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Genetics Research International
Volume 2012, Article ID 576303, 14 pages
http://dx.doi.org/10.1155/2012/576303
Review Article

Epigenetic Mechanisms Underlying Developmental Plasticity in Horned Beetles

Department of Biology, Indiana University, 915 E Third Street, Myers Hall 150, Bloomington, IN 47405-7107, USA

Received 13 September 2011; Accepted 5 December 2011

Academic Editor: Eveline Verhulst

Copyright © 2012 Sophie Valena and Armin P. Moczek. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Raff, The Shape of Life: Genes, Development, and the Evolution of Animal Form, University Of Chicago Press, 1996.
  2. M. J. West-Eberhard, Developmental Plasticity and Evolution, Oxford University Press, New York, NY, USA, 2003.
  3. B. Hallgrimsson and B. K. Hall, Epigenetics: Linking Genotype and Phenotype in Development and Evolution, University of California Press, 2011.
  4. D. W. Pfennig, M. A. Wund, E. C. Snell-Rood, T. Cruickshank, C. D. Schlichting, and A. P. Moczek, “Phenotypic plasticity's impacts on diversification and speciation,” Trends in Ecology and Evolution, vol. 25, no. 8, pp. 459–467, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. A. P. Moczek, S. Sultan, S. Foster et al., “The role of developmental plasticity in evolutionary innovation,” Proceedings of the Royal Society B, vol. 278, no. 1719, pp. 2705–2713, 2011. View at Publisher · View at Google Scholar
  6. S. L. Rutherford and S. Lindquist, “Hsp90 as a capacitor for morphological evolution,” Nature, vol. 396, no. 6709, pp. 336–342, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Specchia, L. Piacentini, P. Tritto et al., “Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons,” Nature, vol. 463, no. 7281, pp. 662–665, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Queitsch, T. A. Sangstert, and S. Lindquist, “Hsp90 as a capacitor of phenotypic variation,” Nature, vol. 417, no. 6889, pp. 618–624, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. L. E. Cowen and S. Lindquist, “Cell biology: Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi,” Science, vol. 309, no. 5744, pp. 2185–2189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Suzuki and H. F. Nijhout, “Evolution of a polyphenism by genetic accommodation,” Science, vol. 311, no. 5761, pp. 650–652, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. A. Wund, J. A. Baker, B. Clancy, J. L. Golub, and S. A. Foster, “A test of the "flexible stem" model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation,” American Naturalist, vol. 172, no. 4, pp. 449–462, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. E. C. Snell-Rood and A. P. Moczek, “Horns and the role of development in the evolution of beetle contests,” in Animal Contests, I. C. W. Hardy and M. Briffa, Eds., Cambridge University Press, Cambridge, UK, 2011. View at Google Scholar
  13. A. P. Moczek, “Phenotypic plasticity and the origins of diversity: a case study on horned beetles,” in Phenotypic Plasticity in Insects: Mechanisms and Consequences, T. Ananthakrishnan and D. Whitman, Eds., pp. 81–134, Science, Plymouth, UK, 2009. View at Google Scholar
  14. A. P. Moczek and D. J. Emlen, “Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes?” Animal Behaviour, vol. 59, no. 2, pp. 459–466, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Otronen, “The effect of body size on the outcome of fights in burying beetles (Nicrophorus),” Annales Zoologici Fennici, vol. 25, no. 2, pp. 191–201, 1988. View at Google Scholar · View at Scopus
  16. L. W. Simmons and D. J. Emlen, “No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius,” Journal of Evolutionary Biology, vol. 21, no. 5, pp. 1227–1235, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. N. L. Watson and L. W. Simmons, “Reproductive competition promotes the evolution of female weaponry,” Proceedings of the Royal Society B, vol. 277, no. 1690, pp. 2035–2040, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. P. Moczek, “The behavioral ecology of threshold evolution in a polyphenic beetle,” Behavioral Ecology, vol. 14, no. 6, pp. 841–854, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Shafiei, A. P. Moczek, and H. F. Nijhout, “Food availability controls the onset of metamorphosis in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae),” Physiological Entomology, vol. 26, no. 2, pp. 173–180, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. D. J. Emlen, J. Hunt, and L. W. Simmons, “Evolution of sexual dimorphism and male dimorphism in the expression of beetle horns: phylogenetic evidence for modularity, evolutionary lability, and constraint,” American Naturalist, vol. 166, no. 4, pp. S42–S68, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Paulian, “Le polymorphisme des males de Coleopteres,” in Exposes de Biometrie et Statistique Biologique IV. Actualites Scientifiques et Industrielles, G. Tessier, Ed., Hermann, Paris, France, 1935. View at Google Scholar
  22. J. L. Tomkins and L. W. Simmons, “Sperm competition games played by dimorphic male beetles: fertilization gains with equal mating access,” Proceedings of the Royal Society B, vol. 267, no. 1452, pp. 1547–1553, 2000. View at Google Scholar · View at Scopus
  23. L. W. Simmons and D. J. Emlen, “Evolutionary trade-off between weapons and testes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 44, pp. 16346–16351, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. L. W. Simmons, D. J. Emlen, and J. L. Tomkins, “Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles,” Evolution, vol. 61, no. 11, pp. 2684–2692, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. H. F. Nijhout and D. J. Emlen, “Developmental biology, evolution competition among body parts in the development and evolution of insect morphology,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 7, pp. 3685–3689, 1998. View at Google Scholar · View at Scopus
  26. A. P. Moczek and H. F. Nijhout, “Trade-offs during the development of primary and secondary sexual traits in a horned beetle,” American Naturalist, vol. 163, no. 2, pp. 184–191, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. D. J. Emlen, “Costs and the diversification of exaggerated animal structures,” Science, vol. 291, no. 5508, pp. 1534–1536, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. H. F. Parzer and A. P. Moczek, “Rapid antagonistic coevolution between primary and secondary sexual characters in horned beetles,” Evolution, vol. 62, no. 9, pp. 2423–2428, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. M. T. Siva-Jothy, “Mate securing tactics and the cost of fighting in the Japanese horned beetle, Allomyrina dichotoma L. (Scarabaeidae),” Journal of Ethology, vol. 5, no. 2, pp. 165–172, 1987. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Madewell and A. P. Moczek, “Horn possession reduces maneuverability in the horn-polyphenic beetle, Onthophagus nigriventris,” Journal of Insect Science, vol. 6, pp. 1–10, 2006. View at Google Scholar · View at Scopus
  31. A. P. Moczek, “Facultative paternal investment in the polyphenic beetle Onthophagus taurus: the role of male morphology and social context,” Behavioral Ecology, vol. 10, no. 6, pp. 641–647, 1999. View at Google Scholar · View at Scopus
  32. A. P. Moczek, “Horn polyphenism in the beetle Onthophagus taurus: larval diet quality and plasticity in parental investment determine adult body size and male horn morphology,” Behavioral Ecology, vol. 9, no. 6, pp. 636–641, 1998. View at Google Scholar · View at Scopus
  33. A. P. Moczek and J. Cochrane, “Intraspecific female brood parasitism in the dung beetle Onthophagus taurus,” Ecological Entomology, vol. 31, no. 4, pp. 316–321, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. B. L. Shepherd, H. D. Prange, and A. P. Moczek, “Some like it hot: body and weapon size affect thermoregulation in horned beetles,” Journal of Insect Physiology, vol. 54, no. 3, pp. 604–611, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. J. R. Verdú, A. Díaz, and E. Galante, “Thermoregulatory strategies in two closely related sympatric Scarabaeus species (Coleoptera: Scarabaeinae),” Physiological Entomology, vol. 29, no. 1, pp. 32–38, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. E. C. Snell-Rood, J. D. Van Dyken, T. Cruickshank, M. J. Wade, and A. P. Moczek, “Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity,” BioEssays, vol. 32, no. 1, pp. 71–81, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. E. C. Snell-Rood, A. Cash, M. V. Han, T. Kijimoto, J. Andrews, and A. P. Moczek, “Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn-polyphenic beetles,” Evolution, vol. 65, no. 1, pp. 231–245, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Kijimoto, J. Costello, Z. Tang, A. P. Moczek, and J. Andrews, “EST and microarray analysis of horn development in Onthophagus beetles,” BMC Genomics, vol. 10, article 1471, p. 504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. A. P. Moczek and D. J. Rose, “Differential recruitment of limb patterning genes during development and diversification of beetle horns,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 22, pp. 8992–8997, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Kijimoto, J. Andrews, and A. P. Moczek, “Programed cell death shapes the expression of horns within and between species of horned beetles,” Evolution and Development, vol. 12, no. 5, pp. 449–458, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. B. R. Wasik and A. P. Moczek, “Decapentaplegic (dpp) regulates the growth of a morphological novelty, beetle horns,” Development Genes and Evolution, vol. 221, no. 1, pp. 17–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. B. R. Wasik, D. J. Rose, and A. P. Moczek, “Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner,” Evolution and Development, vol. 12, no. 4, pp. 353–362, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. E. C. Snell-Rood and A. P. Moczek, “Insulin signaling as a mechanism underlying developmental plasticity and trait integration: the role of FOXO in a nutritional polyphenism,” Heredity. In review.
  44. T. Kijimoto, A. P. Moczek, and J. Andrews, “doublesex regulates morph-, sex-, and species-specific expression of beetle horns,” Nature Communications. In review.
  45. D. J. Emlen, Q. Szafran, L. S. Corley, and I. Dworkin, “Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’,” Heredity, vol. 97, no. 3, pp. 179–191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. A. P. Moczek, “On the origins of novelty in development and evolution,” BioEssays, vol. 30, no. 5, pp. 432–447, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. C. W. Whitfield, A. M. Cziko, and G. E. Robinson, “Gene expression profiles in the brain predict behavior in individual honey bees,” Science, vol. 302, no. 5643, pp. 296–299, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. J. K. Colbourne, M. E. Pfrender, D. Gilbert et al., “The ecoresponsive genome of Daphnia pulex,” Science, vol. 331, no. 6017, pp. 555–561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. J. D. Van Dyken and M. J. Wade, “The genetic signature of conditional expression,” Genetics, vol. 184, no. 2, pp. 557–570, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. J. P. Demuth and M. J. Wade, “Maternal expression increases the rate of bicoid evolution by relaxing selective constraint,” Genetica, vol. 129, no. 1, pp. 37–43, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Cruickshank and M. J. Wade, “Microevolutionary support for a developmental hourglass: gene expression patterns shape sequence variation and divergence in Drosophila,” Evolution and Development, vol. 10, no. 5, pp. 583–590, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. A. Brisson and S. V. Nuzhdin, “Rarity of males in pea aphids results in mutational decay,” Science, vol. 319, no. 5859, p. 58, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. D. Van Dyken and M. J. Wade, “The genetic signature of conditional expression,” Genetics, vol. 184, no. 2, pp. 557–570, 2010. View at Publisher · View at Google Scholar
  54. B. G. Hunt, L. Ometto, Y. Wurm et al., “Relaxed selection is a precursor to the evolution of phenotypic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 38, pp. 15936–15941, 2011. View at Publisher · View at Google Scholar
  55. A. Leichty, D. W. Pfennig, C. Jones, and K. S. Pfennig, “Relaxed genetic constraint is ancestral to the evolution of phenotypic plasticity,” Science. In review.
  56. J. H. Choi, T. Kijimoto, E. Snell-Rood et al., “Gene discovery in the horned beetle Onthophagus taurus,” BMC Genomics, vol. 11, no. 1, article 703, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. H. F. NIjhout, Insect Hormones, Princeton University Press, Princeton, NJ, USA, 1994.
  58. K. Hartfelder and D. J. Emlen, “Endocrine control of insect polyphenism,” Comprehensive Molecular Insect Science, vol. 3, pp. 652–702, 2004. View at Google Scholar
  59. D. J. Emlen and H. F. Nijhout, “Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae),” Journal of Insect Physiology, vol. 45, no. 1, pp. 45–53, 1999. View at Publisher · View at Google Scholar · View at Scopus
  60. A. P. Moczek and H. F. Nijhout, “Developmental mechanisms of threshold evolution in a polyphenic beetle,” Evolution and Development, vol. 4, no. 4, pp. 252–264, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. J. A. Shelby, R. Madewell, and A. P. Moczek, “Juvenile hormone mediates sexual dimorphism in horned beetles,” Journal of Experimental Zoology Part B, vol. 308, no. 4, pp. 417–427, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Cherbas and L. Cherbas, “Molecular aspects of ecdysteroid action,” in Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells, L. I. Gilbert, J. R. Tata, and B. G. Atkinson, Eds., pp. 175–221, Academic Press, San Diego, Calif, USA, 1996. View at Google Scholar
  63. A. J. Zera, “Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators,” Evolution and Development, vol. 9, no. 5, pp. 499–513, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. A. J. Zera, “The endocrine regulation of wing polymorphism in insects: state of the art, recent surprises, and future directions,” Integrative and Comparative Biology, vol. 43, no. 5, pp. 607–616, 2003. View at Google Scholar · View at Scopus
  65. A. J. Zera, T. Sanger, J. Hanes, and L. Harshman, “Purification and characterization of hemolymph juvenile hormone esterase from the cricket, Gryllus assimilis,” Archives of Insect Biochemistry and Physiology, vol. 49, no. 1, pp. 41–55, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. S. A. Ament, Y. Wang, and G. E. Robinson, “Nutritional regulation of division of labor in honey bees: toward a systems biology perspective,” Systems Biology and Medicine, vol. 2, no. 5, pp. 566–576, 2010. View at Google Scholar · View at Scopus
  67. G. V. Amdam and R. E. Page, “The developmental genetics and physiology of honeybee societies,” Animal Behaviour, vol. 79, no. 5, pp. 973–980, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. H. Gotoh, R. Cornette, S. Koshikawa et al., “Juvenile hormone regulates extreme mandible growth in male stag beetles,” PLoS ONE, vol. 6, no. 6, article e21139, 2011. View at Publisher · View at Google Scholar
  69. F. Simonnet and A. P. Moczek, “Conservation and diversification of gene function during mouthpart development in Onthophagus beetles,” Evolution and Development, vol. 13, no. 3, pp. 280–289, 2011. View at Publisher · View at Google Scholar
  70. J. H. Werren, S. Richards, C. A. Desjardins et al., “Functional and evolutionary insights from the genomes of three parasitoid nasonia species,” Science, vol. 327, no. 5963, pp. 343–348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Wang, M. Jorda, P. L. Jones et al., “Functional CpG methylation system in a social insect,” Science, vol. 314, no. 5799, pp. 645–647, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. T. K. Walsh, J. A. Brisson, H. M. Robertson et al., “A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum,” Insect Molecular Biology, vol. 19, no. 2, pp. 215–228, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. E. C. Snell-Rood, A. Troth, and A. P. Moczek, “DNA methylation as a mechanism of nutritional plasticity: insights from horned beetles,” Proceedings of the Royal Society. In review.
  74. A. Zemach, I. E. McDaniel, P. Silva, and D. Zilberman, “Genome-wide evolutionary analysis of eukaryotic DNA methylation,” Science, vol. 328, no. 5980, pp. 916–919, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. K. M. Glastad, B. G. Hunt, S. V. Yi, and M. A. Goodisman, “DNA methylation in insects: on the brink of the epigenomic era,” Insect Molecular Biology, vol. 20, no. 5, pp. 553–565, 2011. View at Publisher · View at Google Scholar
  76. E. Li and A. Bird, “DNA methylation in mammals,” in Epigenetics, C. D. Allis et al., Ed., CSHL Press, Cold Spring Harbor, NY, USA, 2007. View at Google Scholar
  77. M. M. Suzuki and A. Bird, “DNA methylation landscapes: provocative insights from epigenomics,” Nature Reviews Genetics, vol. 9, no. 6, pp. 465–476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. F. Lyko and R. Maleszka, “Insects as innovative models for functional studies of DNA methylation,” Trends in Genetics, vol. 27, no. 4, pp. 127–131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. T. M. Williams and S. B. Carroll, “Genetic and molecular insights into the development and evolution of sexual dimorphism,” Nature Reviews Genetics, vol. 10, no. 11, pp. 797–804, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. D. J. Emlen and C. E. Allen, “Genotype to phenotype: physiological control of trait size and scaling in insects,” Integrative and Comparative Biology, vol. 43, no. 5, pp. 617–634, 2003. View at Google Scholar · View at Scopus
  81. L. W. Simmons, J. L. Tomkins, and J. Hunt, “Sperm competition games played by dimorphic male beetles,” Proceedings of the Royal Society B, vol. 266, no. 1415, pp. 145–150, 1999. View at Publisher · View at Google Scholar · View at Scopus
  82. J. L. Tomkins and L. W. Simmons, “Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics,” Animal Behaviour, vol. 63, no. 5, pp. 1009–1016, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Beldade, A. R. Mateus, and R. A. Keller, “Evolution and molecular mechanisms of adaptive developmental plasticity,” Molecular Ecology, vol. 20, no. 7, pp. 1347–1363, 2011. View at Publisher · View at Google Scholar
  84. S. F. Gilbert and D. Epel, Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution, Sinauer Associates, Sunderland, Mass, USA, 2009.
  85. M. K. Skinner and C. Guerrero-Bosagna, “Environmental signals and transgenerational epigenetics,” Epigenomics, vol. 1, no. 1, pp. 111–117, 2009. View at Google Scholar
  86. R. L. Jirtle and M. K. Skinner, “Environmental epigenomics and disease susceptibility,” Nature Reviews Genetics, vol. 8, no. 4, pp. 253–262, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. L. J. Johnson and P. J. Tricker, “Epigenomic plasticity within populations: its evolutionary significance and potential,” Heredity, vol. 105, no. 1, pp. 113–121, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. K. J. Parsons and R. C. Albertson, “Roles for Bmp4 and CaM1 in shaping the jaw: evo-devo and beyond,” Annual Review of Genetics, vol. 43, pp. 369–388, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. J. S. Keogh, I. A. W. Scott, and C. Hayes, “Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes,” Evolution, vol. 59, no. 1, pp. 226–233, 2005. View at Google Scholar · View at Scopus
  90. A. P. Moczek, T. E. Cruickshank, and A. Shelby, “When ontogeny reveals what phylogeny hides: gain and loss of horns during development and evolution of horned beetles,” Evolution, vol. 60, no. 11, pp. 2329–2341, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. A. P. Moczek, “Pupal remodeling and the evolution and development of alternative male morphologies in horned beetles,” BMC Evolutionary Biology, vol. 7, article 151, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. A. P. Moczek and H. F. Nijhout, “Rapid evolution of a polyphenic threshold,” Evolution and Development, vol. 5, no. 3, pp. 259–268, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. D. J. Emlen, “Diet alters male horn allometry in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae),” Proceedings of the Royal Society B, vol. 264, no. 1381, pp. 567–574, 1997. View at Google Scholar · View at Scopus
  94. A. V. Badyaev, “Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect,” Philosophical Transactions of the Royal Society B, vol. 364, no. 1520, pp. 1125–1141, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Gerhart and M. Kirschner, “The theory of facilitated variation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 1, pp. 8582–8589, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. J. C. Gerhart and M. W. Kirschner, “Facilitated variation,” in Evolution: The Extended Synthesis, M. Pigliucci and B. G. Mueller, Eds., MIT Press, Cambridge, Mass, USA, 2010. View at Google Scholar
  97. A. P. Moczek, “Integrating micro- and macroevolution of development through the study of horned beetles,” Heredity, vol. 97, no. 3, pp. 168–178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  98. D. J. Emlen and H. F. Nijhout, “Hormonal control of male horn length dimorphism in Onthophagus taurus (Coleoptera: Scarabaeidae): a second critical period of sensitivity to juvenile hormone,” Journal of Insect Physiology, vol. 47, no. 9, pp. 1045–1054, 2001. View at Publisher · View at Google Scholar · View at Scopus