Hemichordata (Acorn Worms)

Hemichordates are relatively large vermiform marine invertebrates with a body divided into three unequal regions along the anteroposterior axis—the proboscis (or mouth shield), the collar, and a long unsegmented trunk (Hyman 1959b; Kaul- Strehlow and Rottinger 2015). Nonetheless acorn worms according to Beklemishev (1969d) have “a tendency to multiplication of the organs repeated along its longitudinal axis, and these organs show a tendency to metameric arrangement.” The most conspicuous segmental trait of hemichordates are the gills located at the anterior part of the trunk (Bateson 1884).

The gills are arranged in a regular series up to hundreds of pairs with openings to the exterior of the body (Figure 9.2B) (Horst 1930; Hyman 1959b). Gill slits are intercalated by pharyngeal arches that are supported by a series of trident-like acellular collagenous endoskeleton (Gillis, Fritzenwanker, and Lowe 2012). Repeated dorsal outgrowths named tongue bars develop between pharyngeal arches (Hyman 1959b; Gillis, Fritzenwanker, and Lowe 2012). Pharyngeal arches and tongue bars have a single blood vessel each (Pardos and Benito 1988), and thus the arrangement of the circulatory system closely matches that of the gills (Horst 1930). The gonads, which are also serially paired structures in some species, are intercalated with the gills with the genital pores located between gill slits (Horst 1930).

Selected segmental traits in Xenacoelomorpha

FIGURE 9.2 Selected segmental traits in Xenacoelomorpha. Deuterostomia (Hemichordata and Echinodermata), and Ecdysozoa (Nematoda, Nematomorpha, Kinorhyncha, and Priapulida). Arrowheads indicate serially repeated structures unless otherwise noted. A. Developing musculature in early (left) and late embryo (right) of the acoel Isodiametra pulchra. Asterisk and surrounding arrows mark the forming mouth. Scale bars = 20 pm. Images reprinted from Ladurner and Rieger (2000) with permission from Elsevier. B. Gill pores (gp) in the hemichordate Saccoglossus kowalevskii. Whole body image (left) reprinted from Dunn (2015) with permission from Springer Nature. Close up image (right) courtesy of Casey Dunn. C. Hepatic saccules (hp) in the hemichordate Balanoglossus simodensis. Scale bar = 1 mm. Image reprinted from Miyamoto and Saito (2007) with permission from The Zoological Society of Japan. D. Adult specimen (left) and regenerating arm with skeletal and podial serial elements in the brittle star Amphiura filiformis. Scale bar = 100 pm. Images courtesy of Anna Czarkwiani. E. Segmental stalk (s) in the pentacrinoid larva of the feather star Aporometra wilsoni. Scale bar = 200 pm. Image reprinted from Haig and Rouse (2008) with permission from John Wiley & Sons. F. Cuticular annulation in the nematode Caenorhabditis elegans. Scale bar = 3.8 pm. Image reprinted from Costa, Draper, and Priess


(1997) with permission from Elsevier. G. Concretion rings (cr) in the nematode Desmoscolex cosmopolites. Scale bar = 50 pm. Image reprinted from Lim and Chang (2006) with permission from Taylor & Francis. H. Cuticular annulation in the criconematid nematode Criconema sp. Scale bar = 50 pm. Image courtesy of Tom Powers from Powers (2015) and used with permission. I. Cuticular annulation in the larva of the nematomorph Chordodes janovyi with terminal anterior (as) and posterior spines (ps). Scale bar = 2 pm. Image reprinted from Bolek et al. (2010) with permission from Magnolia Press. J. Profile of the cuticle annulations in the larva of the nematomorph Neochordodes occidentalis. Reprinted from Poinar (2010) with permission from Elsevier. K. Trunk segments in the kinorhynch Echinoderes hispanicus. Scale bar = 30 pm. Image by Herranz et al. (2014) licensed under CC-BY. L. Segmental musculature in the kinorhynch Echinoderes horni showing dorsal (dom), dorsoventral (dvm), and diagonal (dim) bundles. Scale bar = 20 pm. Image by Herranz et al. (2014) licensed under CC-BY. M. Segmental paired neuronal somata in the nervous system of the kinorhynch Echinoderes spinifurca. Scale bar = 20 pm. Image reprinted from Herranz, Pardos, and Boyle (2013) with permission from John Wiley and Sons. N. Cuticular annulation in the priapulid Priapulus caudatus. Scale bar = 1 cm. Own work. O. Longitudinal section of the body wall in the priapulid Halicryptus spinulosus showing the circular musculature (cm), apodemes (a), and inner longitudinal muscle (lm). Scale bar = 10 pm. Image reprinted from Oeschger and Janssen (1991) with permission from Springer Nature. P. Development of the circular musculature in the priapulid Priapulus caudatus. Scale bars = 50 pm. Image by Martln-Duran and Hejnol (2015) licensed under CC-BY. Q. Grid pattern in the abdomen nervous system of the priapulid Tubiluchus troglodytes showing serotonin immunoreactive fibers in the ventral longitudinal cord (vie), circular fibers (cf), longitudinal fibers (If), and gut bundle (mvb) and somata (s). Scale bar = 75 pm. Image reprinted from Rothe and Schmidt-Rhaesa (2010) with permission from John Wiley & Sons.

More posterior in the trunk, some species exhibit a series of paired dorsal outgrowths named hepatic saccules (Figure 9.2C) (Horst 1930; Hyman 1959b; Beklemishev 1969d). These repeated diverticula of the dorsal gut epithelium deform the adjacent body wall epidermis becoming visible externally (Benito, Fernandez, and Pardos 1993; Miyamoto and Saito 2007). Other hemichordate structures such as muscles or neurons have no evident segmental organization—the circular muscles are not evenly spaced, the longitudinal muscles are continuous from end to end, the coelomic cavities are undivided, and the nervous system is a net with no repetitive pattern (Hyman 1959b; Beklemishev 1969d; Kaul-Strehlow et al. 2015).

During development the first pairs of gills can already be formed in the swimming larval stages (Agassiz 1873; Bateson 1884; Morgan 1894; Kaul-Strehlow and Rottinger 2015). They appear progressively from anterior to posterior when endo- dermal evaginations fuse to the overlying ectoderm creating the gill pores (Hyman 1959b). Each gill follows a stereotypic developmental sequence, first as a small round pore that elongates along the anteroposterior axis and subsequently becomes U-shaped due to the growing dorsal tongue bars (Gillis, Fritzenwanker, and Lowe 2012). The number of gill slits continues to increase during adult life (Hyman 1959b; Kaul-Strehlow and Rottinger 2015).

Gene expression studies suggest the molecules patterning the pharyngeal arches of hemichordates, cephalochordates, and vertebrates are largely conserved, further supporting the homology of deuterostome gills (Ogasawara et al. 1999; Rychel and

Swalla 2007; Gillis, Fritzenwanker, and Lowe 2012; Fritzenwanker et al. 2014; Lowe et al. 2015). Pharyngeal arches are thus a rather ancient deuterostome feature and were probably the first segmental traits to evolve in the vertebrate lineage—before the trunk somites or the hindbrain rhombomeres (Graham et al. 2014).

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