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Managing variation in the investigation of organismal development: problems and opportunities

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Abstract

This paper aims to clarify the consequences of new scientific and philosophical approaches for the practical-theoretical framework of modern developmental biology. I highlight normal development, and the instructive-permissive distinction, as key parts of this framework which shape how variation is conceptualised and managed. Furthermore, I establish the different dimensions of biological variation: the units, temporality and mode of variation. Using the analytical frame established by this, I interpret a selection of examples as challenges to the instructive-permissive distinction. These examples include the phenomena of developmental plasticity and transdifferentiation, the role of the microbiome in development, and new methodological approaches to standardisation and the assessment of causes. Furthermore, I argue that investigations into organismal development should investigate the effects of a wider range of kinds of variation including variation in the units, modes and temporalities of development. I close by examining various possible opportunities for producing and using normal development free of the assumptions of the instructive-permissive distinction. These opportunities are afforded by recent developments, which include new ways of producing standards incorporating more natural variation and being based on function rather than structure, and the ability to produce, store, and process large quantities of data.

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Notes

  1. Exceptions that do deal with variation include: Hall and Hallgrímsson (2005); Hallgrímsson et al. (2012); Klingenberg (2010); Minelli (2015).

  2. Though some scientists have adopted a DST approach, it is reasonable to say that DST itself is marginal within developmental biology, partly because of perceptions of its “inutility” and that “it motivates relatively little research” (Shea 2011). I find much of what DST has to say about development compelling, but acknowledge this criticism.

  3. I am informed by an anonymous referee that the origin of the term “permissive” in this sense dates back to Holtzer (1968). While I have not been able to obtain that source, consulting a review of the book in which Holtzer’s work was published I am satisfied that this is indeed the case (DeHaan 1968). Scott Gilbert has also cited Holtzer’s coinage of the term (e.g. Gilbert 2003b, 349).

  4. This problem was perhaps most cogently stated, alongside an early version of the principle of differential gene expression, by Thomas Hunt Morgan in his 1934 book Embryology and Genetics.

  5. Though, it must be stressed that ‘plasticity’ encompasses a large number of different processes and mechanisms that operate in different ways and in relation to environmental factors in different ways, so any inferences deriving from one kind of plasticity may not be applicable to others (Forsman 2014). I have tried to make my own general statements on plasticity to be ones applicable to most types of plasticity, and have stated otherwise when my comments concern particular types.

  6. This concept of heterochrony is inclusive of more kinds of variation than the changes in size and shape dealt with by Stephen J. Gould and Pere Alberch (see Smith 2002).

  7. The type of plasticity in which the result of the environmental input is mediated by the developmental processes of the organism is known as active plasticity, and can be contrasted with passive plasticity, in which the environmental input (such as temperature) is directly proportional to the extent of the change effected (for example by increased temperature speeding up certain metabolic processes) (Forsman 2014, 3).

  8. The proposers of heterogenization believe that it is just as valuable a strategy within a single laboratory as between multiple laboratories.

  9. There are numerous ethical implications of the changes in practice suggested here. Firstly, the number of animals needed for particular experiments will, in the absence of alternatives being used, increase considerably, counteracting attempts to reduce the number of animals used in research, and potentially coming up against legislation which, in the UK at least, strictly calculates the numbers of animals for particular experiments based on statistical significance. Another consideration is that it may even be deemed unethical to reduce the sample size and therefore the number of animals used, because for particular questions asked this may reduce the quality of the results produced, due to not taking the variation of a number of potentially important factors into account.

  10. A question that in a different form was at the heart of Canguilhem’s analysis, inspired by Kurt Goldstein, of the distinction between the normal and the pathological (Canguilhem 2008).

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  1. Department of Sociology, Philosophy and Anthropology, and Egenis, The Centre for the Study of Life Sciences, University of Exeter, Byrne House, St. German’s Road, Exeter, Devon, EX4 4PJ, UK

    James W. E. Lowe

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Lowe, J.W.E. Managing variation in the investigation of organismal development: problems and opportunities. HPLS 37, 449–473 (2015). https://doi.org/10.1007/s40656-015-0089-3

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