The ASMO in its most basic form has been cast as an epithelial organization. The initial formulation took place in the context of early nervous systems and most attention was given to studies on electrical signaling by excitable and contractile epithelia (Josephson 1985; Mackie 1970, 2004a; Meech 2015). However, epithelia are more versatile than this, while the ASMO notion itself stands for a sensorimotor entity rather than a signaling or information processing device. For this purpose, we will discuss the ASMO conditions listed earlier to see how they connect to this wider array of epithelial features.
The ASMO notion subsumes a multicellular body, constituting an ‘inner space’ or domain, which is differentiated from the body’s ‘outer space’ or environment
Having a multicellular body is an obvious but also wide precondition for the ASMO. Without it there would be no multicellular organism at al. As discussed above, epithelia provide the key ingredients for building an integrated body. The flexible and easily to manipulate ‘origami’ sheets provide a good construction material, the two- and later three-dimensional structure provides a scaffold along which chemical signals can travel and where differences in membrane potentials can have their specific signaling effects for development.
This precondition becomes less obvious when attention is given to the word body and the claim that multicellular plants and fungi do not have bodies like animals have. The word ‘body’ conveys the presence of a specific integrated unit, for which the ASMO notion is set to provide an organizational story. This organizational story can also be linked to an ecological context where such bodies make evolutionary sense.
The ASMO is cast as a particular organization that enables sensorimotor relations at a multicellular level that are sensitive to macroscopic, changeable environmental stimulus arrays, such as in touch and vision. The question why, from an evolutionary perspective, it would be relevant to have such an ASMO is not addressed. It is similar to work on disentangling possible eye configurations in some lineage where the evolutionary relevance of eyes can be assumed. Still, the concept of a body has evolutionary features that connect to the ASMO in a plausible way.
The most relevant feature here is probably macrophagy, which means feeding on large food items. The feeding systems of animals take three main forms (Sperling and Vinther 2010). Sponges have a water canal system and water is pumped through the body where bacteria are filtered out and digested intracellularly, making this a form of microphagy. The only described species of the placazoa has a ventral mucociliary sole (Arendt et al. 2015), which consists of an extracellulary space between the underside of the organism and the surface it is positioned on. Barring some weird exceptions, other animals have an internal gut in some form or other, where large food items are digested inside the body but outside of the cells. Sperling and Vinther call the gut possibly the greatest metazoan innovation, which has been the key to the Cambrian prey-predator interactions and even the Cambrian Explosion (see also Arendt et al. 2015).
Macrophagy provides an ecological context where an ASMO becomes highly relevant. Foremost, for a mucociliary sole or a gut to work, the body must be positioned in relation to food items, which involves a sensorimotor process that actively and precisely manipulates the environment at the bodily scale. Interestingly, this life-style also involves the active manipulation of the body itself including regulating the treatment of ingested food, excreting waste, and maintaining a suitable internal homeostasis at a multicellular level by means of complex physiological processes. This fits in with the focus on internal coordination that is behind the ASMO notion and where the classic differentiation between inner physiology and external behavior becomes more diffuse as both constitute their own environments (Jékely et al. 2015a). In contrast, macrophagy need not involve any complex—heterogeneous—environment as long as the food items are plentiful and easy to find for a motile organism.
Epithelial characteristics are also relevant to generating the features relevant for macrophagy, including sealing off internal compartments for various functions (Rosslenbroich 2014). When the contents of such compartments can be buffered against a changing environment the concept of homeostasis can be extended to the multicellular organism level and in this way epithelia play an essential physiological role both during and after development (Skaer and Maddrell 1987; Leys et al. 2009).
The ASMO notion subsumes the presence of contractile epithelia
Many cnidarians have a contractile apparatus that consist to a large extent of contractile epithelia. As such, it is an unproblematic assumption to take such epithelia as a starting point for the ASMO. What the broader view on epithelia adds however is that contractility is a much more general and fundamental aspect of epithelia. Considering the essential role played by cellular contractions and tissue deformations as a part of development, it becomes clear that contractility constitutes a key feature of the animal organization from the very start. In addition, manipulating patterns of differentiated contractions across epithelial surfaces is a basic feature of many developmental processes and thus provides a long-standing counterpoint to manipulating much more fleeting and short-lived patterns of contraction across a contractile surface for reversible movements.
The ASMO notion subsumes complex, standardized body architectures
The ASMO notion is centered on a standardized Pantin surface: the total contractile surface that is available in a particular species (and ultimately an individual organism) for initiating motility (see also Arnellos and Moreno 2015, 2016 for the role of motility in multicellular agency and organismality, respectively). The idea is that the fast reversible movements made by animals can only be organized in a way that is reliable and robust, when they play out across a surface that remains stable in size, topology and extension across many life-time occurrences of these fast movements. Fast and reliable motion will be severely hampered if your body keeps changing its topology. A stable body topology can change shape, sometimes in spectacular ways such as by squid, but the cellular tissue arrangement remains the same during those movements. In addition, a reliable controlling structure in itself involves some form of standardization. Thus, having a stable contractile platform and controlling structure—a nervous system—enables the initiation and maintenance of stable forms of patterning across this surface, which, in turn, leads to increasingly complex and useful forms of outward behavior.
While this is a speculative claim, it is corroborated by the fact that animals that rely on muscle-based motility show standardized body topologies built around collections of muscle groups. It is noteworthy that both Porifera and Placozoa, phyla without clear muscle tissue or a nervous system often lack a standardized body topology. Sponges can take many forms, often adapting to local circumstances, while Trichoplax adhaerens, the only named placozoan species, has no clear symmetry, nor a differentiated anterior-posterior or left–right body-axis (Eitel and Schierwater 2010). This precondition of a standardized body architecture implies that the ASMO requires complex forms of development, which is precisely one of the mainstays of an epithelial organization (Arnellos and Moreno 2016).
The ASMO notion subsumes sensitivity to tension and stress at the level of (intra)cellular processes
Again this is a feature that has now been shown to be essential to developmental patterning. In addition to genetic programs and morphogens, mechanical forces also play a central role in development: The developmental differentiation of a multicellular organization is sensitive to mechanical stresses. Thus, positing a faster and reversible form of tension generation and tension sensitive coordination is more a matter of tweaking and adding to an organization that is already present than adding something totally new. A global and mutual coordination of many compression and tension components is a plausible starting point. In this context, it is interesting to note how some authors use the phrase of sensing to describe the way in which cells within a bodily environment interact with this environment (e.g. Geiger et al. 2009).
The ASMO notion subsumes reversible, contraction-based changes in body-shape
Animals have two major options for becoming motile. They can use some form of muscle contraction or they can use beating cilia. Cilia are omnipresent in small organisms, including many animals. Contractile tissue is also used by small animals, sometimes in conjunction with cilia, but it is essential to enable motility for large animals, large meaning here more than a few millimeters (barring some special cases). The ASMO notion stresses the contractility and feedback provided by a Pantin surface, but without a clear role for cilia-based motility. Still, the neural control of ciliary motility must also have been an important factor for early nervous systems (e.g. Jékely 2011; Jékely et al. 2015b). The discussed work on epithelia provides some options to bring these ideas closer together.
From the presented findings, it becomes clear that contraction is a basic feature of epithelia that derives from the intracellular actomyosin cytoskeleton as well as intercellular adherens junctions. Contraction is essential to development, but it is also used in animals at a behavioral level without directly involving motility. Sponges use (slow) body contractions as a defense mechanism (see below), while placozoa change body shape by contraction (Pearse and Voigt 2007). Of the animals with recognizable muscle, ctenophores (comb jellies) use them to maintain body shape while forward movement is achieved by cilia, and many different worm-like animals also move forward by cilia while steering by muscles that orient the front end of the body (Tyler and Rieger 1999). Taken together, these findings suggest an option where an ASMO first arose as part of an organization that modulated body shape rather than as a ‘behavior machine’ to use Pantin’s phrase. As long as the operation of patterning a Pantin surface together with bodily and environmental feedback is present, these cases still constitute an ASMO.
At present these options remain speculative, but they suggest how there could have been a gradual approach from basic and general epithelial features to the origins of the typical contraction-based animal organization that is here cast as the key factor behind the animal sensitivity to the many fleeting aspects of their macroscopic environment.
To conclude more generally, for all five conditions discussed here there is a good fit between the requirements of the ASMO and the standardly available features of epithelia and the developmental and regulative processes in which they are involved. This suggests that internal organization—in the form of an epithelial organization—and bodily complexity can be cast as the initial key-factor for the origin of the ASMO (see also Arnellos and Moreno 2016). In this case, environmental complexity may have played a relatively minor role. Before turning to possible ways to resist this conclusion by the ECT, we will first discuss Porifera and Cnidaria, returning to this issue in the final section.