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The Gnathifera Phyla Gnathostomulida, Rotifera (Including Acanthocephala), and Micrognathozoa

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The Gnathifera Phyla Gnathostomulida, Rotifera (Including Acanthocephala), and Micrognathozoa CHAPTER 16 The Gnathifera Phyla Gnathostomulida, Rotifera (including Acanthocephala), and Micrognathozoa he clade Gnathifera includes three phyla: Gnathostomulida, Microgna- thozoa, and Rotifera, with the latter including the parasitic acantho- cephalan worms (formerly a separate phylum). The name is derived T from the Greek gnathos, “jaw” and the Latin fera, “to bear,” and refers to the presence of pharyngeal hard parts, i.e., jaws that are either present or secondarily lost in all gnathiferan taxa. Despite their small size, gnathiferans show a remarkable complexity of anatomy, especially in their jaw structures (e.g., the mastax and trophi) and the organization of their muscular and ner- vous systems. Until the mid-1990s, the Gnathostomulida and Rotifera were pooled together with other microscopic taxa in questionable groups such as “Aschelminthes” or “Nemathelminthes”—catchall group- ings that were more or less solely character- ized by hosting microscopic taxa with uncer- Classification of The Animal tain phylogenetic positions. At that time, the Kingdom (Metazoa) Acanthocephala was treated as a distinct phy- lum, but despite their macroscopic size and Non-Bilateria* Lophophorata endoparasitic biology, they were already con- (a.k.a. the diploblasts) PHYLUM PHORONIDA PHYLUM PORIFERA PHYLUM BRYOZOA sidered to be closely related to the Rotifera, PHYLUM PLACOZOA PHYLUM BRACHIOPODA based on ultrastructural similarities in their PHYLUM CNIDARIA ECDYSOZOA integuments. During the 1990s, a number of re- PHYLUM CTENOPHORA Nematoida searchers began to investigate the phylogenetic PHYLUM NEMATODA Bilateria positions of the aschelminth phyla. In 1995, two PHYLUM NEMATOMORPHA (a.k.a. the triploblasts) important papers (by W. H. Ahlrichs, R. M. Scalidophora PHYLUM XENACOELOMORPHA Rieger and S. Tyler) suggested a sister-group PHYLUM KINORHYNCHA Protostomia PHYLUM PRIAPULA relationship between Gnathostomulida and PHYLUM CHAETOGNATHA PHYLUM LORICIFERA Rotifera, based on a proposed homology be- SPIRALIA Panarthropoda tween the jaws in the two groups. The homol- PHYLUM PLATYHELMINTHES PHYLUM TARDIGRADA ogy was supported by ultrastructural data from PHYLUM GASTROTRICHA PHYLUM ONYCHOPHORA transmission electron microscopy, which dem- PHYLUM RHOMBOZOA PHYLUM ARTHROPODA PHYLUM ORTHONECTIDA SUBPHYLUM CRUSTACEA* onstrated that jaws in both taxa are made up by PHYLUM NEMERTEA SUBPHYLUM HEXAPODA rodlike elements that in cross section appear as PHYLUM MOLLUSCA SUBPHYLUM MYRIAPODA translucent areas with a central, electron-dense PHYLUM ANNELIDA SUBPHYLUM CHELICERATA core. Ahlrichs (1995) referred to this group as PHYLUM ENTOPROCTA Deuterostomia PHYLUM CYCLIOPHORA Gnathifera, and he further suggested that the PHYLUM ECHINODERMATA Gnathifera PHYLUM HEMICHORDATA PHYLUM GNATHOSTOMULIDA PHYLUM CHORDATA PHYLUM MICROGNATHOZOA Martin V. Sørensen wrote the introduction and revised PHYLUM ROTIFERA *Paraphyletic group sections on phyla Gnathostomulida and Rotifera. Katrine Worsaae and Reinhardt Møbjerg Kristensen wrote the section on phylum Micrognathozoa. © 2016 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 614 Chapter Sixteen Gnathostomulida Micrognathozoa Rotifera Monogononta Acanthocephala Bdelloidea Seisonidea 3 2 1 Figure 16.1 Phylogenetic tree showing jaw structure hard parts/jaws composed of rods made of a translucent and the relationships within Gnathifera. Synapomorphies material with an electron-dense core, (2) cellular epidermis for the major clades are marked on the tree: (1) pharyngeal with intracellular protein lamina, (3) syncytial epidermis. endoparasitic acanthocephalans were actually no more Morphology-based phylogenies indicate that than highly modified rotifers. Gnathostomulida branches off as the most basal At the same time Gnathifera was taking its shape, gnathiferan, whereas Micrognathozoa and Rotifera another new animal was discovered in mosses from (including Acanthocephala) appear as sister-groups a cold spring in Greenland. It was a tiny, microscopic supported by similarities in the ultrastructure of their invertebrate that in some respects resembled a rotifer, integuments (Figure 16.1). Both free-living Rotifera and in other ways a gnathostomulid, but also pos- and Acanthocephala (see below) have a syncytial epi- sessed several characteristics that were not found in dermis where the outer cuticle has been replaced by any other groups. The animal had jaws that were even an intracellular protein lamina in the epidermal cells. more complex and numerous in elements than those Micrognathozoa has a regular non-syncytial epidermis, found in the two other gnathiferan phyla. Transmission but a similar intracellular protein lamina is found in its electron microscopy showed that the ultrastructure dorsal epidermal plates, and the presence of this lam- of the jaws was nearly identical with that of Rotifera ina is considered synapomorphic for Micrognathozoa and Gnathostomulida. Six years after its discovery, R. and Rotifera-Acanthocephala. M. Kristensen and P. Funch (2000) named the animal Several molecular studies initially suggested a close Limnognathia maerski, and assigned it to a new animal relationship between Gnathostomulida and Rotifera– group Micrognathozoa, which four years later was rec- Acanthocephala, but then in 2015, using larger data- ognized as a third gnathiferan phylum. sets, the Micrognathozoa began to appear as a sister Morphologically, Gnathifera appears to be a group to the Rotifera–Acanthocephala. well-supported monophyletic group that is char- Based on ultrastructural similarities in their integu- acterized by the presence of homologous pharyn- ments, the microscopic rotifers and the macroscopic geal hard parts, and at least one phylogenomic study acanthocephalans have long been considered as like- Bruscahas alsoand Brusca found 3e support for the clade Gnathifera. ly sister taxa. However, more recently an increasing BB3e_16.01m.ai 9/28/15 © 2016 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. THE GNATHIFERA Phyla Gnathostomulida, Rotifera (including Acanthocephala), and Micrognathozoa 615 (C) Figure 16.2 Representative gnathostomulids. (A) Haplognathia simplex. (B) Austrognatharia kirsteueri. (C) Basal plate and jaws of Gnathostomula armata. features of this phylum include a unique jawed pha- ryngeal apparatus and monociliated epidermal cells (Box 16A). The currently described 100 species and 26 amount of evidence from molecular studies have un- genera are divided between two orders. ambiguously shown that Acanthocephala is not the sister of Rotifera, but actually evolved from within the GNATHOSTOMULID CLASSIFICATION Rotifera—presumably as a clade that became obligate endoparasitic, and subsequently went through a series ORDER FILOSPERMOIDEA Body usually very elongate, of dramatic morphological modifications and changes. with slender rostrum; jaws relatively simple; male parts with- Modern acanthocephalans are so modified and adapt- out injectory penis; sperm filiform (with one 9+2 flagellum); ed to their endoparasitic lifestyle that it is hard to find comparative morphological characters that would place them inside Rotifera, but the molecular support BOX 16A Characteristics is strong and includes studies based on selected target loci and expressed sequence tags, as well as the com- of the Phylum plete mitochondrial genomes. Gnathostomulida 1. Triploblastic, bilateral, unsegmented, vermiform acoelomates Phylum Gnathostomulida: 2. Epidermis monolayered; all epithelial cells are The Gnathostomulids monociliated 3. Gut incomplete (anus rudimentary, vestigial, or The phylum Gnathostomulida (Greek, gnathos, “jaw”; absent) stoma, “mouth”) includes about 100 species of minute 4. Pharynx with unique, complex jaw apparatus vermiform hermaphroditic animals (Figure 16.2). These 5. Without circulatory system or special gas exchange meiofaunal creatures were first described by Peter Ax structures in 1956 as turbellarians, but given their own phylum 6. Excretion through protonephridia with monociliated rank by Rupert Riedl in 1969. Gnathostomulids are terminal cells found worldwide, interstitially in marine sands mixed 7. Hermaphroditic with detritus, from the intertidal zone to depths of hundreds of meters. The tiny, elongate body (less than 8. Cleavage spiral and development direct 2 mm long) is usually divisible into head, trunk, and 9. Inhabit marine, interstitial environments in some species a narrow tail region. Distinguishing Brusca and Brusca 3e BB3e_16.02.ai ©9/28/15 2016 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured or disseminated in any form without express written permission from the publisher. 616 Chapter Sixteen female parts without vagina and bursa. (3 genera: Cosmog- monociliated cells are concentrated in the head region. nathia, Haplognathia, and Pterognathia) Gnathostomulid specialists have attached a formidable ORDER BURSOVagInoIDEa Body usually not extremely array of names to these structures, which are of major elongate relative to width; head with shorter rostrum and taxonomic significance. often a constriction in the neck area; jaws complex; male parts with penis, with or without a stylet; sperm cells aflagel- Reproduction and Development late, either dwarf cells or giant conuli; female parts with Gnathostomulids are hermaphrodites. The
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