Abstract
First the ‘Weismann barrier’ and later on Francis Crick’s ‘central dogma’ of molecular biology nourished the gene-centric paradigm of life, i.e., the conception of the gene/genome as a ‘central source’ from which hereditary specificity unidirectionally flows or radiates into cellular biochemistry and development. Today, due to advances in molecular genetics and epigenetics, such as the discovery of complex post-genomic and epigenetic processes in which genes are causally integrated, many theorists argue that a gene-centric conception of the organism has become problematic. Here, we first explore the causal implications of the following two central dogma-related issues: (1) widespread reverse transcription—arguing for an extension from ‘DNA-genome’ to RNA-encompassing ‘NA-genome’ and, thus, from traditional DNA-centrism to a broader ‘NA-centrism’; and (2) the absence of a mechanism of reverse translation—arguing for the ‘structural primacy’ of NA-sequence over protein in cellular biochemistry. Secondly, we explore whether this latter conclusion can be extended to a ‘functional primacy’ of NA-sequence over protein in cellular biochemistry, which would imply a limited kind of ‘gene/NA-centrism’ confined to the subcellular level of NA/protein-based biochemistry. Finally, we explore the conditions—and their (non)fulfilment—for a more generalised form of gene-centrism extendable to higher levels of biological organisation. We conclude that the higher we go in the biological hierarchy, the more dubious gene-centric claims become.
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Notes
In Woodward’s (2010) terminology, the causal arrow or constraint from genetic NA-sequence to three-dimensional protein-structure is characterised by a relative “stability” (cf. our ‘reliability’) and “specificity” (cf. our ‘co-variance’). .
We thank an anonymous reviewer for drawing our attention to this.
Again in Woodward’s (2010) terminology, the causal arrow or constraint from protein-structure to protein-function is characterised by a relative “stability” and “specificity”.
Again, using Woodward’s (2010) framework, the causal arrow or constraint from genetic NA-sequence to protein-function is characterised by a relative “stability” (cf. our ‘reliability’) and “specificity” (cf. our ‘co-variance’).
See previous section.
Cf. Woodward’s (2010) ‘stability’ and ‘specificity’.
Reviewed in the section on “The absence of a mechanism of reverse translation”.
References
Baranov PV, Gurvich OL, Hammer AW, Gesteland RF, Atkins JF (2003) RECODE 2003. Nucleic Acids Res 31:87–89
Brennicke A, Marchfelder A, Binder S (1999) RNA editing. FEMS Microbiol Rev 23:297–316
Brosius J (1999) RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238:115–134
Brosius J (2003) The contribution of RNAs and retroposition to evolutionary novelties. Genetica 118:99–116
Cairns-Smith AG (1985) Seven clues to the origin of life. Cambridge University Press, Canto
Callebaut W, Rasskin-Gutman D (eds) (2005) Modularity: understanding the development and evolution of natural complex systems. MIT Press, Cambridge
Callebaut W, Müller GB, Newman SA (2007) The organismic systems approach: EvoDevo and the streamlining of the naturalistic agenda. In: Sansom R, Brandon R (eds) Integrating evolution and development: from theory to practice. MIT Press, Cambridge, pp 25–92
Crick F (1958) On protein synthesis. Sympos Soc Exp Biol 12:138–163
Crick F (1970) Central dogma of molecular biology. Nature 227:561–563
Dawkins R (1982) The extended phenotype. Oxford University Press, Oxford
Dawkins R (2004) Extended phenotype: but not too extended. A reply to Laland, Turner and Jablonka. Biol Philos 19:377–396
De Backer P, De Waele D, Van Speybroeck L (2010) Ins and outs of systems biology vis-à-vis molecular biology: continuation or clear cut? Acta Biotheor 58:15–49
Gilbert SF, Opitz JM, Raff RA (1996) Resynthesizing evolutionary and developmental biology. Dev Biol 173:357–372
Godfrey-Smith P (2007) Is it a revolution? Biol Philos 22:429–437
Goodman MF (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Ann Rev Biochem 71:17–50
Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge, MA
Griesemer J (2000) The units of evolutionary transition. Selection 1:67–80
Griesemer J (2002) What is “epi” about epigenetics? Ann NY Acad Sci 981:97–110
Griesemer J (2005) The informational gene and the substantial body: On the generalization of evolutionary theory by abstraction. In: Jones MR, Cartwright N (eds) Idealization XII: correcting the model. Idealization and abstraction in the sciences (Poznan studies in the philosophy of sciences and the humanities, vol 86. Rodopi, Amsterdam, pp 59–115
Haig D (2004) The (dual) origin of epigenetics. Cold Spring Harbor Symp Quant Biol 69:67–70
Haig D (2007) Weismann rules! OK? Epigenetics and the Lamarckian temptation. Biol Philos 22:415–428
Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, Lindquist S (2012) Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482:363–368
Hall BK (2003) Unlocking the black box between genotype and phenotype: cell condensations as morphogenetic (modular) units. Biol Philos 18:219–247
Holliday R (1990) Mechanisms for the control of gene activity during development. Biol Rev 65:431–471
International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Jablonka E, Lamb M (1995) Epigenetic inheritance and evolution: the Lamarckian dimension. Oxford University Press, Oxford
Jablonka E, Lamb M (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge, MA
Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84:131–176
Keller EF (2000) The century of the gene. Harvard University Press, Cambridge, MA
Knoop V (2011) When you can’t trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci 68:567–586
Koonin EV (2012) Does the central dogma still stand? Biol Direct 7:27
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
Maas S, Rich A (2000) Changing genetic information through RNA editing. BioEssays 22:790–802
Maydanovych O, Beal PA (2006) Breaking the central dogma by RNA editing. Chem Rev 106(8):3397–3411
Maynard Smith J (1993) The theory of evolution. Cambridge University Press, Canto
Maynard Smith J (2000) The concept of information in biology. Philos Sci 67:177–194
Medina M (2005) Genomes, phylogeny, and evolutionary systems biology. PNAS 102:6630–6635
Moss L (2003) What genes can’t do. MIT Press, Cambridge, MA
Neumann-Held EM, Rehmann-Sutter C (eds) (2006) Genes in development: re-reading the molecular paradigm. Duke University Press, Durham
Noble D (2008) Genes and causation. Philos Trans A Math Phys Eng Sci 366:3001–3015
Noble D (2011) Neo-Darwinism, the modern synthesis, and selfish genes: are they of use in physiology? J Physiol 589:1007–1015
Odling-Smee J, Laland KN (2011) Ecological inheritance and cultural inheritance: what are they and how do they differ? Biol Theory 6:220–230
Oyama S (1985) The ontogeny of information: developmental systems and evolution. Cambridge University Press, Cambridge
Oyama S, Griffiths PE, Gray RD (eds) (2001) Cycles of contingency: developmental systems and evolution. MIT Press, Cambridge, MA
Rando OJ, Verstrepen KJ (2007) Timescales of genetic and epigenetic inheritance. Cell 128:655–668
Richards EJ (2006) Inherited epigenetic variation: revisiting soft inheritance. Nat Rev Genet 7:395–401
Richards CL, Bossdorf O, Pigliucci M (2010) What role does heritable epigenetic variation play in phenotypic evolution? Bioscience 60:232–237
Sarkar S (2000) Information in genetics and developmental biology: comments on Maynard Smith. Philos Sci 67:208–213
Sarkar S (2005) Molecular models of life: philosophical papers on molecular biology. MIT Press, Cambridge, MA
Shapiro JA (2009) Revisiting the central dogma in the 21st century. Natural genetic engineering and natural genome editing. Ann N Y Acad Sci 1178:6–28
Shapiro JA (2011) Evolution: a view from the 21st century. FT Press Science, Upper Saddle River, NJ
Sharp PA (1994) Split genes and RNA splicing. Cell 77:805–815
Stotz K (2006a) Molecular epigenesis: distributed specificity as a break in the central dogma. Hist Philos Life Sci 28:527–544
Stotz K (2006b) With ‘genes’ like that, who needs an environment? Postgenomics’ argument for the ‘ontogeny of information’. Philos Sci 73:905–917
Temin HM (1985) Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol 2:455–468
Temin HM, Mizutani S (1970) RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226:1211–1213
Thieffry D, Sarkar S (1998) Forty years under the central dogma. TiBS 23:312–316
True HL, Berlin I, Lindquist S (2004) Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184–187
Weismann A (1889) Essays upon heredity and kindred biological problems, vol 1. Clarendon Press, Oxford
Weismann A (1893a) The germ-plasm: a theory of heredity (trans: Parker WN, Rönnfeldt H). Charles Scribner’s Sons, New York
Weismann A (1893b) The all-sufficiency of natural selection: a reply to Herbert Spencer. Contemp Rev 64:309–338
Weismann A (1904) The evolution theory (trans: Thomson JA, Thomson M). Edward Arnold, London
Wilkins A (2011) Epigenetic inheritance: where does the field stand today? What do we still need to know? In: Gissis SB, Jablonka E (eds) Transformations of Lamarckism: from subtle fluids to molecular biology. MIT Press, Cambridge, MA, pp 389–393
Winther RG (2001) August Weismann on germ-plasm variation. J Hist Biol 34:517–555
Woodward J (2010) Causation in biology: stability, specificity, and the choice of levels of explanation. Biol Philos 25:287–318
Wu T, Wang J, Changning L et al (2006) NPInter: the noncoding RNAs and protein related biomacromolecules interaction database. Nucleic Acids Res 34:D150–D152
Acknowledgments
We are grateful to an anonymous reviewer for extensive comments on an earlier version of the paper, to Kim Sterelny for additional comments and suggestions, and to Linda Van Speybroeck for both constructive criticism and support during previous stages of the paper. Preparation of the manuscript was made possible by the Special Research Fund (BOF), Ghent University (Project Number: B/11196/02) and by the Fund for Scientific Research Flanders (FWO), Belgium (Project Number: G001013N).
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De Tiège, A., Tanghe, K., Braeckman, J. et al. From DNA- to NA-centrism and the conditions for gene-centrism revisited. Biol Philos 29, 55–69 (2014). https://doi.org/10.1007/s10539-013-9393-z
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DOI: https://doi.org/10.1007/s10539-013-9393-z