Discussion

The segmental traits covered in this chapter have diverse embryonic origins, molecular fingerprints, developmental mechanisms, and end morphologies. This diversity indicates that a segmental organization can evolve in any germ layer or organ system of bilaterians and do so via various ontogenetic pathways. In most cases, however, these traits are often confined to a particular organ or developmental stage, and are not in register with other repetitive structures present in the same organism (Table 9.1).

For example, chaetognaths only have segmental traits in the nervous system, nematomorphs only exhibit cuticular annulations in the larval stages, and the musculature of rotifers and chitons does not match the position of the skeletal plates

Group

Body Wall

Neurons

Muscles

Gonads

Excretion

Gut

Features

Xenacoelomorpha

Circular muscles can be regularly distributed.

Hemichordata

Series of gill pairs intercalated by gonads. Paired series of gut diverticula (hepatic saccules).

Echinodermata

Repeated serial elements (ossicles, neurons, muscles, and vascular channels) along body rays.

Cephalochordata

Somites and repeated muscle bundles. Series of gonads and nephridia. Some dorsal neurons.

Tunicata

Regularly spaced pharynx structures (gill slits, neurons, and vessels). Larval notochord. Circular muscles in planktonic forms. Asexual buds formed by strobilation.

Nematoda

Cuticular annulation and corresponding series of circular F-actin bundles. Series of concretion rings. Serially arranged locomotory neurons.

Nematomorpha

Annulated cuticle in the larva.

Priapulida

Cuticular annulation and corresponding circular muscles. Series of evenly spaced circular neurite bundles.

Kinorhyncha

Cuticular plates (zonites) in the trunk. Paired series of repeated muscle bundles. Transverse commissures and paired ventral neuronal somata.

Loricifera

Thorax cuticle divided in two segments. Not so evenly spaced circular muscle bundles in the abdomen.

Tardigrada

Trunk segments and mesodermal pouches in embryos. Paired appendages and few corresponding repeated muscle sets. Series of trunk ganglia.

Onychophora

Somites and paired ventral organs in embryos. Paired appendages and corresponding nerves and muscles. Series of paired nephridia. Series of blood valves.

(Continued)

Group

Body Wall

Neurons

Muscles

Gonads

Excretion

Gut

Features

Chaetognatha

Series of paired neurons and neuropil microcompartments.

Rolifera

Telescopic skeletal rings. Series of circular or paired lateral muscles.

Acanthocephala

Annular constrictions in the trunk with corresponding series of circular muscles. Series of circular channels.

Micrognathozoa

Paired series of dorsoventral muscles. Two pairs of lateral protonephridia.

Gastrotricha

Series of paired cuticular spines, bristles, and adhesive tubes. Paired series of protonephridia.

Platyhelminthes

Repeated trunk annular infoldings in tapeworms with corresponding series of transverse neuronal commissures, circular musculature, transverse excretory channels, and set of gonads. Series of transverse neuronal commissures and circular musculature, and at times repeated gut diverticula with alternating gonads in free-living flatworms.

Ncmcrtea

Series of circular nerves or transverse commissures and densely packed circular muscles. Paired ovary series intercalated by lateral gut diverticula. Series of paired protonephridia can occur. Annular epidermal constrictions with corresponding gut compartments in one group.

Mollusca

Series of dorsal shell plates. Paired series of dorsoventral retractor muscles. Series of gills, gonads, and nephridiopores can occur.

Brachiopoda

Serial pairs of coelomic and chaetae sacs in larval stage.

Phoronida

Not so regular series of neural commissures and circular musculature in larval stage.

Bryozoa

Stalk formed by a series of annular zooids in abyssal species.

Labels: / Presence of segmental trait(s); /* Presence of segmental trait(s) but limited to subgroup or life stage; —* Presence of trait(s) with incipient segmental organization; — Absence of segmental trait(s).

and shells. In addition, some segmental traits are apomorphies of specific clades. These likely evolved as adaptations to particular environments, such as the association between strong body wall annulation and the occupation of interstitial habitats in nematodes and nemerteans. Given these observations, it seems reasonable to suggest that bilaterian structures with a segmental organization have diverse origins and behave as independent evolutionary units (Scholtz 2010).

In spite of that, segmental traits can be integrated to various degrees in different bilaterians. The cases range from a direct link between circular musculature and cuticular annulation, as seen in priapulids, to the most-notable coordination between external folds, musculature, nervous system, and other segmental structures present in kinorhynchs or tapeworms. This level of integration, generally considered a landmark of the so-called true segmentation, is on par at least in qualitative terms with that of arthropods and annelids. Even though kinorhynchs and tapeworms display some mismatches between segmental traits, this also occurs in arthropods and annelids (Budd 2001; Fusco 2008), suggesting that these arrangements are rather plastic in evolutionary terms.

The fact that one organism can have multiple segmental traits with different evolutionary histories (e.g., Graham et al. 2014), and that these traits can be integrated or disassembled with relative evolutionary ease, dissolves the artificial division between the so-called segmented and non-segmented animals. The evolution of tapeworm segmentation is an example of the gradual, organ-based attainment of an integrated segmental body organization (Olson et al. 2001), which further supports the hypothesis that the overt segmentation in the typical fully segmented animals evolved “system by system” (Budd 2001; Chipman 2019).

Considering all the traits covered in this chapter, the most common organ systems of bilaterians to exhibit a segmental organization are the body wall (e.g., annula- tions), the nervous system (e.g., transverse commissures), and the musculature (e.g., circular fibers).

The body wall is usually segmented by infoldings of the epidermis, such as the ones found in tapeworms, or by the presence of extracellular or intracellular plates, as seen in kinorhynchs and rotifers, respectively. For each case, the cellular processes that establish these boundaries are rather different. For instance, on the body wall of kinorhynchs and chitons, segmentation is achieved by the differential secretion of cellular materials, which produce the skeletal plates/shells and the interseg- mental cuticle that joins each segment. In contrast, to create a fold in a sheet of epithelial cells, coordinated changes in cell shape (i.e., cytoskeleton remodeling) and the modulation of cell-cell and cell-matrix adhesion are required (Schock and Perrimon 2002).

The segmental traits in the nervous system consist mainly of serially repeated transverse commissures, paired neurons, and nerve cord ganglia. The transverse commissures are present in flatworms and nemerteans, but the regularity of the pattern varies considerably, and the architecture of the nervous system is likely correlated with the life habits of the species. In general, the processes that neuronal cells undergo to form a grid pattern have not been investigated in depth.

The circular musculature is a seemingly ubiquitous and plastic trait of bilaterians, but its arrangement can be strikingly regular, and in some cases, directly responsible for the segmental nature of adjacent traits. This is the case for the cuticular annu- lations of priapulids, which match the position of the circular musculature. An analogous situation occurs in nematodes, which despite not having actual circular muscles, the subcellular transverse f-actin fibers of the hypodermal cells are directly associated with the cuticle annulations (Priess and Hirsh 1986).

The segmental organization of circular muscles can arise through different cellular processes. Often, the initial set of muscle cells is positioned irregularly during embryonic development, and progressively self-organizes into an evenly spaced set of circular bundles. In a few cases, however, these initial fibers are already oriented, and the muscle cells differentiate from anterior to posterior (e.g., acoels). Because the frequency of circular muscles is usually group- or species-specific and can vary between different body regions (e.g., Tyler and Hyra 1998), there must be identifiable mechanisms, such as signaling molecules and cell-to-cell interactions, by which these specific arrangements emerge. But what controls the spatial and temporal information to orient and organize these muscle cells remains an open question.

Indeed the cascades of signal transduction-triggering effector molecules in these tissues remain obscure, but some earlier steps during embryonic development, which define the identity and polarity of the cells of each segmental domain, are beginning to be uncovered. The groups that should bring further insights about these molecular mechanisms are chitons and tapeworms (e.g., Wollesen et al. 2015; Koziol 2017) where a combination of molecular techniques and live imaging of developing chiton shells or tapeworm proglottids will provide crucial insights about the cellular processes involved.

The traits examined in this chapter provide only a glance into the diversity and the multitude of ways that a segmental organization can be achieved in the different bilaterian organ systems. Uncovering this rich repertoire of cellular and developmental processes will not only reveal novel segmental patterning mechanisms, but perhaps enable unforeseen insights about the typical segmented groups and bring a much needed comparative light into how these diverse segmental traits of bilaterians have evolved.

 
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