Mollusca (Snails and Squids)
Mollusca is the group of bilaterians comprised of snails, oyster, squids, and other animals with a great diversity of larval and adult body patterns (Ruppert, Fox, and Barnes 2004b). Two particular mollusk groups, the Monoplacophora and the Polyplacophora (e.g., chitons), show a rather notable set of segmental traits, such as
FIGURE 9.4 Selected segmental traits in Spiralia (Nemertea, Mollusca, and Brachiopoda). Arrows indicate serially repeated structures unless otherwise noted. A. Ring nerves (sen) in the nemertean Procephalothrixfiliformis. Scale bar = 100 pm. Image by Beckers, Loesel, and Bartolomaeus (2013) licensed under CC-BY. B. Serially repeated ovaries in the nemertean Carcinonemertes epialti. Scale bar = 100 pm. Image reprinted from Strieker et al. (2002) with permission from John Wiley & Sons. C. Oocytes (oo) intercalated by gut diverticula (id) in the nemertean Tetrastemma phyllospadicola showing the proboscis (pr) and body wall epidermis (ep). Scale bar = 400 pm. Image reprinted from Strieker et al. (2002) with permission from John Wiley & Sons. D. Series of dorsal shell plates in the chiton Totticella lineata. Image by Jerry Kirkhart from Kirkhart (2008) licensed under CC-BY. E. Cell types in the shell field epithelium of the chiton Ischnochiton rissoa. The surface of each cell is color coded. Scale bar = 1 pm. Image reprinted from Kniprath (1980) with permission from Springer Nature. F. Larva of the chiton Mopalia muscosa with developing shell field (arrows), mantle fold (gi), apical tuft (at), and foot (ft). Scale bar = 50 pm. Image reprinted from Wanninger and Wollesen (2015) with permission from Springer Nature. G. Transverse body wall furrows in the trilobed larva of the brachiopod Macandrevia cranium showing the apical lobe (al), the mantle lobe (ml) with ciliary band (cb), and the pedicle lobe (pi). Scale bar = 10 pm. Image reprinted from Zakrzewski, Suh, and Litter (2012) with permission from Elsevier. H. Segmental mesoderm (m) with partitions numbered from 1 to 4 and dorsal chaetae sacs (cs) in the larva of the brachiopod Novocrania anomala. Scale bar = 20 pm. Image by Vellutini and Hejnol (2016) licensed under CC-BY.
serially arranged dorsal shells and repeated pairs of dorsoventral muscles (Lemche and Wingstrand 1959; Wingstrand 1985; Willmer 1990). Compared to other groups covered in this chapter, mollusks have been relatively well-studied in terms of cellular, developmental, and genetic mechanisms during the ontogeny of these segmental traits.
Several mollusk groups exhibit a repeated sequence of paired dorsoventral muscles along the anteroposterior axis (Haszprunar and Wanninger 2000; Wanninger and Wollesen 2015). In general, the numbers vary between seven pairs in larval aplacophorans; seven to eight pairs in adult polyplacophorans; eight pairs in mono- placophorans; three to eight pairs in bivalves; and one to two pairs in gastropods, scaphopods, and cephalopods (Wingstrand 1985; Haszprunar and Wanninger 2000; Scherholz et al. 2013). In chitons, the first muscles appear in the embryo as a series of transverse fibers that develop in an anteroposterior progression along the trunk, but the dorsoventral muscles only become arranged in bundles after metamorphosis (Wanninger and Haszprunar 2002).
Concerning other internal traits of mollusks, both mono- and polyplacophorans have gills and nephridiopores arranged in series along the lateral sides of the body. Not much is known about the development of these structures, but there is evidence that their growth and differentiation is not paired, because the number of structures between left and right sides is not symmetric (Hunter and Brown 1965; Wingstrand 1985; Russel-Hunter 1988). In the nervous system, while transverse commissures can be present (Wingstrand 1985), they are not regularly spaced (Voronezhskaya, Tyurin. and Nezlin 2002; Friedrich et al. 2002).
Chitons have a set of eight dorsal shell plates separated by transverse interseg- mental ridges (Figure 9.4D). These structures originate from embryonic blasto- meres in the second and third quartet micromeres (Heath 1899; Henry, Okusu, and Martindale 2004), and are formed through the differential specialization of epithelial cells (Kowalevsky 1883a; Heath 1899). For instance, the intersegmental ridges are created by a transverse row of mucus-producing cells (known as goblet cells or type-1), while a nearby row of type-4 cells secrete the shell plates (Figure 9.4E) (Kniprath 1980). The goblet cells are surrounded by cells with dense cytoplasm and long microvilli (type-2), while type-4 shell-secreting cells are surrounded by another cell kind (type-3) (Kniprath 1980). Thus, the shell field of chitons is the product of a highly organized epithelium patterned during embryogenesis, and progressively established during larval development (Figure 9.4F), or after metamorphosis in some species (Leise 1984). Albeit gradual, the shell formation does not follow an anteroposterior progression—the central plates appear first and are shortly followed by the first, sixth, and seventh plates, while the eighth plate is formed several days later (Kniprath 1980).
Although we do not yet comprehend the developmental mechanisms regulating the segmental organization of the chiton shell field, gene expression studies began to uncover the molecular identities of these epithelial cells. For instance, the intersegmental cells type-1 and type-2 are known to express the gene engrailed (Jacobs et al. 2000), while the shell-secreting type-4 likely express the genes pax2/5/8 (Wollesen et al. 2015) and gbx (Wollesen et al. 2017) (Figure 9.5A). These genes are usually involved in establishing developmental boundaries (e.g., Raible and Brand 2004), and thus might play a role in the patterning of the shell boundaries in mollusks
FIGURE 9.5 Gene expression patterns in the segmental traits of Mollusca and Brachiopoda. A. Expression of engrailed, pax2/5/8, and gbx in the developing dorsal shell field of the chiton Lepidochitona caverna (left) and Acanthochitona crinita (center and right). Scale bars = 20 pm. Left image reprinted from Jacobs et al. (2000) with permission from John Wiley & Sons. Center image by Wollesen et al. (2015) licensed under CC-BY. Right image by Wollesen et al. (2017) licensed under CC-BY. B. Expression of engrailed, pax2/5/8, and gli in the segmental larval mesoderm of the brachiopod Novocrania anomala. Scale bar = 20 pm. Images by Vellutini and Hejnol (2016) licensed under CC-BY. C. Cell outlines (left) and abutting domains of wntl (green) and engrailed (magenta) at the non-segmental boundaries (arrows) in the larva of the brachiopod Terebratalia transversa. Scale bar = 20 pm. Images by Vellutini and Hejnol (2016) licensed under CC-BY.
(Nederbragt, Loon, and Dictus 2002). This is supported by the observations that the expression of engrailed, pax2/5/8, and gbx is also associated to shell development in a wide range of mollusks (Moshel, Levine, and Collier 1998; Jacobs et al. 2000; Wanninger and Haszprunar 2001; Nederbragt, Loon, and Dictus 2002; O’Brien and Degnan 2003; Iijima et al. 2008; Kin, Kakoi, and Wada 2009; Hashimoto,
Kurita, and Wada 2012; Wanninger and Wollesen 2015; Wollesen et al. 2015, 2017; Scherholz et al. 2017). It remains to be determined if these genes could be involved in the generation of the dorsal shell series in chitons, or if instead they have roles in downstream processes such as boundary formation and cell differentiation.