Central nervous system and sense organs, with special reference to photoreceptor-like sensory elements, in Polygordius appendiculatus (Annelida), an interstitial polychaete with uncertain phylogenetic affinities

Abstract. The phylogenetic position of Polygordius is still pending; relationships with either Opheliidae or with Saccocirrus are the most favored hypotheses. The present study of Polygordius appendiculatus was designed to look for morphological characters supporting either of these two hypotheses. The homology of the anterior appendages, and the structure of the central nervous system and nuchal organ all required clarification; we also examined whether photoreceptor‐like sense organs exist in adults. From their innervation pattern, it is likely that the anterior appendages represent palps. They lack structures typical of palps in Canalipalpata, such as musculature and coelomic cavities, which would be expected in the case of a saccocirrid relationship. Thirteen photoreceptor‐like sense organs were found in front of the brain, the only structures resembling photoreceptors in adults of P. appendiculatus. These multicellular sense organs comprise a supportive cell and several sensory cells enclosing an extracellular cavity. There are three different types of sensory cells: one rhabdomeric and two ciliary. These sensory cells are combined differently into three forms of sense organ: the most frequent uses all three types of sensory cells, the second possesses one rhabdomeric and one ciliary cell type, and the third has two types of ciliary sensory cells. Whereas similar sensory cells are frequently found in various polychaetes, their combination in one sensory organ is unique to Polygordius and is considered to represent an autapomorphy. The nuchal organs exhibit features typical of polychaetes; there are no specific features in common with Saccocirrus. Instead, the covering structures show obvious similarities to Opheliidae, as can also be found in the central nervous system. Altogether, the current observations do not contradict a relationship with opheliids but provide no evidence of a relationship with Saccocirrus as has been found in certain molecular analyses, and thus currently leave the phylogenetic position of Polygordius unresolved.     

Phylogenetic inference regarding Parergodrilidae and Hrabeiella periglandulata ('Polychaeta', Annelida) based on 18S rDNA, 28S rDNA and COI sequences

Parergodrilidae and Hrabeiella periglandulata are Annelida showing different combinations of clitellate-like and aclitellate characters. Similarities between both of these taxa and Clitellata have widely been regarded as the result of convergent evolution due to similar selection pressures. The position of the three taxa in the phylogenetic system of Annelida is still in debate. However, in analyses based on 18S rDNA sequences a close relationship of Parergodrilidae with Orbiniidae and Questidae was suggested. To infer their phylogeny the sequences of the 28S rDNA and of the cytochrome oxidase I (COI) gene of Stygocapitella subterranea , Parergodrilus heideri and H. periglandulata were determined. The data were extended by sequences of various species including species from Clitellata and Orbiniidae. Prior to tree reconstruction the dataset was analysed in detail for phylogenetic content by applying a sliding window analysis, a likelihood mapping and Modeltest V.3.04. Subsequently, generalized parsimony and maximum likelihood methods were employed. Clade robustness was estimated by bootstrapping. In addition, combined analyses of the sequences of 18S rDNA and 28S rDNA as well as of 18S rDNA, 28S rDNA and COI were performed. The combination of the data of the two structure genes and a mitochondrial gene improved the resolution obtained with the single datasets slightly. These analyses support a close relationship of Parergodrilidae and Orbiniidae but cannot resolve the position of H. periglandulata . In every analysis Clitellata cluster within 'Polychaeta', confirming previous investigations.     

Sense organs in polychaetes (Annelida)

Polychaetes possess a wide range of sensory structures. These form sense organs of several kinds, including the appendages of the head region (palps, antennae, tentacular cirri), the appendages of the trunk region and pygidium (parapodial and pygidial cirri), the nuchal organs, the dorsal organs, the lateral organs, the eyes, the photoreceptor-like sense organs, the statocysts, various kinds of pharyngeal papillae as well as structurally peculiar sensory organs of still unknown function and the apical organs of trochophore larvae. Moreover, isolated or clustered sensory cells not obviously associated with other cell types are distributed all over the body. Whereas nuchal organs are typical for polychaetes and are lacking only in a few species, all other kinds of sensory organs are restricted to certain groups of taxa or species. Some have only been described in single species till now. Sensory cells are generally bipolar sensory cells and their cell bodies are either located peripherally within the epidermis or within the central nervous system. These sensory cells are usually ciliated and different types can be disinguished. Structure, function and phylogenetic importance of the sensory structures observed in polychaetes so far are reviewed. For evaluation of the relationships of the higher taxa in Annelida palps, nuchal organs and pigmented ocelli appear to be of special importance.     

Photoreceptive organs in larvae of Spionidae (Annelida) and Sipuncula

A pair of spherical unpigmented ocelli in addition to pigmented eyes have been observed in the anterior part of the prostomium in larvae of more than 40 species of Spionidae examined alive with light microscopy. Ocelli become visible in larvae at the one- to three-segment stage, increase in size as growth proceeds, and probably disintegrate in the course of metamorphosis because they were not observed in adults and settled juveniles. One pair of transparent, spherical bodies is also found in the anterior part of the head of planktotrophic pelagosphera larvae of Sipuncula. These bodies are in a similar position and have a similar appearance and size to unpigmented ocelli in Spionidae larvae. A pair of epidermal invaginations, densely covered with short cilia, is also observed antero-laterally in the head in pelagospheras of one species. These invaginations appear similar to the nuchal organs present in many polychaete larvae. Photoreceptive organs so far reported for sipunculan larvae comprise only pigmented eyes. Unpigmented ocelli and nuchal organs have never been reported in pelagospheras. Further ultrastructural investigations on sipunculan larvae are encouraged to clarify the composition, function and morphogenesis of transparent, spherical bodies and ciliated invaginations in the anterior part of the head. Such investigations may help to better understand the nature of photoreceptive structures and nuchal organs in Sipuncula, and also contribute to phylogenetic hypotheses regarding relationships of the Sipuncula and Annelida.     

Pigmented eyes,photoreceptor‐like sense organs and central nervous system in the polychaete Scoloplos armiger (Orbiniidae,Annelida) and their phylogenetic importance

The phylogenetic position of Orbiniidae within Annelida is unresolved. Conflicting hypotheses place them either in a basal taxon Scolecida, close to Spionida, or in a basal position in Aciculata. Because Aciculata have a specific type of eye, the photoreceptive organs in the orbiniid Scoloplos armiger were investigated to test these phylogenetic hypotheses. Two different types of prostomial photoreceptor‐like sense organs were found in juveniles and one additional in subadults. In juveniles there are four ciliary photoreceptor‐like phaosomes with unbranched cilia and two pigmented eyes. The paired pigmented eyes lie beside the brain above the circumoesophageal connectives. Each consists of one pigmented cell, one unpigmented supportive cell and three everse rhabdomeric sensory cells with vestigial cilia. During development the number of phaosomes increases considerably and numerous unpigmented sense organs appear consisting of one rhabdomeric photoreceptor cell and one supportive cell. The development and morphology of the pigmented eyes of S. armiger suggest that they represent miniaturized eyes of the phyllodocidan type of adult eye rather than persisting larval eyes resulting in small inverse eyes typical of Scolecida. Moreover, the structure of the brain indicates a loss of the palps. Hence, a closer relationship of Orbiniidae to Phyllodocida is indicated. Due to a still extensive lack of ultrastructural data among polychaetes this conclusion cannot be corroborated by considering the structure of the unpigmented ciliary and rhabdomeric photoreceptor‐like sense organs. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Ultrastructure of phaosomous photoreceptors in Stylaria lacustris (Naididae, ‘Oligochaeta’, Clitellata) and their importance for the position of the Clitellata in the phylogenetic system of the Annelida

Many species of Naididae possess a pair of pigmented eyes. Within Clitellata, eyes are generally present in Hirudinea, whereas Naididae are the only oligochaete taxon having these sense organs. The eyes of Naididae are epidermal structures and consist of a multicellular pigment cup in which a single row of five to six photoreceptor cells is embedded. The sensory cells are typical phaosomes: the photoreceptive structures (microvilli) project into a cavity formed by the sensory cell itself. In Stylaria lacustris this cavity opens to the exterior, clearly documenting that it represents an invagination of the apical cell membrane. The density of sensory microvilli is comparatively low and a central vitreous body is lacking. Similar phaosomous photoreceptors, not associated with either pigmented or unpigmented supporting cells, occur in the epidermis of the anterior end. These photoreceptors correspond to those found in other Clitellata, confirming that phaosomes are the only known type of photoreceptor cell occurring in this taxon. As a result of their simple structure they have been regarded as plesiomorphic for Annelida. However, an out‐group comparison with eyes and photoreceptors occurring in polychaetes and other spiralians reveals that they, in fact, are a rather specialized type of photoreceptor. Despite the simple structure, they most likely represent an autapomorphy of Clitellata. It follows that in all probability, these phaosomes are a secondarily evolved type of photoreceptor, which arose within the oligochaete clade after the primary photoreceptors present in the out‐groups had been lost. This loss might have occurred during evolution of a burrowing life style within the sediment and subsequent invasion of the terrestrial environment.     

Proacrosome and acrosome of the spermatozoon in Acanthobdella peledina (Annelida: Clitellata)

Summary

Proacrosome and acrosome of the primitive leech Acanthobdella peledina are described by means of transmission electron microscopy. The proacrosome develops in early spermatids and has the shape of a pot-bellied urn with an opening towards the nucleus. Its wall is formed by a thin vesicle. In its interior, many sections of tubular structures are visible. This urn is seated atop a short, electron-dense tube. The resultant acrosome is unusually elongated, with a helically coiled acrosomal tube forming its base. Above the tube the thin acrosomal vesicle encloses a central space, within which is the acrosomal rod. The acrosomal structures clearly indicate a sister-group relationship to the Euhirudinea, but do not corroborate the notion of close kinship with the Branchiobdellidae.     

Ultrastructure of pigmented adult eyes in errant polychaetes (Annelida): implications for annelid evolution

The evolution of photoreceptor cells and eyes in Metazoa is far from being resolved, although recent developmental and structural studies have provided strong evidence for a common origin of photoreceptor cells and existence of sister cell types already in early metazoans. These sister cell types are ciliary and rhabdomeric photoreceptor cells, depending on which part of each cell is involved in photoreception proper. However, a crucial point in eye evolution is how the enormous structural diversity of photoreceptor cells and visual systems developed, given the general molecular conservation of the photoreceptor cells. One example of this diversity can be observed in Annelida. Within the polychaetes the errant forms, taxon Aciculata, constitute the only group possessing true multicellular eyes in the adult stage. Thus far these organs have been investigated only in taxa of Phyllodocida, a subgroup of Aciculata. Data on Eunicida and Amphinomida as well as certain phyllodocidan taxa had been lacking. The ultrastructure of these adult eyes was investigated in various species of errant polychaetes, belonging to Amphinomidae, Eunicidae and Hesionidae, to elucidate whether they provide any phylogenetic clues regarding either the evolution of visual systems in Annelida or lophotrochozoan phylogeny in general. These eyes are composed of numerous supportive pigment cells and rhabdomeric photoreceptor cells and sometimes additional cell types. As a rule the pigment and rhabdomeric cell types form a continuous epithelium in which the two types intermingle. Presence of granules with shading pigment in sensory cells is a common feature but is apparently restricted to a taxon comprising Phyllodocida and Eunicida s. str. Very likely a lens-like structure does not belong to the ground pattern of annelid eyes, despite its presence in Phyllodocida. These lens-like structures are formed by secretions or cellular processes of the pigment cells. In many species the eye cup communicates with the exterior via a small cuticularized canal. This canal is interpreted as a rudiment due to the mode of formation in the epidermis. With respect to current phylogenetic hypotheses, these multicellular eyes have either been developed in the stem species of a taxon Aciculata nested within the polychaetes or have been evolved in the stem lineage of Annelida. Similarities to gastropod eyes are interpreted as convergent and not as indication of common origin. Except for the photoreceptor cells proper, the structure of the adult eyes in polychaetes most likely does not help to resolve lophotrochozoan phylogeny.     

Immunohistochemical (cLSM) and ultrastructural analysis of the central nervous system and sense organs in Aeolosoma hemprichi (Annelida, Aeolosomatidae)

The Aeolosomatidae are very small limnetic or terrestrial annelids of apparently simple organisation and uncertain phylogenetic position. They have been placed either at the base of the Clitellata, as a highly derived taxon within the Clitellata closely related to the Naididae, or as their sister group within the „Polychaeta”. A combined immunohistochemical (cLSM) and ultrastructural investigation of the central nervous system and the sense organs in Aeolosoma hemprichi was undertaken to look for characters which might support one of these theories. The position of the brain within the prostomium and the organisation of the ventral nerve cord, with its intraepithelial paired longitudinal nerves lying far apart from each other and the presence of a median longitudinal nerve, are atypical for the Clitellata and clearly differ from the situation found in Naididae. Moreover, the circumoesophageal connectives are bifurcated and enter the brain as dorsal and ventral roots; this arrangement is unknown in Clitellata, in which these connectives are unbranched. An ultrastructural analysis of the ciliated pits located laterally in the furrow between prostomium and peristomium in A. hemprichi and other Aeolosomatidae show that they are in fact nuchal organs. Such presumed chemosensory organs are typical of „Polychaeta” and absent in all Clitellata. Two pairs of ciliary sense organs are present in the prostomium in front of the brain of A. hemprichi. Although similarly organised sensory structures occur in many species of the Clitellata, they differ in position and certain ultrastructural features and are known from other Annelida as well. These results clearly support the exclusion of the Aeolosomatidae from the Clitellata and do not provide any evidence for a sister-group relationship between these two taxa. Accepted: 8 February 2000     

Early development of metanephridia in the caudal budding zone of a clitellate annelid, Dero digitata (Naidida): an electron-microscopical study

Ultrastructural analysis has revealed that metanephridia in Dero digitata arise from three nephroblast cells in the frontal epithelium of a septum suggesting its mesodermal origin. Each cell has a fixed developmental destination, one nephroblast cell produces the entire canal part and two cells give rise to the nephrostome. The nephroblast cell nearest to the body wall enlarges and proliferates a first set of canal cells, then one of the two proximally adjacent nephroblast cells differentiates into the envelope of the nephrostome generating the marginal cilia of the opening (mantle cell) and the second one transforms into the anteriormost cell of the funnel, producing a flame of cilia that beats into the canal lumen (flame cell). Thereafter, new canal cells appear, mainly by mitosis of the first cell, enlarging the body of the nephridium whose further differentiation was not analysed. Comparison with other clitellate species suggests a mantle cell (or some marginal cells) and a flame cell (or a central cell) to be special characters of the metanephridium in the stem species of the Clitellata and that, compared to many polychaete species, its early development assumes a special course by a precocious determination and arrangement of nephroblast cells, which, in both groups, probably originate from an identical mesodermal stem cell. Results further indicate that the nonclitellate Aeolosomatidae, by virtue of corresponding nephrostomata, are possibly closer related to the Clitellata.     

Sipunculid‐like ocellar tubes in a polychaete,Fauveliopsis cf. adriatica (Annelida,Fauveliopsidae): implications for eye evolution

Abstract. A retractable head region somewhat resembling the introvert of sipunculans is a characteristic feature of members of the annelid taxon Fauveliopsidae. The morphology of fauvelopsids is not well known, and additional data might help to resolve their relationships with other annelids and sipunculans. Ultrastructural investigations of the anterior end of adults of Fauveliopsis cf. adriatica revealed peculiar brain and sensory structures. From the neuropil of the brain, two pairs of lobes mainly composed of neuronal somata extend posteriorly into the peristomium and the following segment. The nuchal organs are embedded in the median pair of lobes, as are additional photoreceptor‐like sensory structures, the ocellar tubes, which are found at the bases of epidermal follicles that extend deeply into the brain. The retractor muscles of the prostomium are attached to the apices of these follicles, which are lined by tendon and supportive cells. The lumen of each follicle is completely filled with cuticular material that forms a rod. Monociliary sensory cells are present all along the length of each follicle; their cilia extend into the cuticle, and are oriented parallel to the longitudinal axis of the tube. Basally, each follicle forms an ovoid extension that is devoid of cuticular material and densely filled with numerous sensory processes—microvilli and cilia—of bipolar sensory cells. The terminal end of the 40‐μm‐deep follicle is formed by two conspicuous cells that contain numerous densely packed vesicles that resemble pigment granules. The ocellar tubes of fauveliopsids are strikingly similar to the ocular tubes of sipunculids. These similarities may reflect common ancestry or may represent convergent evolution; both alternatives are partially supported by previous morphological and molecular studies.     

Ultrastructure of the nuchal organs in the polychaete Platynereis dumerilii (Annelida,Nereididae)

Abstract. We examined the nuchal organs of adults of the nereidid polychaete Platynereis dumerilii by means of scanning and transmission electron microscopy. The most prominent features of the nuchal organs are paired ciliary bands located dorsolaterally at the posterior margin of the prostomium. They are composed of primary sensory cells and multiciliated supporting cells, both covered by a thin cuticle. The supporting cells have motile cilia that penetrate the cuticle and are responsible for the movement of water. Subapically, they have a narrowed neck region; the spaces between the neck regions of these supporting cells comprise the olfactory chamber. The dendrites of the sensory cells give rise to a single modified cilium that crosses the olfactory chamber; numerous thin microvillus-like processes, presumably extending from the sensory cells, also traverse the olfactory chamber. At the periphery of the ciliated epithelium runs a large nervous process between the ciliated supporting cells. It consists of smaller bundles of sensory dendrites that unite to form the nuchal nerve, which leaves the ciliated epithelium basally and runs toward the posterior part of the brain, where the perikarya of the sensory cells are located in clusters. The ciliated epithelium of the nuchal organs is surrounded by non-ciliated, peripheral epidermal cells. Those immediately adjacent to the ciliated supporting cells have a granular cuticle; those further away have a smooth cuticle. The nuchal organs of epitokous individuals of P. dumerilii are similar to those described previously in other species of polychaetes and are a useful model for understanding the development of nuchal organs in polychaetes.     

Anatomy of the serotonergic nervous system of an entoproct creeping-type larva and its phylogenetic implications

Abstract. Although the internal phyletic relationships of Spiralia (and Lophotrochozoa) remain unresolved, recent progress has been made due to molecular phylogenetic analyses as well as developmental studies of crucial taxa such as Mollusca, Sipuncula, or Annelida. Despite this progress, the phylogenetic position of a number of phyla, such as Entoprocta, remains problematic, mainly due to their unique morphology, their aberrant mode of development, and their exclusion in most large-scale phylogenetic analyses. In order to extend the morphological dataset of this enigmatic taxon, we herein describe the anatomy of the serotonergic nervous system of the creeping-type larva of Loxosomella murmanica . The apical organ is very complex and comprises six to eight centrally positioned flask cells and eight bipolar peripheral cells. In addition, a prototroch nerve ring, an anterior nerve loop, a paired buccal nerve, and an oral nerve ring are found. Moreover, the larva of L. murmanica has one pair of pedal and one pair of lateral longitudinal nerve cords and thus expresses a tetraneurous condition. Several paired serotonergic perikarya, which form contact with the pedal nerve cords but not with the lateral ones, are found along the anterior–posterior axis. The combination of a complex larval serotonergic apical organ and (adult) tetraneury, comprising one pair of ventral and one pair of more dorsally situated lateral longitudinal nerve cords without ganglia, has so far only been reported for basal molluscs and may be diagnostic for a mollusc–entoproct clade. In addition, the larva of Loxosomella expresses a mosaic of certain neural features that are also found in other larval or adult Spiralia, e.g., a prototroch nerve ring, an anterior nerve loop, and a buccal nervous system.     

Development of the nervous system in hatchlings of Spadella cephaloptera (Chaetognatha), and implications for nervous system evolution in Bilateria

Chaetognaths (arrow worms) play an important role as predators in planktonic food webs. Their phylogenetic position is unresolved, and among the numerous hypotheses, affinities to both protostomes and deuterostomes have been suggested. Many aspects of their life history, including ontogenesis, are poorly understood and, though some aspects of their embryonic and postembryonic development have been described, knowledge of early neural development is still limited. This study sets out to provide new insights into neurogenesis of newly hatched Spadella cephaloptera and their development during the following days, with attention to the two main nervous centers, the brain and the ventral nerve center. These were examined with immunohistological methods and confocal laser-scan microscopic analysis, using antibodies against tubulin, FMRFamide, and synapsin to trace the emergence of neuropils and the establishment of specific peptidergic subsystems. At hatching, the neuronal architecture of the ventral nerve center is already well established, whereas the brain and the associated vestibular ganglia are still rudimentary. The development of the brain proceeds rapidly over the next 6 days to a state that resembles the adult pattern. These data are discussed in relation to the larval life style and behaviors such as feeding. In addition, we compare the larval chaetognath nervous system and that of other bilaterian taxa in order to extract information with phylogenetic value. We conclude that larval neurogenesis in chaetognaths does not suggest an especially close relationship to either deuterostomes or protostomes, but instead displays many apomorphic features.     

Delimitation and phylogeny of Aletris (Nartheciaceae) with implications for perianth evolution

Aletris,containing approximately 21 species,is the largest genus in Nartheciaceae,and is disjunctively distributed in eastern Asia and eastern North America.Its delimitation has been controversial beca...     

Expression and evolution studies of ets genes in a primitive coelomate,the polychaete annelid,Hediste (Nereis) diversicolor

The Ets family includes numerous proteins with a highly conserved DNA-binding domain of 85 amino acids named the ETS domain. Phylogenetic analyses from ETS domains revealed that this family could be divided into 13 groups, among them are ETS and ERG. The ets genes are present in the Metazoan kingdom and we have previously characterized the Nd ets and Nd erg genes in the polychaete annelid Hediste diversicolor. Here, we isolated a fragment encoding the ETS domain from Nd Ets, by genomic library screening. By Northern blot analysis, we showed that this gene was transcribed as one major mRNA of 2.6 kb and one minor mRNA of 3.2 kb. By in situ hybridization, we observed that Nd ets was expressed in the intestine and oocytes and that Nd erg was expressed in cellular clumps present in the coelomic cavity, in an area of proliferating cells situated between the last metamere and the pygidium. Finally, we showed that Nd erg shared the expression pattern of Nd ets in oocytes. Molecular modeling studies have revealed that the spatial structure of ETS domain of Nd Ets and Nd Erg was conserved, in comparison to the murine Ets-1 and human Fli-1 proteins, respectively.