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The return of the whole organism

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Abstract

The long trend towards analysis at lower and lower levels is starting to reverse. The new integrative studies must make use of the resources uncovered by molecular biology but should also use the characteristics of whole organisms to measure the outcomes of developmental processes. Two examples are given of how movement between levels of analysis is being used with increasing power and promise. The first is the study of behavioural imprinting in birds where many of the molecular and neural mechanisms involved have been uncovered and are now being integrated to explain the behaviour of the whole animal. The second is the triggering during sensitive periods in early life by environmental events of one of several alternative modes of development leading to different phenotypes. A renewed focus on the whole organism is also starting to change the face of evolutionary biology. The decision-making and adaptability of the organism is recognized an important driver of evolution and is increasingly seen as an alternative to the gene-focused views.

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References

  • Akam M, Holland P, Ingham P and Wray G 1994The evolution of developmental mechanisms (Cambridge: Company of Biologists)

    Google Scholar 

  • Baldwin J M 1896 A new factor in evolution;Am. Nat. 30 441–451, 536–553

    Article  Google Scholar 

  • Barker D J P 1998Mothers, babies and health in later life (Edinburgh: Churchill Livingstone)

    Google Scholar 

  • Bateson P 1981 Discontinuities in development and changes in the organization of play in cats; inBehavioral development (eds) K Immelmann, G W Barlow, L Petrinovich and M Main (Cambridge: Cambridge University Press) pp 28l-295

    Google Scholar 

  • Bateson P 1988 The active role of behaviour in evolution; inProcess and metaphors in evolution (eds) M-W Ho and S Fox (Chichester: Wiley) pp 191–207

    Google Scholar 

  • Bateson P 1990 Is imprinting such a special case?;Philos. Trans. R. Soc. London B 329 125–131

    Article  Google Scholar 

  • Bateson P 2000 What must be known in order to understand imprinting?; inThe evolution of cognition (eds) C Heyes and L Huber (Cambridge, Mass: The MIT Press) pp 85–102

    Google Scholar 

  • Bateson P 2001 Fetal experience and good adult design;Int. J. Epidemiol. 26 561–570

    CAS  Google Scholar 

  • Bateson P 2004 The active role of behaviour in evolution;Biol. Philos. 19 283–294

    Article  Google Scholar 

  • Bateson P and D’Udine B 1986 Exploration in two inbred strains of mice and their hybrids: additive and interactive models of gene expression;Anim. Behav. 34 1026–1032

    Article  Google Scholar 

  • Bateson P and Horn G 1994 Imprinting and recognition memorya neural-net model;Anim. Behav. 48 695–715

    Article  Google Scholar 

  • Bateson P and Martin P 2000Design for a life: How behaviour develops (London: Vintage Paperbacks)

    Google Scholar 

  • Bateson P and Young M 1981 Separation from mother and the development of play in cats;Anim. Behav. 29 l73-l80

    Article  Google Scholar 

  • Bateson P, Martin P and Young M 1981 Effects of interrupting cat mothers’ lactation with bromocriptine on the subsequent play of their kittens;Physiol. Behav. 27 84l-845

    Article  Google Scholar 

  • Bateson P, Mendl M and Feaver J 1990 Play in the domestic cat is enhanced by rationing the mother during lactation;Anim. Behav. 40 514–525

    Article  Google Scholar 

  • Bateson P, Horn G and Rose S P R 1975 Imprinting: Correlations between behaviour and incorporation of (14C) Uracil into chick brain;Brain Res. 84 207–220

    Article  CAS  PubMed  Google Scholar 

  • Bateson P, Rose S P R and Horn G 1973 Imprinting: lasting effects on uracil incorporation into chick brain;Science 181 576–578

    Article  CAS  PubMed  Google Scholar 

  • Bateson P, Barker D, Clutton-Brock T, Deb D, D’Udine, B Foley R A, Gluckman P, Godfrey K, Kirkwood T, Lahr M M, McNamara J, Metcalfe N B, Monaghan P, Spencer H G and Sultan S E 2004 Developmental plasticity and human health;Nature (London) 430 419–421

    Article  CAS  Google Scholar 

  • Bateson W 1909 Heredity and variation in modern lights; inDarwin and modern science (ed.) A C Seward (Cambridge: Cambridge University Press) pp 85–101

    Google Scholar 

  • Bock G R and Goode J A e 1998The limits of reductionism in biology Novartis Foundation Symposium 213, (Chichester: Wiley)

    Book  Google Scholar 

  • Broadhurst P L 1979 The experimental approach to behavioural evolution; inTheoretical advances in behavioural genetics (eds) J R Royce and L P Mos (Alphen aan den Rijn: Sitjthoff and Noordhoff) pp 350–375

    Google Scholar 

  • Caro T M and Bateson P 1986 Organisation and ontogeny of alternative tactics;Anim. Behav. 34 1483–1499

    Article  Google Scholar 

  • Cipolla-Neto J, Horn G and McCabe B J 1982 Hemispheric asymmetry and imprinting: the effect of sequential lesions to the hyperstriatum ventrale;Exp. Brain Res. 48 22–27

    Article  CAS  PubMed  Google Scholar 

  • Dobzhansky T 1937Genetics and origin of species (New York: Columbia University Press)

    Google Scholar 

  • Evans J D and Wheeler D E 2000 Expression profiles during honeybee caste determination;Genome Biol. 2 1–6

    Article  Google Scholar 

  • Evans J D and Wheeler D E 2001 Gene expression and the evo lution of insect polyphenisms;Bioessays 54 62–68

    Article  Google Scholar 

  • Gomendio M, Cassinello J, Smith M W and Bateson P 1995 Maternal state affects intestinal changes of rat pups at weaning;Behav. Ecol. Sociobiol. 37 71–80

    Article  Google Scholar 

  • Gottlieb G 1992Individual development and evolution (New York: Oxford University Press)

    Google Scholar 

  • Gottlieb G 1997Synthesizing nature-nurture: prenatal roots of instinctive behaviour, (Mahwah: Erlbaum)

    Google Scholar 

  • Hales C N and Barker D J P 1992 Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis;Diabetologia 35 595–601

    Article  CAS  PubMed  Google Scholar 

  • Hales C N, Desai M and Ozanne S E 1997 The thrifty phenotype hypothesis: how does it look after 5 years?;Diabetic Med. 14 189–195

    Article  CAS  PubMed  Google Scholar 

  • Heyes C and Huber L 2000The evolution of cognition (Cambridge: MIT Press)

    Book  Google Scholar 

  • Hollis K L ten Cate C and Bateson P 1991 Stimulus representation: a subprocess of imprinting and conditioning;J. Comp. Psychol. 105 307–317

    Article  CAS  PubMed  Google Scholar 

  • Honey R C Horn G Bateson P and Walpole M 1995 Functionally distinct memories for imprinting stimuli: behavioral and neural dissociations;Behav. Neurosci. 109 689–698

    Article  CAS  PubMed  Google Scholar 

  • Horn G 1985Memory, Imprinting and the brain (Oxford: Oxford University Press)

    Book  Google Scholar 

  • Horn G 1998 Visual imprinting and the neural mechanisms of recognition memory;Trends Neurosci. 21 300–305

    Article  CAS  PubMed  Google Scholar 

  • Horn G 2000 In memory; inBrain, perception, memory: Advances in cognitive neuroscience (ed.) J J Bolhuis (Oxford: Oxford University Press) pp 329–363

    Chapter  Google Scholar 

  • Horn G, McCabe B J and Bateson PPG 1979 An autoradiographic study of the chick brain after imprinting;Brain Res. 168 361–373

    Article  CAS  PubMed  Google Scholar 

  • Horn G, Rose S P R and Bateson PPG 1973 Monocular imprinting and regional incorporation of tritiated uracil into the brains of intact and ’split-brain’ chicks;Brain Res. 56 227–237

    Article  CAS  PubMed  Google Scholar 

  • Johnson M H and Horn G 1986 Dissociation between recognition memory and associative learning by a restricted lesion to the chick forebrain;Neuropsychologia 24 329–340

    Article  CAS  PubMed  Google Scholar 

  • Johnston T D and Edwards L 2002 Genes, interactions and the development of behavior;Psycholog. Rev. 109 26–23

    Article  Google Scholar 

  • Lee T M and Zucker I 1988 Vole infant development is influenced perinatally by maternal photoperiodic history;Am. J. Physiol. 255 R831-R838

    CAS  PubMed  Google Scholar 

  • Lehrman D S 1970 Semantic and conceptual issues in the naturenurture problem; inDevelopment and Evolution of Behavior eds) L R Aronson, E Tobach, D S Lehrman and J S Rosenblatt (San Francisco: Freeman) pp 17–52

    Google Scholar 

  • Lott D F 1991Intraspecific variation in the social systems of wild veterbrates (Cambridge: Cambridge University Press)

    Google Scholar 

  • Lloyd Morgan C 1896 On modification and variation;Science 4 733–740

    Article  Google Scholar 

  • Martin P 1984 The meaning of weaning;Anim. Behav. 32 1024–1026

    Article  Google Scholar 

  • Martin P and Bateson P 1985 The influence of experimentally manipulating a component of weaning on the development of play in domestic cats;Anim. Behav. 33 511–518

    Article  Google Scholar 

  • Mather K and Jinks J L 1971Biometrical genetics (London: Chapman and Hall)

    Book  Google Scholar 

  • Mayr E 1963Animal species and evolution (Cambridge: Harvard University Press)

    Book  Google Scholar 

  • McNamara J M and Houston A I 1996 State-dependent lifehistories;Nature (London) 380 215–221

    Article  CAS  Google Scholar 

  • Moran N A 1992 The evolutionary maintenance of alternative phenotypes;Am. Nat. 139 249–278

    Article  Google Scholar 

  • Muller H J 1940 Bearing of the Drosophila work on systematics; inThe new systematics (ed.) J S Huxley (Oxford: Oxford University Press) pp 125–268

    Google Scholar 

  • Odling-Smee F J, Laland K N and Feldman M W 2003Niche construction: The neglected process of evolution (Princeton: Princeton University Press)

    Google Scholar 

  • Orr H A and Presgraves D C 2000 Speciation by postzygotic isolation: forces, genes and molecules;BioEssays 22 1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Osborn H F 1896 Ontogenic and phylogenic variation;Science 4 786–789

    Article  CAS  PubMed  Google Scholar 

  • Oyama S, Griffiths P E and Gray R D 2001Cycles of contingency: developmental systems and evolution (Cambridge: MIT Press)

    Google Scholar 

  • Piaget J 1979Behaviour and evolution (London: Routledge and Kegan Paul)

    Google Scholar 

  • Raff R A 1996The shape of life: genes, development and evolution of animal form (Chicago: University of Chicago Press)

    Book  Google Scholar 

  • Rowell C H F 1971 The variable coloration of the Acridoid grasshoppers;Adv. Insect Physiol. 8 145–198

    Article  Google Scholar 

  • Schlichting C D and Pigliucci M 1998Phenotypic evolution: A reaction norm perspective (Sunderland: Sinauer)

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Smith E F S 1991 Early social development in hooded rats(Rattus norvegicus): a link between weaning and play;Anim. Behav. 41 513–524

    Article  Google Scholar 

  • Solomonia R O, Kiguradzw T, McCabe B J and Hprn G 2000 Neural cell adhesion molecules, CAM kinase II and long-term memory in the chick;Neuroreport 11 3139–3143

    Article  CAS  PubMed  Google Scholar 

  • Spalding D A 1873 Instinct with original observations on young animals;Macmillan’s Mag. 27 282–293

    Google Scholar 

  • Tan P L and Counsilman J J 1985 The influence of weaning on prey-catching behaviour in kittens;Z. Tierpsychol. 70 148–164

    Article  Google Scholar 

  • Waddington C H 1953 Genetic assimilation of an acquired character;Evolution 7 118–126

    Article  Google Scholar 

  • Waddington C H 1957The strategy of the genes (London: Allen and Unwin)

    Google Scholar 

  • Wcislo W T 1989 Behavioral environments and evolutionary change;Annu. Rev. Ecol. Syst. 20 137–169

    Article  Google Scholar 

  • Weber B H and Depew D J (eds) 2003Evolution and learning (Cambridge: MIT Press)

    Google Scholar 

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

    Book  Google Scholar 

  • Wright S 1963 Genic interaction; inMethodology in mammalian genetics (ed.) W J Burdette (San Francisco: Holden Day) pp 159–192

    Google Scholar 

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Bateson, P. The return of the whole organism. J Biosci 30, 31–39 (2005). https://doi.org/10.1007/BF02705148

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