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Microbes modeling ontogeny

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Abstract

Model organisms are central to contemporary biology and studies of embryogenesis in particular. Biologists utilize only a small number of species to experimentally elucidate the phenomena and mechanisms of development. Critics have questioned whether these experimental models are good representatives of their targets because of the inherent biases involved in their selection (e.g., rapid development and short generation time). A standard response is that the manipulative molecular techniques available for experimental analysis mitigate, if not counterbalance, this concern. But the most powerful investigative techniques and molecular methods are applicable to single-celled organisms (‘microbes’). Why not use unicellular rather than multicellular model organisms, which are the standard for developmental biology? To claim that microbes are not good representatives takes us back to the original criticism leveled against model organisms. Using empirical case studies of microbes modeling ontogeny, we break out of this circle of reasoning by showing: (a) that the criterion of representation is more complex than earlier discussions have emphasized; and, (b) that different aspects of manipulability are comparable in importance to representation when deciding if a model organism is a good model. These aspects of manipulability harbor the prospect of enhancing representation. The result is a better understanding of how developmental biologists conceptualize research using experimental models and suggestions for underappreciated avenues of inquiry using microbes. More generally, it demonstrates how the practical aspects of experimental biology must be scrutinized in order to understand the associated scientific reasoning.

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Notes

  1. “The motivation for their study is not simply to understand how that particular animal develops, but to use it as an example of how all animals develop” (Slack 2006, 61). “Basic research aimed at understanding the general principles of life uses model organisms such as the frog, chicken, fish, and mouse” (Nüsslein-Volhard 2006, 138).

  2. Much of the funding for developmental biology in the United States comes from the National Institutes of Health. A similar pattern holds in other national contexts. For example, the Welcome Trust makes the connection explicit: “Yeast, fruit flies, nematode worms and mice: just some of the model organisms whose study is bringing insights into the role of genes in the human body” (http://genome.wellcome.ac.uk/node30073.html, our emphasis). It is difficult to escape questions of human biomedical applicability when assessing model organism use, but we will not explore it here (see Ankeny and Leonelli 2011; Bolker 2009 for further discussion).

  3. There is an ambiguity in talk of model organisms “representing” other organisms. One possibility is that this representing is done indirectly through abstract models (“representations”) constructed from data derived from the study of developmental model organisms. Another possibility is that the material entity itself is a “direct” representation of other organisms. Although we think both possibilities have merit in understanding the reasoning practices of developmental biology, our argument does not depend on its resolution one way or another. Therefore, we will continue using the phrasing of model organisms representing other organisms.

  4. “The past two decades have brought major breakthroughs in our understanding of the molecular and genetic circuits that control a myriad of developmental events in vertebrates and invertebrates. These detailed studies have revealed surprisingly deep similarities in the mechanisms underlying developmental processes across a wide range of bilaterally symmetric metazoans … [these] comparisons have defined a common core of genetic pathways guiding development” (Bier and McGinnis 2003, 25, our emphasis).

  5. Hickson et al. (2009) argue that metastatic colonization in cancer cells is controlled by a quorum-sensing mechanism directly akin to bacterial cell–cell communication.

  6. “For a large number of problems there will be some animal of choice or a few such animals on which it can be most conveniently studied” (Krogh 1929, 202).

  7. Note that this distinction is not identical to Bolker’s two modes of representation: exemplary and surrogate (Bolker 2009). Both general and Krogh-principle model organisms can instantiate exemplary modes (serving basic research by exemplifying a larger group) and surrogate modes (providing indirect experimental access phenomena that are difficult to work with).

  8. Representation often takes a back seat in descriptions of the advantages of model organisms, such as in the Welcome Trust’s account of zebrafish, where the preferable model features are almost all manipulation related: “The zebrafish comes close to being the ideal model organism for vertebrate development because it appears to combine the best features of all the other models. … zebrafish embryos develop externally and can be viewed and manipulated at all stages. … zebrafish development is more rapid than in the frog, the organisation of the embryo is simpler and … the embryo is transparent. Like the mouse, the zebrafish is amenable to genetic analysis and has a similar generation interval (2–3 months). However, zebrafish are smaller than mice and they produce more offspring in a shorter time. … It is easy to induce new mutations in zebrafish and large-scale screens have been carried out to identify mutations causing defects in particular biological processes, such as the developing nervous system” (http://genome.wellcome.ac.uk/doc_WTD020806.html).

  9. “Neither the frog nor the chicken is favoured for its genetic amenability. …An additional disadvantage of Xenopus laevis for genetic analysis is that the species is tetraploid. …The predominant reason for the use of Xenopus and chickens as models is that they produce large, robust embryos whose development occurs outside the body of the mother. …the embryos are much more accessible than those of mammals. …The accessibility of the embryos means they can be surgically manipulated or treated with proteins and chemicals that interfere with normal development” (http://genome.wellcome.ac.uk/doc_WTD020805.html).

  10. “Because mice do not require Dmrt1 for primary sex determination, they may not be typical vertebrates, but the genetic and molecular tools that are available in the mouse have allowed a detailed dissection of Dmrt1 function” (Matson and Zarkower 2012, 169, our emphasis).

  11. “One of the most attractive features of C. elegans is that it can be handled like a microbe. Large numbers of worms can be maintained inexpensively on lawns of bacteria growing on standard agar plates, but viable cultures can be stored as frozen stocks and then revived when required” (http://genome.wellcome.ac.uk/doc_WTD020809.html, our emphasis).

  12. Others have noted this possibility but tended to be pessimistic because of our lack of knowledge: “Many problems in eukaryotic cell biology can be most easily studied in unicellular organisms, such as yeast…. Other problems, however, currently can be studied meaningfully only in intact animals. This may be because we do not know how to mimic crucial aspects of the organismal environment in vitro, because cell–cell interactions play an important role, or because the process under study involves a behavior that is not currently understood in terms of the properties of individual cells. Examples include pattern formation in the embryo and the development and function of organ systems” (Rubin 1988, 1453, our emphasis).

  13. These kinds of questions are pertinent apart from microbial models. Developmental biology already has synthetic models that break continuity with natural organisms, such as tissue explants from Xenopus (Sive et al. 2007). “Keller” explants are portions of dorsal mesendoderm and ectoderm that must be dissected out of intact embryos, assembled into a non-natural rectangular shape, flattened (‘sandwiched’) between a slide and cover slip (or equivalent), and cultured in vitro. They facilitate the observation of convergent extension, a type of morphogenesis, relevant to the developmental phenomenon of gastrulation. This suggests further treatment of what it means for something to be a “synthetic” model of development and the different ways one achieves this result (e.g., de novo construction versus extraction from a living entity).

  14. We owe special thanks to an anonymous referee for stressing this point explicitly.

  15. This also has been demonstrated experimentally in Dictyostelium: “the single-cell bottleneck is a powerful stabilizer of cellular cooperation in multicellular organisms” (Kuzdzal-Fick et al. 2011, 1548).

  16. There are precedents in the history of philosophy of science that elevate manipulative capacities as a mark of epistemic worthiness, such as Bacon’s notion of maker’s knowledge (Pérez-Ramos 1989), but the intended scope of our remarks is with respect to the critical literature surrounding model organisms over the past three decades.

  17. The same strategy applies to models of evolution: a regular movement between microbial and metazoan models of evolution is a potent methodology for the dissection of the mechanics of evolutionary processes because it maximizes experimental manipulation in conjunction with representational calibration derived from multiple model organism types.

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Acknowledgments

We benefited from the feedback and critical comments provided by Ana Escalante, Brian Hall, Masayori Inouye, Sabina Leonelli, Katherine Liu, Maureen O’Malley, Maria Rebolleda-Gomez, Pauline Schaap, Beckett Sterner, Greg Velicer, and anonymous reviewers for the journal. Their assistance should not be interpreted as an endorsement of our argument. Special thanks to participants of the symposium “Molecules, Organisms, Systems: Developing Multilevel Integrated Insights into Biological Processes” at the 23rd biennial meeting of the Philosophy of Science Association (San Diego, November 2012), where a subset of this material was presented and discussed, and to participants of a colloquium presentation of this manuscript at the Department of History and Philosophy of Science, Indiana University (January 2013). ACL is grateful to Matthew Spates for helpful discussion and research assistance. MT dedicates this article to Sumiko Inouye, a fellow developmental microbiologist and close friend, who will be greatly missed.

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  1. Department of Philosophy, Minnesota Center for Philosophy of Science, University of Minnesota, 831 Heller Hall, 271 19th Ave. S., Minneapolis, MN, 55455-0310, USA

    Alan C. Love

  2. Department of Ecology, Evolution, and Behavior, Biotechnology Institute, University of Minnesota, 100 Ecology, 1987 Upper Buford Circle, St. Paul, MN, 55108, USA

    Michael Travisano

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Love, A.C., Travisano, M. Microbes modeling ontogeny. Biol Philos 28, 161–188 (2013). https://doi.org/10.1007/s10539-013-9363-5

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