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The pre-Mendelian, pre-Darwinian world: Shifting relations between genetic and epigenetic mechanisms in early multicellular evolution

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Abstract

The reliable dependence of many features of contemporary organisms on changes in gene content and activity is tied to the processes of Mendelian inheritance and Darwinian evolution. With regard to morphological characters, however, Mendelian inheritance is the exception rather than the rule, and neo-Darwinian mechanisms in any case do not account for the origination (as opposed to the inherited variation) of such characters. It is proposed, therefore, that multicellular organisms passed through a pre-Mendelian, pre-Darwinian phase, whereby cells, genes and gene products constituted complex systems with context-dependent, self-organizing morphogenetic capabilities. An example is provided of a plausible ’core’ mechanism for the development of the vertebrate limb that is both inherently pattern forming and morphogenetically plastic. It is suggested that most complex multicellular structures originated from such systems. The notion that genes are privileged determinants of biological characters can only be sustained by neglecting questions of evolutionary origination and the evolution of developmental mechanisms.

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References

  • Alber M, Hentschel H G E, Kazmierczak B and Newman S A 2005 Existence of solutions to a new model of biological pattern formation;J. Math. Analysis Appl. (in press)

  • Baldwin J M 1902Development and evolution (New York: Macmillan)

    Book  Google Scholar 

  • Bateson P 2005 The return of the whole organism;J. Biosci. 30 31–39

    Article  PubMed  Google Scholar 

  • Bateson W 1913Problems of genetics (New Haven: Yale University Press)

    Book  Google Scholar 

  • Behera N and Nanjundiah V 2004 Phenotypic plasticity can potentiate rapid evolutionary change;J. Theor. Biol. 226 177–184

    Article  PubMed  Google Scholar 

  • Bonner J T 1967The cellular slime molds 2nd edition (Princeton: Princeton University Press)

    Book  Google Scholar 

  • Bradshaw H D and Schemske D W 2003 Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers;Nature (London) 426 176–178

    Article  CAS  Google Scholar 

  • Callender L A 1988 Gregor Mendel: an opponent of descent with modification;Hist. Sci. 26 41–75

    Article  Google Scholar 

  • Chaturvedi R, Huang C, Kazmierczak B, Schneider T, Izaguirre, J A, Glimm T, Hentschel H G E, Newman S A, Glazier J A and Alber M 2005 On multiscale approaches to three-dimensional modelling of morphogenesis;Interface (R. Soc. London) (in press)

  • Darwin C 1859On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life (London: John Murray)

    Book  Google Scholar 

  • Darwin C 1872The origin of species: by means of natural selection, or the preservation of favoured races in the struggle for life 6th edition (London: John Murray)

    Google Scholar 

  • Dayal S, Kiyama T, Villinski J T, Zhang N, Liang S and Klein W H 2004 Creation of cis-regulatory elements during sea urchin evolution by co-option and optimization of a repetitive sequence adjacent to the spec2a gene;Dev. Biol. 273 436–453

    Article  CAS  PubMed  Google Scholar 

  • Dunn L C 1965A short history of genetics (New York: McGraw-Hill)

    Google Scholar 

  • Fisher R A 1930The genetical theory of natural selection (Oxford: Clarendon Press)

    Book  Google Scholar 

  • Frenz D A, Akiyama S K, Paulsen D F and Newman S A 1989a Latex beads as probes of cell surface-extracellular matrix interactions during chondrogenesis: evidence for a role for amino-terminal heparin-binding domain of fibronectin;Dev. Biol. 136 87–96

    Article  CAS  PubMed  Google Scholar 

  • Frenz D A, Jaikaria N S and Newman S A 1989b The mechanism of precartilage mesenchymal condensation: a major role for interaction of the cell surface with the amino-terminal heparin-binding domain of fibronectin;Dev. Biol. 136 97–103

    Article  CAS  PubMed  Google Scholar 

  • Gilbert S F 2005 Mechanisms for the environmental regulation of gene expression;J. Biosci. 30 67–74

    Article  Google Scholar 

  • Griffiths P E and Neumann-Held E M 1999 The many faces of the gene;BioScience 49 656–662

    Article  Google Scholar 

  • Goldschmidt R B 1940The material basis of evolution (New Haven: Yale University Press)

    Google Scholar 

  • Gottlieb L D 1984 Genetics and morphological evolution in plants;Am. Nat. 123 681–709

    Article  Google Scholar 

  • Hentschel H G, Glimm T, Glazier J A and Newman S A 2004 Dynamical mechanisms for skeletal pattern formation in the vertebrate limb;Proc. R. Soc. London B. Biol. Sci. 271 1713–1722

    Article  CAS  Google Scholar 

  • Hollick J B, Dorweiler J E and Chandler V L 1997 Paramutation and related allelic interactions;Trends Genet. 13 302–308

    Article  CAS  PubMed  Google Scholar 

  • Jablonka E and Lamb M J 1995Epigenetic inheritance and evolution (Oxford, UK: Oxford University Press)

    Google Scholar 

  • Jenkin F 1867 Review of ’The origion of species’;North Br. Rev. 46 277–318

    Google Scholar 

  • Johnston T D and Gottlieb G 1990 Neophenogenesis: a developmental theory of phenotypic evolution;J. Theor. Biol. 147 471–495

    Article  CAS  PubMed  Google Scholar 

  • Kosher R A, Savage M P and Chan S C 1979 In vitro studies on the morphogenesis and differentition of the mesoderm subjacent to the apical ectodermal ridge of the embryonic chick limb bud;J. Embryol. Exp. Morphol. 50 75–97

    CAS  PubMed  Google Scholar 

  • Kosher R A, Walker K H and Ledger P W 1982 Temporal and spatial distribution of fibronectin during development of the embryonic chick limb bud;Cell. Differ. 11 217–228

    Article  CAS  PubMed  Google Scholar 

  • Lamarck J B 1809 (1984)Zoological philosophy: an exposition with regard to the natural history of animals (Chicago: University of Chicago Press)

    Google Scholar 

  • Leonard C M, Fuld H M, Frenz D A, Downie S A, Massague J and Newman S A 1991 Role of transforming growth factorbeta in chondrogenic pattern formation in the embryonic limb: stimulation of mesenchymal condensation and fibronectin gene expression by exogenous TGF-beta and evidence for endogenous TGF-beta-like activity;Dev. Biol. 145 99–109

    Article  CAS  PubMed  Google Scholar 

  • Martin G R 1998 The roles of FGFs in the early development of vertebrate limbs;Genes Dev. 12 1571–1586

    Article  CAS  PubMed  Google Scholar 

  • Mayr E 1982The growth of biological thought: diversity, evolution, and inheritance (Cambridge, Mass.: Belknap Press)

    Google Scholar 

  • McLaren A and Michie D 1958 An effect of the uterine environment upon skeletal morphology in the mouse;Nature (London) 181 1147–1148

    Article  CAS  Google Scholar 

  • Meinhardt H and Gierer A 2000 Pattern formation by local selfactivation and lateral inhibition;Bioessays 22 753–760

    Article  CAS  PubMed  Google Scholar 

  • Michaud E J, Bultman S J, Stubbs L J and Woychik R P 1993 The embryonic lethality of homozygous lethal yellow mice (Ay/Ay) is associated with the disruption of a novel RNA-binding protein;Genes Dev. 7 1203–1213

    Article  CAS  PubMed  Google Scholar 

  • Miura T and Maini P K 2004 Periodic pattern formation in reaction-diffusion systems: an introduction for numerical simulation;Anat. Sci. Int. 79 112–123

    Article  PubMed  Google Scholar 

  • Miura T and Shiota K 2000 TGFbeta2 acts as an “activator” molecule in reaction-diffusion model and is involved in cell sorting phenomenon in mouse limb micromass culture.;Dev. Dyn. 217 241–249

    Article  CAS  PubMed  Google Scholar 

  • Moftah M Z, Downie S A, Bronstein N B, Mezentseva N, Pu J, Maher P A and Newman S A 2002 Ectodermal FGFs induce perinodular inhibition of limb chondrogenesis in vitro and in vivo via FGF receptor 2;Dev. Biol. 249 270–282

    Article  CAS  PubMed  Google Scholar 

  • Moss L 2003What genes can’t do (Cambridge, Mass.: MIT Press)

    Google Scholar 

  • Müller G B 1990 Developmental mechanisms at the origin of morphological novelty: A side-effect hypothesis; inEvolutionary innovations (ed.) M Nitecki (Chicago: University of Chicago Press) pp 99–130

    Google Scholar 

  • Müller G B and Wagner G P 2003 Innovation; inKeywords and concepts in evolutionary developmental biology (eds) B K Hall and W M Olson (Cambridge, MA: Harvard University Press) pp 218–227

    Google Scholar 

  • Newman S A 1994 Generic physical mechanisms of tissue morphogenesis: A common basis for development and evolution;J. Evol. Biol. 7 467–488

    Article  Google Scholar 

  • Newman S A 2003 From physics to development: the evolution of morphogenetic mechanisms; inOrigination of organismal form: beyond the gene in developmental and evolutionary biology (eds) G B Müller and S A Newman (Cambridge, MA.: MIT Press) pp 221–239

    Google Scholar 

  • Newman S A 2005 EvoDevo 1-0: William Bateson’s physicalist ideas; inFrom embryology to evo-devo: a history of evolutionary development (eds) J Maienschein and M Laubichler (Cambridge, MA: MIT Press) (in press)

    Google Scholar 

  • Newman S A and Comper W D 1990 ’Generic’ physical mechanisms of morphogenesis and pattern formation;Development 110 1–18

    Article  CAS  PubMed  Google Scholar 

  • Newman S A and Forgacs G 2005 Complexity and self-organization in biological development and evolution; inComplexity in chemistry, biology and ecology (eds) D Bonchev and D H Rouvray (Berlin: Springer) (in press)

    Google Scholar 

  • Newman S A and Frisch H L 1979 Dynamics of skeletal pattern formation in developing chick limb;Science 205 662–668

    Article  CAS  PubMed  Google Scholar 

  • Newman S A and Müller G B 2000 Epigenetic mechanisms of character origination;J. Exp. Zool. 288 304–317

    Article  CAS  PubMed  Google Scholar 

  • Newman S A and Tomasek J J 1996 Morphogenesis of connective tissues; inExtracellular matrix (ed.) W D Comper (Amsterdam: Harwood Academic Publishers) pp 335–369

    Google Scholar 

  • Oberlender S A and Tuan R S 1994 Expression and functional involvement of N-cadherin in embryonic limb chondrogenesis;Development 120 177–187

    Article  CAS  PubMed  Google Scholar 

  • Orel V 1996Gregor Mendel: the first geneticist (Oxford; New York: Oxford University Press)

    Google Scholar 

  • Ornitz D M and Marie P J 2002 FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease;Genes Dev. 16 1446–1465

    Article  CAS  PubMed  Google Scholar 

  • Oyama S 2000The ontogeny of information: developmental systems and evolution, 2nd Edition (Durham: Duke University Press)

    Book  Google Scholar 

  • Pal C and Miklos I 1999 Epigenetic inheritance, genetic assimilation and speciation;J. Theor. Biol. 200 19–37

    Article  CAS  PubMed  Google Scholar 

  • Peters K G, Werner S, Chen G and Williams L T 1992 Two FGF receptor genes are differentially expressed in epithelial and mesenchymal tissues during limb formation and organogenesis in the mouse;Development 114 233–243

    Article  CAS  PubMed  Google Scholar 

  • Reilly K M 2004 The importance of genome architecture in cancer susceptibility: location, location, location;Cell Cycle 3 1378–1382

    Article  CAS  PubMed  Google Scholar 

  • Salazar-Ciudad I, Newman S A and Solé R 2001 Phenotypic and dynamical transitions in model genetic networks. I. Emergence of patterns and genotype-phenotype relationships;Evol. Dev. 3 84–94

    Article  CAS  PubMed  Google Scholar 

  • Saunders J W Jr1948 The proximo-distal sequence of origin of the parts of the chick wing and the role of the ectoderm;J. Exp. Zool. 108 363–402

    Article  PubMed  Google Scholar 

  • Schmalhausen I I 1949Factors of evolution (Philadelphia: Blakiston)

    Google Scholar 

  • Shapiro M D, Hanken J and Rosenthal N 2003 Developmental basis of evolutionary digit loss in the Australian lizard Hemiergis;J. Exp. Zool. B Mol. Dev. Evol. 297 48–56

    Article  PubMed  Google Scholar 

  • Simpson G G 1953 The Baldwin effect;Evolution 7 110–117

    Article  Google Scholar 

  • Stern C and Sherwood E R 1966The origin of genetics: a Mendel source book (San Francisco: W H Freeman)

    Google Scholar 

  • Szebenyi G, Savage M P, Olwin B B and Fallon J F 1995 Changes in the expression of fibroblast growth factor receptors mark distinct stages of chondrogenesis in vitro and during chick limb skeletal patterning;Dev. Dyn. 204 446–456

    Article  CAS  PubMed  Google Scholar 

  • Tautz D 1996 Selector genes, polymorphisms, and evolution;Science 271 160–161

    Article  CAS  PubMed  Google Scholar 

  • Tickle C 2003 Patterning systemsfrom one end of the limb to the other;Dev. Cell 4 449–458

    Article  CAS  PubMed  Google Scholar 

  • Tomasek J J, Mazurkiewicz J E and Newman S A 1982 Nonuniform distribution of fibronectin during avian limb development;Dev. Biol. 90 118–126

    Article  CAS  PubMed  Google Scholar 

  • Trut L N 1999 Early canid domestication: the farm-fox experiment;Am. Sci. 87 160–169

    Article  Google Scholar 

  • Turing A 1952 The chemical basis of morphogenesis;Philos. Trans. R. Soc. London B 237 37–72

    Article  Google Scholar 

  • Waddington C H 1942 Canalization of development and the inheritance of acquired characters.;Nature (London) 150 563–565

    Article  Google Scholar 

  • Weaver I C, Cervoni N, Champagne F A, D’Alessio A C, Sharma S, Seckl J R, Dymov S, Szyf M and Meaney M J 2004 Epigenetic programming by maternal behavior;Nat. Neurosci. 7 847–854

    Article  CAS  PubMed  Google Scholar 

  • West-Eberhard M J 1998 Evolution in the light of developmental and cell biology, and vice versa;Proc. Natl. Acad. Sci. USA 95 8417–8419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West-Eberhard M J 2003Developmental plasticity and evolution (Oxford; New York: Oxford University Press)

    Book  Google Scholar 

  • Wilson G N 1998 Correlated heart/limb anomalies in Mendelian syndromes provide evidence for a cardiomelic developmental field;Am. J. Med. Genet. 76 297–305

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Cell Biology and Anatomy, Basic Science Building, New York Medical College, 10595, Valhalla, NY, USA

    Stuart A. Newman

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Newman, S.A. The pre-Mendelian, pre-Darwinian world: Shifting relations between genetic and epigenetic mechanisms in early multicellular evolution. J Biosci 30, 75–85 (2005). https://doi.org/10.1007/BF02705152

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