Abstract and Keywords
The phylum Rotifera consists of approximately 2,000 described species of free-living, aquatic, mostly limnic organisms and about 900 aquatic or terrestrial, completely gutless, parasites. Many of the free-living types can be distinguished by the ciliary ‘wheel organ’ or corona from which the phylum derived its name, but it is either highly modified or completely absent in others. The Rotifera comprises four main groups: Monogononta, Bdelloidea, Seisonidea, and Acanthocephala. The acanthocephalans were originally considered a separate phylum, but are now regarded as a sister group (or an in-group) of one of the free-living groups on the basis of the ultrastructure of the epidermis. In addition, the general structure of the mastax jaws, along with the ultrastructure of the jaws having parallel cuticular tubules with a dense core, suggests that the rotifers are closely related to the micrognathozoans and gnathostomulids. Studies on monogonont development have focused on the pelagic genus Asplanchna.
Rotifera (including Acanthocephala) consists of about 2000 described species of free-living, usually less than a millimetre-long, aquatic, mostly limnic organisms and a group of about 900 aquatic or terrestrial, completely gutless parasites (Acanthocephala), with the juveniles occurring in arthropods and the 2-mm to almost 1-metre-long adults living in the alimentary canal of vertebrates. The free-living types have direct development, whereas the acanthocephalans have complicated life cycles with more than one host.
Many of the free-living types can be recognized by the ciliary ‘wheel organ’ or corona that has given name to the phylum, but it is highly modified or completely absent in others. The anterior end, with the wheel organ in the free-living forms, and the proboscis of the acanthocephalans can be retracted into the main body. Four main groups are recognized: Monogononta (with parthenogenetic phases and sexual phases with small haploid males), Bdelloidea (only parthenogenetic females without meiosis), Seisonidea (with similar males and females), and Acanthocephala (dioecious, highly specialized without gut). The acanthocephalans were earlier regarded as a separate phylum, but the ultrastructure of the epidermis points to them being a sister group (or an in-group) of one of the free-living groups. The interrelationships between the four groups must be characterized as unresolved (see below), but the monophyly of the group now seems unquestioned. The name Syndermata has been used for the traditional rotifer groups plus the acanthocephalans by a number of German authors (for example Ahlrichs 1997; Ax 2001; Herlyn et al. 2003; Witek et al. 2008), but it appears completely unnecessary to introduce a new name for the group, just because the acanthocephalans have turned out to be an ingroup.
Monogononts have a single ovary; their life cycles are complicated with parthenogenetic generations of females producing diploid eggs and sexual generations of females that produce haploid eggs; non-fertilized eggs develop into haploid males and fertilized eggs become resting eggs. The males are much smaller than the females and lack the gut in most species. Several types have a wheel organ (Fig. 34.1) that is a typical protostomian downstream-collecting ciliary system with prototroch (called trochus), adoral ciliary zone, and metatroch (called cingulum), but others are strongly modified.
Bdelloids are parthenogenetic with paired ovaries. The evolution of a large clade without sexual reproduction is unique in the Metazoa (Welch and Meselson 2000). A number of karyological and ecological (p.186)
Seisonidea, with the only genus Seison with two species, are epibionts on the crustacean Nebalia. Males and females are similar, with the wheel organ reduced to a small ciliated field with short lateral rows of compound cilia.
Adult acanthocephalans are cylindrical or slightly flattened with a retractile, cylindrical proboscis with recurved hooks, ideal for anchoring the parasite to the intestinal wall of the host; many species have rings of smaller or larger spines or hooks on the whole body. There is no trace of an alimentary canal at any stage, and it cannot be seen directly if the proboscis represents the anterior part of the body with a reduced, terminal mouth or a dorsal attachment organ (see below). Also the dorsal-ventral orientation has been questioned. Their eggs are fertilized and develop into the acanthor stage before the eggs are shed and leave the host with the faeces. When ingested by an intermediate host the acanthor hatches in the intestine and enters the intestinal wall; here it develops into the acanthella stage and further into the cystacanth, which is the stage capable of infecting the final host.
Many tissues of rotifers are syncytial, but the number of nuclei in most organs is nevertheless constant, and divisions do not occur after hatching; this implies that the power of regeneration is almost absent.
The body epithelium of the free-living types has a usually very thin extracellular cuticle probably consisting of glycoproteins and an intracellular skeletal lamina (sometimes referred to as an intracellular cuticle) apposed to the inner side of the apical cell membrane. This intracellular lamina may be of different thickness in various parts of the body and in different species; homogeneous in Asplanchna, lamellate in Notommata, and with a honeycomb-like structure in Brachionus; it has characteristic pores with drop-shaped invaginations of the cell membrane, and the general structure is identical in all the free-living groups (Ahlrichs 1997). The intracellular skeletal lamina consist of intermediate filaments of a scleroprotein of the keratine-type; chitin has not been found.
The acanthocephalan body wall consists of a syncytial ectoderm, a thick basal membrane, an outer layer of circular muscles, and an inner layer of longitudinal muscles; a rete system of tubular, anastomosing cells with lacunar canals is found on the inner side of (p.187) the longitudinal muscles in Macracanthorhynchus and between the two muscle layers in Oligacanthorhynchus. The ectoderm or tegument has very few gigantic nuclei with fixed positions. The apical cell membrane shows numerous branched, tubular invaginations that penetrate an intracellular skeletal lamina consisting of a thin, outer, electron-dense layer and a thicker, somewhat less electron-dense layer.
The ectoderm of the ciliary bands found in bdelloids and monogononts consists of large cells with several nuclei and connected by various types of cell junctions, whereas the ectoderm of the main body region is a thin syncytium. All ciliated epithelial cells are multiciliate. The ectoderm of the ciliary bands has the usual surface structure with microvilli and a layer of normal, extracellular cuticle between the tips of the microvilli. Also some of the sensory organs have this type of cuticle. The buccal epithelium appears to lack a cuticle and the cilia have modified, electron-dense tips. The pharyngeal epithelium has multiple layers of double membranes that also cover the cilia. The borderline between these two epithelia marks the origin of a flattened, funnel-shaped structure called the velum that consists of two thick layers of parallel membranes lining a ring of long cilia with somewhat blown-up cell membranes. The muscular mastax carries a complicated system of cuticular jaws (trophi), which are thickened parts of a continuous membrane with more than 50% chitin in Brachionus (Klusemann et al. 1990). The whole structure is extracellular; the several reports of intracellular mastax structures are probably erroneous. The jaws have a tubular structure with basal, electron-lucent canals surrounding a cytoplasmic core (Ahlrichs 1995; Rieger and Tyler 1995). The jaws contain important systematic information (Sørensen 2002). The conspicuous hooks of larval and adult acanthocephalans are outgrowths from the connective tissue and contain chitin (Taraschewski 2000). This shows that the hooks are not homologous with the mastax.
The wheel organ shows an enormous variation (Figs. 22.4–5, 34.1). Some creeping types, such as Dicranophorus have a ventral, circumoral zone of single cilia used in creeping; predatory, planktonic forms, such as Asplanchna, have a pre-oral, almost-complete ring of compound cilia used in swimming; planktotrophic forms that may be planktonic or sessile, such as Hexarthra, Conochilus, and Floscularia, have an adoral zone of single cilia bordered by a pre-oral prototroch and a post-oral metatroch, with the whole ciliary system surrounding the apical field; many other variations are found, and Acyclus and Cupelopagis lack the corona in the adult stage (Beauchamp 1965). Proto- and metatroch consist of compound cilia, and the whole complex is a downstream-collecting system (Strathmann et al. 1972).
Particles captured by the corona are transported through the ciliated buccal tube to the mastax with the jaws (see above). The macrophagous species can protrude the jaws from the mouth and grasp algal filaments or prey. The movements of the jaws are coordinated by the mastax ganglion, which receives input from ciliated sense organs at the bottom of its lumen and from the brain. Various types of jaws are characteristic of larger systematic groups and are correlated with feeding behaviour. A partly ciliated oesophagus leads to the stomach, which is syncytial and without cilia in bdelloids and cellular with cilia in monogononts. There is a ciliated intestine opening into a short cloaca and a dorsal anus. A few genera lack the intestine, so only the protonephridia and the genital organs open into the cloaca.
The nervous system generally comprises a dorsal brain, a mastax ganglion, a pedal ganglion associated with a pair of toes ventral to the rectum, and a number of peripheral nerves with various types of cells. The brain comprises about 150 to 250 cells with species-specific numbers (Nachtwey 1925; Peters 1931). The monogononts Notommata and Asplanchna (Hochberg 2007, 2009) have rather similar brains (with about 28 identifiable serotonergic cells in Asplanchna); the planktonic Asplanchna lacks the toes and the pedal ganglion. The bdelloid Macrotrachela (Leasi et al. 2009) shows a similar general brain morphology, but with different numbers and positions of the neurons. A pair of lateroventral nerves connect the lateroposterior parts of the brain with the pedal ganglion. Photoreceptors of a number of different types, such as the phaosomes with peculiar expanded cilia, are found (p.188) embedded in the brain of many species. The pedal ganglion is usually associated with the feet and the cloaca, but separate ganglia for the two regions are found in some species (Remane 1929–1933). One or a pair of dorsal antennae and a pair of lateral antennae are small sensory organs comprising one or a few primary sensory cells with a tuft of cilia. Each transverse muscle is innervated by one or two large nerve cells, which gives a superficial impression of segmentation (Zelinka 1888; Stossberg 1932).
The acanthocephalan brain comprises a low, species-specific number of cells. Nerves have been tracked to the muscles of the body wall and the proboscis, to paired genital ganglia, to a pair of sense organs at the base of the proboscis, and to a pair of sensory and glandular structures, called the apical organ, at the tip of the proboscis (Gee 1988); both structure and function of the apical organ are in need of further investigations based on a number of species before definite statements about its homology to other apical organs can be made.
Almost all the muscles of the free-living forms are narrow bands with one nucleus. They attach to the body wall through an epithelial cell with hemidesmosomes and tonofibrils. The two large retractor muscles of the corona are coupled to other muscles through gap junctions and send a cytoplasmic extension to the brain where synapses occur; other muscles are innervated by axons from the ganglia. Bdelloids have the body wall divided into a series of rings, and both the anterior and posterior end can be telescoped into the middle rings; there are one or two annular muscles in each ring and longitudinal muscles between neighbouring rings or extending over two to three rings (Zelinka 1886, 1888). There is practically no connective tissue, and collagen genes are absent in Brachionus (Suga et al. 2007). The spacious body cavity functions as a hydrostatic skeleton in protrusion of the corona.
The proboscis of the acanthocephalans has several associated sets of muscles that are involved in protrusion, eversion, and retraction (Taraschewski 2000). The proboscis region can be protruded by the muscles of the body wall and retracted by the neck-retractor muscles that surround the lemnisci and attach to the body wall. The inverted proboscis lies in a receptacle that has a single or double wall of muscles. The contraction of these muscles everts the proboscis, with the receptacle fluid functioning as the hydrostatic skeleton, and a contraction of the neck retractors squeezes fluid from the lemnisci to the wall of the proboscis that swells. A retractor muscle from the tip of the proboscis to the bottom of the receptacle inverts the proboscis, and the receptacle can be retracted further into the body by the contraction of the receptacle retractor that extends from the bottom of the receptacle to the ventral body wall. There is a spacious body cavity, which functions as a hydrostatic organ. It contains an enigmatic organ called the ligament sac(s), which develops in all types but degenerates in some forms. The ligament sac(s) and the gonads develop in the acanthella from a central mass of cells between the brain and the cloaca, and it is generally believed that a median string, called the ligament, represents endoderm. There is either a single, or a dorsal and a ventral sac that communicate anteriorly. The sacs are acellular, fibrillar structures that contain collagen (Haffner 1942). The posterior end of the (dorsal) ligament sac is connected with the uterine bell (see below).
There is a paired-protonephridial system (Riemann and Ahlrichs 2010), with one to many flame cells. Monogononts have large terminal cells with a filtering weir of longitudinal slits supported by internal pillars, the bdelloids have similar but smaller cells and lack pillars, and Seison has a weir with longitudinal spiral rows of pores and lack pillars. Among the acanthocephalans, only the Oligacanthorhynchidae have protonephridia. Each protonephridium is a syncytium with three nuclei situated centrally and many radiating flame bulbs with high numbers of cilia. An unpaired, ciliated excretory canal opens into the urogenital canal.
Female monogononts have an unpaired, sac-shaped germovitellarium, and the males have a single testis; both types of gonads open into the cloaca. The ovaries contain a number of oocytes, which is fixed at birth. The sperm has an elongate head with the axoneme following the nucleus in the posterior part; the tail contains the axoneme with the cell membrane expanded (p.189) laterally into a longitudinal undulating membrane with a supporting structure (Melone and Ferraguti 1994, 1999). The bdelloids have paired germovitellaria. The parthenogenetic eggs become surrounded by a chitinous shell secreted by the embryo. Females of Seison have paired ovaria without vitellaria and the males have paired testes with a common sperm duct. The sperm superficially resembles that of the monogonents, but the cilium is free from the elongate nucleus and situated
Studies on monogonont development have centred on the pelagic genus Asplanchna (Lechner 1966), with additional observations on Ploesoma (Beauchamp 1956) and Lecane (Pray 1965). Lechner (1966) reinterpreted some of the reports on the early development (Fig. 34.2 and Table 34.1) and Nachtwey (1925) described organogenesis. The cleavage is total and unequal and the 4-cell stage has three smaller A–C blastomeres and a large D blastomere; the polar bodies are situated at the apical pole. The D cell divides unequally, and its large descendant (1D) comes to occupy the blastoporal pole, while the smaller descendant (1d) and the A–C cells form an apical ring. The 1D macromere gives off another small cell, and all the other blastomeres divide equally, with the spindles parallel to the primary axis. The embryo now consists of four rows of cells, with the large 2D cell occupying the blastoporal pole. The smaller cells divide further and slide along the macromere that becomes internalized in an epibolic gastrulation; the movements continue as an invagination, forming an archenteron, where it appears that the stomach originates either from a–c cells or exclusively from b cells, and the pharynx from all four quadrants. The 2D cell gives off two abortive micromeres and the 4D cell gives rise to the germovitellarium. The stronger gastrulation movement of the dorsal side (b cells) (p.190)
Table 34.1. Cell lineage of Asplanchna girodi. The original notation is given in parentheses. (Modified from Lechner 1966.)
The eggs are highly determined already before the polar bodies are given off, and the powers of regulation are very limited (Lechner 1966).
The cleavage pattern shows no sign of a spiral arrangement of the blastomeres, but as far as the cell lineage is known, the cleavage is clearly of the D-quadrant type (Fig. 21.1). The cerebral ganglion develops from cells near the apical pole, and the lack of a larval stage may have caused a loss of a ciliated apical ganglion. The ciliary bands have the very same structure and function as those of larvae and adults of spiralians, such as annelids and molluscs (Fig. 22.4-5), but the cell lineage has not been studied.
Bdelloid embryology is poorly known; there is no meiosis. Zelinka (1891) studied the development of Callidina (now Mniobia). The embryos become curved and the report is difficult to follow in detail, but the development appears to resemble that of the monogononts.
The development of Seison has not been studied.
Acanthocephalan embryology has been studied by a number of authors (Schmidt 1985). The polar bodies are situated at one pole of the ellipsoidal egg and mark the future anterior end. The first two cleavages result in an embryo with one anterior (B), two median (A and C), and one posterior (D) cell; the blastomeres are usually of equal size, but the posterior cell is larger than the others in a few species. The embryo becomes syncytial at a stage of 4–36 cells according to the species. Meyer (1928, 1932–1933, 1936, 1938) elegantly followed the cell lineage (or rather the nuclear lineage) of Macracanthorhynchus (Fig. 34.3), and reported a cleavage with a primary axis slightly oblique to the longitudinal axis of the egg; the A and C cells of the (p.191) 4-cell stage are in contact along the whole primary axis, and the spindles of the following cleavages are almost parallel. After the 34-cell stage, the cells begin to fuse, soon forming one large syncytium, and the cleavage pattern and the movements of the nuclei become difficult to follow. At the stage of 163 nuclei, small inner nuclei of the ganglion and of the musculature
The monophyly of a group comprising the free-living rotifers and the acanthocephalans is supported by the presence of the unique epidermis with the intracellular skeletal lamina, and molecular studies almost unanimously support monophyly (Giribet et al. 2004; García-Varela and Nadler 2006; Sørensen and Giribet 2006; Witek et al. 2008). However, almost every possible phylogenetic hypothesis for interrelationships of the four groups has been proposed. They are probably all monophyletic, and a number of molecular studies favour a sister-group relationship between Bdelloidea and Acanthocephala (Giribet et al. 2004; García-Varela and Nadler 2006). I have chosen to retain the name Rotifera for the whole group, and to treat the four subgroups separately pending additional information.
(p.192) Conway Morris and Crompton (1982) found so many similarities between the Burgess Shale priapulan Ancalagon and the living acanthocephalans that they considered priapulans and acanthocephalans as sister groups. The overall resemblance between the two groups is considerable, but the intracellular nature of both the ‘cuticle’ and the spines on the ‘proboscis’ in acanthocephalans is in strong contrast to the true cuticular structure of these organs in priapulans, which demonstrates that the resemblance is completely superficial.
Already Hatschek (1878, 1891) stressed the similarities of the ciliary bands of rotifers and trochophora larvae of annelids and molluscs and proposed that the common ancestor of these groups had a larva of this type. Lang (1888) proposed that the rotifers are neotenic, i.e. sexually mature trochophores. However, the idea of ancestral trochophore-like ciliary bands in rotifers fell into disregard when Beauchamp (1907, 1909) published his comparative studies on the ciliary bands of several rotifers. His conclusions were that the types with the trochophore-type ciliation have evolved several times from an ancestral type with a circumoral ciliary field used in creeping, and that the rotifer ciliation could be derived from the general ciliation of a flatworm via the ventral ciliation of the gastrotrichs. Jägersten (1972) hesitantly supported the old idea that the rotifers have the trochophore ciliation and that this is an ‘original larval feature’, and this was also favoured by Clément (1993).
I believe that the rotiferan wheel organ, with proto- and metatroch of compound cilia bordering an adoral zone of single cilia and functioning as a downstream-collecting system, is homologous with the similar bands of the trochophores of annelids, molluscs, and entoprocts. The various other types of wheel organs can be interpreted as adaptations to other feeding types, and the parasitic acanthocephalans are highly derived. The trochophore is definitely a larval form (Chapter 22) and the rotifers must therefore be interpreted as neotenic—not as neotenic annelids, but as neotenic descendants of the protostomian ancestor, gastroneuron. The planktotrophic rotifers must therefore represent the ancestral type, which have become temporarily or permanently attached; sessile forms have planktonic juvenile stages, and changes between pelagic and sessile habits may have taken place several times; the macrophagous types, which may be pelagic or creeping, have reduced ciliary bands and must be regarded as specialized.
A close relationship with the micrognathozoans and gnathostomulids is indicated both by the general structure of the mastax jaws (Fig. 31.2) and by the ultrastructure of the jaws that consists of parallel cuticular tubules with a dense core.
The molecular analyses are discussed further in Chapter 31.
Interesting subjects for future research
1. Cell lineage of a species with prototroch—traits of spiral cleavage
2. Hox genes of species with and without anus
3. Embryology of Seison and bdelloids
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