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Multicellular agency: an organizational view

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Abstract

We argue that the transition from unicellular to multicellular (MC) systems raises important conceptual challenges for understanding agency. We compare several MC systems (from bacterial swarms to colonies and plants, and to lower metazoans) displaying different forms of collective behavior, and we analyze whether these actions can be considered organismically integrated and attributable to the whole. We distinguish between a ‘constitutive’ and an ‘interactive’ dimension of organizational complexity, and we argue that MC agency requires a radical entanglement between the related processes which we call “the constitutive-interactive closure principle”. We explain in detail that this is not possible without a regulatory center functionally integrating the two dimensions, and we also argue that, in turn, this type of regulation would not be possible without a special type of organization between the cells required for the development and maintenance of systems capable of integrated behavior.

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Notes

  1. Accordingly, functions such as digestion, sweating, freezing in front of headlights, schreck reactions and helpless writhing, coughing or sneezing, etc., do not count as actions, since they do not provide a modification of the environment that could be functional for the system.

  2. Oriented growth and bending movements of plants and sessile animals are not considered as actively directional movements (see next section; and also Burge 2009, pp. 257–259 for a relevant discussion). A genuinely motile agent does not have to stand and passively wait to accept whatever the environment will bring at it, but on the contrary, it may move and thus take the initiative in exploiting the environmental resources.

  3. Over the course of the history of life, cells have assembled into groups, bringing forth several types of relatively stable MC associations: biofilms, filaments, colonies, various types of aggregations, and full-fledged MC organisms.

  4. There is also a significant increase in size that these MC communities achieve, which results in the aggregative/collective effects of several unicellular actions (e.g., breaking down of large food sources by the collective excretion of enough hydrolytic enzymes, resistance to chemical substances—e.g., penicillin-resistant biofilms, etc.). We don’t consider these ‘passive’ effects of multicellularity and their implications as pertaining to agency.

  5. This requirement casts aside cases such as digestion, blood circulation, heart beating, tanning, sweating, etc., which are the result of endogenously driven processes that are functional for the system but they don’t result in the functional changing of the environment.

  6. Even in very primitive forms of sensorimotor coordination, such as in E.coli (and many other bacterial) chemotaxis, the Two Components Signal Transduction system, which acts as a memory and inner connection between sensors and effectors, operates in a different timescale than core metabolic processes, to the point that such kind of taxes are considered second-order processes with respect to metabolism (van Duijn et al. 2006).

  7. See Moreno and Mossio (2015) for an extended discussion on the idea of closure in biology.

  8. For instance, the influence of developing leaves extends to great distances along the axis of the plant, while it is severely restricted in other orientations.

  9. An interactive process can be more or less complex according to the number of functional constraints required for the guidance of a given action. For example, a (successful) execution and guidance of a fast escaping swimming behavior of a fish in an irregular tridimensional marine environment (e.g., in a submarine cave) requires a much greater number of functional constraints compared to what is needed for the rigid movement of closing its leaves by a Dionaea plant in order to trap an insect.

  10. We will consider an action as integrated if its issuance is attributable to the whole MC system (instead of only to a part of it) and if its effects contribute to the production and maintenance of the whole MC constitutive organization (instead of only to one aspect of it). This definition will be explained and developed throughout this article, especially in “The ‘constitutive-interactive closure principle’ explains integrated MC agency” section.

  11. M. xanthus cells form structured biofilms with motility-mediated expansion (formation of tentacle-like packs cell groups and synchronized rippling waves of oscillating cells) when other microbial nutrients are available in the environment, and massive spore-filled aggregates that rise upwards from the substratum to form fruiting bodies, mainly when exposed to low or no nutrients.

  12. Somatic cells are terminally differentiated, they have an eyespot—a primitive visual system used like radar to scan the environment for light sources—and they do not divide. Hence, contrary to germ cells, they have flagella that continuously beat and provide the MC system with a phototactic motility.

  13. Besides the well-known case of the Venus flytrap there are other examples of plants capable of fast movement, such as Mimosa pudica, the Telegraph plant (Codariocalyx motorius), sundews (Drosera) with relatively slow movements compared to the other cases, and bladderworts (Utricularia).

  14. This way of getting nutrients and energy is an adaptation found in several plants living in soils poor in nutrients (Ellison 2006).

  15. It has been hypothesized and experimentally supported that when a hair is touched there is a threshold of ion buildup, which is stored as an increase in ion concentration for a short time. The touch of a second hair within about twenty seconds will cumulatively trigger the passing of the threshold, thus activating the closing of the leaves (Volkov et al. 2007).

  16. An epithelium is defined as a sheet of polarized cells that are joined by belt-like junctions around their apical margins, and with an extracellular matrix (ECM) being present only apically and basally (the basal lamina). Jellyfish are almost wholly epithelial and the simplest MC animals at the tissue grade of organization (Tyler 2003).

  17. Two types of cells with contractile properties are known across MC animals: true muscle cells and epitheliomuscular cells. All muscular structures described so far in Cnidaria are epitheliomuscular (Burton 2008).

  18. Despite the underlying distributed nature of these nervous systems, some jellyfish present a nerve cell density that is at least six times higher in the head region than in the body column. In certain medusas, the RFamide sensory neurons are more abundant in the manubrium along the bell margin, in the tentacle bulbs, and along the tentacles. For example, Aglantha digitale, in addition to their diffuse nerve net, possess an elaborate nerve ring around their central opening (manubrium) and around the oral opening. These characteristics are considered to reflect a considerable degree of centralization (Galliot et al. 2009; Satterlie 2011).

  19. The complete germ-soma differentiation in V. carteri concerns the separation of somatic and reproductive characteristics that used to be integrated in the unicellular ancestor, and not the development of new structures related to the production and execution of new actions.

  20. The wide repertoire of neural-based movements demonstrated by the eumetazoa was physiologically and metabolically possible only through the formation of body cavities, and as such, through the creation of extra internal space for the development of organs. The internalization of physiological functions is a common characteristic of the evolutionary developments that accompanied the explosion of behaviors in MC animals (Rosslenbroich 2009).

  21. Eumetazoa is the clade comprising all animal groups except the Porifera (sponges) and Placozoa.

  22. Due to lack of space, the deep relationship between epithelial-based development and the building a body organization that permits a complex form of motility will not be discussed in this paper. For a detailed treatment see Arnellos and Moreno (2015).

  23. Porifera and Placazoa—the only metazoans lacking NS—are essentially sessile. Only some marine and freshwater species of sponges can move (very slowly) across the seabed through the cumulative amoeboid or crawling locomotion of the individual cells that compose their lower surfaces (Bond and Harris 1988). Some tufted larvae (mainly in their parenchymella stage) similarly show phototactic responses that are the result of independent responses (either photonegative or photopositive) of individual cells (operating both as sensors and effectors) in the ciliated posterior tuft of the larva (Maldonado et al. 2003).

  24. The apical sensory organ seems to play the role of chemo- and mechano-sensory structure with neuroendocrine functions involved in larvae migration and metamorphosis also in free swimming invertebrate as well as in bilaterian larvae such as gastropods, nematodes, etc. (Voronezhskaya and Khabarova 2003; Marlow et al. 2014).

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Acknowledgments

We would like to thank Leonardo Bich and Werner Callebaut for reading earlier versions of the paper and making useful comments and suggestions. A.A. would like to thank the fellows and participants of the KLI Colloquia for their vivid discussion. A.M. acknowledges the grants of the Basque Government IT 590-13 and of the Spanish Ministerio de Industria e Innovación FFI2011-25665 and BFU2012-39816-C02-02. Finally, we would like to thank the two anonymous reviewers for useful suggestions that contributed to the improvement of the manuscript.

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The authors declare that they have no conflict of interest.

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  1. The KLI Institute, Martinstraße 12, 3400, Klosterneuburg, Austria

    Argyris Arnellos

  2. IAS-Research Centre for Life, Mind and Society, Department of Logic and Philosophy of Science, University of the Basque Country, Avda. Tolosa 70, 20018, Donostia, San Sebastián, Spain

    Alvaro Moreno

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  1. Argyris Arnellos
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Correspondence to Argyris Arnellos or Alvaro Moreno.

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Arnellos, A., Moreno, A. Multicellular agency: an organizational view. Biol Philos 30, 333–357 (2015). https://doi.org/10.1007/s10539-015-9484-0

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