The division of labour model for nervous system evolution

If a cell type is defined by the expression of differentiation cassettes for specific cellular functions, this tightly links a cell type to its functions within the organism.

But since new cell types evolve from preexisting ones, it is evident that the evolu-tion of new cell types can happen only in two condievolu-tions: either by segregaevolu-tion of functions from a multifunctional cell type, or with the evolution of completely new functions (for example, together with the evolution of new genes).

Segregation of functions must have been the dominating mechanism in early

evolution of neuronal cell types, since the cell types of basal metazoans are mul-tifunctional. The observation of myoepithelial cells (sensory and contractile cells) in cnidarians prompted Mackie (1970) to hypothesize that muscle cells and neu-rons evolved after functional segregation from a multifunctional cell type; the newly evolved cell types remained in contact, in order to perform the original function (fig. 1.4A). This “division of labour” model can be extended to other cell types, and can explain the evolution of simple neural circuits, starting from multifunctional sensory-motor cells (Arendt et al., 2008; Jékely, 2011).

A division of labour model has been proposed for the evolution of simple eye-spots, like the Platynereis larval eyes (Arendt et al. 2009, fig. 1.4B). This hypothesis starts from the observation that cnidarian larvae have multifunctional cells, with a shading pigment, a rhabdom (for the packaging of opsin) and a locomotor cilium;

the activity of the cilium depends on the directional light response from the same cell. In Platynereis, the three functions are subdivided between three cell types: a shading pigment cell and a photoreceptor cell, which form the larval eye, and a multiciliated prototroch cell. These three cells are functionally interconnected, since the larval eye innervates directly the prototroch cell, and in this way controls the ciliary beating of that cell (Jékely et al., 2008).

Mathematical modelling showed that division of labour processes are generally advantageous in biological systems (Gavrilets, 2010; Rueffler et al., 2011). It is not hard to imagine why this was advantageous also in the context of nervous system evolution. The segregation of functions between cell types allows each new cell type to specialize further on its new exclusive function. After the segregation of the sen-sory and the motor components, another immediate advantage was the possibility to integrate multiple sensory inputs for a finer control of the locomotor output. More-over, division of labour can elegantly explain the evolution of interneurons, which do not exist in basal metazoans (Marlow et al., 2009; Galliot and Quiquand, 2011), and constitute the key acquisition of more complex, or “integrative” nervous systems.

Finally, the rise in body plan complexity was accompanied by the specialization of tissue types, and the physical segregation of sense organs, brain, neuroendocrine organs and musculature.

The widespread occurrence of division of labour in the nervous system evolution must be taken in account whenever cell types are compared across distantly related taxa. In simple marine ciliated larvae, like the Platynereis trochophore, sensory cells innervate directly the ciliated cells responsible of locomotion, while in more complex

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Figure 1.4: Examples of division of labour in nervous system evolution. A. Evolution of sensory-motor circuits from myoepithelial cells, according to Mackie (1970). Myoepithelial cells, like those existing in Cnidaria (1) start to sink internally (2). Protoneurons evolve, which sense environmental information externally and control myocyte contraction; the epithelial cells are electrically coupled (3). After another step of division of labour, specialized neurosensory cells and motorneurons evolve (4). They form a minimal circuit for the control of myocyte contraction. Image from Mackie (1970).

B. The evolution of simple eyespots from an ancestral multifunctional cell. Multifunctional cells (1) are locomotor ciliated cells (LCC) that can sense light direction (PRC: photoreceptor; SPC: shading pigment cell). Some cells specialize in sensing light direction, while the others keep the original role in locomotion; a similar situation is present in some cnidarian larvae (2). The specialized PRC/SPC move away from the epithelium (3) and, after another step of division of labour, specialize in a PRC and a SPC (4). Image from Arendt et al. (2008).

organisms, sister cell types with the same sensory modality might control muscle-driven locomotion indirectly, through more complex neural circuits.

1.4. Studying marine larvae uncovers the earliest steps in brain evolution Animal nervous systems have an astonishing diversity in forms, complexity and functions, yet they evolved from an obscure common ancestor.

In ancestral forms, locomotion was driven by cilia, like in extant marine larvae.

Basal metazoans, like the Cnidaria, have non-centralized nervous systems consist-ing of simple nerve nets, made by bipolar sensory neurons, neurosecretory cells and ganglion cells, but not “true” interneurons (Marlow et al., 2009; Galliot and Quiquand, 2011). In these animals, the control of locomotion is exerted by mul-tifunctional neurons, which are sensory cells and motorneurons at the same time.

In Bilateria, this simple neuronal organization is elaborated further in circuits that integrate the sensory information, and produce a coherent motor output. The estab-lishment of the first integrative systems to control locomotion was probably one of the first steps in nervous system centralization.

For these reasons, primary ciliated larvae, like the trochophore larvae of annelids, represent an ideal system to understand these early evolutionary events. First, they still move with cilia, which is the ancestral form of animal locomotion, since muscles evolved only later (Jékely, 2011). Second, they retain sensory-motor cells to control directly ciliary beating, like the larval eyes (Jékely et al., 2008) and several peptider-gic neurons of the larval medial brain described in Platynereis (Conzelmann et al., 2011). But more importantly, most authors agree that primary ciliated larvae of pro-tostomes and deuterostomes are homologous, as indicated by the conservation of morphological traits and molecular markers (Jägersten, 1972; Nielsen, 2005; Marlow et al., 2012; Santagata et al., 2012). Following these ideas, the life cycle of early bilate-rians comprised a pelagic larval stage, thus studying extant primary ciliated larvae of marine invertebrates can give insights into how early nervous systems evolved.