THE ECDYSOZOA (AGUINALDO ET AL. 1997)

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Ecdysozoa (ek-di-so-ZO-uh) is a combination of Greek roots that mean stripping or molting [=ekdusis (ἔκδυσις)] and animal [=zoa (ζώο)]. The reference is to those animals that molt. Ecdysozoa as a formal name at the rank of superphylum was coined by Aguinaldo et al. (1997).

INTRODUCTION TO THE ECDYSOZOA Ecdysozoa is the sister group to Spiralia in the Protostomata. The ecdysozoans chiefly are united by the tendency to molt or cast off the outer covering, a process called ecdysis from which the name of the group stems (Aguinaldo et al. 1997; Valentine 2004; see Figure 1). The cuticle illustrated in Figure 1-A, though of an arthropod, is characterstic of the ecdysozoans in general. In addition, they do not have ciliary fields over the outside of the body, nor do they tend to have ciliary feeding mechanisms. Although this would seem to follow from the occurrence of a thick cuticular covering, Telford et al. (2008) and Edgecombe et al. (2011) note that Gastrotricha (a phylum in the Spiralia) does have both a thick cuticle and a body covered by cilia. Haase et al. (2001) report that horseradish proxidase is a tissue-specific marker for Ecdysozoa. Other ecdysozoan synapomorphies listed by Harvey et al. (2010) include: – molting is controlled by characteristic hormones called ecdysteroids – the cuticle has 3 layers (see Figure 1A): epicuticle, exocuticle, and endocuticle – epicuticle is trilaminate – alpha-chitin in inner layer Some taxa have lost the true coelom and have become blastocoelic (pseudocoelomic). Arthropods are eucoelomic, but in mature animals the coelom is greatly reduced. The open circulatory system uses a secondarily produced cavity, the hemocoel. Valentine (2004) suggests that another synapomorphic character is direct development or development in which larvae are similar in general form to the mature adult, a character that has altered significantly in many arthropod groups.

FIGURE 1. The arthropod cuticle with characters common to the Ecdysozoa. A. Structure of the arthropod cuticle showing the epicuticle (EPI), exocuticle (EXO), and endocuticle (END). The bottom layer is the epidermis. The blue dot indicates an epidermal cell with an emergent seta. The green dot is a glandular cell that secretes epicuticle. B.-D. Stages in the ecdysis of arthropod cuticle. Yellow indicates ecdysterone, a class of hormones shared by members of the Ecdysozoa . A. was created by Philcha and placed into the Public Domain. B-D. were drawn by Halvard and placed into the Public Domain.

FIGURE 2. ALTERNATIVE TOPOLOGIES FOR THE ECDYSOZOA. The topology of the Ecdysozoan clade (all phyla in bold) and the position of the Ecdysozoa (clade within the box) relative to the major groups of the bilaterian animals. Ecdysozoa has three monophyletic groups, each designated by letter: the Panarthropoda (Nielsen 1997, PA), the Nematoidea (Schmidt-Rhaesa 1998, N), and Scalidophora (Schmidt-Rhaesa 1998, S). The cladogram is a consensus between Gabriel and Goldstein (2007), Telford et al. (2008), Philippe et al. (2005), Webster et al. (2006), and Edgecombe et al. (2011). Cladogram A shows three nested clades with Scalidophora as sister to Panarthropoda + Nematoida. Cladogram B unites the Nematoida and Scalidifera into a clade called Cycloneuralia (Ahlrichs 1995, C).

Aguinaldo et al. (1997) identified the Ecdysozoa, but it was made up of an assemblage of animals that seemed very different (e.g. nematodes, insects, and priapulids) and was challenged right away (e.g. Wagele et al. 1999). The generally-accepted relationships and evolutionary scenario was the the Articulata Hypothesis (read an excellent review of the Articulata Hypothesis by Scholtz 2002). Briefly stated, this view, based primarily on morphology, said that Arthropods and their relatives (Onychophora and Tardigrada) were sisters to other segmented animals like Annelida (Ax 1999; Brusca and Brusca 2003; Nielsen 2001; Westheide and Rieger 1996). This is a very old perspective. Cuvier (1817) united all of the segmented invertebrates (mainly annelids and arthropods) into a taxon that he called Articulata; thus, this view was deeply-ingrained in zoology. Some molecular phylogenies also were equivocal (e.g. Blair et al. 2002; Wagele et al. 1999) and the Coelomate Hypothesis, the view that animals with a true coelom were closely related began to receive some support (described in Philip et al. 2005). Telford (2004) noted that there was no general agreement on the Ecdysozoa Hypothesis because molecular sequences other than SSU rRNA yielded very different pictures of the bilaterians with little support for the Ecdysozoa. More robust analyses with large numbers of taxa and multiple genes and whole genomes, however, show very strong evidence for the existence of the Ecdysozoa as a major bilaterian clade (Telford et al. 2008; Philippe et al. 2005; and Webster et al. 2006; see Figure 2). Nielsen (2003) attempted to save the Articulata Hypothesis by suggesting that Annelida was a sister group to the Ecdysozoa. Nevertheless, Edgecombe et al. (2011) state very strongly that although morphological synapomorphies have been offered to support both the Coelomate Hypothesis and the Articulata Hypothesis, neither one has support through molecular analysis. The structure of the Ecdysozoa as a higher taxon also has been in flux (note the differences in Figure 2A and 2B). Telford et al. (2008) and Garey (2001) describe the Ecdysozoa as a monophyletic group with three clades. Telford et al. (2008) call these groups (superphyla?): Scalidophora, Nematoida, and Panarthropoda (Figure 2. S, N, and PA, respectively). Scalidophora and Nematoida have been grouped together in a sister relationship as the Cycloneuralia (e.g. Dunn et al. 2008, see Figure 2B). This clade has some support, from morphology (e.g. the presence of an introvert and the ganglia of the brain forming a ring around the esophagus. Scalidophora (Schmidt-Rhaesa 1998) includes the priapulids and kinorhynchs, both groups that have an introvert with similar musculature and scalids (Schmidt-Rhaesa 1998, and Nielsen 2001). They also include the Loricifera in this group though Telford et al. (2008) caution that there is little work on them and the similarities may be superficial. The Palaeoscolecida (see Figure 3) is a group of extinct animals that appear to be very similar to Priapulida and may shed some light on the origin of the Ecdysozoa (Han et al. 2007). Harvey et al. (2010), however, conclude in their analysis that palaeoscolecids are stem priapulids only and thus are far removed from the common ancestor that gave rise to the ecdysozoans. They possess characters that are typical of the scalidiferans: an introvert and an annulated body with distinctive superficial structures that may be scalids. Figure 3C reflects the general view of how the palaeoscolecids may have given rise to burrowing worms like priapulids and then to segmented animals that lived on the surface of the mud. Initially, those animals had protuberances at intervals down the segmented body. Then, the two ventral-most protuberances became longer to become walking legs. The Nematoida (a term coined by Schmidt-Rhaesa 1998 and called Nematozoa by Zrzavy et al. 1998) includes Nematoda and Nematomorpha, phyla that share obvious morphological similarities. Furthermore, Telford et al. (2008) list 5 morphological synapomorphies, first identified by Nielsen (2001). The molecular support, though present, is weak (Telford et al. 2008, Petersen and Ernesse 2001, and Mallatt et al. 2003). Figure 2A shows a generally-accepted view of Nematoida as sisters to the Panarthropoda. The likely explanation for their loss of morphological complexity (though not a concomitant loss in developmental life history complexity) is that the Nematoida sprang from a parasitic group. Indeed, the Nematomorpha is entirely parasitic and many of the Nematoda also are parasitic. The free-living nematodes may have become so secondarily. There is strong support for the Panarthropoda as a clade which includes the phyla Tardigrada, Onychophora, and Arthropoda. They are associated by many morphological characters, including serially repeated legs which end in claws (Telford et al. 2008). Most molecular support for the group also is strong (e.g. Patel et al. 1989, Garey 2001, and Gabriel and Goldstein 2007). The position of the tardigrades, however, remains questionable. Lartillot and Phillippe (2008) and Dunn et al. (2008) show that tardigrades may have greater affinities with the nematodes than they do with the arthropods. Campbell et al. (2011) used microRNAs and phylogenomics in their analyses, which they claimed reduced the influence of the long branches in Nematoda, and caused the Tardigrada to group together with the Onychophora and Arthropoda in the Panarthropoda. If so, Cycloneuralia is not monophyletic, and the topology of ecdysozoan phylogeny would be closer to Figure 2A. Please consult The Major Clades of the Animal Kingdom for some views on the relationships of the protostome phyla with each other and with the other phyla of protostomes.

	FIGURE 3. PALAEOSCOLECIDS. A. A fossil of a middle Cambrian palaeoscolecid from China. Note the segmented, worm-like body with an anterior introvert-like cone. B. is an illustration of a similar animal with the detail of a body scale. C. A possible scenario for the evolution of a Priapulid-like ancestor and the evolution of worm-like animals that give rise to worms that move on the surface of the mud, first with four stubby, equally-sized peg-like knobs on body segments. Then, the ventral two knobs become larger and articulated to become Onycophora-like legs. Images A and C. from Harvey et al. (2010), Figure 1. Image B from Han et al. (2007), Figure 6.

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By Jack R. Holt. Last revised: 02/05/2015