Advertisement

Journal of Biosciences

, Volume 40, Issue 1, pp 159–204 | Cite as

Stochastic developmental variation, an epigenetic source of phenotypic diversity with far-reaching biological consequences

  • Günter Vogt
Review

Abstract

This article reviews the production of different phenotypes from the same genotype in the same environment by stochastic cellular events, nonlinear mechanisms during patterning and morphogenesis, and probabilistic self-reinforcing circuitries in the adult life. These aspects of phenotypic variation are summarized under the term ‘stochastic developmental variation’ (SDV) in the following. In the past, SDV has been viewed primarily as a nuisance, impairing laboratory experiments, pharmaceutical testing, and true-to-type breeding. This article also emphasizes the positive biological effects of SDV and discusses implications for genotype-to-phenotype mapping, biological individuation, ecology, evolution, and applied biology. There is strong evidence from experiments with genetically identical organisms performed in narrowly standardized laboratory set-ups that SDV is a source of phenotypic variation in its own right aside from genetic variation and environmental variation. It is obviously mediated by molecular and higher-order epigenetic mechanisms. Comparison of SDV in animals, plants, fungi, protists, bacteria, archaeans, and viruses suggests that it is a ubiquitous and phylogenetically old phenomenon. In animals, it is usually smallest for morphometric traits and highest for life history traits and behaviour. SDV is thought to contribute to phenotypic diversity in all populations but is particularly relevant for asexually reproducing and genetically impoverished populations, where it generates individuality despite genetic uniformity. In each generation, SDV produces a range of phenotypes around a well-adapted target phenotype, which is interpreted as a bet-hedging strategy to cope with the unpredictability of dynamic environments. At least some manifestations of SDV are heritable, adaptable, selectable, and evolvable, and therefore, SDV may be seen as a hitherto overlooked evolution factor. SDV is also relevant for husbandry, agriculture, and medicine because most pathogens are asexuals that exploit this third source of phenotypic variation to modify infectivity and resistance to antibiotics. Since SDV affects all types of organisms and almost all aspects of life, it urgently requires more intense research and a better integration into biological thinking.

Keywords

Clonal organisms development ecology epigenetics evolution genotype-to-phenotype mapping individuality infectivity and resistance phenotypic variation stochasticity 

Notes

Acknowledgements

The author is grateful to the following colleagues for providing pictures and information: Martin Ackermann (Zurich), Gregory S Archer (Davis), Gregory A Babitt (Rochester), Jürgen Berger and Ralf J Sommer (Tübingen), Brian Bagatto (Akron), John Daugman (Cambridge), Jan Dijksterhuis and Han Wösten (Utrecht), David Fenwick (Penzance), Theodore H Friend (College Station), Mikael Häggström (Uppsala), David S Haskell (Sewanee), John F Hasler (Bogart), Anil K Jain (East Lansing), Nikos C Kyrpides (Walnut Creek), Winfried Lampert (Plön), Eric C Lai (New York), David IK Martin (Oakland), Erskine L Palmer and Russell Regnery (Atlanta), Soo-Bong Park (Suwon), Jorge A Piedrahita (Raleigh), Pascal Radtke (Düsseldorf), George E Seidel Jr (Fort Collins), Michael R Strand (Athens), Stefano Tiozzo (Villefranche-sur-Mer), Rogier R van Vugt (Leiden), Larry Wadsworth and Mark Westhusin (College Station), and Alex Wild (Champaign-Urbana). Many thanks also to Vidyanand Nanjundiah (Bangalore) and an anonymous referee for constructive criticism and numerous suggestions that helped to improve the manuscript.

References

  1. Acar M, Mettetal JT and van Oudenaarden A 2008 Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40 471–475PubMedGoogle Scholar
  2. Ackermann M 2013 Microbial individuality in the natural environment. ISME J. 7 465–467PubMedCentralPubMedGoogle Scholar
  3. Ackermann H-W and Smirnoff WA 1983 A morphological investigation of 23 baculoviruses. J. Invertebr. Pathol. 41 269–280Google Scholar
  4. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt W-D and Doebeli M 2008 Self-destructive cooperation mediated by phenotypic noise. Nature 454 987–990PubMedGoogle Scholar
  5. Adam M, Murali B, Glenn NO and Potter SS 2008 Epigenetic inheritance based evolution of antibiotic resistance in bacteria. BMC Evol. Biol. 8 52PubMedCentralPubMedGoogle Scholar
  6. Adelman DE 2005 The false promise of the genomics revolution for environmental law. Harv. Environ. Law Rev. 29 117–178Google Scholar
  7. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, et al. 2012 The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59 429–493Google Scholar
  8. Ahluwalia JK, Hariharan M, Bargaje R, Pillai B and Brahmachari V 2009 Incomplete penetrance and variable expressivity: is there a microRNA connection? BioEssays 31 981–992PubMedGoogle Scholar
  9. Alwes F and Scholtz G 2006 Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev. Genes Evol. 216 169–184PubMedGoogle Scholar
  10. Ambrose SH 1998 Late Pleistocene human population bottlenecks, volcanic winter, and differentiation of modern humans. J. Hum. Evol. 34 623–651PubMedGoogle Scholar
  11. Angers B, Castonguay E and Massicotte R 2010 Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Mol. Ecol. 19 1283–1295PubMedGoogle Scholar
  12. Aranda-Anzaldo A and Dent MAR 2003 Developmental noise, ageing and cancer. Mech. Ageing Dev. 124 711–720PubMedGoogle Scholar
  13. Archer GS, Dindot S, Friend TH, Walker S, Zaunbrecher G, Lawhorn B and Piedrahita JA 2003a Hierarchical phenotypic and epigenetic variation in cloned swine. Biol. Reprod. 69 430–436PubMedCentralPubMedGoogle Scholar
  14. Archer GS, Friend TH, Piedrahita J, Nevill CH and Walker S 2003b Behavioral variation among cloned pigs. Appl. Anim. Behav. Sci. 82 151–161Google Scholar
  15. Arias AM and Hayward P 2005 Filtering transcriptional noise during development: concepts and mechanisms. Nat. Rev. Genet. 7 34–44Google Scholar
  16. Ariew A and Lewontin RC 2004 The confusions of fitness. Brit. J. Phil. Sci. 55 347–363Google Scholar
  17. Ashe A, Sapetschnig A, Weick E-M, Mitchell J, Bagijn MP, Cording AC, Doebley A-L, Goldstein LD, et al. 2012 piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150 88–99PubMedCentralPubMedGoogle Scholar
  18. Astauroff BL 1930 Analyse der erblichen Störungsfälle der bilateralen Symmetrie im Zusammenhang mit der selbständigen Variabilität ähnlicher Strukturen. Z. indukt. Abst. Vererbungsl. 55 183–262Google Scholar
  19. Avendaño MS, Leidy C and Pedraza JM 2013 Tuning the range and stability of multiple phenotypic states with coupled positive-negative feedback loops. Nat. Commun. 4 2605PubMedGoogle Scholar
  20. Avery SV 2006 Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4 577–587PubMedGoogle Scholar
  21. Avise JC 2008 Clonality: the genetics, ecology, and evolution of sexual abstinence in vertebrate animals (New York: Oxford University Press)Google Scholar
  22. Babbitt GA 2008 How accurate is the phenotype? – An analysis of developmental noise in a cotton aphid clone. BMC Dev. Biol. 8 19Google Scholar
  23. Bailey DW 1982 How pure are inbred strains of mice? Immunol. Today 3 210–214PubMedGoogle Scholar
  24. Bairu MW, Aremu AO and van Staden J 2011 Somaclonal variation in plants: causes and detection methods. Plant Growth Regul. 63 147–173Google Scholar
  25. Balaban NQ 2011 Persistence: mechanisms for triggering and enhancing phenotypic variability. Curr. Opin. Genet. Dev. 21 768–775PubMedGoogle Scholar
  26. Balázsi G, van Oudenaarden A and Collins JJ 2011 Cellular decision-making and biological noise: from microbes to mammals. Cell 144 910–925PubMedCentralPubMedGoogle Scholar
  27. Baldwin JM 1896 A new factor in evolution. Am. Nat. 30 441–451Google Scholar
  28. Bartel DP and Chen C-Z 2004 Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5 396–400PubMedGoogle Scholar
  29. Barthélémy D and Caraglio Y 2007 Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann. Bot. 99 375–407PubMedCentralPubMedGoogle Scholar
  30. Barton NH and Charlesworth B 1998 Why sex and recombination? Science 281 1986–1990PubMedGoogle Scholar
  31. Batada NN and Hurst LD 2007 Evolution of chromosome organization driven by selection for reduced gene expression noise. Nat. Genet. 39 945–949PubMedGoogle Scholar
  32. Beatty J 2006 Chance variation: Darwin on orchids. Philos. Sci. 73 629–641Google Scholar
  33. Beatty J 2010 Reconsidering the importance of chance variation; in Evolution: the extended synthesis (eds) M Pigliucci and GB Müller (Cambridge: MIT Press) pp 21–44Google Scholar
  34. Beaumont HJE, Gallie J, Kost C, Ferguson GC and Rainey PB 2009 Experimental evolution of bet hedging. Nature 462 90–93PubMedGoogle Scholar
  35. Beck JA, Lloyd S, Hafezparast M, Lennon-Pierce M, Eppig JT, Festing MFW and Fisher EMC 2000 Genealogies of mouse inbred strains. Nat. Genet. 24 23–25PubMedGoogle Scholar
  36. Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K and Weigel D 2011 Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480 245–249PubMedGoogle Scholar
  37. Bell G 1982 The masterpiece of nature: the evolution and genetics of sexuality (London: Croom Helm)Google Scholar
  38. Bell AM 2007 Animal personalities. Nature 447 539–540PubMedGoogle Scholar
  39. Ben-Ami F and Hodgson AN 2005 Ovoviviparity and the structure of the brood pouch in Melanoides tuberculata (Gastropoda: Prosobranchia: Thiaridae). J. Morphol. 263 322–329PubMedGoogle Scholar
  40. Benzer S 1953 Induced synthesis of enzymes in bacteria analyzed at the cellular level. Biochim. Biophys. Acta 11 383–395Google Scholar
  41. Biesecker LG and Spinner NB 2013 A genomic view of mosaicism and human disease. Nat. Rev. Genet. 14 307–320PubMedGoogle Scholar
  42. Bigger JW 1944 Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244 497–500Google Scholar
  43. Bird A 2002 DNA methylation patterns and epigenetic memory. Genes Dev. 16 6–21PubMedGoogle Scholar
  44. Boettiger AN and Levine M 2009 Synchronous and stochastic patterns of gene activation in the Drosophila embryo. Science 325 471–473PubMedCentralPubMedGoogle Scholar
  45. Bolger DT and Case TJ 1992 Intra- and interspecific interference behaviour among sexual and asexual geckos. Anim. Behav. 44 21–30Google Scholar
  46. Bosl WJ and Li R 2010 The role of noise and positive feedback in the onset of autosomal dominant diseases. BMC Syst. Biol. 4 93PubMedCentralPubMedGoogle Scholar
  47. Bossdorf O, Arcuri D, Richards CL and Pigliucci M 2010 Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana. Evol. Ecol. 24 541–553Google Scholar
  48. Braendle C and Flatt T 2006 A role for genetic accommodation in evolution? BioEssays 28 868–873PubMedGoogle Scholar
  49. Breithaupt T and Eger P 2002 Urine makes the difference: chemical communication in fighting crayfish made visible. J. Exp. Biol. 205 1221–1232PubMedGoogle Scholar
  50. Breuker CJ, Patterson JS and Klingenberg CP 2006 A single basis for developmental buffering of Drosophila wing shape. PLoS ONE 1 e7PubMedCentralPubMedGoogle Scholar
  51. Brock DW 2002 Human cloning and our sense of self. Science 296 314–316PubMedGoogle Scholar
  52. Brown CR, Mao C, Falkovskaia E, Jurica MS and Boeger H 2013 Linking stochastic fluctuations in chromatin structure and gene expression. PLoS Biol. 11 e1001621PubMedCentralPubMedGoogle Scholar
  53. Browne RA, Moller V, Forbes VE and Depledge MH 2002 Estimating genetic and environmental components of variance using sexual and clonal Artemia. J. Exp. Mar. Biol. Ecol. 267 107–119Google Scholar
  54. Bruder CEG, Piotrowski A, Gijsbers AACJ, Andersson R, Erickson S, et al. 2008 Phenotypically concordant and discordant monozygotic twins display different DNA copy-number-variation profiles. Am. J. Hum. Genet. 82 763–771Google Scholar
  55. Buss LW 1987 The evolution of individuality (Princeton: Princeton University Press)Google Scholar
  56. Butlin R, Schön I and Martens K 1998 Asexual reproduction in nonmarine ostracods. Heredity 81 473–480Google Scholar
  57. Butterfield NJ 2000 Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiol. 26 386–404Google Scholar
  58. Caballero L, Benítez M, Alvarez-Buylla ER, Hernández S, Arzola AV and Cocho G 2012 An epigenetic model for pigment patterning based on mechanical and cellular interactions. J. Exp. Zool. (Mol. Dev. Evol.) 318 209–223Google Scholar
  59. Calo S, Billmyre RB and Heitman J 2013 Generators of phenotypic diversity in the evolution of pathogenic microorganisms. PLoS Pathog. 9 e1003181PubMedCentralPubMedGoogle Scholar
  60. Canli T (ed) 2006 Biology of personality and individual differences (New York: Guilford Press)Google Scholar
  61. Casadesús J and Low DA 2013 Programmed heterogeneity: epigenetic mechanisms in bacteria. J. Biol. Chem. 288 13929–13935PubMedCentralPubMedGoogle Scholar
  62. Case TJ 1990 Patterns of coexistence in sexual and asexual species of Cnemidophorus lizards. Oecologia 83 220–227PubMedGoogle Scholar
  63. Castonguay E and Angers B 2012 The key role of epigenetics in the persistence of asexual lineages. Genet. Res. Int. 2012 534289PubMedCentralPubMedGoogle Scholar
  64. Cavalier-Smith T 2006 Cell evolution and Earth history: stasis and revolution. Phil. Trans. R. Soc. B 361 969–1006PubMedCentralPubMedGoogle Scholar
  65. Cavalier-Smith T 2010 Deep phylogeny, ancestral groups and the four ages of life. Phil. Trans. R. Soc. B 365 111–132PubMedCentralPubMedGoogle Scholar
  66. Chan IS and Ginsburg GS 2011 Personalized medicine: progress and promise. Annu. Rev. Genomics Hum. Genet. 12 217–244PubMedGoogle Scholar
  67. Chang HH, Hemberg M, Barahona M, Ingber DE and Huang S 2008 Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 453 544–548PubMedGoogle Scholar
  68. Charlesworth B and Charlesworth D 2010 Elements of evolutionary genetics (Greenwood Village: Roberts and Company Publishers)Google Scholar
  69. Chase HB 1939 Studies on the tricolor pattern of the Guinea pig. I. The relations between different areas of the coat in respect to the presence of color. Genetics 24 610–621PubMedCentralPubMedGoogle Scholar
  70. Chen Z-X and Riggs AD 2011 DNA methylation and demethylation in mammals. J. Biol. Chem. 286 18347–18353PubMedCentralPubMedGoogle Scholar
  71. Childs DZ, Metcalf CJE and Rees M 2010 Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants. Proc. R. Soc. B 277 3055–3064Google Scholar
  72. Clarke PGH 2012 The limits of brain determinacy. Proc. R. Soc. B 279 1665–1674PubMedCentralPubMedGoogle Scholar
  73. Cohn M and Horibata K 1959 Analysis of the differentiation and of the heterogeneity within a population of Escherichia coli undergoing induced ß-galactosidase synthesis. J. Bacteriol. 78 613–623PubMedCentralPubMedGoogle Scholar
  74. Cornish-Bowden A and Nanjundiah V 2006 The basis of dominance; in The biology of genetic dominance (ed) RA Veitia (Georgetown: Landes Bioscience) pp 1–16Google Scholar
  75. Cortijo S, Wardenaar R, Colomé-Tatché M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, et al. 2014 Mapping the epigenetic basis of complex traits. Science 343 1145–1148PubMedGoogle Scholar
  76. Couso JP 2009 Segmentation, metamerism and the Cambrian explosion. Int. J. Dev. Biol. 53 1305–1316PubMedGoogle Scholar
  77. Crispo E 2007 The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61 2469–2479PubMedGoogle Scholar
  78. Cropley JE, Suter CM, Beckman KB and Martin DIK 2010 CpG methylation of a silent controlling element in the murine A vyallele is incomplete and unresponsive to methyl donor supplementation. PLoS ONE 5 e9055PubMedCentralPubMedGoogle Scholar
  79. Czyz W, Morahan JM, Ebers GC and Ramagopalan SV 2012 Genetic, environmental and stochastic factors in monozygotic twin discordance with a focus on epigenetic differences. BMC Med. 10 93PubMedCentralPubMedGoogle Scholar
  80. Dacks J and Roger AJ 1999 The first sexual lineage and the relevance of facultative sex. J. Mol. Evol. 48 779–783PubMedGoogle Scholar
  81. Daugman J and Downing C 2001 Epigenetic randomness, complexity and singularity of human iris patterns. Proc. R. Soc. B 268 1737–1740PubMedCentralPubMedGoogle Scholar
  82. Davey Smith G 2011 Epidemiology, epigenetics and the ‘Gloomy Prospect’: embracing randomness in population health research and practice. Int. J. Epidemiol. 40 537–562Google Scholar
  83. Davidson RJ 2001 Towards a biology of personality and emotion. Ann. N.Y. Acad. Sci. 935 191–207PubMedGoogle Scholar
  84. Davidson CJ and Surette MG 2008 Individuality in bacteria. Annu. Rev. Genet. 42 253–268PubMedGoogle Scholar
  85. Davis MA 2009 Invasion biology (Oxford: Oxford University Press)Google Scholar
  86. Dawson NJ 1970 Body composition of inbred mice (Mus musculus). Comp. Biochem. Physiol. 37 589–593Google Scholar
  87. Daxinger L and Whitelaw E 2012 Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 13 153–162PubMedGoogle Scholar
  88. Dayel MJ, Alegado RA, Fairclough SR, Levin TC, Nichols SA, McDonald K and King N 2011 Cell differentiation and morphogenesis in the colony-forming choanoflagellate Salpingoeca rosetta. Dev. Biol. 357 73–82PubMedCentralPubMedGoogle Scholar
  89. Debat V and David P 2001 Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol. Evol. 16 555–561Google Scholar
  90. Debat V and Peronnet F 2013 Asymmetric flies: the control of developmental noise in Drosophila. Fly 7 70–77Google Scholar
  91. Debat V, Alibert P, David P, Paradis E and Auffray J-C 2000 Independence between developmental stability and canalization in the skull of the house mouse. Proc. R. Soc. B 267 423–430PubMedCentralPubMedGoogle Scholar
  92. De Kroon H and van Groenendael J (eds) 1997 The ecology and evolution of clonal plants (Leiden: Backhuys Press)Google Scholar
  93. Delbrück M 1945 The burst size distribution in the growth of bacterial viruses (bacteriophages). J. Bacteriol. 50 131–135PubMedCentralGoogle Scholar
  94. Delvigne F and Goffin P 2014 Microbial heterogeneity affects bioprocess robustness: dynamic single-cell analysis contributes to understanding of microbial populations. Biotechnol. J. 9 61–72PubMedGoogle Scholar
  95. De Meeûs T, Prugnolle F and Agnew P 2007 Asexual reproduction: genetics and evolutionary aspects. Cell. Mol. Life Sci. 64 1355–1372Google Scholar
  96. De Meeûs T, Prugnolle F and Agnew P 2009 Asexual reproduction in infectious diseases; in Lost sex. The evolutionary biology of parthenogenesis (eds) I Schön, K Martens and P van Dijk (Dordrecht: Springer) pp 517–533Google Scholar
  97. Denamur E and Matic I 2006 Evolution of mutation rates in bacteria. Mol. Microbiol. 60 820–827PubMedGoogle Scholar
  98. De Schepper S, Debergh P, van Bockstaele E, de Loose M, Gerats A and Depicker A 2003 Genetic and epigenetic aspects of somaclonal variation: flower colour bud sports in azalea, a case study. South African J. Bot. 69 117–128Google Scholar
  99. Dhar N and McKinney JD 2007 Microbial phenotypic heterogeneity and antibiotic tolerance. Curr. Opin. Microbiol. 10 30–38PubMedGoogle Scholar
  100. Dietrich J-E and Hiiragi T 2007 Stochastic patterning in the mouse pre-implantation embryo. Development 134 4219–4231PubMedGoogle Scholar
  101. Dijksterhuis J and Wösten H (eds) 2013 Development of Aspergillus niger. Studies in Mycology 74 (Utrecht: CBS-KNAW Fungal Biodiversity Centre)Google Scholar
  102. Dohle W, Gerberding M, Hejnol A and Scholtz G 2004 Cell lineage, segment differentiation, and gene expression in crustaceans; in Evolutionary developmental biology of Crustacea (ed) G Scholtz (Lisse: Balkema) pp 95–133Google Scholar
  103. Dos Santos RV and da Silva LM 2013 The noise and the KISS in the cancer stem cells niche. J. Theoret. Biol. 335 79–87Google Scholar
  104. Dybdahl MF and Kane SL 2005 Adaptation vs. phenotypic plasticity in the success of a clonal invader. Ecology 86 1592–1601Google Scholar
  105. Eckert CG 2002 The loss of sex in clonal plants. Evol. Ecol. 15 501–520Google Scholar
  106. Elango N, Kim S-H, NISC Comparative Sequencing Program, Vigoda E and Yi SV 2008 Mutations of different molecular origins exhibit contrasting patterns of regional substitution rate variation. PLoS Comput. Biol 4 e1000015PubMedCentralPubMedGoogle Scholar
  107. Eldar A and Elowitz MB 2010 Functional roles for noise in genetic circuits. Nature 467 167–173PubMedCentralPubMedGoogle Scholar
  108. Elliott D 1998 Uniqueness, individuality, and human cloning. J. Appl. Philos. 15 217–230Google Scholar
  109. Elowitz MB, Levine AJ, Siggia ED and Swain PS 2002 Stochastic gene expression in a single cell. Science 297 1183–1186PubMedGoogle Scholar
  110. Extavour CG and Akam M 2003 Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130 5869–5884PubMedGoogle Scholar
  111. Falconer DS and Mackay TFC 1996 Introduction to quantitative genetics, 4th ed. (Harlow: Longman)Google Scholar
  112. Farca Luna AJ, Hurtado-Zavala JI, Reischig T and Heinrich R 2009 Circadian regulation of agonistic behavior in groups of parthenogenetic marbled crayfish, Procambarus sp. J. Biol. Rhythms 24 64–72PubMedGoogle Scholar
  113. Favor J and Neuhäuser-Klaus A 1994 Genetic mosaicism in the house mouse. Annu. Rev. Genet. 28 27–47PubMedGoogle Scholar
  114. Feinberg AP and Irizarry RA 2010 Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. PNAS 107 1757–1764PubMedCentralPubMedGoogle Scholar
  115. Field LM and Blackman RL 2003 Insecticide resistance in the aphid Myzus persicae (Sulzer): chromosome location and epigenetic effects on esterase gene expression in clonal lineages. Biol. J. Linn. Soc. 79 107–113Google Scholar
  116. Figueiredo LM, Cross GAM and Janzen CJ 2009 Epigenetic regulation in African trypanosomes: a new kid on the block. Nat. Rev. Microbiol. 7 504–513PubMedGoogle Scholar
  117. Finch CE and Kirkwood TBL 2000 Chance, development, and aging (New York: Oxford University Press)Google Scholar
  118. Finnerty JR, Pang K, Burton P, Paulson D and Martindale MQ 2004 Origins of bilateral symmetry: Hox and Dpp expression in a sea anemone. Science 304 1335–1337PubMedGoogle Scholar
  119. Fischer A 2014 Epigenetic memory: the Lamarckian brain. EMBO J. 33 945–967PubMedGoogle Scholar
  120. Flamme A 1977 Untersuchungen über die Ursachen der phänotypischen Varianz quantitativer Merkmale bei Laboratoriumsratten. Doktorarbeit (Hannover: Technische Universität Hannover)Google Scholar
  121. Forde BG 2009 Is it good noise? The role of developmental instability in the shaping of a root system. J. Exp. Bot. 60 3989–4002PubMedGoogle Scholar
  122. Fox Keller E 2010 The mirage of a space between nature and nurture (Durham: Duke University Press)Google Scholar
  123. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suñer D, Cigudosa JC, et al. 2005 Epigenetic differences arise during the lifetime of monozygotic twins. PNAS 102 10604–10609PubMedCentralPubMedGoogle Scholar
  124. Frank SA 2010 Somatic evolutionary genomics: mutations during development cause highly variable genetic mosaicism with risk of cancer and neurodegeneration. PNAS 107 1725–1730PubMedCentralPubMedGoogle Scholar
  125. Fraser D and Kærn M 2009 A chance at survival: gene expression noise and phenotypic diversification strategies. Mol. Microbiol. 71 1333–1340PubMedGoogle Scholar
  126. Fraser HB, Hirsh AE, Giaever G, Kumm J and Eisen MB 2004 Noise minimization in eukaryotic gene expression. PLoS Biol. 2 834–838Google Scholar
  127. Freed NE, Silander OK, Stecher B, Böhm A, Hardt W-D and Ackermann M 2008 A simple screen to identify promoters conferring high levels of phenotypic noise. PLoS Genet. 4 e1000307PubMedCentralPubMedGoogle Scholar
  128. Freeman DC, Graham JH and Emlen JM 1993 Developmental stability in plants: symmetries, stress and epigenesis. Genetica 89 97–119Google Scholar
  129. Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, et al. 2007 The invasion paradox: reconciling pattern and process in species invasions. Ecology 88 3–17PubMedGoogle Scholar
  130. Fungairiño SG, Fernández C, Serrano JM, López F and Acosta FJ 2005 Developmental instability and plant potential fitness in a Mediterranean perennial plant, Retama sphaerocarpa (L.) Boiss. Acta Oecol. 27 43–48Google Scholar
  131. Fusco G and Minelli A 2010 Phenotypic plasticity in development and evolution: facts and concepts. Phil. Trans. R. Soc. B 365 547–556PubMedCentralPubMedGoogle Scholar
  132. Galton F 1876 The history of twins, as a criterion of the relative powers of nature and nurture. J. Anthropol. Inst. GB Ireland 5 391–406Google Scholar
  133. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, Farinelli L, Miska E, et al. 2014 Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17 667–669PubMedCentralPubMedGoogle Scholar
  134. Gärtner K 1985 Versuchstierkunde und ‘intangible variance’– eine dritte Komponente der kontinuierlichen Variabilität neben Erbgut und Umwelt. Verh. Dtsch. Zool. Ges. 78 61–75Google Scholar
  135. Gärtner K 1990 A third component causing random variability beside environment and genotype. A reason for the limited success of a 30 year long effort to standardize laboratory animals? Lab. Anim. 24 71–77PubMedGoogle Scholar
  136. Gärtner K 2012 Commentary: Random variability of quantitative characteristics, an intangible epigenomic product, supporting adaptation. Int. J. Epidemiol. 41 342–346PubMedGoogle Scholar
  137. Gärtner K, Bube P, Flamme A, Peters K and Pfaff J 1976 Komponenten biologischer Variabilität und die Grenzen ihrer Manipulierbarkeit. Z. Versuchstierk. 18 146–158Google Scholar
  138. Gärtner K, Ostheimer C and Rapp K 1991 Der Einfluß der uterinen Umwelt auf Körperlängen und Körpergewicht, untersucht an monozygoten Rinderzwillingen nach Embryotransfer auf eine oder zwei Ammen. Reprod. Domest. Anim. 26 235–250Google Scholar
  139. Ghalambor CK, McKay JK, Carroll SP and Reznick DN 2007 Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21 394–407Google Scholar
  140. Gierer A and Meinhardt H 1972 A theory of biological pattern formation. Kybernetik 12 30–39PubMedGoogle Scholar
  141. Gilbert JJ and Schröder T 2007 Intraclonal variation in propensity for mixis in several rotifers: variation among females and with maternal age. Hydrobiol. 593 121–128Google Scholar
  142. Gill DE, Chao L, Perkins SL and Wolf JB 1995 Genetic mosaicism in plants and clonal animals. Annu. Rev. Ecol. Syst. 26 423–444Google Scholar
  143. Goll MG and Bestor TH 2005 Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74 481–514PubMedGoogle Scholar
  144. Görür G 2009 Zinc and cadmium accumulation in cabbage aphid (Brevicoryne brassicae) host plants and developmental instability. Insect Sci. 16 65–71Google Scholar
  145. Gosling SD 2008 Personality in non-human animals. Soc. Pers. Psychol. Compass 2 985–1001Google Scholar
  146. Gould SJ and Lloyd EA 1999 Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism? PNAS 96 11904–11909PubMedCentralPubMedGoogle Scholar
  147. Graham JH, Raz S, Hel-Or H and Nevo E 2010 Fluctuating asymmetry: methods, theory, and applications. Symmetry 2 466–540Google Scholar
  148. Grüneberg H 1954 Variation within inbred strains of mice. Nature 173 674–676PubMedGoogle Scholar
  149. Hageman SJ, Bayer MM and Todd CD 1999 Partitioning phenotypic variation: genotypic, environmental and residual components from bryozoan skeletal morphology. J. Nat. Hist. 33 1713–1735Google Scholar
  150. Haig D 2007 Weismann rules! Ok? Epigenetics and the Lamarckian temptation. Biol. Phil. 22 415–428Google Scholar
  151. Hall MC, Dworkin I, Ungerer MC and Purugganan M 2007 Genetics of microenvironmental canalization in Arabidopsis thaliana. PNAS 104 13717–13722PubMedCentralPubMedGoogle Scholar
  152. Hallgrímsson B and Hall BK (eds) 2005 Variation: a central concept in biology (New York: Elsevier Academic Press)Google Scholar
  153. Hallgrímsson B and Hall BK (eds) 2011a Epigenetics: linking genotype and phenotype in development and evolution (Berkeley: University of California Press)Google Scholar
  154. Hallgrímsson B and Hall BK 2011b Epigenetics: the context of development; in Epigenetics: linking genotype and phenotype in development and evolution (eds) B Hallgrímsson and BK Hall (Berkely: University of California Press) pp 424–438Google Scholar
  155. Hammel JU, Herzen J, Beckmann F and Nickel M 2009 Sponge budding is a spatiotemporal morphological patterning process: insights from synchrotron radiation-based x-ray microtomography into the asexual reproduction of Tethya wilhelma. Front. Zool. 6 19PubMedCentralPubMedGoogle Scholar
  156. Hansen KD, Timp W, Corrada Bravo H, Sabunciyan S, Langmead B, McDonald OG, Wen B, Wu H, et al. 2011 Increased methylation variation in epigenetic domains across cancer types. Nat. Genet. 43 768–775PubMedCentralPubMedGoogle Scholar
  157. Hauser M-T, Aufsatz W, Jonak C and Luschnig C 2011 Transgenerational epigenetic inheritance in plants. Biochim. Biophys. Acta 1809 459–468PubMedCentralPubMedGoogle Scholar
  158. Heithoff DM, Sinsheimer RL, Low DA and Mahan MJ 1999 An essential role for DNA adenine methylation in bacterial virulence. Science 284 967–970PubMedGoogle Scholar
  159. Henderson IR and Jacobsen SE 2007 Epigenetic inheritance in plants. Nature 447 418–424PubMedGoogle Scholar
  160. Hendrikse JL, Parsons TE and Hallgrímsson B 2007 Evolvability as the proper focus of evolutionary developmental biology. Evol. Dev. 9 393–401PubMedGoogle Scholar
  161. Herman JJ, Spencer HG, Donohue K and Sultan SE 2014 How stable ‘should’ epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution 68 632–643PubMedGoogle Scholar
  162. Hernández-Hernández V, Niklas KJ, Newman SA and Benítez M 2012 Dynamical patterning modules in plant development and evolution. Int. J. Dev. Biol. 56 661–674PubMedGoogle Scholar
  163. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, et al. 2002 Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419 808–814PubMedGoogle Scholar
  164. Herranz H and Cohen SM 2010 MicroRNAs and gene regulatory networks: managing the impact of noise in biological systems. Genes Dev. 24 1339–1344PubMedCentralPubMedGoogle Scholar
  165. Hiendleder S 2007 Mitochondrial DNA inheritance after SCNT. Adv. Exp. Med. Biol. 591 103–116PubMedGoogle Scholar
  166. Hirsch S, Baumberger R and Grossniklaus U 2012 Epigenetic variation, inheritance, and selection in plant populations. Cold Spring Harb. Symp. Quant. Biol. 77 97–104PubMedGoogle Scholar
  167. Ho AS, Turcan S and Chan TA 2013 Epigenetic therapy: use of agents targeting deacetylation and methylation in cancer management. OncoTargets Ther. 6 223–232Google Scholar
  168. Hoffmann AA, Reynolds KT, Nash MA and Weeks AR 2008 A high incidence of parthenogenesis in agricultural pests. Proc. R. Soc. B 275 2473–2481PubMedCentralPubMedGoogle Scholar
  169. Hornstein E and Shomron N 2006 Canalization of development by microRNAs. Nat. Genet. 38 S20–24PubMedGoogle Scholar
  170. Huang S 2009 Non-genetic heterogeneity of cells in development: more than just noise. Development 136 3853–3862PubMedCentralPubMedGoogle Scholar
  171. Hughes RN 1989 A functional biology of clonal animals (London: Chapman and Hall)Google Scholar
  172. Huh D and Paulsson J 2011 Non-genetic heterogeneity from stochastic partitioning at cell division. Nat. Genet. 43 95–100PubMedCentralPubMedGoogle Scholar
  173. Hull DL 1980 Individuality and selection. Annu. Rev. Ecol. Syst. 11 311–332Google Scholar
  174. Hunt BG, Brisson JA, Yi SV and Goodisman MAD 2010 Functional conservation of DNA methylation in the pea aphid and the honeybee. Genome Biol. Evol. 2 719–728PubMedCentralPubMedGoogle Scholar
  175. Iguchi K, Matsubara N and Hakoyama H 2001 Behavioural individuality assessed from two strains of cloned fish. Anim. Behav. 61 351–356Google Scholar
  176. Indrasamy H, Woods RE, McKenzie JA and Batterham P 2000 Fluctuating asymmetry for specific bristle characters in Notch mutants of Drosophila melanogaster. Genetica 109 151–159PubMedGoogle Scholar
  177. Jablonka E 2012 Epigenetic variations in heredity and evolution. Clin. Pharmacol. Therapeut. 92 683–688Google Scholar
  178. Jablonka E and Lamb MJ 2014 Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life, revised edition (Cambridge: MIT Press)Google Scholar
  179. Jablonka E and Raz G 2009 Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Quart. Rev. Biol. 84 131–176PubMedGoogle Scholar
  180. Jaenisch R and Bird A 2003 Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 245–254PubMedGoogle Scholar
  181. Jain AK, Prabhakar S and Pankanti S 2002 On the similarity of identical twin fingerprints. Pattern Recog. 35 2653–2663Google Scholar
  182. Johannsen W 1913 Elemente der exakten Erblichkeitslehre, mit Grundzügen der biologischen Variationsstatistik, 2. Ausgabe (Jena: Gustav Fischer Verlag)Google Scholar
  183. Johnston RJ Jr and Desplan C 2010 Stochastic mechanisms of cell fate specification that yield random or robust outcomes. Annu. Rev. Cell Dev. Biol. 26 689–719PubMedCentralPubMedGoogle Scholar
  184. Johnston IG, Gaal B, das Neves RP, Enver T, Iborra FJ and Jones NS 2012 Mitochondrial variability as a source of extrinsic cellular noise. PLoS Comput. Biol. 8 e1002416PubMedCentralPubMedGoogle Scholar
  185. Jones JPG, Rasamy JR, Harvey A, Toon A, Oidtmann B, Randrianarison MH, Raminosoa N and Ravoahangimalala OR 2009 The perfect invader: a parthenogenic crayfish poses a new threat to Madagascar’s freshwater biodiversity. Biol. Invasions 11 1475–1482Google Scholar
  186. Kaelin CB and Barsh GS 2013 Genetics of pigmentation in dogs and cats. Annu. Rev. Anim. Biosci. 1 125–156PubMedGoogle Scholar
  187. Kærn M, Elston TC, Blake WJ and Collins JJ 2005 Stochasticity in gene expression: from theories to phenotypes. Nat. Rev. Genet. 6 451–464PubMedGoogle Scholar
  188. Kaminsky ZA, Tang T, Wang S-C, Ptak C, Oh GHT, Wong AHC, Feldcamp LA, Virtanen C, et al. 2009 DNA methylation profiles in monozygotic and dizygotic twins. Nat. Genet. 41 240–245PubMedGoogle Scholar
  189. Kaneko K and Furusawa C 2008 Relevance of phenotypic noise to adaptation and evolution. IET Syst. Biol. 2 234–246PubMedGoogle Scholar
  190. Karp A 1994 Origins, causes and uses of variation in plant tissue cultures; in Plant cell and tissue culture (eds) IK Vasil and AT Thorpe (Dordrecht: Springer) pp 139–151Google Scholar
  191. Kasbekar DP, Madigan S and Katz ER 1985 Self-induced nystatin resistance in Dictyostelium discoideum. Antimicrob. Agents Chemother. 27 974–976Google Scholar
  192. Kenrick P and Crane PR 1997 The origin and early evolution of plants on land. Nature 389 33–39Google Scholar
  193. Kilfoil ML, Lasko P and Abouheif E 2009 Stochastic variation: from single cells to superorganisms. HFSP J. 3 379–385PubMedCentralPubMedGoogle Scholar
  194. Kim KH and Sauro HM 2012 Adjusting phenotypes by noise control. PLoS Comput. Biol. 8 e1002344PubMedCentralPubMedGoogle Scholar
  195. Kirkwood TBL 2012 Commentary: Ageing – what’s all the noise about? Developments after Gärtner. Int. J. Epidemiol. 41 351–352PubMedGoogle Scholar
  196. Kirkwood TBL and Finch CE 2002 The old worm turns more slowly. Nature 419 794–795PubMedGoogle Scholar
  197. Kirkwood TBL, Feder M, Finch CE, Franceschi C, Globerson A, Klingenberg CP, LaMarco K, Omholt S, et al. 2005 What accounts for the wide variation in life span of genetically identical organisms reared in a constant environment? Mech. Ageing Dev. 126 439–443PubMedGoogle Scholar
  198. Kitano H 2004 Biological robustness. Nat. Rev. Genet. 5 826–837PubMedGoogle Scholar
  199. Klingenberg CP 2003 A developmental perspective on developmental instability: theory, models and mechanisms; in Developmental instability: causes and consequences (ed) M Polak (Oxford: Oxford University Press) pp 14–34Google Scholar
  200. Klingenberg CP 2006 Dominance, nonlinear developmental mapping and developmental stability; in The biology of genetic dominance (ed) RA Veitia (Georgetown: Landes Bioscience) pp 37–51Google Scholar
  201. Knoll AH, Javaux EJ, Hewitt D and Cohen P 2006 Eukaryotic organisms in Proterozoic oceans. Phil. Trans. R. Soc. B 361 1023–1038PubMedCentralPubMedGoogle Scholar
  202. Koehler AV, Springer YP, Keeney DB and Poulin R 2011 Intra- and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biol. J. Linn. Soc. 103 106–116Google Scholar
  203. Kohli RM and Zhang Y 2013 TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502 472–479PubMedCentralPubMedGoogle Scholar
  204. Kong AW-K, Zhang D and Lu G 2006 A study of identical twins’ palmprints for personal verification. Pattern Recog. 39 2149–2156Google Scholar
  205. Koonin EV 2012 The logic of chance: the nature and origin of biological evolution (Upper Saddle River: Pearson Education)Google Scholar
  206. Koonin EV, Senkevich TG and Dolja VV 2006 The ancient Virus World and evolution of cells. Biol. Direct 1 29PubMedCentralPubMedGoogle Scholar
  207. Kovalchuk I 2012 Transgenerational epigenetic inheritance in animals. Front. Genet. 3 76PubMedCentralPubMedGoogle Scholar
  208. Kroes R, Galli C, Munro I, Schilter B, Tran L-A, Walker R and Würtzen G 2000 Threshold of toxicological concern for chemical substances present in the diet: a practical tool for assessing the need for toxicity testing. Food Chem. Toxicol. 38 255–312PubMedGoogle Scholar
  209. Kücken M 2007 Models for fingerprint pattern formation. Forensic Sci. Int. 171 85–96PubMedGoogle Scholar
  210. Kupiec J-J 2009 The origin of individuals (Singapore: World Scientific)Google Scholar
  211. Laird PW 2010 Principles and challenges of genome-wide DNA methylation analysis. Nat. Rev. Genet. 11 191–203PubMedGoogle Scholar
  212. Lajus DL and Alekseev VR 2004 Phenotypic variation and developmental instability of life-history traits: a theory and a case study on within-population variation of resting eggs formation in Daphnia. J. Limnol. 63 37–44Google Scholar
  213. Lande R, Engen S and Sæther B-E 2003 Stochastic population dynamics in ecology and conservation (Oxford: Oxford University Press)Google Scholar
  214. Landry CR and Rifkin SA 2012 The genotype-phenotype maps of systems biology and quantitative genetics: distinct and complementary. Adv. Exp. Med. Biol. 751 371–398PubMedGoogle Scholar
  215. Landry AM, Landry DJ, Gentry LR, Green HL, Reggio B, Koonce KL, Echelard Y and Godke RA 2005 Endocrine profiles and growth patterns of cloned goats. Clon. Stem Cells 7 214–225Google Scholar
  216. Larkin PJ and Scowcroft WR 1981 Somaclonal variation – a novel source of variability from cell cultures for plant improvement. Theor. Appl. Genet. 60 197–214PubMedGoogle Scholar
  217. Larsen E 2005 Developmental origins of variation; in Variation: a central concept in biology (eds) B Hallgrímsson and BK Hall (New York: Elsevier Academic Press) pp 113–129Google Scholar
  218. Latzel V, Allan E, Silveira AB, Colot V, Fischer M and Bossdorf O 2013 Epigenetic diversity increases the productivity and stability of plant populations. Nat. Commun. 4 2875PubMedGoogle Scholar
  219. Lawrence JG and Retchless AC 2009 The interplay of homologous recombination and horizontal gene transfer in bacterial speciation. Meth. Mol. Biol. 532 29–53Google Scholar
  220. Leamy LJ and Klingenberg CP 2005 The genetics and evolution of fluctuating asymmetry. Annu. Rev. Ecol. Evol. Syst. 36 1–21Google Scholar
  221. Leamy LJ, Meagher S, Taylor S, Carroll L and Potts WK 2001 Size and fluctuating asymmetry of morphometric characters in mice: their associations with inbreeding and t-haplotype. Evolution 55 2333–2341PubMedGoogle Scholar
  222. LeDoux J 2002 Synaptic self: how our brains become who we are (New York: Penguin)Google Scholar
  223. Lee H, Popodi E, Tang H and Foster PL 2012 Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. PNAS 109 E2774–2783PubMedCentralPubMedGoogle Scholar
  224. Lehner B 2010 Conflict between noise and plasticity in yeast. PLoS Genet. 6 e1001185PubMedCentralPubMedGoogle Scholar
  225. Lennartsson A and Ekwall K 2009 Histone modification patterns and epigenetic codes. Biochim. Biophys. Acta 1790 863–868PubMedGoogle Scholar
  226. Lenormand T, Roze D and Rousset F 2009 Stochasticity in evolution. Trends Ecol. Evol. 24 157–165PubMedGoogle Scholar
  227. Levy SF and Siegal ML 2008 Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol. 6 e264PubMedCentralPubMedGoogle Scholar
  228. Lewejohann L, Zipser B and Sachser N 2011 “Personality” in laboratory mice used for biomedical research: a way of understanding variability? Dev. Psychobiol. 53 624–630PubMedGoogle Scholar
  229. Lewontin RC 1970 The units of selection. Annu. Rev. Ecol. Syst. 1 1–18Google Scholar
  230. Lewontin RC 2000 The triple helix: gene, organism, and environment (Cambridge: Harvard University Press)Google Scholar
  231. Lewus P and Ford RM 1999 Temperature-sensitive motility of Sulfolobus acidocaldarius influences population distribution in extreme environments. J. Bacteriol. 181 4020–4025PubMedCentralPubMedGoogle Scholar
  232. Li X, Cassidy JJ, Reinke CA, Fischboeck S and Carthew RW 2009 A microRNA imparts robustness against environmental fluctuation during development. Cell 137 273–282PubMedCentralPubMedGoogle Scholar
  233. Li J, Min R, Vizeacoumar FJ, Jin K, Xin X and Zhang Z 2010 Exploiting the determinants of stochastic gene expression in Saccharomyces cerevisiae for genome-wide prediction of expression noise. PNAS 107 10472–10477PubMedCentralPubMedGoogle Scholar
  234. Libby E and Rainey PB 2011 Exclusion rules, bottlenecks and the evolution of stochastic phenotype switching. Proc. R. Soc. B 278 3574–3583PubMedCentralPubMedGoogle Scholar
  235. Liebl AL, Schrey AW, Richards CL and Martin LB 2013 Patterns of DNA methylation throughout a range expansion of an introduced songbird. Integr. Comp. Biol. 53 351–358PubMedGoogle Scholar
  236. Lim JP and Brunet A 2013 Bridging the transgenerational gap with epigenetic memory. Trends Genet. 29 176–186PubMedCentralPubMedGoogle Scholar
  237. López-Garrido J, Cota I and Casadesús J 2012 Epigenetic gene regulation in bacteria; in Epigenetic regulation and epigenomics (ed) RA Meyers (Weinheim: Wiley-VHC) pp 1107–1138Google Scholar
  238. Losick R and Desplan C 2008 Stochasticity and cell fate. Science 320 65–68PubMedCentralPubMedGoogle Scholar
  239. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C and Maleszka R 2010 The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8 e1000506PubMedCentralPubMedGoogle Scholar
  240. Lynch M and Conery JS 2000 The evolutionary fate and consequences of duplicate genes. Science 290 1151–1155PubMedGoogle Scholar
  241. Lynch M, Sung W, Morris K, Coffey N, Landry CR, Dopman EB, Dickinson WJ, Okamoto K, et al. 2008 A genome-wide view of the spectrum of spontaneous mutations in yeast. PNAS 105 9272–9277PubMedCentralPubMedGoogle Scholar
  242. Maamar H, Raj A and Dubnau D 2007 Noise in gene expression determines cell fate in Bacillus subtilis. Science 317 526–529PubMedGoogle Scholar
  243. Macagno ER, Lopresti V and Levinthal C 1973 Structure and development of neuronal connections in isogenic organisms: variations and similarities in the optic system of Daphnia magna. Proc. Natl. Acad. Sci. USA 70 57–61PubMedCentralPubMedGoogle Scholar
  244. Mahner M and Kary M 1997 What exactly are genomes, genotypes and phenotypes? And what about phenomes? J. Theor. Biol. 186 55–63PubMedGoogle Scholar
  245. Maiti S, Kumar KHBG, Castellani CA, O’Reilly R and Singh SM 2011 Ontogenetic de novo copy number variations (CNVs) as a source of genetic individuality: studies on two families with MZD twins for schizophrenia. PLoS ONE 6 e17125PubMedCentralPubMedGoogle Scholar
  246. Malandrin L, Huber H and Bernander R 1999 Nucleoid structure and partition in Methanococcus jannaschii: an archaeon with multiple copies of the chromosome. Genetics 152 1315–1323PubMedCentralPubMedGoogle Scholar
  247. Margulis L and Schwartz KV 1997 Five kingdoms: an illustrated guide to the phyla of life on earth, 3rd ed. (San Francisco: WH Freeman)Google Scholar
  248. Markow TA and Gottesman II 1989 Dermatoglyphic fluctuating asymmetry in twins and singletons. Hereditas 110 211–215PubMedGoogle Scholar
  249. Mark Welch DB and Meselson M 2000 Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288 1211–1215PubMedGoogle Scholar
  250. Marshall WL and Berbee ML 2010 Population-level analyses indirectly reveal cryptic sex and life history traits of Pseudoperkinsus tapetis (Ichthyosporea, Opisthokonta): a unicellular relative of the animals. Mol. Biol. Evol. 27 2014–2026PubMedGoogle Scholar
  251. Martin GM 2009 Epigenetic gambling and epigenetic drift as an antagonistic pleiotropic mechanism of aging. Aging Cell 8 761–764PubMedGoogle Scholar
  252. Martin GM 2014 Nature, nurture, and chance: their roles in interspecific and intraspecific modulations of aging. Ann. Rev. Gerontol. Geriat. 34 267–284Google Scholar
  253. Marusyk A, Almendro V and Polyak K 2012 Intra-tumour heterogeneity: a looking glass for cancer? Nat. Rev. Cancer 12 323–334PubMedGoogle Scholar
  254. Maves L and Schubiger G 1998 A molecular basis for transdetermination in Drosophila imaginal discs: interactions between wingless and decapentaplegic signaling. Development 125 115–124PubMedGoogle Scholar
  255. Maynard Smith J, Smith NH, O’Rourke M and Spratt BR 1993 How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90 4384–4388Google Scholar
  256. McAdams HH and Arkin A 1997 Stochastic mechanisms in gene expression. Proc. Natl. Acad. Sci. USA 94 814–819PubMedCentralPubMedGoogle Scholar
  257. McCrae RR, Jang KL, Livesley WJ, Riemann R and Angleitner A 2001 Sources of structure: genetic, environmental, and artifactual influences on the covariation of personality traits. J. Pers. 69 511–535PubMedGoogle Scholar
  258. Medrano M, Herrera CM and Bazaga P 2014 Epigenetic variation predicts regional and local intraspecific functional diversity in a perennial herb. Mol. Ecol. 23 4926–4938PubMedGoogle Scholar
  259. Meinhardt H 2009 The algorithmic beauty of sea shells, 4th ed. (Berlin: Springer)Google Scholar
  260. Meng TC, Somani S and Dhar P 2004 Modeling and simulation of biological systems with stochasticity. In Silico Biol. 4 24Google Scholar
  261. Mergeay J, Verschuren D and De Meester L 2006 Invasion of an asexual American water flea clone throughout Africa and rapid displacement of a native sibling species. Proc. R. Soc. B 273 2839–2844PubMedCentralPubMedGoogle Scholar
  262. Meyer HM and Roeder AHK 2014 Stochasticity in plant cellular growth and patterning. Front. Plant Sci. 5 420PubMedCentralPubMedGoogle Scholar
  263. Miguel C and Marum L 2011 An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J. Exp. Bot. 62 3713–3725PubMedGoogle Scholar
  264. Milán M, Campuzano S and García-Bellido A 1996 Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc. Natl. Acad. Sci. USA 93 640–645PubMedCentralPubMedGoogle Scholar
  265. Miller-Jensen K, Dey SS, Schaffer DV and Arkin AP 2011 Varying virulence: epigenetic control of expression noise and disease processes. Trends Biotechnol. 29 517–525PubMedGoogle Scholar
  266. Miller-Jensen K, Skupsky R, Shah PS, Arkin AP and Schaffer DV 2013 Genetic selection for context-dependent stochastic phenotypes: Sp1 and TATA mutations increase phenotypic noise in HIV-1 gene expression. PLoS Comput. Biol. 9 e1003135PubMedCentralPubMedGoogle Scholar
  267. Mills SK and Beatty JH 1979 The propensity interpretation of fitness. Phil. Sci. 46 263–286Google Scholar
  268. Milton CC, Huynh B, Batterham P, Rutherford SL and Hoffmann AA 2003 Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. PNAS 100 13396–13401PubMedCentralPubMedGoogle Scholar
  269. Milton CC, Ulane CM and Rutherford S 2006 Control of canalization and evolvability by Hsp90. PLoS ONE 1 e75PubMedCentralPubMedGoogle Scholar
  270. Molenaar PCM, Boomsma DI and Dolan CV 1993 A third source of developmental differences. Behav. Genet. 23 519–524PubMedGoogle Scholar
  271. Moore RC and Purugganan MD 2005 The evolutionary dynamics of plant duplicate genes. Curr. Opin. Plant Biol. 8 122–128PubMedGoogle Scholar
  272. Müller GB and Newman SA 2003 Origination of organismal form: beyond the gene in development and evolutionary biology (Cambridge: MIT Press)Google Scholar
  273. Murray JD 2003 Mathematical biology. II: Spatial models and biomedical applications, 3rd ed. (New York: Springer)Google Scholar
  274. Nanjundiah V 2003 Phenotypic plasticity and evolution by genetic assimilation; in Origination of organismal form: beyond the gene in development and evolutionary biology (eds) GB Müller and SA Newman (Cambridge: MIT Press) pp 245–264Google Scholar
  275. Nanjundiah V and Bhogle AS 1995 The precision of regulation in Dictyostelium discoideum: implications for cell-type proportioning in the absence of spatial pattern. Ind. J. Biochem. Biophys. 32 404–416Google Scholar
  276. Nanjundiah V and Newman SA 2009 Forword Special Issue on Phenotypic and Developmental Plasticity. J. Biosci. 34 493–494PubMedGoogle Scholar
  277. Neildez-Nguyen TMA, Parisot A, Vignal C, Rameau P, Stockholm D, Picot J, Allo V, Le Bec C, et al. 2008 Epigenetic gene expression noise and phenotypic diversification of clonal cell populations. Differentiation 76 33–40PubMedGoogle Scholar
  278. Newman HH 1913 The modes of inheritance of aggregates of meristic (integral) variates in the polyembryonic offspring of the nine-banded armadillo. J. Exp. Zool. 15 145–192Google Scholar
  279. Newman SA and Bhat R 2007 Activator-inhibitor dynamics of vertebrate limb pattern formation. Birth Defects Res. C 81 305–319Google Scholar
  280. Newman SA and Müller GB 2000 Epigenetic mechanisms of character origination. J. Exp. Zool. B (Mol. Dev. Evol.) 288 304–317Google Scholar
  281. Newman SA and Müller GB 2005 Origination and innovation in the vertebrate limb skeleton: an epigenetic perspective. J. Exp. Zool. B (Mol. Dev. Evol.) 304 593–609Google Scholar
  282. Newman HH and Patterson JT 1909 A case of normal identical quadruplets in the nine-banded armadillo, and its bearing on the problems of identical twins and of sex determination. Biol. Bull. 17 181–187Google Scholar
  283. Newman JRS, Ghaemmaghami S, Ihmels J, Breslow DK, Noble M, DeRisi JL and Weissman JS 2006 Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441 840–846PubMedGoogle Scholar
  284. Niepel M, Spencer SL and Sorger PK 2009 Non-genetic cell-to-cell variability and the consequences for pharmacology. Curr. Opin. Chem. Biol. 13 556–561PubMedCentralPubMedGoogle Scholar
  285. Nijhout HF, Maini PK, Madzvamuse A, Wathen AJ and Sekimura T 2003 Pigmentation pattern formation in butterflies: experiments and models. C. R. Biol. 326 717–727PubMedGoogle Scholar
  286. Nikel PI, Silva-Rocha R, Benedetti I and de Lorenzo V 2014 The private life of environmental bacteria: pollutant biodegradation at the single cell level. Environ. Microbiol. 16 628–642PubMedGoogle Scholar
  287. Ning L, Liu G, Li G, Hou Y, Tong Y and He J 2014 Current challenges in the bioinformatics of single cell genomics. Front. Oncol. 4 7PubMedCentralPubMedGoogle Scholar
  288. Novick A and Weiner M 1957 Enzyme induction as an all-or-none phenomenon. Proc. Natl. Acad. Sci. USA 43 553–566PubMedCentralPubMedGoogle Scholar
  289. O’Connor TD and Mundy NI 2009 Genotype-phenotype associations: substitution models to detect evolutionary associations between phenotypic variables and genotypic evolutionary rate. Bioinformatics 25 i94–100PubMedCentralPubMedGoogle Scholar
  290. Oey H and Whitelaw E 2012 Commentary: Gärtner’s ‘third component’: still an open question. Int. J. Epidemiol. 41 356–358PubMedGoogle Scholar
  291. Orias E and Bradshaw AD 1992 Stochastic developmental variation in the ratio of allelic rDNAs among newly differentiated, heterozygous macronuclei of Tetrahymena thermophila. Dev. Genet. 13 87–93PubMedGoogle Scholar
  292. Osella M, Bosia C, Corá D and Caselle M 2011 The role of incoherent microRNA-mediated feedforward loops in noise buffering. PLoS Comput. Biol. 7 e1001101PubMedCentralPubMedGoogle Scholar
  293. Overton WF 1973 On the assumptive base of the nature-nurture controversy: additive versus interactive conceptions. Hum. Dev. 16 74–89PubMedGoogle Scholar
  294. Paigen K 2003 One hundred years of mouse genetics: an intellectual history. I. The classical period (1902-1980). Genetics 163 1–7PubMedCentralPubMedGoogle Scholar
  295. Palmer AR and Strobeck C 1986 Fluctuating asymmetry: measurement, analysis, patterns. Ann. Rev. Ecol. Syst. 17 391–421Google Scholar
  296. Parsons PA 1992 Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68 361–364PubMedGoogle Scholar
  297. Patnaik PR 2006 External, extrinsic and intrinsic noise in cellular systems: analogies and implications for protein synthesis. Biotechnol. Mol. Biol. Rev. 1 121–127Google Scholar
  298. Patra P and Klumpp S 2013 Population dynamics of bacterial persistence. PLoS ONE 8 e62814PubMedCentralPubMedGoogle Scholar
  299. Patterson JS and Klingenberg CP 2007 Developmental buffering: how many genes? Evol. Dev. 9 525–526PubMedGoogle Scholar
  300. Pearl R 1906 Variation in Chilomonas under favourable and unfavourable conditions. Biometrika 5 53–72Google Scholar
  301. Pearson K, Lee A, Warren E, Fry A and Fawcett CD 1901 Mathematical contributions to the theory of evolution. IX. On the principle of homotyposis and its relation to heredity, to the variability of the individual, and to that of the race. Part I. Homotyposis in the vegetable kingdom. Proc. R. Soc. 68 1–5Google Scholar
  302. Peaston AE and Whitelaw E 2006 Epigenetics and phenotypic variation in mammals. Mamm. Genome 17 365–374PubMedCentralPubMedGoogle Scholar
  303. Pfennig DW and Servedio MR 2013 The role of transgenerational epigenetic inheritance in diversification and speciation. Non-Genet. Inherit. 1 17–26Google Scholar
  304. Piersma T and van Gils JA 2011 The flexible phenotype: a body centred integration of ecology, physiology, and behaviour (Oxford: Oxford University Press)Google Scholar
  305. Pietrzak B 2011 Interclonal differences in age-specific performance in Daphnia magna. J. Limnol. Spec. Insert 70 345–352Google Scholar
  306. Pigliucci M 2001 Phenotypic plasticity: beyond nature and nurture (Baltimore: Johns Hopkins University Press)Google Scholar
  307. Pigliucci M 2010 Genotype-phenotype mapping and the end of the ‘genes as blueprintʼ metaphor. Phil. Trans. R. Soc. B. 365 557–566PubMedCentralPubMedGoogle Scholar
  308. Pigliucci M and Müller GB (eds) 2010 Evolution: the extended synthesis (Cambridge: MIT Press)Google Scholar
  309. Pigliucci M, Murren CJ and Schlichting CD 2006 Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209 2362–2367PubMedGoogle Scholar
  310. Pilbrough W, Munro TP and Gray P 2009 Intraclonal protein expression heterogeneity in recombinant CHO cells. PLoS ONE 4 e8432PubMedCentralPubMedGoogle Scholar
  311. Pimentel D 2005 Environmental and economic costs of the application of pesticides primarily in the United States. Environ. Dev. Sustain. 7 229–252Google Scholar
  312. Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russel L, et al. 2001 Economic and environmental threats of alien plant, animal, and microbe invasions. Agric. Ecosyst. Environ. 84 1–20Google Scholar
  313. Plomin R 2011 Commentary: Why are children in the same family so different? Non-shared environment three decades later. Int. J. Epidemiol. 40 582–592PubMedCentralPubMedGoogle Scholar
  314. Plomin R and Daniels D 1987 Why are children in the same family so different from one another? Behav. Brain Sci. 10 1–60Google Scholar
  315. Ponczek LM and Blackstone NW 2001 Effect of cloning rate on fitness-related traits in two marine hydroids. Biol. Bull. 201 76–83PubMedGoogle Scholar
  316. Probst AV, Dunleavy E and Almouzni G 2009 Epigenetic inheritance during the cell cycle. Nat. Rev. Mol. Cell Biol. 10 192–206PubMedGoogle Scholar
  317. Pujadas E and Feinberg AP 2012 Regulated noise in the epigenetic landscape of development and disease. Cell 148 1123–1131PubMedCentralPubMedGoogle Scholar
  318. Queitsch C, Sangster TA and Lindquist S 2002 Hsp90 as a capacitor of phenotypic variation. Nature 417 618–624PubMedGoogle Scholar
  319. Raddatz G, Guzzardo PM, Olova N, Fantappié MR, Rampp M, Schaefer M, Reik W, Hannon GJ, et al. 2013 Dnmt2-dependent methylomes lack defined DNA methylation patterns. PNAS 110 8627–8631PubMedCentralPubMedGoogle Scholar
  320. Ràfols I, MacWilliams HK, Maeda Y and Sawada Y 2014 On the conflict between precision and robustness in the proportion regulation of cell types. arXiv 1401.7872Google Scholar
  321. Raj A and van Oudenaarden A 2008 Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135 216–226PubMedCentralPubMedGoogle Scholar
  322. Rakyan VK, Blewitt ME, Druker R, Preis JI and Whitelaw E 2002 Metastable epialleles in mammals. Trends Genet. 18 348–351PubMedGoogle Scholar
  323. Raser JM and O’Shea EK 2005 Noise in gene expression: origins, consequences, and control. Science 309 2010–2013PubMedCentralPubMedGoogle Scholar
  324. Reed DR, Bachmanov AA and Tordoff MG 2007 Forty mouse strain survey of body composition. Physiol. Behav. 91 593–600PubMedCentralPubMedGoogle Scholar
  325. Reeve ECR and Robertson FW 1954 Studies in quantitative inheritance VI. Sternite chaeta number in Drosophila: a metameric quantitative character. Z. indukt. Abst. Vererbungsl. 86 269–288Google Scholar
  326. Richard M and Yvert G 2014 How does evolution tune biological noise? Front. Genet. 5 374PubMedCentralPubMedGoogle Scholar
  327. Riis T, Lambertini C, Olesen B, Clayton JS, Brix H and Sorrell BK 2010 Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation? Ann. Bot. 106 813–822PubMedCentralPubMedGoogle Scholar
  328. Ringrose L and Paro R 2007 Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134 223–232PubMedGoogle Scholar
  329. Ripa J, Olofsson H and Jonzén N 2010 What is bet-hedging, really? Proc. R. Soc. B 277 1153–1154PubMedCentralPubMedGoogle Scholar
  330. Rodin SN and Riggs AD 2003 Epigenetic silencing may aid evolution by gene duplication. J. Mol. Evol. 56 718–729PubMedGoogle Scholar
  331. Rodríguez López CM, Wetten AC and Wilkinson MJ 2010 Progressive erosion of genetic and epigenetic variation in callus-derived cocoa (Theobroma cacao) plants. New Phytol. 186 856–868PubMedGoogle Scholar
  332. Rollo CD 1995 Phenotypes: their epigenetics, ecology and evolution (New York: Chapman and Hall)Google Scholar
  333. Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, Ekman D and Liberles DA 2007 Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J. Exp. Zool. B. (Mol. Dev. Evol.) 308 58–73Google Scholar
  334. Roy SK 1963 The variation of organs of individual plants. J. Genet. 58 147–176Google Scholar
  335. Rubin H 1990 The significance of biological heterogeneity. Cancer Metastasis Rev. 9 1–20PubMedGoogle Scholar
  336. Rubin GM and Lewis EB 2000 A brief history of Drosophila’s contributions to genome research. Science 287 2216–2218PubMedGoogle Scholar
  337. Sablowski R 2004 Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol. 14 605–611PubMedGoogle Scholar
  338. Sahijram L, Soneji JR and Bollamma KT 2003 Analyzing somaclonal variation in micropropagated bananas (Musa spp.). In Vitro Cell Dev. Biol. Plant 39 551–556Google Scholar
  339. Sakai K-I and Shimamoto Y 1965 Developmental instability in leaves and flowers of Nicotiana tabacum. Genetics 51 801–813PubMedCentralPubMedGoogle Scholar
  340. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, et al. 2001 The population biology of invasive species. Annu. Rev. Ecol. Syst. 32 305–332Google Scholar
  341. Salathia N and Queitsch C 2007 Molecular mechanisms of canalization: Hsp90 and beyond. J. Biosci. 32 457–463PubMedGoogle Scholar
  342. Sangster TA, Salathia N, Undurraga S, Milo R, Schellenberg K, Lindquist S and Queitsch C 2008 HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. PNAS 105 2963–2968PubMedCentralPubMedGoogle Scholar
  343. Saunders E, Tindall BJ, Fähnrich R, Lapidus A, Copeland A, et al. 2010 Complete genome sequence of Haloterrigena turkmenica type strain (4kT). Stand. Genomic Sci. 2 107–116Google Scholar
  344. Saze H 2008 Epigenetic memory transmission through mitosis and meiosis in plants. Sem. Cell Dev. Biol. 19 527–536Google Scholar
  345. Scheiner SM 1993 Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24 35–68Google Scholar
  346. Schilthuizen M and Gravendeel B 2012 Left-right asymmetry in plants and animals: a gold mine for research. Contrib. Zool. 81 75–78Google Scholar
  347. Schimz A and Hildebrand E 1992 Nonrandom structures in the locomotor behavior of Halobacterium: a bifurcation route to chaos? Proc. Natl. Acad. Sci. USA 89 457–460PubMedCentralPubMedGoogle Scholar
  348. Schlichting CD and Pigliucci M 1998 Phenotypic evolution: a reaction norm perspective (Sunderland: Sinauer Associates)Google Scholar
  349. Schlichting CD and Wund MA 2014 Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accomodation. Evolution 68 656–672PubMedGoogle Scholar
  350. Scholtz G 1992 Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation, and early neurogenesis. Roux’s Arch. Dev. Biol. 202 36–48Google Scholar
  351. Schön I, Martens K and van Dijk P (eds) 2009 Lost sex: the evolutionary biology of parthenogenesis (Dordrecht: Springer)Google Scholar
  352. Schuett W, Dall SRX, Baeumer J, Kloesener MH, Nakagawa S, Beinlich F and Eggers T 2011 ‘Personality’ variation in a clonal insect: the pea aphid, Acyrthosiphon pisum. Dev. Psychobiol. 53 631–640PubMedGoogle Scholar
  353. Seidel GE Jr 2002 Genetic and phenotypic similarity among members of mammalian clonal sets; in Principles of cloning (eds) J Cibelli, RP Lanza, KHS Campbell and MD West (Amsterdam: Academic Press) pp 215–225Google Scholar
  354. Seidel GE Jr, Elsden RP and Hasler JF 2003 Embryo transfer in dairy cattle (Fort Atkinson: Hoards and Sons)Google Scholar
  355. Sharma A 2013 Transgenerational epigenetic inheritance: focus on soma to germline information transfer. Progr. Biophys. Mol. Biol. 113 439–446Google Scholar
  356. Shelton DE, Desnitskiy AG and Michod RE 2012 Distributions of reproductive and somatic cell numbers in diverse Volvox (Chlorophyta) species. Evol. Ecol. Res. 14 707–727PubMedCentralPubMedGoogle Scholar
  357. Shin T, Kraemer D, Pryor J, Liu L, Rugila J, Howe L, Buck S, Murphy K, et al. 2002 A cat cloned by nuclear transplantation. Nature 415 859PubMedGoogle Scholar
  358. Shomron N 2010 MicroRNAs and developmental robustness: a new layer is revealed. PLoS Biol. 8 e1000397PubMedCentralPubMedGoogle Scholar
  359. Shushu DD, Comar JM and Abegaz BM 2009 Somaclonal variation in in vitro regenerated Ledebouria graminifolia (Hyacinthaceae), an indigenous bulb in Botswana and its potential exploitation as an ornamental plant. J. Biol. Sci. 9 152–158Google Scholar
  360. Simons BD and Clevers H 2011 Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 145 851–862PubMedGoogle Scholar
  361. Simpson SJ, Sword GA and Lo N 2011 Polyphenism in insects. Curr. Biol. 21 R738–749PubMedGoogle Scholar
  362. Singh GP 2013 Coupling between noise and plasticity in E. coli. G3 Genes Genomes Genet. 32 2115–2120Google Scholar
  363. Singh A and Weinberger LS 2009 Stochastic gene expression as a molecular switch for viral latency. Curr. Opin. Microbiol. 12 460–466PubMedCentralPubMedGoogle Scholar
  364. Skinner MK, Manikkam M, Haque MM, Zhang B and Savenkova MI 2012 Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol. 13 R91PubMedCentralPubMedGoogle Scholar
  365. Skirvin RM, McPheeters KD and Norton M 1994 Sources and frequency of somaclonal variation. HortScience 29 1232–1237Google Scholar
  366. Smith LC and Murphy BD 2004 Genetic and epigenetic aspects of cloning and potential effects on offspring of cloned mammals. Clon. Stem Cells 6 126–132Google Scholar
  367. Smith MS, Milton I and Strand MR 2010 Phenotypically plastic traits regulate caste formation and soldier function in polyembryonic wasps. J. Evol. Biol. 23 2677–2684PubMedCentralPubMedGoogle Scholar
  368. Smith EA, Collette SB, Boynton TA, Lillrose T, Stevens MR, Bekker MF, Eggett E and St Clair SB 2011 Developmental contributions to phenotypic variation in functional leaf traits within quaking aspen clones. Tree Physiol. 31 68–77PubMedGoogle Scholar
  369. Smits WK, Kuipers OP and Veening J-W 2006 Phenotypic variation in bacteria: the role of feedback regulation. Nat. Rev. Microbiol. 4 259–271PubMedGoogle Scholar
  370. Sozzani R and Benfey PN 2011 High-throughput phenotyping of multicellular organisms: finding the link between genotype and phenotype. Genome Biol. 12 219PubMedCentralPubMedGoogle Scholar
  371. Spiller DG, Wood CD, Rand DA and White MRH 2010 Measurement of single-cell dynamics. Nature 465 736–745PubMedGoogle Scholar
  372. Spratt BG 2004 Exploring the concept of clonality in bacteria. Meth. Mol. Biol. 266 323–352Google Scholar
  373. Spudich JL and Koshland DE Jr 1976 Non-genetic individuality: chance in the single cell. Nature 262 467–471PubMedGoogle Scholar
  374. Srinivasan DG and Brisson JA 2012 Aphids: a model for polyphenism and epigenetics. Genet. Res. Intern. 2012 431–531Google Scholar
  375. Stamps J and Groothuis TGG 2010 The development of animal personality: relevance, concepts and perspectives. Biol. Rev. 85 301–325PubMedGoogle Scholar
  376. Starrfelt J and Kokko H 2012 Bet-hedging – a triple trade-off between means, variances and correlations. Biol. Rev. 87 742–755PubMedGoogle Scholar
  377. Stewart-Savage J, Wagstaff BJ and Yund PO 1999 Developmental basis of phenotypic variation in egg production in a colonial ascidian: primary oocyte production versus oocyte development. Biol. Bull. 196 63–69PubMedGoogle Scholar
  378. Storrs EE and Williams RJ 1968 A study of monozygous quadruplet armadillos in relation to mammalian inheritance. Proc. Natl. Acad. Sci. USA 60 910–914PubMedCentralPubMedGoogle Scholar
  379. Suomalainen E, Saura A and Lokki J 1987 Cytology and evolution in parthenogenesis (Boca Raton: CRC Press)Google Scholar
  380. Takahashi KH, Rako L, Takano-Shimizu T, Hoffmann AA and Lee SF 2010 Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol. Biol. 10 284PubMedCentralPubMedGoogle Scholar
  381. Taylor JS and Raes J 2004 Duplication and divergence: the evolution of new genes and old ideas. Annu. Rev. Genet. 38 615–643PubMedGoogle Scholar
  382. Taylor JW, Jacobson DJ and Fisher MC 1999 The evolution of asexual fungi: reproduction, speciation and classification. Annu. Rev. Phytopathol. 37 197–246PubMedGoogle Scholar
  383. Thattai M and van Oudenaarden A 2001 Intrinsic noise in gene regulatory networks. PNAS 98 8614–8619PubMedCentralPubMedGoogle Scholar
  384. Thattai M and van Oudenaarden A 2004 Stochastic gene expression in fluctuating environments. Genetics 167 523–530PubMedCentralPubMedGoogle Scholar
  385. The 1000 Genomes Project Consortium 2010 A map of human genome variation from population-scale sequencing. Nature 467 1061–1073PubMedCentralGoogle Scholar
  386. Tibayrenc M and Ayala FJ 2012 Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. PNAS 109 E3305–3313PubMedCentralPubMedGoogle Scholar
  387. Tordoff MG, Bachmanov AA and Reed DR 2007a Forty mouse strain survey of water and sodium intake. Physiol. Behav. 91 620–631PubMedCentralPubMedGoogle Scholar
  388. Tordoff MG, Bachmanov AA and Reed DR 2007b Forty mouse strain survey of voluntary calcium intake, blood calcium, and bone mineral content. Physiol. Behav. 91 632–643PubMedCentralPubMedGoogle Scholar
  389. Trillmich F and Hudson R 2011 The emergence of personality in animals: the need for a developmental approach. Dev. Psychobiol. 53 505–509PubMedGoogle Scholar
  390. Tsuru S, Ichinose J, Kashiwagi A, Ying B-W, Kaneko K and Yomo T 2009 Noisy cell growth rate leads to fluctuating protein concentration in bacteria. Phys. Biol. 6 036015PubMedGoogle Scholar
  391. Tsutsui ND, Suarez AV, Holway DA and Case TJ 2000 Reduced genetic variation and the success of an invasive species. PNAS 97 5948–5953PubMedCentralPubMedGoogle Scholar
  392. Turing AM 1952 The chemical basis of morphogenesis. Phil. Trans. R. Soc. B 237 37–72Google Scholar
  393. Turkheimer E and Waldron M 2000 Nonshared environment: a theoretical, methodological, and quantitative review. Psychol. Bull. 126 78–108PubMedGoogle Scholar
  394. Turck F and Coupland G 2014 Natural variation in epigenetic gene regulation and its effects on plant developmental traits. Evolution 68 620–631PubMedGoogle Scholar
  395. Turko AJ, Earley RL and Wright PA 2011 Behaviour drives morphology: voluntary emersion patterns shape gill structure in genetically identical mangrove rivulus. Anim. Behav. 82 39–47Google Scholar
  396. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykręt D, Dedieu A, Peaucelle A, Ludynia M, et al. 2012 Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149 439–451PubMedGoogle Scholar
  397. Van Praag H, Kempermann G and Gage FH 2000 Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1 191–195PubMedGoogle Scholar
  398. Van Valen L 1962 A study of fluctuating asymmetry. Evolution 16 125–142Google Scholar
  399. Veening J-W, Smits WK and Kuipers OP 2008 Bistability, epigenetics and bet-hedging in bacteria. Annu. Rev. Microbiol. 62 193–210PubMedGoogle Scholar
  400. Veitia RA 2005 Stochasticity or the fatal ‘imperfection’ of cloning. J. Biosci. 30 21–30PubMedGoogle Scholar
  401. Verhoeven KJF and Preite V 2014 Epigenetic variation in asexually reproducing organisms. Evolution 68 644–655PubMedGoogle Scholar
  402. Verstrepen KJ and Fink GR 2009 Genetic and epigenetic mechanisms underlying cell-surface variability in Protozoa and Fungi. Annu. Rev. Genet. 43 1–24PubMedGoogle Scholar
  403. Vickaryous MK and Hall BK 2006 Human cell type diversity, evolution, development, and classification with special reference to cells derived from the neural crest. Biol. Rev. 81 425–455PubMedGoogle Scholar
  404. Vinck A, Terlou M, Pestman WR, Martens EP, Ram AF, van den Hondel CAMJJ and Wösten HAB 2005 Hyphal differentiation in the exploring mycelium of Aspergillus niger. Mol. Microbiol. 58 693–699PubMedGoogle Scholar
  405. Viney M and Reece SE 2013 Adaptive noise. Proc. R. Soc. B 280 20131104PubMedCentralPubMedGoogle Scholar
  406. Vogt G 2007 Exposure of the eggs to 17α-methyl testosterone reduced hatching success and growth and elicited teratogenic effects in postembryonic life stages of crayfish. Aquat. Toxicol. 85 291–296PubMedGoogle Scholar
  407. Vogt G 2008 The marbled crayfish: a new model organism for research on development, epigenetics and evolutionary biology. J. Zool. 276 1–13Google Scholar
  408. Vogt G 2010 Suitability of the clonal marbled crayfish for biogerontological research: a review and perspective, with remarks on some further crustaceans. Biogerontol. 11 643–669Google Scholar
  409. Vogt G 2011 Marmorkrebs: natural crayfish clone as emerging model for various biological disciplines. J. Biosci. 36 377–382PubMedGoogle Scholar
  410. Vogt G 2012 Hidden treasures in stem cells of indeterminately growing bilaterian invertebrates. Stem Cell Rev. Rep. 8 305–317Google Scholar
  411. Vogt G 2015 Research on stem cells, aging, cancer resistance, and epigenetics in marbled crayfish and relatives: potential benefits for human biology and medicine; in Freshwater crayfish: global overview (eds) T Kawai, Z Faulkes and G Scholtz (Boca Raton: CRC Press) pp 115–157Google Scholar
  412. Vogt G and Rug M 1999 Life stages and tentative life cycle of Psorospermium haeckeli, a species of the novel DRIPs clade from the animal-fungal dichotomy. J. Exp. Zool. 283 31–42Google Scholar
  413. Vogt G, Tolley L and Scholtz G 2004 Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. J. Morphol. 261 286–311PubMedGoogle Scholar
  414. Vogt G, Huber M, Thiemann M, van den Boogaart G, Schmitz OJ and Schubart CD 2008 Production of different phenotypes from the same genotype in the same environment by developmental variation. J. Exp. Biol. 211 510–523PubMedGoogle Scholar
  415. Vogt G, Wirkner CS and Richter S 2009 Symmetry variation in the heart-descending artery system of the parthenogenetic marbled crayfish. J. Morphol. 270 221–226PubMedGoogle Scholar
  416. Vogt G, Raddatz G, Falckenhayn C, Hanna K, Musch T and Lyko F 2013 Ökologische Anpassung invasiver Arten durch epigenetische Mechanismen: ein Teilaspekt des Marmorkrebs-Projekts am Deutschen Krebsforschungszentrum Heidelberg, in Internationale Flusskrebstagung (Schleiden-Gemünd: Biologische Station StädteRegion Aachen) pp 109–113Google Scholar
  417. Vrijenhoek RC 1998 Animal clones and diversity: are natural clones generalists or specialists? BioScience 48 617–628Google Scholar
  418. Waddington CH 1942 Canalization of development and the inheritance of acquired characters. Nature 150 563–565Google Scholar
  419. Waddington CH 1953 Genetic assimilation of an acquired character. Evolution 7 118–126Google Scholar
  420. Waddington CH 1957 The strategy of the genes: a discussion of some aspects of theoretical biology (London: Gorge Allen and Unwin)Google Scholar
  421. Wagner GP, Pavlicev M and Cheverud JM 2007 The road to modularity. Nat. Rev. Genet. 8 921–931PubMedGoogle Scholar
  422. Walsh TK, Brisson JA, Robertson HM, Gordon K, Jaubert-Possamai S, Tagu D and Edwards OR 2010 A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum. Insect Mol. Biol. 19 215–228PubMedGoogle Scholar
  423. Wang D and Bodovitz S 2010 Single cell analysis: the new frontier in ‘omics’. Trends Biotechnol. 28 281–290PubMedCentralPubMedGoogle Scholar
  424. Wang Z and Zhang J 2011 Impact of gene expression noise on organismal fitness and the efficacy of natural selection. PNAS 108 E67–76PubMedCentralPubMedGoogle Scholar
  425. Wang G-Z, Lercher MJ and Hurst LD 2011 Transcriptional coupling of neighboring genes and gene expression noise: evidence that gene orientation and noncoding transcripts are modulators of noise. Genome Biol. Evol. 3 320–331PubMedGoogle Scholar
  426. Warren E 1899 An observation on inheritance in parthenogenesis. Proc. R. Soc. 65 154–158Google Scholar
  427. Warren E 1902 Variation and inheritance in the parthenogenetic generations of the aphis Hyalopterus trirhodus (Walker). Biometrika 1 129–154Google Scholar
  428. Weigel D and Colot V 2012 Epialleles in plant evolution. Genome Biol. 13 249PubMedCentralPubMedGoogle Scholar
  429. West-Eberhard MJ 2003 Developmental plasticity and evolution (New York: Oxford University Press)Google Scholar
  430. Williams RJ and Pelton RB 1966 Individuality in nutrition: effects of vitamin A-deficient and other deficient diets on experimental animals. Proc. Natl. Acad. Sci. USA 55 126–134PubMedCentralPubMedGoogle Scholar
  431. Wilson EO 1975 Sociobiology: the new synthesis (Cambridge: Harvard University Press)Google Scholar
  432. Wilson J 1999 Biological individuality: the identity and persistence of living entities (Cambridge: Cambridge University Press)Google Scholar
  433. Wilson R 2007 The biological notion of individual; in Stanford Encyclopedia of Philosophy (Stanford: Center for the Study of Language and Information, Stanford University)Google Scholar
  434. Woese CR, Kandler O and Wheelis ML 1990 Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA 87 4576–4579PubMedCentralPubMedGoogle Scholar
  435. Woods HA 2014 Mosaic physiology from developmental noise: within-organism physiological diversity as an alternative to phenotypic plasticity and phenotypic flexibility. J. Exp. Biol. 217 35–45PubMedGoogle Scholar
  436. Woolff CM 1997 Does the genotype for schizophrenia often remain unexpressed because of canalization and stochastic events during development? Psychol. Med. 27 659–668Google Scholar
  437. Wright S 1920 The relative importance of heredity and environment in determining the piebald pattern of guinea-pigs. Proc. Natl. Acad. Sci. USA 6 320–332PubMedCentralPubMedGoogle Scholar
  438. Wright S and Chase HB 1936 On the genetics of the spotted pattern of the guinea pig. Genetics 21 758–787PubMedCentralPubMedGoogle Scholar
  439. Xia J, Han L and Zhao Z 2012 Investigating the relationship of DNA methylation with mutation rate and allele frequency in the human genome. BMC Genomics 13 S7PubMedCentralPubMedGoogle Scholar
  440. Yang B-C, Lee S-H, Hwang S, Lee H-C, Im G-S, Kim D-H, Lee D-K, Lee K-T, et al. 2012 Phenotypic characterization of Hanwoo (native Korean cattle) cloned from somatic cells of a single adult. BMB Rep. 45 38–43PubMedGoogle Scholar
  441. Yvert G 2014 ‘Particle genetics’: treating every cell as unique. Trends Genet. 30 49–56PubMedCentralPubMedGoogle Scholar
  442. Yvert G, Ohnuki S, Nogami S, Imanaga Y, Fehrmann S, Schacherer J and Ohya Y 2013 Single-cell phenomics reveals intra-species variation of phenotypic noise in yeast. BMC Syst. Biol. 7 54PubMedCentralPubMedGoogle Scholar
  443. Zhang Z, Qian W and Zhang J 2009 Positive selection for elevated gene expression noise in yeast. Mol. Syst. Biol. 5 299PubMedCentralPubMedGoogle Scholar
  444. Zhang Y-Y, Fischer M, Colot V and Bossdorf O 2013 Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 197 314–322PubMedGoogle Scholar
  445. Zhu S and Chen H 1995 Megascopic multicellular organisms from the 1700-million-year-old Tuanshanzi Formation in the Jixian area, north China. Science 270 620–622Google Scholar
  446. Zhurov V, Terzin T and Grbić M 2004 Early blastomere determines embryo proliferation and caste fate in a polyembryonic wasp. Nature 432 764–769PubMedGoogle Scholar
  447. Zordan RE, Galgoczy DJ and Johnson AD 2006 Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. PNAS 103 12807–12812PubMedCentralPubMedGoogle Scholar
  448. Zou X, Ma W, Solov’yov IA, Chipot C and Schulten K 2012 Recognition of methylated DNA through methyl-CpG binding domain proteins. Nucl. Acids Res. 40 2747–2758PubMedCentralPubMedGoogle Scholar

Copyright information

© Indian Academy of Sciences 2015

Authors and Affiliations

  1. 1.Faculty of BiosciencesUniversity of HeidelbergHeidelbergGermany

Personalised recommendations