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Epigenetic Mechanisms Underlying Developmental Plasticity in Horned Beetles

DOI: 10.1155/2012/576303

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All developmental plasticity arises through epigenetic mechanisms. In this paper we focus on the nature, origins, and consequences of these mechanisms with a focus on horned beetles, an emerging model system in evolutionary developmental genetics. Specifically, we introduce the biological significance of developmental plasticity and summarize the most important facets of horned beetle biology. We then compare and contrast the epigenetic regulation of plasticity in horned beetles to that of other organisms and discuss how epigenetic mechanisms have facilitated innovation and diversification within and among taxa. We close by highlighting opportunities for future studies on the epigenetic regulation of plastic development in these and other organisms. 1. Introduction Organismal form and function emerge during ontogeny through complex interactions between gene products, environmental conditions, and ontogenetic processes [1, 2]. The causes, nature, and consequences of these interactions are the central foci of epigenetics [3]. Broadly, epigenetics seeks to understand how phenotypes emerge through developmental processes, and how that emergence is altered to enable evolutionary modification, radiation, and innovation. Epigenetic mechanisms can operate at any level of biological organization above the sequence level, from the differential methylation of genes to the somatic selection of synaptic connections and the integration of tissue types during organogenesis. Here, we take this inclusive definition of epigenetics and apply it to the phenomenon of developmental plasticity, defined as a genotype’s or individual’s ability to respond to changes in environmental conditions through changes in its phenotypes [4]. All developmental plasticity is, by definition, epigenetic in origin, as the genotype of the responding individual remains unaltered in the process. It is the nature, origins, and consequences of the underlying epigenetic mechanisms that we focus on in this review. We do so with specific reference to horned beetles, an emerging model system in evo-devo in general and the evolutionary developmental genetics of plasticity in particular. We begin our review with a general introduction to the concept of developmental plasticity. We then introduce our focal organisms, horned beetles, summarize the most relevant forms of plasticity that have evolved in these remarkable organisms, review what is known about the underlying epigenetic mechanisms, and highlight future research directions. Lastly, we discuss how studies in Onthophagus species could provide


[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.
[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.
[6]  S. L. Rutherford and S. Lindquist, “Hsp90 as a capacitor for morphological evolution,” Nature, vol. 396, no. 6709, pp. 336–342, 1998.
[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.
[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.
[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.
[10]  Y. Suzuki and H. F. Nijhout, “Evolution of a polyphenism by genetic accommodation,” Science, vol. 311, no. 5761, pp. 650–652, 2006.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[18]  A. P. Moczek, “The behavioral ecology of threshold evolution in a polyphenic beetle,” Behavioral Ecology, vol. 14, no. 6, pp. 841–854, 2003.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[27]  D. J. Emlen, “Costs and the diversification of exaggerated animal structures,” Science, vol. 291, no. 5508, pp. 1534–1536, 2001.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[46]  A. P. Moczek, “On the origins of novelty in development and evolution,” BioEssays, vol. 30, no. 5, pp. 432–447, 2008.
[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.
[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.
[49]  J. D. Van Dyken and M. J. Wade, “The genetic signature of conditional expression,” Genetics, vol. 184, no. 2, pp. 557–570, 2010.
[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.
[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.
[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.
[53]  J. D. Van Dyken and M. J. Wade, “The genetic signature of conditional expression,” Genetics, vol. 184, no. 2, pp. 557–570, 2010.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[86]  R. L. Jirtle and M. K. Skinner, “Environmental epigenomics and disease susceptibility,” Nature Reviews Genetics, vol. 8, no. 4, pp. 253–262, 2007.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.


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