Evolutionary Biology

, 38:258 | Cite as

Heritability is not Evolvability

  • Thomas F. HansenEmail author
  • Christophe Pélabon
  • David Houle
Research Article


Short-term evolutionary potential depends on the additive genetic variance in the population. The additive variance is often measured as heritability, the fraction of the total phenotypic variance that is additive. Heritability is thus a common measure of evolutionary potential. An alternative is to measure evolutionary potential as expected proportional change under a unit strength of selection. This yields the mean-scaled additive variance as a measure of evolvability. Houle in Genetics 130:195–204, (1992) showed that these two ways of scaling additive variance are often inconsistent and can lead to different conclusions as to what traits are more evolvable. Here, we explore this relation in more detail through a literature review, and through theoretical arguments. We show that the correlation between heritability and evolvability is essentially zero, and we argue that this is likely due to inherent positive correlations between the additive variance and other components of phenotypic variance. This means that heritabilities are unsuitable as measures of evolutionary potential in natural populations. More generally we argue that scaling always involves non-trivial assumptions, and that a lack of awareness of these assumptions constitutes a systemic error in the field of evolutionary biology.


Evolvability Heritability Genetic variance Quantitative genetics Measurement theory Scaling 



We thank the many participants in the measurement-theory discussion group at the University of Oslo during 2008 and 2009 for discussions of the topic of this paper. DH was supported in this research by a visiting professorship at CEES and TFH by grant #177857 from the Norwegian Research Council.

Supplementary material

11692_2011_9127_MOESM1_ESM.xls (346 kb)
Supplementary File S1: Excel sheet with data used in this study: The data are organized by study and species. We give a short description of the trait, which should allow identification in the original study. We give classification of the trait and its scale type as described in the main text. We classify the organisms involved into some very general categories. The column “measure” indicates the type of estimate of additive genetic variance that was used. Finally, we indicate if any traits from the study were not used with the same coded reason as explained in the supplementary file S2. We report estimates with three decimal digits and at least two significant digits, but this should not be taken as an indication of the true number of significant digits, which was often impossible to discern. The column "Ie" gives the mean-scaled residual variance computed as explained in the main text, and should not be mistaken for residual or environmental variance reported in the original study. (XLS 345 kb)
11692_2011_9127_MOESM2_ESM.doc (66 kb)
Supplementary file S2: List of studies of quantitative genetic variation published in Evolution and Journal of Evolutionary Biology from 1992-2009 that are not included in our database (S1). For each paper we indicate the reason we could not include it. This is divided into five categories: 1. MBS: Missing basic statistics. This means that we could not find sufficient basic statistics necessary to compute evolvabilities or heritabilities, or that some necessary numbers were given with only a single significant digit (but we did include variance and heritability estimates given as “0”). 2. IS: Incompatible scales: Information to compute heritability and evolvability were given, but not on the same scale (e.g. heritabilities were reported for log-transformed traits). 3. NST: Not suitable scale type: Traits were on a scale type that did not allow mean or variance standardization (e.g. interval scales on which means are not meaningful). 4. IIM: Incomplete or inconsistent methods: This includes cases where we could not find sufficient information to be sure what the reported numbers represented (e.g. the scale of reported numbers was unclear), or cases where there were inconsistencies in the reported method or results (e.g. alternative ways of computing the same statistics gave different results and we could not locate the error). 5. DG: Different groups: The necessary statistics were not given for the same groups of individuals (e.g. we did not compute evolvabilities based on trait means calculated for a different population than the one in which the additive variance was estimated). The papers we considered were found based on reading titles and abstracts of every original research paper published in the two journals in the given period, and then further checking those that gave some indication of being a quantitative genetics study. Due to the large number of papers we needed to check, we could not spend a long time to resolve apparent problems and inconsistencies. We excluded many studies and traits were we had doubts as to exactly what had been done or reported, and have excluded some data that might have been included after more careful considerations or consultation with authors. We apologize for such omissions. Also, the exclusion of data does not imply that there was anything wrong with the study, as the studies we consulted often had different goals that did not necessitate the types of statistics and information that we required. We hope that this list can be of use for other surveys of quantitative genetic information. (DOC 66 kb)
11692_2011_9127_MOESM3_ESM.pdf (351 kb)
Supplementary Figure 1: Plot of heritability against evolvability for narrow-sense estimates only (excluding negative estimates). The correlation is 0.09 ± 0.02 for positive values. (PDF 350 kb)
11692_2011_9127_MOESM4_ESM.pdf (176 kb)
Supplementary Figure 2: Plot of heritability against “evolvability” for full-sib estimates only (excluding negative estimates). The correlation is 0.23 ± 0.05 for positive values. (PDF 175 kb)
11692_2011_9127_MOESM5_ESM.pdf (206 kb)
Supplementary Figure 3: Plot of heritability against “evolvability” for broad-sense estimates only (excluding negative estimates). The correlation is 0.14 ± 0.07 for positive values. (PDF 206 kb)
11692_2011_9127_MOESM6_ESM.pdf (231 kb)
Supplementary Figure 4: Plot of narrow-sense heritability against evolvability for linear size traits (excluding negative estimates). The correlation is 0.01 ± 0.05 for positive values. (PDF 230 kb)


  1. Agrawal, A. A., Conner, J. K., Johnson, M. T. J., & Wallsgrove, R. (2002). Ecological genetics of an induced plant defence against herbivores: Additive genetic variance and costs of phenotypic plasticity. Evolution, 56, 2206–2213.PubMedGoogle Scholar
  2. Agrawal, A. F., & Stinchcombe, J. R. (2009). How much do genetic covariances alter the rate of adaptation. Proceedings of the Royal Society B: Biological Sciences, 276, 1182–1191.CrossRefGoogle Scholar
  3. Arnold, S. J., Pfrender, M. E., & Jones, A. G. (2001). The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica, 112(113), 9–32.PubMedCrossRefGoogle Scholar
  4. Arnold, S. J., & Phillips, P. C. (1999). Hierarchical comparison of genetic variance-covariance matrices. II. Coastal-inland divergence in the garter snake, Thamnophis elegans. Evolution, 53, 1516–1527.CrossRefGoogle Scholar
  5. Ashman, T. L. (2003). Constraints on the evolution of males and sexual dimorphism: Field estimates of genetic architecture of reproductive traits in three populations of gynodioecious Fragaria virginiana. Evolution, 57, 2012–2025.PubMedGoogle Scholar
  6. Asteles, P. A., Moore, A. J., & Preziosi, R. F. (2006). A comparison of methods to estimate cross-environment genetic correlations. Journal of Evolutionary Biology, 19, 114–122.CrossRefGoogle Scholar
  7. Bacigalupe, L. D., Nespolo, R. F., Bustamante, D. M., & Bozinovic, F. (2004). The quantitative genetics of sustained energy budget in a wild mouse. Evolution, 58, 421–429.PubMedGoogle Scholar
  8. Barton, N. H., & Turelli, M. (1989). Evolutionary quantitative genetics: how little do we know? Annual Review of Genetics, 23, 337–370.PubMedCrossRefGoogle Scholar
  9. Beraldi, D., Mcrae, A. F., Gratten, J., Slate, J., Visscher, P. M., & Pemberton, J. M. (2007). Mapping quantitative trait loci underlying fitness-related traits in a free-living sheep population. Evolution, 61, 1403–1416.PubMedCrossRefGoogle Scholar
  10. Berwaerts, K., Matthysen, E., & Van Dyck, H. (2008). Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: A quantitative genetic assessment. Evolution, 62, 2525–2533.PubMedCrossRefGoogle Scholar
  11. Birkhead, T. R., Pellatt, E. J., Matthews, I. M., Roddis, N. J., Hunter, F. M., McPhie, F., et al. (2006). Genic capture and the genetic basis of sexually selected traits in the zebra finch. Evolution, 60, 2389–2398.PubMedGoogle Scholar
  12. Blows, M. W. (2007). A tale of two matrices: Multivariate approaches in evolutionary biology. Journal of Evolutionary Biology, 20, 1–8.PubMedCrossRefGoogle Scholar
  13. Blows, M. W., Chenoweth, S. F., & Hine, E. (2004). Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. The American Naturalist, 163, 329–340.PubMedCrossRefGoogle Scholar
  14. Blows, M. W., & Higgie, M. (2003). Genetic constraints on the evolution of mate recognition under natural selection. The American Naturalist, 161, 240–253.PubMedCrossRefGoogle Scholar
  15. Blows, M. W., & Hoffmann, A. A. (2005). A reassessment of genetic limits to evolutionary change. Ecology, 86, 1371–1384.CrossRefGoogle Scholar
  16. Blows, M. W., & Walsh, B. (2009). Spherical cows grazing in flatland: Constraints to selection and adaptation. In J. Vanderwerf, H. U. Graser, R. Frankham, & C. Gondro (Eds.), Adaptation and fitness in animal populations – evolutionary and breeding perspectives on genetic resource management. Berlin: Springer.Google Scholar
  17. Boake, C. R. B., & Konigsberg, L. (1998). Inheritance of male courtship behavior, aggressive success, and body size in Drosophila silvestris. Evolution, 52, 1487–1492.CrossRefGoogle Scholar
  18. Brandt, L. S. E., & Greenfield, M. D. (2004). Condition-dependent traits and the capture of genetic variance in male advertisement song. Journal of Evolutionary Biology, 17, 821–828.PubMedCrossRefGoogle Scholar
  19. Brodie, E. D. (1993). Homogeneity of the genetic variance-covariance matrix for antipredator traits in 2 natural-populations of the garter snake Thamnophis ordinoides. Evolution, 47, 844–854.CrossRefGoogle Scholar
  20. Brookfield, J. F. Y. (2009). Evolution and evolvability: Celebration Darwin 200. Biology Letters, 5, 44–46.PubMedCrossRefGoogle Scholar
  21. Bryant, E. H., & Meffert, L. M. (1995). An analysis of selectional response in relation to a population bottleneck. Evolution, 49, 626–634.CrossRefGoogle Scholar
  22. Bürger, R. (2000). The mathematical theory of selection, recombination, and mutation. Chichester: Wiley.Google Scholar
  23. Burton, G. W. (1952). Quantitative inheritance in grasses. Proceedings of the Sixth International Grassland Congress, 6, 277–283.Google Scholar
  24. Cadee, N. (2000). Genetic and environmental effects on morphology and fluctuating asymmetry in nestling barn swallows. Journal of Evolutionary Biology, 13, 359–370.CrossRefGoogle Scholar
  25. Campbell, D. R. (1996). Evolution of floral traits in a hermaphroditic plant: Field measurements of heritabilities and genetic correlations. Evolution, 50, 1442–1453.CrossRefGoogle Scholar
  26. Campbell, D. R. (1997). Genetic and environmental variation in life-history traits of a monocarpic perennial: A decade-long field experiment. Evolution, 51, 373–382.CrossRefGoogle Scholar
  27. Carter, A. J. R., Hermisson, J., & Hansen, T. F. (2005). The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theoretical Population Biology, 68, 179–196.PubMedCrossRefGoogle Scholar
  28. Caruso, C. M. (2004). The quantitative genetics of floral trait variation in Lobelia: Potential constraints on adaptive evolution. Evolution, 58, 732–740.PubMedGoogle Scholar
  29. Caruso, C. M., Maherali, H., Mikulyuk, A., Carlson, K., & Jackson, R. B. (2005). Genetic variance and covariance for physiological traits in Lobelia: Are there constraints on adaptive evolution? Evolution, 59, 826–837.PubMedGoogle Scholar
  30. Charmantier, A., Kruuk, L. E. B., Blondel, J., & Lambrechts, M. M. (2004a). Testing for microevolution in body size in three blue tit populations. Journal of Evolutionary Biology, 17, 732–743.PubMedCrossRefGoogle Scholar
  31. Charmantier, A., Kruuk, L. E. B., & Lambrechts, M. M. (2004b). Parasitism reduces the potential for evolution in a wild bird population. Evolution, 58, 203–206.PubMedGoogle Scholar
  32. Cheetham, A. H., Jackson, J. B. C., & Hayek, L. A. C. (1993). Quantitative genetics of bryozoan phenotypic evolution. 1. Rate tests for random change versus selection in differentiation of living species. Evolution, 47, 1526–1538.CrossRefGoogle Scholar
  33. Cheetham, A. H., Jackson, J. B. C., & Hayek, L. A. C. (1994). Quantitative genetics of bryozoan phenotypic evolution. 2. Analysis of selection and random change in fossil species using reconstructed genetic-parameters. Evolution, 48, 360–375.CrossRefGoogle Scholar
  34. Chenoweth, S. F., Rundle, H. D., & Blows, M. W. (2010). The contribution of selection and genetic constraints to phenotypic divergence. The American Naturalist, 175, 186–196.PubMedCrossRefGoogle Scholar
  35. Cheverud, J. (1996). Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology, 9, 5–42.CrossRefGoogle Scholar
  36. Coltman, D. W., O’Donoghue, P., Hogg, J. T., & Festa-Bianchet, M. (2005). Selection and genetic (CO) variance in bighorn sheep. Evolution, 59, 1372–1382.PubMedGoogle Scholar
  37. Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K., & Pemberton, J. M. (2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution, 55, 2116–2125.PubMedGoogle Scholar
  38. Conner, J. K., Franks, R., & Stewart, C. (2003). Expression of additive genetic variances and covariances for wild radish floral traits: Comparison between field and greenhouse environments. Evolution, 57, 487–495.PubMedGoogle Scholar
  39. Conner, J., & Via, S. (1993). Patterns of phenotypic and genetic correlations among morphological and life-history traits in wild radish, Raphanus raphanistrum. Evolution, 47, 704–711.CrossRefGoogle Scholar
  40. Cotter, S. C., Kruuk, L. E. B., & Wilson, K. (2004). Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology, 17, 421–429.PubMedCrossRefGoogle Scholar
  41. Czesak, M. E., & Fox, C. W. (2003a). Evolutionary ecology of egg size and number in a seed beetle: Genetic trade-off differs between environments. Evolution, 57, 1121–1132.PubMedGoogle Scholar
  42. Czesak, M. E., & Fox, C. W. (2003b). Genetic variation in male effects on female reproduction and the genetic covariance between the sexes. Evolution, 57, 1359–1366.PubMedGoogle Scholar
  43. de Visser, J. A. G. M., Hermisson, J., Wagner, G. P., Ancel Meyers, L., Bagheri-Chaichian, H., Blanchard, J., et al. (2003). Evolution and detection of genetic robustness. Evolution, 57, 1959–1972.PubMedCrossRefGoogle Scholar
  44. De Winter, A. J. (1992). The gentic basis and evolution of acoustic mate recognition in a Ribautodelphax planthopper (homoptera, Delphacidae) 1. The female call. Journal of Evolutionary Biology, 5, 249–265.CrossRefGoogle Scholar
  45. Estes, S., & Arnold, S. J. (2007). Resolving the paradox of stasis: Models with stabilizing selection explain evolutionary divergence on all timescales. The American Naturalist, 169, 227–244.PubMedCrossRefGoogle Scholar
  46. Evanno, G., Castella, E., & Coudet, J. (2006). Evolutionary aspects of population structure for molecular and quantitative traits in the freshwater snail Radix balthica. Journal of Evolutionary Biology, 19, 1071–1072.PubMedCrossRefGoogle Scholar
  47. Evans, A. S., & Marshall, M. (1996). Developmental instability in Brassica compestris (Cruciferae): Fluctuating asymmetry of foliar and floral traits. Journal of Evolutionary Biology, 9, 717–736.CrossRefGoogle Scholar
  48. Evans, M. R., Roberts, M. L., Buchanan, K. L., & Goldsmith, A. R. (2006). Heritabilty of corticosterone response and changes in life history traits during selection in the zebra finch. Journal of Evolutionary Biology, 19, 343–352.PubMedCrossRefGoogle Scholar
  49. Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics (4th ed.). UK: Longman.Google Scholar
  50. Feldman, M. W., & Lewontin, R. C. (1975). The heritability hang-up. Science, 190, 1163–1168.PubMedCrossRefGoogle Scholar
  51. Fenster, C. B., & Carr, D. E. (1997). Genetics of sex allocation in mimulus (Scrophulariaceae). Journal of Evolutionary Biology, 10, 641–661.CrossRefGoogle Scholar
  52. Fernandez, J., Rodriguez-Ramilo, S. T., Perez-Figueroa, A., Lopez-Fanjul, C., & Caballero, A. (2003). Lack of nonadditive genetic effects on early fecundity in Drosophila melanogaster. Evolution, 57, 558–565.PubMedGoogle Scholar
  53. Fisher, R. A. (1951). Limits to intensive production in animals. British Agriculture Bulletin, 4, 217–218.Google Scholar
  54. Fox, C. W. (1993). A quantitative genetic-analysis of oviposition preference and larval performance on 2 hosts in the bruchid beetle, Callosobruchus maculatus. Evolution, 47, 166–175.CrossRefGoogle Scholar
  55. Fox, C. W., Czesak, M. E., Mousseau, T. A., & Roff, D. A. (1999). The evolutionary genetics of an adaptive maternal effect: Egg size plasticity in a seed beetle. Evolution, 53, 552–560.CrossRefGoogle Scholar
  56. Friberg, U., Lew, T. A., Byrne, P. G., & Rice, W. R. (2005). Assessing the potential for an ongoing arms race within and between the sexes: Selection and heritable variation. Evolution, 59, 1540–1551.PubMedGoogle Scholar
  57. Futuyma, D. J. (2010). Evolutionary constraint and ecological consequences. Evolution, 64, 1865–1884.PubMedCrossRefGoogle Scholar
  58. Garant, D., Sheldon, B. C., & Gustafsson, L. (2004). Climatic and temporal effects on the expression of secondary sexual characters: Genetic and environmental components. Evolution, 58, 634–644.PubMedGoogle Scholar
  59. Garcia-Gonzales, F., & Simmons, L. W. (2005). The evolution of polyandry: Intrinsic sire effects contribute to embryo viability. Journal of Evolutionary Biology, 18, 1097–1103.CrossRefGoogle Scholar
  60. Gardner, K. M., & Latta, R. G. (2008). Heritable variation and genetic correlation of quantitative traits within and between ecotypes of Avena barbata. Journal of Evolutionary Biology, 21, 737–748.PubMedCrossRefGoogle Scholar
  61. Gomez, J. M., Abdelaziz, M., Munoz-Pajares, J., & Perfectti, F. (2009). Heritability and genetic correlation of corolla shape and size in Erysimum mediohispanicum. Evolution, 63, 1820–1831.PubMedCrossRefGoogle Scholar
  62. Gomez-Mestre, I., Touchon, J. C., Caccoccio, V. L., & Warkentin, K. M. (2008). Genetic variation in pathogen-induced early hatching of toad embryos. Journal of Evolutionary Biology, 21, 791–800.PubMedCrossRefGoogle Scholar
  63. Gomulkiewicz, R., & Houle, D. (2009). Demographic and genetic constraints on evolution. The American Naturalist, 174, E218–E229.PubMedCrossRefGoogle Scholar
  64. Gould, S. J. (1981). The mismeasure of man. Baskerville: Pelican Books.Google Scholar
  65. Grabowski, M. W., Polk, J. D., & Roseman, C. C. (2011). Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism. Evolution, 65, 1336–1356.PubMedCrossRefGoogle Scholar
  66. Gray, D. A., & Cade, W. H. (1999). Quantitative genetics of sexual selection in the field cricket, Gryllus integer. Evolution, 53, 848–854.CrossRefGoogle Scholar
  67. Groeters, F. R., & Dingle, H. (1996). Heritability of wing length in nature for the milkweed bug, Oncopeltus fasciatus. Evolution, 50, 442–447.CrossRefGoogle Scholar
  68. Hallgrimsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36, 355–376.CrossRefGoogle Scholar
  69. Han, K. P., & Lincoln, D. E. (1994). The evolution of carbon allocation to plant secondary metabolites—a genetic-analysis of cost in Diplacus aurantiacus. Evolution, 48, 1550–1563.CrossRefGoogle Scholar
  70. Hansen, T. F. (2003). Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems, 69, 83–94.PubMedCrossRefGoogle Scholar
  71. Hansen, T. F. (2006). The evolution of genetic architecture. Annual Review of Ecology, Evolution and Systematics, 37, 123–157.CrossRefGoogle Scholar
  72. Hansen, T. F., Alvarez-Castro, J. M., Carter, A. J. R., Hermisson, J., & Wagner, G. P. (2006). Evolution of genetic architecture under directional selection. Evolution, 60, 1523–1536.PubMedGoogle Scholar
  73. Hansen, T. F., Armbruster, W. S., Carlson, M. L., & Pélabon, C. (2003a). Evolvability and genetic constraint in Dalechampia blossoms: Genetic correlations and conditional evolvability. Journal of Experimental Zoology, 296B, 23–39.CrossRefGoogle Scholar
  74. Hansen, T. F., & Houle, D. (2004). Evolvability, stabilizing selection, and the problem of stasis. In M. Pigliucci & K. Preston (Eds.), Phenotypic integration: Studying the ecology and evolution of complex phenotypes. Oxford: Oxford University press.Google Scholar
  75. Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.PubMedCrossRefGoogle Scholar
  76. Hansen, T. F., Pélabon, C., Armbruster, W. S., & Carlson, M. L. (2003b). Evolvability and genetic constraint in Dalechampia blossoms: Components of variance and measures of evolvability. Journal of Evolutionary Biology, 16, 754–765.PubMedCrossRefGoogle Scholar
  77. Hansen, T. F., & Wagner, G. P. (2001). Modeling genetic architecture: A multilinear model of gene interaction. Theoretical Population Biology, 59, 61–86.PubMedCrossRefGoogle Scholar
  78. Hawthorne, D. J. (1997). Ecological history and evolution in a novel environment: Habitat heterogeneity and insect adaptation to a new host. Evolution, 51, 153–162.CrossRefGoogle Scholar
  79. Hegyi, G., Torok, J., & Toth, L. (2002). Qualitative population divergence in proximate determination of a sexually selected trait in the collared flycatcher. Journal of Evolutionary Biology, 15, 710–719.CrossRefGoogle Scholar
  80. Hendrickx, F., Maelfait, J. P., & Lens, L. (2008). Effect of metal stress on life history divergence and quantitative genetic architecture in a wolf spider. Journal of Evolutionary Biology, 21, 183–193.PubMedGoogle Scholar
  81. Hendrikse, J. L., Parsons, T. E., & Hallgrimsson, B. (2007). Evolvability as the proper focus of evolutionary developmental biology. Evolution & Development, 9, 393–401.CrossRefGoogle Scholar
  82. Hereford, J., Hansen, T. F., & Houle, D. (2004). Comparing strengths of directional selection: How strong is strong? Evolution, 58, 2133–2143.PubMedGoogle Scholar
  83. Hoffman, E. A., Mobley, K. B., & Jones, A. G. (2006). Male pregnancy and the evolution of body segmentation in seahorses and pipefishes. Evolution, 60, 404–410.PubMedGoogle Scholar
  84. Hoffmann, A. A., & Schiffer, M. (1998). Changes in the heritability of five morphological traits under combined environmental stresses in Drosophila melanogaster. Evolution, 52, 1207–1212.CrossRefGoogle Scholar
  85. Horne, T. J., & Ylönen, H. (1998). Heritabilities of dominance-related traits in male bank voles (Clethrionomys glareolus). Evolution, 52, 894–899.CrossRefGoogle Scholar
  86. Houle, D. (1992). Comparing evolvability and variability of quantitative traits. Genetics, 130, 195–204.PubMedGoogle Scholar
  87. Houle, D. (1998). How should we explain variation in the genetic variance of traits? Genetica, 102(103), 241–253.PubMedCrossRefGoogle Scholar
  88. Houle, D. (2001). Characters as the units of evolutionary change. In G. P. Wagner (Ed.), The character concept in evolutionary biology. Massachusetts: Academic press.Google Scholar
  89. Houle, D., Morikawa, B., & Lynch, M. (1996). Comparing mutational variabilities. Genetics, 143, 1467–1483.PubMedGoogle Scholar
  90. Houle, D., Pélabon, C., Wagner, G. P., & Hansen, T. F. (2011). Measurement and meaning in biology. The Quarterly Review of Biology, 86, 3–34.PubMedCrossRefGoogle Scholar
  91. House, C. M., Evans, G. M. V., Smiseth, P. T., Stamper, C. E., Walling, C. A., & Moore, A. J. (2008). The evolution of repeated mating in the burying beetle, Nicrophorus vespilloides. Evolution, 62, 2004–2014.PubMedCrossRefGoogle Scholar
  92. House, C. M., & Simmons, L. W. (2005). The evolution of male genitalia: patterns of genetic variation and covariation in the genital sclerites of the dung beetle Onthophagus taurus. Journal of Evolutionary Biology, 18, 1281–1292.PubMedCrossRefGoogle Scholar
  93. Hughes, K. A. (1995). The evolutionary genetics of male life-history characters in Drosophila melanogaster. Evolution, 49, 521–537.CrossRefGoogle Scholar
  94. Hunt, G. (2007). Evolutionary divergence in directions of high phenotypic variance in the Ostracode genus Poseidonamicus. Evolution, 61, 1560–1576.PubMedCrossRefGoogle Scholar
  95. Ivy, T. M. (2007). Good genes, genetic compatibility and the evolution of polyandry: Use of the diallel cross to address competing hypotheses. Journal of Evolutionary Biology, 20, 479–487.PubMedCrossRefGoogle Scholar
  96. Jacoby, R., & Glauberman, N. (1995). The bell curve debate: History, documents, opinions. New York: Times Books.Google Scholar
  97. Jensen, H., Sæther, B. E., Ringsby, T. H., Tufto, J., Griffith, S. G., & Ellegren, H. (2003). Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus). Journal of Evolutionary Biology, 16, 1296–1307.PubMedCrossRefGoogle Scholar
  98. Jensen, H., Steinsland, I., Ringsby, T. H., & Sæther, B. E. (2008). Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): The role of indirect selection within and between sexes. Evolution, 62, 1275–1293.PubMedCrossRefGoogle Scholar
  99. Jia, F. Y., Greenfield, M. D., & Collins, R. D. (2000). Genetic variance of sexually selected traits in waxmoths: Maintenance by genotype × environment interaction. Evolution, 54, 953–967.PubMedGoogle Scholar
  100. Johnson, M. T. J., Agrawal, A. A., Maron, J. L., & Salminen, J. P. (2009). Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. Journal of Evolutionary Biology, 22, 1295–1307.PubMedCrossRefGoogle Scholar
  101. Johnson, T., & Barton, N. (2005). Theoretical models of selection and mutation on quantitative traits. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 360, 1411–1425.PubMedCrossRefGoogle Scholar
  102. Juenger, T., & Bergelson, J. (2000). The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: Herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution, 54, 764–777.PubMedGoogle Scholar
  103. Kaczorowski, R. L., Juenger, T. E., & Holtsford, T. R. (2008). Heritability and correlation structure of nectar and floral morphology traits in Nicotiana alata. Evolution, 62, 1738–1750.PubMedCrossRefGoogle Scholar
  104. Karoly, K., & Conner, J. K. (2000). Heritable variation in a family-diagnostic trait. Evolution, 54, 1433–1438.PubMedGoogle Scholar
  105. Kause, A., Saloniemi, I., Haukioja, E., & Hanhimaki, S. (1999). How to become large quickly: Quantitative genetics of growth and foraging in a flush feeding lepidopteran larva. Journal of Evolutionary Biology, 12, 471–482.CrossRefGoogle Scholar
  106. Kause, A., Saloniemi, I., Morin, J. P., Haukioja, E., Hanhimaki, S., & Ruohomaki, K. (2001). Seasonally varying diet quality and the quantitative genetics of development time and body size in birch feeding insects. Evolution, 55, 1992–2001.PubMedGoogle Scholar
  107. Kellermann, V. M., van Heerwaarden, B., Hoffmann, A. A., & Sgro, C. M. (2006). Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution, 60, 1104–1108.PubMedCrossRefGoogle Scholar
  108. Ketola, T., & Kotiaho, J. S. (2009). Inbreeding, energy use and condition. Journal of Evolutionary Biology, 22, 770–781.PubMedCrossRefGoogle Scholar
  109. Kilpimaa, J., Van de Casteele, T., Jokinen, I., Mappes, J., & Alatalo, R. V. (2005). Genetic and environmental variation in antibody and T-cell mediated responses in the great tit. Evolution, 59, 2483–2489.PubMedGoogle Scholar
  110. Kirkpatrick, M. (2009). Patterns of quantitative genetic variation in multiple dimensions. Genetica, 136, 271–284.PubMedCrossRefGoogle Scholar
  111. Kobayashi, A., Tanaka, Y., & Shimada, M. (2003). Genetic variation of sex allocation in the parasitoid wasp Heterospilus prosopidis. Evolution, 57, 2659–2664.PubMedGoogle Scholar
  112. Koelwijn, H. P., & Hunscheid, M. P. H. (2000). Intraspecific variation in sex allocation in hermaphroditic Plantago coronopus (L.). Journal of Evolutionary Biology, 13, 302–315.CrossRefGoogle Scholar
  113. Kontiainen, P., Brommer, J. E., Karell, P., & Petiainen, H. (2008). Heritability, plasticity and canalization of Ural owl egg size in a cyclic environment. Journal of Evolutionary Biology, 21, 88–96.PubMedGoogle Scholar
  114. Kruuk, L. E. B., Slate, J., Pemberton, J. M., Brotherstone, S., Guinness, F., & Clutton-Brock, T. (2002). Antler size in red deer: Heritability and selection but no evolution. Evolution, 56, 1683–1695.PubMedGoogle Scholar
  115. Kruuk, L. E. B., Slate, J., Pemberton, J. M., & Clutton-Brock, T. H. (2003). Fluctuating asymmetry in a secondary sexual trait: no associations with individual fitness, environmental stress or inbreeding, and no heritability. Journal of Evolutionary Biology, 16, 101–113.PubMedCrossRefGoogle Scholar
  116. Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution, 30, 314–334.CrossRefGoogle Scholar
  117. Lande, R. (1977). On comparing coefficients of variation. Systematic Zoology, 26, 214–217.CrossRefGoogle Scholar
  118. Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain:body size allometry. Evolution, 33, 402–416.CrossRefGoogle Scholar
  119. Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37, 1210–1226.CrossRefGoogle Scholar
  120. Larsson, K. (1993). Inheritance of body size in the Barnacle Goose under different environmental conditions. Journal of Evolutionary Biology, 6, 195–208.CrossRefGoogle Scholar
  121. Lauteri, M., Pliura, A., Monteverdi, M. C., Brugnoli, E., Villani, F., & Eriksson, G. (2004). Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. Journal of Evolutionary Biology, 17, 1286–1296.PubMedCrossRefGoogle Scholar
  122. Layzer, D. (1974). Heritability analysis of IQ scores: Science or numerology? Science, 183, 1259–1266.PubMedCrossRefGoogle Scholar
  123. Le Galliard, J. F., Massot, M., Landys, M. M., Meylan, S., & Clobert, J. (2006). Ontogenetic sources of variation is sexual size dimorphism in a viviparous lizard. Journal of Evolutionary Biology, 19, 690–704.PubMedCrossRefGoogle Scholar
  124. Leamy, L. (1999). Heritability of directional and fluctuating asymmetry for mandibular characters in random-bred mice. Journal of Evolutionary Biology, 12, 146–155.CrossRefGoogle Scholar
  125. Lew, T. A., Morrow, E. H., & Rice, W. R. (2006). Standing genetic variance for female resistance to harm from males and its relationship to intralocus sexual conflict. Evolution, 60, 97–105.PubMedGoogle Scholar
  126. Linder, J. E., & Rice, W. R. (2005). Natural selection and genetic variation for female resistance to harm from males. Journal of Evolutionary Biology, 18, 568–575.PubMedCrossRefGoogle Scholar
  127. Long, T. A. F., Miller, P. M., Stewart, A. D., & Rice, W. R. (2009). Estimating heritability of female lifetime fecundity in a locally a adapted Drosophila melanogaster population. Journal of Evolutionary Biology, 22, 637–643.PubMedCrossRefGoogle Scholar
  128. Lynch, M., Pfrender, M., Spitze, K., Lehman, N., Hicks, J., Allen, D., et al. (1999). The quantitative and molecular genetic architecture of a subdivided species. Evolution, 53, 100–110.CrossRefGoogle Scholar
  129. Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative characters. Massachusetts: Sinauer.Google Scholar
  130. MacColl, A. D. C., & Hatchwell, B. J. (2003). Heritability of parental effort in a passerine bird. Evolution, 57, 2191–2195.PubMedGoogle Scholar
  131. Magalhaes, S., Fayard, J., Janssen, A., Carbonell, D., & Olivieiri, I. (2007). Adaptation in a spider mite population after long-term evolution on a single host plant. Journal of Evolutionary Biology, 20, 2016–2027.PubMedCrossRefGoogle Scholar
  132. Manier, M. K., Seyler, C. M., & Arnold, S. A. (2007). Adaptive divergence within and between ecotypes of the terrestrial garter snake, Thamnophis elegans, assessed with Fst—Qst comparisons. Journal of Evolutionary Biology, 20, 1705–1719.PubMedCrossRefGoogle Scholar
  133. Mappes, T., & Koskela, E. (2004). Genetic basis of the trade-off between offspring number and quality in the bank vole. Evolution, 58, 645–650.PubMedGoogle Scholar
  134. Marroig, G., & Cheverud, J. M. (2005). Size as a line of least evolutionary resistance: Diet and adaptive morphological radiation in New World monkeys. Evolution, 59, 1128–1142.PubMedGoogle Scholar
  135. Marroig, G., Shirai, L. T., Porto, A., de Oliveria, F. B., & De Conto, V. (2009). The evolution of modularity in the mammalian skull II: Evolutionary consequences. Evolutionary Biology, 36, 136–148.CrossRefGoogle Scholar
  136. Mazer, S. J., Delesalle, V. A., & Neal, P. R. (1999). Responses of floral traits to selection on primary sexual investment in Spergularia marina: The battle between the sexes. Evolution, 53, 717–731.CrossRefGoogle Scholar
  137. McAdam, A. G., & Boutin, S. (2003). Effects of food abundance on genetic and maternal variation in the growth rate of juvenile red squirrels. Journal of Evolutionary Biology, 16, 1249–1256.PubMedCrossRefGoogle Scholar
  138. McGuigan, K., & Blows, M. W. (2010). Evolvability of individual traits in a multivariate context: Patitioning the additive genetic variance into common and specific components. Evolution, 64, 1899–1911.PubMedGoogle Scholar
  139. McGuigan, K., Chenoweth, S. F., & Blows, M. W. (2005). Phenotypic divergence along lines of genetic variance. The American Naturalist, 165, 32–43.PubMedCrossRefGoogle Scholar
  140. Meffert, L. M., Hicks, S. K., & Regan, J. L. (2002). Nonadditive genetic effects in animal behavior. The American Naturalist, 160, S198–S213.PubMedCrossRefGoogle Scholar
  141. Merilä, J. (1997). Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution, 51, 526–536.CrossRefGoogle Scholar
  142. Merilä, J., & Gustafsson, L. (1993). Inheritance of size and shape in a natural population of collared flycatchers, Ficedula albicollis. Journal of Evolutionary Biology, 6, 375–395.CrossRefGoogle Scholar
  143. Merilä, J., & Sheldon, B. C. (1999). Genetic architecture of fitness and nonfitness traits: Empirical patterns and development of ideas. Heredity, 83, 103–109.PubMedCrossRefGoogle Scholar
  144. Merilä, J., Sheldon, B. C., & Ellegren, H. (1998). Quantitative genetics of sexual size dimorphism in the collared flycatcher, Ficedula albicollis. Evolution, 52, 870–876.CrossRefGoogle Scholar
  145. Messina, F. J., & Fry, J. D. (2003). Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. Journal of Evolutionary Biology, 16, 501–509.PubMedCrossRefGoogle Scholar
  146. Miller, B. L. W., & Sinervo, B. (2007). Heritable body size mediates apparent life-history trade-offs in a simultaneous hermaphrodite. Journal of Evolutionary Biology, 20, 1554–1562.PubMedCrossRefGoogle Scholar
  147. Milner, J. M., Pemberton, J. M., Brotherstone, S., & Albon, S. D. (2000). Estimating variance components and heritabilities in the wild: A case study using the “animal model” approach. Journal of Evolutionary Biology, 13, 804–813.CrossRefGoogle Scholar
  148. Mitteroecker, P., & Bookstein, F. (2007). The conceptual and statistical relationship between modularity and morphological integration. Systematic Biology, 56, 818–836.PubMedCrossRefGoogle Scholar
  149. Mitteroecker, P., & Bookstein, F. (2009). The ontogenetic trajectory of the phenotypic covariance matrix, with examples from craniofacial shape in rats and humans. Evolution, 63, 727–737.PubMedCrossRefGoogle Scholar
  150. Morrow, E. H., Leijon, A., & Meerupati, A. (2008). Hemiclonal analysis reveals significant genetic, environmental and genotype x environment effects on sperm size in Drosophila melanogaster. Journal of Evolutionary Biology, 21, 1692–1702.PubMedCrossRefGoogle Scholar
  151. Mousseau, T. A., & Roff, D. A. (1987). Natural selection and the heritability of fitness components. Heredity, 59, 181–197.PubMedCrossRefGoogle Scholar
  152. Nespolo, R. F., Bacigalupe, L. D., & Bozinovic, F. (2003). Heritability of energetics in a wild mammal, the leaf-eared mouse (Phyllotis darwini). Evolution, 57, 1679–1688.PubMedGoogle Scholar
  153. Nespolo, R. F., Bustamante, D. M., Bacigalupe, L. D., & Bozinovic, F. (2005). Quantitative genetics of bioenergetics and growth-related traits in the wild mammal, Phyllotis darwini. Evolution, 59, 1829–1837.PubMedGoogle Scholar
  154. Nilsson, J. Å., Åkesson, M., & Nilsson, J. F. (2009). Heritability of resting metabolic rate in a wild population of blue tits. Journal of Evolutionary Biology, 22, 1867–1874.PubMedCrossRefGoogle Scholar
  155. Noach, E. J. K., de Jong, G., & Scharloo, W. (1996). Phenotypic plasticity in morphological traits in two populations of Drosophila melanogaster. Journal of Evolutionary Biology, 9, 831–844.CrossRefGoogle Scholar
  156. ONeil, P. (1997). Natural selection on genetically correlated phenological characters in Lythrum salicaria L (Lythraceae). Evolution, 51, 267–274.CrossRefGoogle Scholar
  157. Ostrowski, M. F., Jarne, P., & David, P. (2002). A phallus for free? Quantitative genetics of sexual trade-offs in the snail Bulinus truncatus. Journal of Evolutionary Biology, 16, 7–16.CrossRefGoogle Scholar
  158. Palmer, A. R. (2000). Quasireplication and the contract of error: Lessons from sex ratios, heritabilities and fluctuating asymmetry. Annual Review of Ecology and Systematics, 31, 441–480.CrossRefGoogle Scholar
  159. Parker, T. H., & Garant, D. (2004). Quantitative genetics of sexually dimorphic traits and capture of genetic variance by a sexually-selected condition-dependent ornament in red junglefowl (Gallus gallus). Journal of Evolutionary Biology, 17, 1277–1285.PubMedCrossRefGoogle Scholar
  160. Pavlicev, M., Cheverud, J. M., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.CrossRefGoogle Scholar
  161. Pélabon, C., Hansen, T. F., Carlson, M. L., & Armbruster, W. S. (2004). Variational and genetic properties of developmental stability in Dalechampia scandens. Evolution, 58, 504–514.PubMedGoogle Scholar
  162. Pelletier, F., Reale, D., Garant, D., Coltman, D. W., & Festa-Bianchet, M. (2007). Selection on heritable seasonal phenotypic plasticity of body mass. Evolution, 61, 1969–1979.PubMedCrossRefGoogle Scholar
  163. Perez, A., & Garcia, C. (2002). Evolutionary responses of Drosophila melanogaster to selection at different larval densities: Changes in genetic variation, specialization and phenotypic plasticity. Journal of Evolutionary Biology, 15, 524–536.CrossRefGoogle Scholar
  164. Perry, G. M. L., Audet, C., Laplatte, B., & Bernatchez, L. (2004). Shifting patterns in genetic control at the embryo-alevin boundary in brook charr. Evolution, 58, 2002–2012.PubMedGoogle Scholar
  165. Pettay, J. E., Charmantier, A., Wilson, A. J., & Lummaa, V. (2008). Age-specific genetic and maternal effects in fecundity of preindustrial Finnish women. Evolution, 62, 2297–2304.PubMedCrossRefGoogle Scholar
  166. Platenkamp, G. A. J., & Shaw, R. G. (1992). Environmental and genetic constraints on adaptive population differentiation in Anthoxanthum odoratum. Evolution, 46, 341–352.CrossRefGoogle Scholar
  167. Platenkamp, G. A. J., & Shaw, R. G. (1993). Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution, 47, 540–555.CrossRefGoogle Scholar
  168. Podolsky, R. H., Shaw, R. G., & Shaw, F. H. (1997). Population structure of morphological traits in Clarkia dudleyana. II. Constancy of within-population genetic variance. Evolution, 51, 1785–1796.CrossRefGoogle Scholar
  169. Polak, M., & Starmer, W. T. (2001). The quantitative genetics of fluctuating asymmetry. Evolution, 55, 498–511.PubMedCrossRefGoogle Scholar
  170. Polly, D. (2008). Developmental dynamics and G-matrices: Can morphometric spaces be used to model phenotypic evolution? Evolutionary Biology, 35, 83–96.CrossRefGoogle Scholar
  171. Price, T., & Schluter, D. (1991). On the heritability of life-history traits. Evolution, 45, 853–861.CrossRefGoogle Scholar
  172. Radwan, J. (1998). Heritability of sperm competition success in the bulb mite, Rhizoglyphus robini. Journal of Evolutionary Biology, 11, 321–327.Google Scholar
  173. Rauter, C. M., & Moore, A. J. (2002). Evolutionary importance of parental care performance, food resources, and indirect genetic effects in a burying beetle. Journal of Evolutionary Biology, 15, 407–417.CrossRefGoogle Scholar
  174. Reale, D., Berteaux, D., McAdam, A. G., & Boutin, S. (2003). Lifetime selection on heritable life-history traits in a natural population of red squirrels. Evolution, 57, 2416–2423.PubMedGoogle Scholar
  175. Reale, D., & Festa-Bianchet, M. (2000). Mass-dependent reproductive strategies in wild bighorn ewes: A quantitative genetic approach. Journal of Evolutionary Biology, 13, 679–688.CrossRefGoogle Scholar
  176. Ritland, K., & Ritland, C. (1996). Inferences about quantitative inheritance based on natural population structure in the yellow monkey flower, Mimulus guttatus. Evolution, 50, 1074–1082.CrossRefGoogle Scholar
  177. Rodriguez, R. L., & Greenfield, M. D. (2003). Genetic variance and phenotypic plasticity in a component of female mate choice in an ultrasonic moth. Evolution, 57, 1304–1313.PubMedGoogle Scholar
  178. Roff, D. A. (1995). Antagonistic and reinforcing pleiotropy: A study of differences in development time in wing dimorphic insects. Journal of Evolutionary Biology, 8, 405–419.CrossRefGoogle Scholar
  179. Roff, D. A., & Mousseau, T. A. (1987). Quantitative genetics and fitness: Lessons from Drosophila. Heredity, 58, 103–118.PubMedCrossRefGoogle Scholar
  180. Rolff, J., Armitage, S. A. O., & Coltman, D. W. (2005). Genetic constraints and sexual dimorphism in immune defense. Evolution, 59, 1844–1850.PubMedGoogle Scholar
  181. Rønning, B., Jensen, H., Moe, B., & Bech, C. (2007). Basal metabolic rate: Heritability and genetic correlations with morphological traits in the zebra finch. Journal of Evolutionary Biology, 20, 1815–1822.PubMedCrossRefGoogle Scholar
  182. Routley, M. B., & Husband, B. C. (2005). Responses to selection on male-phase duration in Chamerion angustifolium. Journal of Evolutionary Biology, 18, 1050–1059.PubMedCrossRefGoogle Scholar
  183. Ryder, J. J., & Siva-Jothy, M. T. (2001). Quantitative genetics of immune function and body size in the house cricket, Acheta domesticus. Journal of Evolutionary Biology, 14, 646–653.CrossRefGoogle Scholar
  184. Sakai, A. K., Weller, S. G., Culley, T. M., Campbell, D. R., Dunbar-Wallis, A. K., & Andres, A. (2008). Sexual dimorphism and the genetic potential for evolution of sex allocation in the gynodioecious plant, Schiedea salicaria. Journal of Evolutionary Biology, 21, 18–29.PubMedGoogle Scholar
  185. Santos, M. (1996). Apparent directional selection of body size in Drosophila buzzatii: Larval crowding and male mating success. Evolution, 50, 2530–2535.CrossRefGoogle Scholar
  186. Santos, M. (2001). Fluctuating asymmetry is nongenetically related to mating success in Drosophila buzzatii. Evolution, 55, 2248–2256.PubMedGoogle Scholar
  187. Santos, M. (2002). Genetics of wing size asymmetry in Drosophila buzzatii. Journal of Evolutionary Biology, 15, 720–734.CrossRefGoogle Scholar
  188. Santos, M., Ruiz, A., Quezada-Diaz, J. E., Barbadilla, A., & Fontdevila, A. (1992). The evolutionary history of Drosophila buzzatii. XX. Positive phenotypic covariance between field adult fitness components and body size. Journal of Evolutionary Biology, 5, 403–422.CrossRefGoogle Scholar
  189. Sarkissian, T. S., & Harder, L. D. (2001). Direct and indirect responses to selection on pollen size in Brassica rapa L. Journal of Evolutionary Biology, 14, 456–468.CrossRefGoogle Scholar
  190. Schlichting, C. D., & Murren, C. J. (2004). Evolvability and the raw materials for adaptation. In Q. C. B. Cronk, J. Whitton, R. H. Ree, & I. E. P. Taylor (Eds.), Plant adaptation: Molecular genetics and ecology. Ottawa: NRC Research press.Google Scholar
  191. Schluter, D. (2000). The ecology of adaptive radiation. Oxford: Oxford university press.Google Scholar
  192. Sgro, C. M., & Hoffmann, A. A. (1998). Effects of temperature extremes on genetic variances for life history traits in Drosophila melanogaster as determined from parent-offspring comparisons. Journal of Evolutionary Biology, 11, 1–20.CrossRefGoogle Scholar
  193. Shaw, R. G., & Platenkamp, G. A. J. (1993). Quantitative genetics of response to competitors in Nemophila menziesii—a greenhouse study. Evolution, 47, 801–812.CrossRefGoogle Scholar
  194. Shaw, F. H., Shaw, R. G., Wilkinson, G. S., & Turelli, M. (1995). Changes in genetic variances and covariances, G whiz! Evolution, 49, 1260–1267.CrossRefGoogle Scholar
  195. Sherrard, M. E., Maherali, H., & Latta, R. G. (2009). Water stress alters the genetic architecture of functional traits associated with drought adaptation in Avena barbata. Evolution, 63, 702–715.PubMedCrossRefGoogle Scholar
  196. Simmons, L. W. (2003). The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sexy-sperm hypothesis. Journal of Evolutionary Biology, 16, 624–634.PubMedCrossRefGoogle Scholar
  197. Simmons, L. W., & Garcia-Gonzalez, F. (2007). Female crickets trade offspring viability for fecundity. Journal of Evolutionary Biology, 20, 1617–1623.PubMedCrossRefGoogle Scholar
  198. Simmons, L. W., & Kotiaho, J. S. (2002). Evolution of ejaculates: Patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution, 56, 1622–1631.PubMedGoogle Scholar
  199. Simons, A. M., Carriere, Y., & Roff, D. A. (1998). The quantitative genetics of growth in a field cricket. Journal of Evolutionary Biology, 11, 721–733.CrossRefGoogle Scholar
  200. Simons, A. M., & Johnston, M. O. (2006). Environmental and genetic sources of diversification in the timing of seed germination: Implications for the evolution of bet hedging. Evolution, 60, 2280–2292.PubMedGoogle Scholar
  201. Simons, A. M., & Roff, D. A. (1994). The effect of environmental variability on the heritabilities of traits of a field cricket. Evolution, 48, 1637–1649.CrossRefGoogle Scholar
  202. Steigenga, M. J., Zwaan, B. J., Brakefield, P. M., & Fischer, K. (2005). The evolutionary genetics of egg size plasticity in a butterfly. Journal of Evolutionary Biology, 18, 281–289.PubMedCrossRefGoogle Scholar
  203. Stinchcombe, J. R. (2005). Measuring natural selection on proportional traits: Comparisons of three types of selection estimates for resistance and susceptibility to herbivore damage. Evolutionary Ecology, 19, 363–373.CrossRefGoogle Scholar
  204. Stinchcombe, J. R., Agrawal, A. F., Hohenlohe, P. A., Arnold, S. J., & Blows, M. W. (2008). Estimating nonlinear selection gradients using quadratic regression coefficients: Double or nothing? Evolution, 62, 2435–2440.PubMedCrossRefGoogle Scholar
  205. Stirling, D. G., Reale, D., & Roff, D. A. (2002). Selection, structure and the heritability of behaviour. Journal of Evolutionary Biology, 15, 277–289.CrossRefGoogle Scholar
  206. Teplitsky, C., Mills, J. A., Yarrall, J. W., & Merila, J. (2009). Heritability of fitness components in a wild bird population. Evolution, 63, 716–726.PubMedCrossRefGoogle Scholar
  207. Theriault, V., Garant, D., Bernatchez, L., & Dodson, J. J. (2007). Heritability of life-history tactics and genetic correlation with body size in a natural population of brook charr (Salvelinus fontinalis). Journal of Evolutionary Biology, 20, 2266–2277.PubMedCrossRefGoogle Scholar
  208. Thessing, A., & Ekman, J. (1994). Selection on the genetical and environmental components of tarsal growth in juvenile willow tits (Parus montanus). Journal of Evolutionary Biology, 7, 713–726.CrossRefGoogle Scholar
  209. Thiede, D. A. (1998). Maternal inheritance and its effect on adaptive evolution: A quantitative genetic analysis of maternal effects in a natural plant population. Evolution, 52, 998–1015.CrossRefGoogle Scholar
  210. Thomas, M. L., & Simmons, L. W. (2008). Cuticular hydrocarbons are heritable in the cricket Teleogryllus oceanicus. Journal of Evolutionary Biology, 21, 801–806.PubMedCrossRefGoogle Scholar
  211. Tonsor, S. J., & Goodnight, C. J. (1997). Evolutionary predictability in natural populations: Do mating system and nonadditive genetic variance interact to affect heritabilities in Plantago lanceolata? Evolution, 51, 1773–1784.CrossRefGoogle Scholar
  212. Tucic, B., & Stojkovic, B. (2001). Shade avoidance syndrome in Picea moorika seedlings: A growth-room experiment. Journal of Evolutionary Biology, 14, 444–455.CrossRefGoogle Scholar
  213. Turelli, M. (1984). Heritable genetic variation via mutation-selection balance: Lerch’s zeta meets the abdominal bristle. Theoretical Population Biology, 25, 138–193.PubMedCrossRefGoogle Scholar
  214. Van Kleunen, M., & Ritland, K. (2004). Predicting evolution of floral traits associated with mating system in a natural plant population. Journal of Evolutionary Biology, 17, 1389–1399.PubMedCrossRefGoogle Scholar
  215. Van Tienderen, P. M. (2000). Elasticities and the link between demographic and evolutionary dynamics. Ecology, 81, 666–679.CrossRefGoogle Scholar
  216. Verhoeven, K. J. F., Biere, A., Nevo, E., & Van Damme, J. M. M. (2004). Differential selection of growth rate-related traits in wild barley, Hordeum spontaneum, in contrasting greenhouse nutrient environments. Journal of Evolutionary Biology, 17, 184–196.PubMedCrossRefGoogle Scholar
  217. Wagner, G. P. (1989). Multivariate mutation-selection balance with constrained pleiotropic effects. Genetics, 122, 223–234.PubMedGoogle Scholar
  218. Wagner, G. P., & Altenberg, L. (1996). Complex adaptations and evolution of evolvability. Evolution, 50, 967–976.CrossRefGoogle Scholar
  219. Wagner, G. P., Booth, G., & Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution, 51, 329–347.CrossRefGoogle Scholar
  220. Wagner, G. P., Pavlicev, M., & Cheverud, J. M. (2007). The road to modularity. Nature Reviews Genetics, 8, 921–931.PubMedCrossRefGoogle Scholar
  221. Walsh, B., & Blows, M. W. (2009). Abundant genetic variation + strong selection = multivariate genetic constraints: a geometric view of adaptation. Annual Review of Ecology, Evolution and Systematics, 40, 41–59.CrossRefGoogle Scholar
  222. Watkins, T. B. (2001). A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla. Evolution, 55, 1668–1677.PubMedGoogle Scholar
  223. Wayne, M. L., Hackett, J. B., & Mackay, T. F. C. (1997). Quantitative genetics of ovariole number in Drosophila melanogaster. 1. Segregating variation and fitness. Evolution, 51, 1156–1163.CrossRefGoogle Scholar
  224. Weber, S. L., & Scheiner, S. M. (1992). The genetics of phenotypic plasticity. IV. Chromosomal localization. Journal of Evolutionary Biology, 5, 109–120.CrossRefGoogle Scholar
  225. Weller, S. G., Sakai, A. K., Culley, T. M., Campbell, D. R., & Dunbar-Wallis, A. K. (2006). Predicting the pathway to wind pollination: heritabilities and genetic correlations of inflorescence traits associated with wind pollination in Schiedea salciaria (Caryophllaceae). Journal of Evolutionary Biology, 19, 331–342.PubMedCrossRefGoogle Scholar
  226. Willi, Y., van Buskirk, J., & Hoffmann, A. A. (2006). Limits to the adaptive potential of small populations. Annual Review of Ecology, Evolution and Systematics, 37, 433–458.CrossRefGoogle Scholar
  227. Wilson, A. J. (2008). Why h2 does not always equal VA/VP ? Journal of Evolutionary Biology, 21, 647–650.PubMedCrossRefGoogle Scholar
  228. Wilson, A. J., Coltman, D. W., Pemberton, J. M., Overall, A. D. J., Byrne, K. A., & Kruuk, L. E. B. (2005). Maternal genetic effects set the potential for evolution in a free-living vertebrate population. Journal of Evolutionary Biology, 18, 405–414.PubMedCrossRefGoogle Scholar
  229. Wilson, A. J., Hutchings, J. A., & Ferguson, M. M. (2003). Selective and genetic constraints on the evolution of body size in a stream-dwelling salmonid fish. Journal of Evolutionary Biology, 16, 584–594.PubMedCrossRefGoogle Scholar
  230. Windig, J. J. (1994). Reaction norms and the genetic basis of phenotypic plasticity in the wing patern of the butterfly Bicyclus anynana. Journal of Evolutionary Biology, 7, 665–695.CrossRefGoogle Scholar
  231. Winn, A. A. (2004). Natural selection, evolvability and bias due to environmental covariance in the field in an annual plant. Journal of Evolutionary Biology, 17, 1073–1083.PubMedCrossRefGoogle Scholar
  232. Woods, R. E., Hercus, M. J., & Hoffmann, A. A. (1998). Estimating the heritability of fluctuating asymmetry in field Drosophila. Evolution, 52, 816–824.CrossRefGoogle Scholar
  233. Worley, A. C., & Barrett, S. C. H. (2000). Evolution of floral display in Eichhornia paniculata (Pontederiaceae): genetic correlation between flower size and number. Journal of Evolutionary Biology, 14, 469–481.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Thomas F. Hansen
    • 1
    Email author
  • Christophe Pélabon
    • 2
  • David Houle
    • 3
  1. 1.Department of Biology, Centre for Ecological and Evolutionary SynthesisUniversity of OsloOsloNorway
  2. 2.Department of Biology, Centre for Conservation BiologyNorwegian University of Science and TechnologyTrondheimNorway
  3. 3.Department of Biological ScienceFlorida State UniversityTallahasseeUSA

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