Epigenetic resolution of the 'curse of complexity' in adaptive evolution of complex traits

Journal of Physiology

Volumn 592, Issue 11, 2014, Pages 2251-2260

  Badyaev, Alexander V ^a  

^a University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ADAPTIVE EVOLUTION; ARTICLE; BIOLOGICAL TRAIT; CELL DIFFERENTIATION; CELL LINEAGE; EPIGENETICS; EVOLUTION; GENE LOSS; GENE SEQUENCE; GENOMICS; GENOTYPE; HUMAN; INHERITANCE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SOMATIC CELL; STEM CELL; ANIMAL; ECOSYSTEM; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETIC VARIABILITY; GENETICS; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; ECOSYSTEM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENETIC VARIATION;

EID: 84901497338     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.272625     Document Type: Article

References (83)

1. Adkins RM, Thomas F, Tylavsky FA & Krushkal J (2011). Parental ages and levels of DNA methylation in the newborn are correlated. BMC Med Genet 12, 47.
2. Badyaev AV (2007). Evolvability and robustness in colour displays: Bridging the gap between theory and data. Evol Biol 34, 61-71.
3. Badyaev AV (2008). Maternal effects as generators of evolutionary change: A reassessment. Ann N Y Acad Sci 1133, 151-161.
4. Badyaev AV (2011). Origin of the fittest: Link between emergent variation and evolutionary change as a critical question in evolutionary biology. Proc Biol Sci 278, 1921-1929.
5. Badyaev AV (2013). 'Homeostatic hitchhiking': a mechanism for the evolutionary retention of complex adaptations. Integr Comp Biol 53, 913-922.
6. Badyaev AV, Hamstra TL, Oh KP & Acevedo Seaman D (2006). Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proc Natl Acad Sci U S A 103, 14406-14411.
7. Badyaev AV & Uller T (2009). Parental effects in ecology and evolution: Mechanisms, processes, and implications. Philos Trans R Soc Lond B Biol Sci 364, 1169-1177.
8. Badyaev AV & Walsh JB (2014). Epigenetic processes and genetic architecture in character origination and evolution. In Quantitative Genetics in the Wild, ed. Charmantier A, Garant D & Kruuk LEB, pp. 177-189. Oxford University Press.
9. Baldwin JM (1902). Development and Evolution. Macmillan, New York.
10. Breen MS, Kemena C, Vlasov PK, Notredame C & Kondrashov FA (2012). Epistasis as the primary factor in molecular evolution. Nature 490, 535-538.
11. Carneiro M & Hartl DL (2010). Adaptive landscapes and protein evolution. Proc Natl Acad Sci U S A 107, 1747-1751.
12. Chetverikov SS (1926). On certain aspects of the evolutionary process from the standpoint of modern genetics. J Exp Biol A 2, 1-40.
13. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, Aicher W, Bühring H, Mattheus U, Mack A, Wagner HH, Minger S, Matzkies M, Reppel M, Hescheler J, Sievert K, Stenzl A & Skutella T (2008). Generation of pluripotent stem cells from adult human testis. Nature 456, 344-349.
14. Cortijo S, Wardenaar R, Colome-Tatche M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, Aury JM, Wincker P, Roudier F, Jansen RC, Colot V & Johannes F (2014). Mapping the epigenetic basis of complex traits. Science 343, 1145-1148.
15. Cowley DE & Atchley WR (1992). Quantitative genetic models for development, epigenetic selection and phenotypic evolution. Evolution 46, 495-518.
16. Darwin C (1859). The Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London.
17. Davidson EH (2006). The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Academic Press, San Diego.
18. Day T & Bonduriansky R (2011). A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am Nat 178, E18-E36.
19. de Vos MGJ, Poelwijk FJ, Battich N, Ndika JDT & Tans SJ (2013). Environmental dependence of genetic constraint. PLoS Genet 9, e1003580.
20. Dobzhansky T (1974). Chance and creativity in evolution. In Studies in the Philosophy of Biology, ed. Ayala F & Dobzhansky T, pp. 307-338. McMillan, London.
21. Draghi JA, Parsons TL, Wagner GP & Plotkin JB (2010). Mutational robustness can facilitate adaptation. Nature 463, 353-355.
22. Duckworth RA (2008). Adaptive dispersal strategies and the dynamics of a range expansion. Am Nat 172, S4-S17.
23. Duckworth RA (2009). Maternal effects and range expansion: A key factor in a dynamic process? Philos Trans R Soc Lond B Biol Sci 364, 1075-1086
24. Duckworth RA & Badyaev AV (2007). Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci U S A 104, 15017-15022.
25. Duckworth RA & Kruuk LEB (2009). Evolution of genetic integration between dispersal and colonization ability in a bird. Evolution 63, 968-977.
26. Espinosa-Soto C, Martin OC & Wagner A (2011). Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits. BMC Evol Biol 11, 5.
27. Feinberg AP & Irizarry RA (2010). Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc Natl Acad Sci U S A 107, Suppl. 1, 1757-1764.
28. Furrow RE & Feldman MW (2014). Genetic variation and the evolution of epigenetic regulation. Evolution 68, 673-683.
29. Gafni O, Weinberger L, Mansour AA, Manor YS, Chomsky E, Ben-Yosef D, Kalma Y, Viukov S, Maza I, Zviran A, Rais Y, Shipony Z, Mukamel Z, Krupalnik V, Zerbib M, Geula S, Caspi I, Schneir D, Shwartz T, Gilad S, Amann-Zalcenstein D, Benjamin S, Amit I, Tanay A, Massarwa R, Novershtern N & Hanna JH (2013). Derivation of novel human ground state naive pluripotent stem cells. Nature 504, 282-286.
30. Gavrilets S (2004). Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, NJ, USA.
31. Geoghegan JL & Spencer HG (2013a). The adaptive invasion of epialleles in a heterogeneous environment. Theor Popul Biol 88, 1-8.
32. Geoghegan JL & Spencer HG (2013b). Exploring epiallele stability in a population-epigenetic model. Theor Popul Biol 83, 136-144.
33. Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan K-K, Cheng C, Mu XJ, Khurana E, Rozowsky J, Alexander R, et al. (2012). Architecture of the human regulatory network derived from ENCODE data. Nature 489, 91-100.
34. Hamstra TL & Badyaev AV (2009). Comprehensive investigation of ectoparasite community and abundance across life history stages of avian host. J Zool 278, 91-99.
35. Helanterä H & Uller T (2010). The Price equation and extended inheritance. Philos Theor Biol 2, 1-17.
36. Huang S, Ernberg I & Kauffman S (2009). Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin Cell Dev Biol 20, 869-876.
37. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar S & Costsarelis G (2007). Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316-320.
38. Jablonka E (2001). The systems of inheritance. In Cycles of Contigency: Developmental Systems and Evolution, ed. Oyama S, Griffiths PE & Gray RD, pp. 99-116. MIT Press, Cambridge, MA, USA.
39. Jablonka E & Lamb MJ (2006). Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life. A Bradford Book.
40. Kauffman S & Levin S (1987). Towards a general theory of adaptive walks on rugged landscapes. J Theor Biol 128, 11-45.
41. Kauffman SA (1969). Metabolic stability and epigenesis in randomly constructed genetic nets. J Theor Biol 22, 437-467.
42. Kelsey G & Feil R (2013). New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos Trans R Soc Lond B Biol Sci 368, 20110336.
43. Kim K, Doi A, Wen B, Ng K, Zhao R, Cahan P, Kim J, Aryee MJ, Ji H, Ehrlich LIR, Yabuuchi A, Takeuchi A, Cunniff KC, Hongguang H, McKinney-Freeman S, Naveiras O, Yoon TJ, Irizarry RA, Jung N, Seita J, Hanna J, Murakami P, Jaenisch R, Weissleder R, Orkin SH, Weissman IL, Feinberg AP & Daley GQ (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
44. Klironomos FD, Berg J & Collins S (2013). How epigenetic mutations can affect genetic evolution: model and mechanism. BioEssays 35, 571-578.
45. Koonin EV (2011). The Logic of Chance: The Nature and Origin of Biological Evolution. FT Press Science.
46. Lynch M (2007). The Origins of Genome Architecture. Sinauer Associates, Sunderland, MA, USA.
47. Lynch M (2010). Scaling expectations for the time to establishment of complex adaptations. Proc Natl Acad Sci U S A 107, 16577-16582.
48. Lynch M & Abegg A (2010). The rate of establishment of complex adaptations. Mol Biol Evol 27, 1404-1414.
49. Lynch M & Walsh B (1998). Genetics and Analysis of Quantitative Traits. Sinauer Associates, Sunderland, MA, USA.
50. Maynard Smith J (1970). Natural selection and the concept of a protein space. Nature 225, 563-564.
51. Mayr E (1963). Animal Species and Evolution. Harvard University Press, Cambridge, MA, USA.
52. Mayr E & Provine WB (eds) (1980). The Evolutionary Synthesis: Perspectives on the Unification of Biology. Harvard University Press, Cambridge, MA, USA.
53. Mezentseva NV, Kumaratilake JS & Newman SA (2008). The brown adipocyte differentiation pathway in birds: an evolutionary road not taken. BMC Biol 6, 17.
54. Nakaki F, Hayashi K, Ohta H, Kurimoto K, Yabuta Y & Saitou M (2013). Induction of mouse germ-cell fate by transcription factors in vitro. Nature 501, 222-226.
55. Newman SA (2011). Thermogenesis, muscle hyperplasia, and the origin of birds. Bioessays 33, 653-656.
56. Newman SA (2012). Physico-genetic determinants in the evolution of development. Science 338, 217-219.
57. Newman SA, Mezentseva N & Badyaev AV (2013). Gene loss, thermogenesis and the origin of birds. Ann N Y Acad Sci 1289, 36-47.
58. Newman SA & Müller GB (2005). Origination and innovation in the vertebrate limb skeleton: an epigenetic perspective. J Exp Zool B Mol Dev Evol 304, 593-609.
59. Obokata H, Sasai Y, Niwa H, Kadota M, Andrabi M, Takata N, Tokoro M, Terashita Y, Yonemura S, Vacanti CA & Wakayama T (2014a). Bidirectional developmental potential in reprogrammed cells with acquired pluripotency. Nature 505, 676-680.
60. Obokata H, Wakayama T, Sasai Y, Kojima K, Vacanti MP, Niwa H, Yamato M & Vacanti CA (2014b). Stimulus-triggered fate conversion of somatic cells into pluripotency. Nature 505, 641-647.
61. Oyama S (2000). The Ontogeny of Information: Developmental Systems and Evolution. Duke University Press, Durham.
62. Poelwijk FJ, Kiviet DJ, Weinreich DM & Tans SJ (2007). Empirical fitness landscapes reveal accessible evolutionary paths. Nature 445, 383-386.
63. Rais Y, Zviran A, Geula S, Gafni O, Chomsky E, Viukov S, Mansour AA, Caspi I, Krupalnik V, Zerbib M, Maza I, Mor N, Baran D, Weinberger L, Jaitin DA, Lara-Astiaso D, Blecher-Gonen R, Shipony Z, Mukamel Z, Hagai T, Gilad S, Amann-Zalcenstein D, Tanay A, Amit I, Novershtern N & Hanna JH (2013). Deterministic direct reprogramming of somatic cells to pluripotency. Nature 502, 65-70.
64. Rando Thomas A & Chang Howard Y (2012). Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148, 46-57.
65. Roux F, Colome-Tatche M, Edelist C, Wardenaar R, Guerche P, Hospital F, Colot V, Jansen RC & Johannes F (2011). Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 188, 1015-1017.
66. Schmalhausen II (1938). Organism as a Whole in Individual Development and History. Academy of Sciences, USSR, Leningrad.
67. Schmalhausen II (1969). Problems of Darwinism. Nauka, Leningrad.
68. Siegal ML & Bergman A (2002). Waddington's canalization revisited: Developmental stability and evolution. Proc Natl Acad Sci U S A 99, 10528-10532.
69. Smallwood SA & Kelsey G (2012). De novo DNA methylation: a germ cell perspective. Trends Genet 28, 33-42.
70. Smith ZD & Meissner A (2013). DNA methylation: roles in mammalian development. Nat Rev Genet 14, 204-220.
71. Stebbins GL & Hartl DL (1988). Comparative evolution: Latent potentials for anagenetic advance. Proc Natl Acad Sci U S A 85, 5141-5145.
72. Tal O, Kisdi E & Jablonka E (2010). Epigenetic contribution to covariance between relatives. Genetics 184, 1037-1050.
73. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ & Natale DA (2003). The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4, 41.
74. Teschendorff AE, West J & Beck S (2013). Age-associated epigenetic drift: implications, and a case of epigenetic thrift? Hum Mol Genet 22, R7-R15.
75. Uller T (2013). Non-genetic inheritance and evolution. In Philosophy of Biology: A Companion for Educators, ed. Kampourakis K, pp. 267-287. Springer Verlag.
76. Uller T & Helanterä H (2014). Heredity and evolutionary theory. In Challenges to Evolutionary Theory, ed. Walsh H & Huneman, In press. Oxford University Press.
77. Waddington CH (1953). Genetic assimilation of an acquired character. Evolution 7, 119-127.
78. Wagner A (2011). The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems. Oxford University Press.
79. Wagner GP, Kenney-Hunt JP, Pavlicev M, Peck JR, Waxman D & Cheverud JM (2008). Pleiotropic scaling of gene effects and the 'cost of complexity'. Nature 452, 470-472.
80. Waxman D & Peck JR (1998). Pleiotropy and the preservation of perfection. Science 279, 1210-1213.
81. West-Eberhard MJ (2005). Phenotypic accommodation: adaptive innovation due to developmental plasticity. J Exp Zool B Mol Dev Evol 304, 610-618.
82. West J, Widschwendter M & Teschendorff AE (2013). Distinctive topology of age-associated epigenetic drift in the human interactome. Proc Natl Acad Sci U S A 110, 14138-14143.
83. Wolf YI, Novichkov PS, Karev GP, Koonin EV & Lipman DJ (2009). The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc Natl Acad Sci U S A 106, 7273-7280.