The animal sensorimotor organization: a challenge for the environmental complexity thesis

In addition to genetic signals and soluble morphogens, such developmental processes are also regulated by the mechanical forces mentioned above that act as “mechanochemical actuators” (Kim et al. 2014). Given the relevance for the ASMO notion it is worthwhile to highlight this component of developmental patterning:

mechanical forces play a central role in morphogenesis and tissue patterning, and […] physical cues are as important as chemical factors for developmental control throughout virtually all stages of embryogenesis. Although the contribution of physical forces to cell and tissue deformation in the embryo has been recognized for over a century, it is only recently that mechanical stresses have been shown to function as informative signals that produce specific changes in molecular biochemistry and gene expression through the process of cellular mechanotransduction (Mammoto and Ingber 2010, p. 1416).

In this context, Geiger et al. (2009) talk about “environmental sensing” by epithelial cells as they are sensitive to and integrating a wide array of chemical as well as physical cues that act on the focal adhesions. Connections through adherens junctions also ensure that stress induced in one cell spreads to adjacent cells, which provides a way to integrate activity at an intercellular scale, as also occurs by supracellular actomyosin cables (Röper 2013). Such sensitivity is not only passive as cells themselves also respond actively to applied forces, which can lead to “an autoregulatory feedback control that ensures the robust sculpting of cells and tissues during developmental growth and morphogenesis” (Mao and Baum 2015, p. 98).

Taking the relevance of mechanotransduction into account, Ingber (2006) states that prestress at all levels of the tissue organization ensures that various molecular scale mechanochemical transduction mechanisms proceed simultaneously and produce a concerted response. He argues that this should be understood in terms of a tensional integrity (tensegrity) architecture that consists of opposing tension and compression elements that balance one another by providing an internal resting tension that stabilizes the whole structure (ibid., p. 821). In this way, a global and mutual coordination of the many separate intra- and intercellular events at a wide variety of size scales could be achieved.

Finally, we should not forget the ongoing relevance of electrical signaling, where epithelial conduction is an important predecessor or parallel organization for nervous systems (Mackie 1970, 2004a; Meech 2015). We should also mention more recent developments about the developmental and regenerative relevance of bioelectrical signals (e.g. Tseng and Levin 2013; Pai et al. 2015). According to Levin (2013), the spatiotemporal gradients of endogenous transmembrane voltage potentials serve as instructive patterning cues for large-scale anatomy, providing organ identity, positional information, and prepattern template cues for morphogenesis. The promise here is that morphogenesis actually can be manipulated by these patterning signals.

To conclude, epithelia are an extremely versatile tissue configuration that has been intensely studied for its role in morphogenesis and development. In the following, we will apply these findings and theories about epithelia to further develop and clarify the notion of the animal sensorimotor organization.

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.

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).

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 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).

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).

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.

Here we position the ASMO notion with respect to the characteristic features of two basic animal phyla: Porifera and Cnidaria. These phyla arguably straddle the divide between animals with and without both a standardized body and an ASMO. In this way, we aim to show how different forms of an epithelia-based multicellular organization can exist and how the ASMO notion can be positioned in this landscape.

As a word of warning, the discussion in this paper targets a relatively abstract level of description. It aims to explain how a collection of individual cells and their products can constitute an organization that is sensitive to and able to deal with increasingly fleeting and changeable macroscopic aspects of the multicellular body and the environment. It cannot be taken for granted that anything living today resembles the various intermediate forms that must have lived so many years ago. Still, Porifera and Cnidaria are representatives of basic animal forms and a lot can be learned from them. The question asked here is whether they do or do not exemplify the ASMO notion and what we can learn from the answer.

Porifera (sponges) are sessile aquatic animals that are found in almost all benthic habitats. Sponges have no clear body symmetry and can take many different shapes. As mentioned above, sponges have no gut but an extensively branched water canal system that extends throughout their bodies. Water is taken into the sponge body through tiny holes (ostia) in pore cells in the surface epithelium from where it goes to chambers with choanocytes that, operating like cilia, generate this feeding and respiratory current. Finally the water is expelled through a large opening, the osculum. Sponges feed on picoplankton, such as bacteria and viruses, by filtering the water in a highly efficient way. Food uptake takes place within cells, which is a form of microphagy.

Despite a long-standing discussion, sponges can be considered as epithelial organisms (Leys et al. 2009; Leys and Riesgo 2012). Sponge epithelia function as both sensory and contractile tissue, and they are the primary conduits of behavior coordination (Nickel et al. 2011; Leys and Hill 2012; Leys 2015). Sponges lack nerve cells and so far no electrical signaling has been witnessed within cellular sponges (Leys 2015).2 The propagation of signals along the whole sponge can take from 30 min to a full hour, although individual pores can be closed in some tens of seconds. In her review, Leys (2015) names juxtacrine signaling by chemical signals from one cell to the next along the epithelia as the most likely candidate.

Given the notion of an ASMO, the contractile behavior of sponges and its coordination are most relevant. Sponges use contractions in response to touch and to regulate the flow of water through their bodies and expel obstructions (Elliott and Leys 2007). They have contractile cells called actinocytes that come close to some form of smooth muscle (Elliott and Leys 2007). How these contractions are coordinated is not fully clear, but this seems to depend on this juxtacrine chemical signaling (Leys 2015). In any case, very slow contraction waves can be observed that are in many ways similar to peristaltic contractions (Elliott and Leys 2007). Sponges tune the canal diameter to a high degree to modify water flow (Leys 2015). Sponges can expel sediments by contracting and expanding the osculum and canals and pumping out water at a velocity that carries waste products some distance away (Leys 2015). Uptake of unwanted particles can be limited by the contraction of the ostia and the canals, which can be triggered for example by turbulence or the amount of sediment. All in all, it can be concluded that “sponges have, without nerves or true muscle, evolved a way of coordinating contractions of cells to generate an effective mechanism of controlling water flow” (Elliott and Leys 2007, p. 3746).

Given this general description, to what extent do sponges exhibit an ASMO? Sponges fulfil some but not all of the conditions discussed above. The easiest cases are the presence of contractile epithelia and body contractions, which are both a clear yes. The condition concerning sensitivity to tension at the (intra)cellular level is also plausibly fulfilled, considering the sensitivity to canal width and the developmental processes involved in building the sponge body. The other two are a different matter however. Sponge bodies are not standardized in the way eumetazoan bodies are. The bodies of individuals often adapt during development to the specific local circumstances and are in this sense more like plants that can also take many individual shapes even when their local characteristics are typical for the species involved. The contractile surface is subsequently also not standardized and not suitable for quick reversible changes of shape. Finally, there is a less than clear distinction between an inner and outer body space. The water canal system is pervasive and involves a very high throughput of material that flows right through the body making it part of the environment rather than the body itself. In contrast, the mesohyl, the sponge body’s inner space that is actually closed off from the environment and molecularly controlled, seems to function mainly for support.

All in all sponges do not have an ASMO as formulated above. But, maybe surprisingly, it looks like a near miss: Sponges do have a contractile body and various (though slow) feedback processes to control these contractions. When compared to clear examples of an ASMO, such as the Cnidaria discussed below, these differences look not exceptionally large and can be summarized as a difference in speed, integration and specificity. To become sensitive to often fleeting environmental happenings an ASMO must operate much faster than what is seen in sponges. Speed is also needed to integrate any behavioral response for the whole animal and making it specifically tailored for different behavioral tasks. To clarify these claims, we will have a quick glance at Cnidaria.

Jellyfish are the best known Cnidaria and we will use them here as their representatives. Jellyfish are free-swimming marine animals consisting of a gelatinous bell and trailing tentacles. Their body architecture is characterized by a central digestive compartment, two epithelial layers and mesoglea in between. They have muscle, a nervous system—as well as conductive epithelia—and simple sensory organs distributed radially around the body. Jellyfish move forward by a form of jet propulsion brought about by contracting their bell-like bodies and expelling the water from the central cavity, the elastic mesoglea extends the bell again (see Mackie 2004b; Satterlie 2002). Cnidarians regulate their physiology by means of neuroendocrine cells that synthesize peptide-signaling molecules (acting as neurotransmitters or neurohormones), which are dispersed primarily through diffusion. Almost all neurotransmitters, neurohormones and non-neuronal hormones are present in Cnidaria and they are central in regulating developmental and physiological processes, such as the induction or inhibition of neural differentiation, neurogenesis, and oocyte maturation, morphogenesis and spawning (e.g. Koizumi 2002; Takahashi and Hatta 2011). In general, jellyfish have the capacity for diverse contraction-based motile interactions with the environment that are mainly manifested as swimming with increased maneuverability combined with directional movements of various parts of their body.

Jellyfish and cnidarians more generally exemplify a full ASMO: a multi-cellular body with an inner space, contractile epithelia and even muscle, a complex standardized body architecture, sensitivity to tension can be assumed, and changes in body shape as well as motility are achieved by body contraction. Jellyfish thus show that a clear and recognizable ASMO is present at a very ‘basic’ level, and can be achieved with limited neural coordination. This basic level involves a clearly standardized and differentiated body, integrated in a way that enables fast reversible movements that are well coordinated in feeding, escaping and other behavior. Organizationally, the neural and other bodily complexities that evolved within the bilaterians can be interpreted as filling in the new option space that became available when the ASMO first arose.