Nematoda (Round Worms)
Nematoda is a speciose group of elongated and cylindrical worms with a characteristic unsegmented external appearance (Hyman 1951e). It is not uncommon, however, for nematodes to exhibit regularly spaced circumferential indentations in their cuticle along the anteroposterior axis, which are known as annuli (Lee 1967). The nematode Caenorhabditis elegans has a consistent pattern of cuticular annulation throughout its life cycle (Figure 9.2F) (Cox, Staprans, and Edgar 1981; Costa, Draper, and Priess 1997). However, these cuticular rings are more pronounced in two other nematode groups, the Desmoscolecida (Decraemer and Rho 2013) and the Tylenchida (Subbotin 2013).
Desmoscolecida are diminutive and mostly marine nematodes that are characterized by a strongly annulated cuticle ornamented by outer rings of aggregated material (Figure 9.2G) (Decraemer and Rho 2013). These so-called concretion rings are formed by the accumulation of grains, clay, and even bacteria, which are caught up by the differential secretion of mucus between annuli and probably shaped by the body movement (Riemann and Riemann 2010). The cuticle of juveniles is annulated, but it does not exhibit concretion rings; these form during adult life (Lorenzen 1971; Decraemer 1978; Riemann and Riemann 2010). Within Tylenchida, a group of plant-parasitic nematodes of great economic importance (Subbotin 2013), some species show an even more striking pattern of cuticle annulation (Figure 9.2H). These worms often exhibit annuli with crenated margins or scales with evident regularity (Powers et al. 2016). In both Desmoscolecida and Tylenchida, the presence of a strong cuticular annulation might be an adaptation to interstitial sand and soil environments.
The origin of the cuticular annulation is directly associated with the arrangement and differentiation of the hypodermal cells during the early development of the nematode C. elegans. Prior to elongation, the embryos secrete an extracellular layer that remains attached to the dorsal and ventral hypodermal cells in regular intervals, forming circumferential ridges along the anteroposterior axis (Priess and Hirsh 1986). There are numerous ridges per hypodermal cell, and each ridge corresponds to the position of a submembranous filamentous actin bundle (Priess and Hirsh 1986). The arrangement is maintained throughout development and the pattern of circumferential actin bundles coincides with the localization of each cuticular annulation in larval and adult stages (Costa, Draper, and Priess 1997; Francis and Waterston 1991; Hardin and Lockwood 2004). The attachment, mediated by catenin and cadherin proteins (Costa et al. 1998), is essential for the changes in cell shape that elongate the embryo and for the mechanical coupling between the hypodermis and the adult cuticle (Priess and Hirsh 1986; Costa, Draper, and Priess 1997; Hardin and Lockwood 2004).
The cuticle annulation of nematodes is a fine example on how an external trait is inherently linked and derived from the segmental organization of intracellular components. In this case, the basis for establishing a repetitive arrangement lies within the realm of protein localization and polarity in the cytoplasm. Many of these cell adhesion proteins have already been identified (Hardin and Lockwood 2004) and may play a role in organizing the circumferential filamentous actin bundles in C. elegans (Ding et al. 2003). Nevertheless, the key factors regulating the spacing of these intracellular structures remain unknown.
Another nematode trait exhibiting a certain degree of repetition is the postem- bryonic locomotory neurons (White et al. 1976; Sulston and Horvitz 1977; Walthall 1995). The ganglia of each class of motoneurons become serially arranged in a repeated manner along the body axis of C. elegans during the larval stages (White et al. 1976; Sulston and Horvitz 1977; Walthall 1995). The embryo of C. elegans
does not show such arrangement (Sulston et al. 1983). The organization of locomo- tory neurons in segmental pattern also occurs in Ascaris and might be a widespread feature of nematodes (Stretton et al. 1978; Johnson and Stretton 1987).