and cost of pollinator rewards in Dalechampia scandens (Euphorbiaceae). Ann. Bot. 109, 1331-1339. (doi: 10. 1093/Aob/Mcs091).
42. Armbruster WS. 1988 Multilevel comparative analysis of the morphology, function, and evolution of Dalechampia blossoms. Ecology 69, 1746-1761. (doi: 10. 2307/1941153).
43. Armbruster WS. 1986 Reproductive interactions between sympatric Dalechampia species: are natural assemblages random or organized? Ecology 67, 522-533. (doi: 10. 2307/1938595).
44. Armbruster WS. 1990 Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. Am. Nat. 135, 14-31. (doi: 10. 1086/285029).
45. Pélabon C, Carlson ML, Hansen TF, Armbruster WS. 2005 Effects of crossing distance on offspring fitness and developmental stability in Dalechampia scandens (Euphorbiaceae). Am. J. Bot. 92, 842-851. (doi: 10. 3732/Ajb. 92. 5. 842).
46. Pélabon C, Carlson ML, Hansen TF, Yoccoz NG, Armbruster WS. 2004 Consequences of interpopulation crosses on developmental stability and canalization of floral traits in Dalechampia scandens (Euphorbiaceae). J. Evol. Biol. 17, 19-32. (doi: 10. 1046/j. 1420-9101. 2003. 00663. x).
47. Hansen TF, Armbruster WS, Carlson ML, Pélabon C. 2003 Evolvability and genetic constraint in Dalechampia blossoms: genetic correlations and conditional evolvability. J. Exp. Zool. B 296B, 23-39. (doi: 10. 1002/Jez. B. 00014).
48. Pélabon C, Hansen TF, Carlson ML, Armbruster WS. 2004 Variational and genetic properties of developmental stability in Dalechampia scandens. Evolution 58, 504-514. (doi: 10. 1111/j. 0014-3820. 2004. tb01674. x).
49. Nei M, Tajima F, Tateno Y. 1983 Accuracy of estimated phylogenetic trees from molecular data. II. Gene-frequency data. J. Mol. Evol. 19, 153-170. (doi: 10. 1007/Bf02300753).
50. Falahati-Anbaran M, Stenøyen HK, Pélabon C, Bolstad GH, Pérez-Barrales R, Hansen TF, Armbruster WS. 2013 Development of microsatellite markers for the Neotropical vine Dalechampia scandens (Euphorbiaceae). Appl. Plant Sci. 1, 1200492.
51. Hadfield JD. 2010 MCMC Methods for multiresponse generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1-22.
52. Gelman A. 2006 Prior distributions for variance parameters in hierarchical models (comment on article by Browne and Draper). Bayesian Anal. 1, 515-533. (doi: 10. 1214/06-BA117A).
53. McGuigan K, Blows MW. 2010 Evolvability of individual traits in a multivariate context: partitioning the additive genetic variance into common and specific components. Evolution 64, 1899-1911. (doi: 10. 1111/j. 1558-5646. 2010. 00968. x).
54. Lynch M. 1991 Methods for the analysis of comparative data in evolutionary biology. Evolution 45, 1065-1080. (doi: 10. 2307/2409716).
55. Hadfield JD, Nakagawa S. 2010 General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494-508. (doi: 10. 1111/j. 1420-9101. 2009. 01915. x).
56. Wagner GP, Altenberg L. 1996 Complex adaptations and the evolution of evolvability. Evolution 50, 967-976. (doi: 10. 2307/2410639).
57. R Core Team. 2013 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www. R-project. org.
58. Bolstad GH, Armbruster WS, Pélabon C, Pérez-Barrales R, Hansen TF. 2010 Direct selection at the blossom level on floral reward by pollinators in a natural population of Dalechampia schottii: fulldisclosure honesty? New Phytol. 188, 370-384. (doi: 10. 1111/j. 1469-8137. 2010. 03429. x).
59. Armbruster WS, Antonsen L, Pélabon C. 2005 Phenotypic selection on Dalechampia blossoms: honest signaling affects pollination success. Ecology 86, 3323-3333. (doi: 10. 1890/04-1873).
60. Armbruster WS, Gong YB, Huang SQ. 2011 Are pollination 'syndromes' predictive? Asian Dalechampia fit Neotropical models. Am. Nat. 178, 135-143. (doi: 10. 1086/660279).
61. Hansen TF, Armbruster WS, Antonsen L. 2000 Comparative analysis of character displacement and spatial adaptations as illustrated by the evolution of Dalechampia blossoms. Am. Nat. 156, S17-S34. (doi: 10. 1086/303413).
62. Armbruster WS. 1991 Multilevel analysis of morphometric data from natural plant populations: insights into ontogenic, genetic, and selective correlations in Dalechampia scandens. Evolution 45, 1229-1244. (doi: 10. 2307/2409730).
63. Armbruster WS. 2002 Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. J. Evol. Biol. 15, 468-486. (doi: 10. 1046/j. 1420-9101. 2002. 00399. x).
64. Arnold SJ, Phillips PC. 1999 Hierarchical comparison of genetic variance-covariance matrices. II. Coastalinland divergence in the garter snake, Thamnophis elegans. Evolution 53, 1516-1527. (doi: 10. 2307/2640897).
65. Baer CF, Lynch M. 2003 Correlated evolution of life-history with size at maturity in Daphnia pulicaria: patterns within and between populations. Genet. Res. 81, 123-132. (doi: 10. 1017/S00166 72303006098).
66. Blows MW, Higgie M. 2003 Genetic constraints on the evolution of mate recognition under natural selection. Am. Nat. 161, 240-253. (doi: 10. 1086/345783).
67. Bégin M, Roff DA. 2003 The constancy of the G matrix through species divergence and the effects of quantitative genetic constraints on phenotypic evolution: a case study in crickets. Evolution 57, 1107-1120. (doi: 10. 1111/j. 0014-3820. 2003. tb00320. x).
68. Bégin M, Roff DA. 2004 From micro-to macroevolution through quantitative genetic variation: positive evidence from field crickets. Evolution 58, 2287-2304. (doi: 10. 1111/j. 0014-3820. 2004. tb01604. x).
69. Marroig G, Cheverud JM. 2005 Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution 59, 1128-1142. (doi: 10. 1111/j. 0014-3820. 2005. tb01049. x).
70. McGuigan K, Chenoweth SF, Blows MW. 2005 Phenotypic divergence along lines of genetic variance. Am. Nat. 165, 32-43. (doi: 10. 1086/426600).
71. Chapuis E, Martin G, Goudet J. 2008 Effects of selection and drift on G matrix evolution in a heterogeneous environment: a multivariate Qst-Fst test with the freshwater snail Galba truncatula. Genetics 180, 2151-2161. (doi: 10. 1534/genetics. 108. 092452).
72. Chenoweth SF, Rundle HD, Blows MW. 2010 The contribution of selection and genetic constraints to phenotypic divergence. Am. Nat. 175, 186-196. (doi: 10. 1086/649594).
73. Colautti RI, Barrett SCH. 2011 Population divergence along lines of genetic variance and covariance in the invasive plant Lythrum salicaria in eastern North America. Evolution 65, 2514-2529. (doi: 10. 1111/j. 1558-5646. 2011. 01313. x).
74. Martínez-Abadías N, Esparza M, Sjovold T, González-José R, Santos M, Hernández M, Klingenberg CP. 2012 Pervasive genetic integration directs the evolution of human skull shape. Evolution 66, 1010-1023. (doi: 10. 1111/j. 1558-5646. 2011. 01496. x).
75. Berger D, Postma E, Blanckenhorn WU, Walters RJ. 2013 Quantitative genetic divergence and standing genetic (co)variance in thermal reaction norms along latitude. Evolution 67, 2385-2399. (doi: 10. 1111/evo. 12138).
76. Boell L. 2013 Lines of least resistance and genetic architecture of house mouse (Mus musculus) mandible shape. Evol. Dev. 15, 197-204. (doi: 10. 1111/ede. 12033).
77. Innocenti P, Chenoweth SF. 2013 Interspecific divergence of transcription networks along lines of genetic variance in Drosophila: dimensionality, evolvability, and constraint. Mol. Biol. Evol. 30, 1358-1367. (doi: 10. 1093/molbev/mst047).
78. Mitchell-Olds T. 1996 Pleiotropy causes long-term genetic constraints on life-history evolution in Brassica rapa. Evolution 50, 1849-1858. (doi: 10. 2307/2410742).
79. Schluter D. 1996 Ecological causes of adaptive radiation. Am. Nat. 148, S40-S64. (doi: 10. 1086/285901).
80. Tarka M, Akesson M, Hasselquist D, Hansson B. 2014 Intralocus sexual conflict over wing length in a wild migratory bird. Am. Nat. 183, 62-73. (doi: 10. 1086/674072).
81. Badyaev AV, Foresman KR. 2000 Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proc. R. Soc. Lond. B 267, 371-377. (doi: 10. 1098/rspb. 2000. 1011).
82. Ackermann RR, Cheverud JM. 2002 Discerning evolutionary processes in patterns of tamarin (genus Saguinus) craniofacial variation. Am. J. Phys. Anthropol. 117, 260-271. (doi: 10. 1002/Ajpa. 10038).
83. Ackermann RR, Cheverud JM. 2004 Detecting genetic drift versus selection in human evolution. Proc. Natl Acad. Sci. 101, 17 946-17 951. (doi: 10. 1073/pnas. 0405919102).
84. Baker RH, Wilkinson GS. 2003 Phylogenetic analysis of correlation structure in stalk-eyed flies (Diasemopsis, Diopsidae). Evolution 57, 87-103. (doi: 10. 1111/j. 0014-3820. 2003. tb00218. x).
85. Renaud S, Auffray JC, Michaux J. 2006 Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Evolution 60, 1701-1717. (doi: 10. 1111/j. 0014-3820. 2006. tb00514. x).
86. Renaud S, Pantalacci S, Auffray JC. 2011 Differential evolvability along lines of least resistance of upper and lower molars in island house mice. PLoS ONE 6, e18951. (doi: 10. 1371/journal. pone. 0018951).
87. Hunt G. 2007 Evolutionary divergence in directions of high phenotypic variance in the ostracode genus Poseidonamicus. Evolution 61, 1560-1576. (doi: 10. 1111/j. 1558-5646. 2007. 00129. x).
88. Revell LJ, Harmon LJ, Langerhans RB, Kolbe JJ. 2007 A phylogenetic approach to determining the importance of constraint on phenotypic evolution in the Neotropical lizard Anolis cristatellus. Evol. Ecol. Res. 9, 261-282.
89. Charvet CJ, Darlington RB, Finlay BL. 2013 Variation in human brains may facilitate evolutionary change toward a limited range of phenotypes. Brain Behav. Evol. 81, 74-85. (doi: 10. 1159/000345940).
90. Grabowski MW. 2013 Hominin obstetrics and the evolution of constraints. Evol. Biol. 40, 57-75. (doi: 10. 1007/s11692-012-9174-7).
91. Mitteroecker P, Bookstein F. 2008 The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62, 943-958. (doi: 10. 1111/j. 1558-5646. 2008. 00321. x).
92. Grabowski MW, Polk JD, Roseman CC. 2011 Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism. Evolution 65, 1336-1356. (doi: 10. 1111/j. 1558-5646. 2011. 01226. x).
93. Lofsvold D. 1988 Quantitative genetics of morphological-differentiation in Peromyscus. II. Analysis of selection and drift. Evolution 42, 54-67. (doi: 10. 2307/2409115).
94. Venable DL, Búrquez A. 1990 Quantitative genetics of size, shape, life-history, and fruit characteristics of the seed heteromorphic composite Heterosperma pinnatum. II. Correlation structure. Evolution 44, 1748-1763. (doi: 10. 2307/2409504).
95. Andersson S. 1997 Genetic constraints on phenotypic evolution in Nigella (Ranunculaceae). Biol. J. Linnean Soc. 62, 519-532. (doi: 10. 1111/j. 1095-8312. 1997. tb00319. x).
96. Merilä J, Björklund M. 1999 Population divergence and morphometric integration in the greenfinch (Carduelis chloris)-evolution against the trajectory of least resistance? J. Evol. Biol. 12, 103-112. (doi: 10. 1046/j. 1420-9101. 1999. 00013. x).
97. Badyaev AV, Hill GE. 2000 The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution 54, 1784-1794. (doi: 10. 1111/j. 0014-3820. 2000. tb00722. x).
98. Chenoweth SF, Blows MW. 2008 Qst meets the G matrix: the dimensionality of adaptive divergence in multiple correlated quantitative traits. Evolution 62, 1437-1449. (doi: 10. 1111/j. 1558-5646. 2008. 00374. x).
99. Berner D, Stutz WE, Bolnick DI. 2010 Foraging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution 64, 2265-2277. (doi: 10. 1111/j. 1558-5646. 2010. 00982. x).
100. Kimmel CB, Cresko WA, Phillips PC, Ullmann B, Currey M, von Hippel F, Kristjánsson BK, Gelmond O, McGuigan K. 2012 Independent axes of genetic variation and parallel evolutionary divergence of opercle bone shape in threespine stickleback. Evolution 66, 419-434. (doi: 10. 1111/j. 1558-5646. 2011. 01441. x).
101. Houle D, Pélabon C, Wagner GP, Hansen TF. 2011 Measurement and meaning in biology. Q. Rev. Biol. 86, 3-34. (doi: 10. 1086/658408).
102. Houle D. 1992 Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
103. Hansen TF, Voje KL. 2011 Deviation from the line of least resistance does not exclude genetic constraints: a comment on Berner et al. (2010). Evolution 65, 1821-1822. (doi: 10. 1111/j. 1558-5646. 2011. 01281. x).
104. Houle D, Mezey J, Galpern P. 2002 Interpretation of the results of common principal components analyses. Evolution 56, 433-440. (doi: 10. 1111/j. 0014-3820. 2002. tb01356. x).
105. Ovaskainen O, Karhunen M, Zheng CZ, Arias JMC, Merilä J. 2011 A new method to uncover signatures of divergent and stabilizing selection in quantitative traits. Genetics 189, U621-U729. (doi: 10. 1534/genetics. 111. 129387).
106. Karhunen M, Merilä J, Leinonen T, Cano JM, Ovaskainen O. 2013 DRIFTSEL: an R package for detecting signals of natural selection in quantitative traits. Mol. Ecol. Resour. 13, 746-754. (doi: 10. 1111/1755-0998. 12111).
107. Whitlock MC. 2008 Evolutionary inference from QST. Mol. Ecol. 17, 1885-1896. (doi: 10. 1111/j. 1365-294X. 2008. 03712. x).
108. Leinonen T, McCairns RJS, O'Hara RB, Merila J. 2013 QST-FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat. Rev. Genet. 14, 179-190. (doi: 10. 1038/nrg3395).
109. Armbruster WS, Pélabon C, Bolstad GH, Hansen TF. 2014 Integrated phenotypes: understanding trait covariation in plants and animals. Phil. Trans. R. Soc. B 369, 20130245. (doi: 10. 1098/rstb. 2013. 0245).
110. Hansen TF. 2011 Epigenetics: adaptation or contingency? In Epigenetics: linking genotype and phenotype in development and evolution (eds B Hallgrimsson, BK Hall), pp. 357-376. Berkley, CA: University of California Press.
111. Blows MW, Chenoweth SF, Hine E. 2004 Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 163, 329-340. (doi: 10. 1086/381941).
112. Blows MW, Hoffmann AA. 2005 A reassessment of genetic limits to evolutionary change. Ecology 86, 1371-1384. (doi: 10. 1890/04-1209).
113. Voje KL, Hansen TF, Egset CK, Bolstad GH, Pelabon C. 2014 Allometric constraints and the evolution of allometry. Evolution 68, 866-885. (doi: 10. 1111/evo. 12312).
114. Gingerich PD. 1983 Rates of evolution: effects of time and temporal scaling. Science 222, 159-161. (doi: 10. 1126/science. 222. 4620. 159).
115. Uyeda JC, Hansen TF, Arnold SJ, Pienaar J. 2011 The million-year wait for macroevolutionary bursts. Proc. Natl Acad. Sci. 108, 15 908-15 913. (doi: 10. 1073/pnas. 1014503108).
116. Johnson T, Barton N. 2005 Theoretical models of selection and mutation on quantitative traits. Phil. Trans. R. Soc. B 360, 1411-1425. (doi: 10. 1098/rstb. 2005. 1667).