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.     

Ultrastructure of the nuchal organ and cerebral organ in Onchnesoma squamatum (Sipuncula, Phascolionidae)

 The ultrastructure of the nuchal organ and cerebral organ is described for the first time in a species of the Sipuncula, Onchnesoma squamatum. The nuchal organ is an unpaired structure lying outside and dorsal to the tentacular crown; furrows give the organ a paired appearance. The cerebral organ is an unciliated pad anterior to the nuchal organ. The nuchal organ consists of ciliated supporting cells, non-ciliated supporting cells and bipolar primary sensory cells. The cerebral organ is composed of unciliated supporting cells and numerous bipolar sensory cells. This clearly favours the hypothesis that this structure has a sensory function in adults rather than being a vestige of a larval organ. The sensory cells are similar in both organs and exhibit features indicative of chemoreception. Since the density of the sensory cells is low in the nuchal organ, an exclusively sensory function is questioned. There is some evidence that the two organs represent a functional unit. The present findings do not support the view that the nuchal organs of Sipuncula and ”Polychaeta” are homologous, but instead suggest that they are convergent structures. Accepted: 18 September 1996     

Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology

An ontogenetic analysis of the olfactory organ and the number and distribution of internal taste buds was carried out in two neon gobies (Elacatinus lori and Elacatinus colini) with the goal of revealing morphological trends that might inform an understanding of the roles of olfaction and taste in larval orientation behaviour. The pattern of development of the olfactory organ is unremarkable and enclosure of the olfactory epithelium occurs concurrently with metamorphosis and settlement in both species. Like other gobies, juvenile and adult E. lori and E. colini lack complex olfactory lamellae, and lack the accessory nasal sacs present in some adult gobies that could facilitate active olfactory ventilation (i.e., sniffing). A small number of internal taste buds are present at hatch with most found in the caudal region of the buccal cavity (on gill arches, roof of buccal cavity). As taste bud number increases, they demonstrate an anterior spread to the lips, buccal valves and tongue (i.e., tissue covering the basihyal). In the absence of an active ventilatory mechanism for the olfactory organs, the water that moves through the buccal cavity with cyclic gill ventilation may provide chemical cues allowing the internal taste buds to play a role in chemical-mediated orientation and reef-seeking behavior in pelagic larval fishes.     

Larval apical sensory organ in a neritimorph gastropod,an ancient gastropod lineage with feeding larvae

The Neritimorpha is an ancient clade of gastropods that may have acquired larval planktotrophy independently of the evolution of this developmental mode in other gastropods (caenogastropods and heterobranchs). Neritimorphs are therefore centrally important to questions about larval evolution within the Gastropoda, but there is very little information about developmental morphology through metamorphosis for this group. We used immunolabeling (antibodies binding to acetylated α-tubulin and serotonin) and serial ultrathin sections for transmission electron microscopy to characterize the apical sensory organ in planktotrophic larvae of a marine neritimorph. The apical sensory organ of gastropod larvae is a highly conserved multicellular sensory structure that includes an apical ganglion and often an associated ciliary structure. Surprisingly, the apical ganglion of Nerita melanotragus (Smith, 1884) does not have typical ampullary neurons, a type of sensory neuron consisting of a cilia filled inpocketing that has been described in all other major gastropod groups. N. melanotragus has cilia-filled pockets embedded within the apical ganglion, but these so-called “sensory cups” are cassettes of multiple cells: one supporting cell and up to three multiciliated sensory cells. We suggest that an internalized pocket that is filled with cilia and open to the exterior via a narrow pore may be essential architectural features for whatever sensory cues are detected by ampullary neurons and sensory cups; however, morphogenesis of these features at the cellular level has undergone evolutionary change. We also note a correlation between the number of sensory elements consisting of cilia-filled pockets within the larval apical sensory organ of gastropods and morphological complexity of the velum or length of the trochal ciliary bands.     

Fine structure of the doliolaria larva of the feather star Florometra serratissima (Echinodermata: Crinoidea), with special emphasis on the nervous system

The epidermis of the doliolaria larva of the Florometra serratissima is differentiated into distinct structures including an apical organ, adhesive pit, ganglion, ciliary bands, nerve plexus, and vestibular invagination. All these structures possess unique cell-types, suggesting that they are functionally specialized in the larva, except the vestibular invagination that becomes the postmetamorphic stomodeum. The epidermis also contains yellow cells, amoeboid-like cells, and secretory cells. The enteric sac, hydrocoel, axocoel, and somatocoels have differentiated but are probably not functional in the doliolaria stage. Mesenchymal cells, around the enteric sac and coeloms, appear to be actively secreting the endoskeleton and connective tissue fibers. The nervous system is composed of a nerve plexus, ganglion, and sensory receptor cells in the apical organ. The apical organ is a larval specialization of the anterior end; the ganglion is located in the base of the epidermis at the anterior dorsal end of the larva. The nerve plexus underlies most of the epidermis, although it is more prominent in the anterior region. Here, processes from sensory receptor cells of the apical organ, as well as those from nerve cells, contribute to the plexus. These processes contain one or a combination of organelles including vesicles, vacuoles, microtubules, and mitochondria. The configuration of glyoxylic acid-induced fluorescence, revealing catecholamine activity, correlates to the apical organ, nerve cells, and nerve plexus. Morphological evidence suggests that the nervous system may function in initiation and control of settlement, attachment, and metamorphosis. The crinoid larval nervous system is discussed and compared to that found in other larval echinoderms.     

Role of proneural genes in the formation of the larval olfactory organ of <Emphasis Type="Italic">Drosophila</Emphasis>

In this paper, we address the role of proneural genes in the formation of the dorsal organ in the Drosophila larva. This organ is an intricate compound comprising the multineuronal dome—the exclusive larval olfactory organ—and a number of mostly gustatory sensilla. We first determine the numbers of neurons and of the different types of accessory cells in the dorsal organ. From these data, we conclude that the dorsal organ derives from 14 sensory organ precursor cells. Seven of them appear to give rise to the dome, which therefore may be composed of seven fused sensilla, whereas the other precursors produce the remaining sensilla of the dorsal organ. By a loss-of-function approach, we then analyze the role of atonal, amos, and the achaete-scute complex (AS-C), which in the adult are the exclusive proneural genes required for chemosensory organ specification. We show that atonal and amos are necessary and sufficient in a complementary way for four and three of the sensory organ precursors of the dome, respectively. AS-C, on the other hand, is implicated in specifying the non-olfactory sensilla, partially in cooperation with atonal and/or amos. Similar links for these proneural genes with olfactory and gustatory function have been established in the adult fly. However, such conserved gene function is not trivial, given that adult and larval chemosensory organs are anatomically very different and that the development of adult olfactory sensilla involves cell recruitment, which is unlikely to play a role in dome formation. N. Grillenzoni and V. de Vaux contributed equally to this work.     

Organization of the vomeronasal organ in a plethodontid salamander

Salamanders in the family Plethodontidae show a unique behavior (nose-tapping) and have unique structures (nasolabial grooves) that may be used specifically to convey chemicals to the vomeronasal organ. The nasal structure of Plethodon cinereus was studied to determine if there is enhanced development of the vomeronasal organ compared with other salamander families that would correlate with use of these unique features. The vomeronasal organ in salamanders is found in a ventrolateral diverticulum of each main olfactory organ. P. cinereus has a more anteriorly placed vomeronasal organ within the diverticulum, and the posterior limit of each nasolabial groove is adjacent to the anterior limit of the vomeronasal organs. This suggests that the grooves deliver chemicals preferentially to the vomeronasal organs instead of to the main olfactory organs. In addition, the vomeronasal sensory epithelium is thickest anteriorly and is at its thinnest at about the level corresponding to the location of the vomeronasal organ in other salamander families. These adaptations suggest a specific mechanism of odorant delivery to the vomeronasal organ in plethodontid salamanders not found in other salamander families.     

Developmental constraint of insect audition

Background

Insect ears contain very different numbers of sensory cells, from only one sensory cell in some moths to thousands of sensory cells, e.g. in cicadas. These differences still await functional explanation and especially the large numbers in cicadas remain puzzling. Insects of the different orders have distinct developmental sequences for the generation of auditory organs. These sensory cells might have different functions depending on the developmental stages. Here we propose that constraints arising during development are also important for the design of insect ears and might influence cell numbers of the adults.

Presentation of the hypothesis

We propose that the functional requirements of the subadult stages determine the adult complement of sensory units in the auditory system of cicadas. The hypothetical larval sensory organ should function as a vibration receiver, representing a functional caenogenesis.

Testing the hypothesis

Experiments at different levels have to be designed to test the hypothesis. Firstly, the neuroanatomy of the larval sense organ should be analyzed to detail. Secondly, the function should be unraveled neurophysiologically and behaviorally. Thirdly, the persistence of the sensory cells and the rebuilding of the sensory organ to the adult should be investigated.

Implications of the hypothesis

Usually, the evolution of insect ears is viewed with respect to physiological and neuronal mechanisms of sound perception. This view should be extended to the development of sense organs. Functional requirements during postembryonic development may act as constraints for the evolution of adult organs, as exemplified with the auditory system of cicadas.     

Metamorphosis of <Emphasis Type="Italic">Hydractinia echinata</Emphasis>—natural versus artificial induction and developmental plasticity

Many marine invertebrates reproduce through a larval stage. The settlement and metamorphosis of most of the species are synchronised and induced by environmental organisms, mainly bacteria. The hydrozoan Hydractinia echinata has become a model organism for metamorphosis of marine invertebrates. In this species, bacteria, e.g. Pseudoalteromonas espejiana, are the natural inducers of metamorphosis. Like in other species of marine invertebrates, metamorphosis can be induced artificially by monovalent cations, e.g. Cs⁺. In this study, we present systematic data that metamorphosis—with both inducing compounds, the natural one from bacteria and the artificial one Cs⁺—are indeed similar with respect to (a) the morphological progression, (b) the localisation of the primary induction signal in the larva, (c) the pattern of apoptotic cells occurring during the initial 10 h of metamorphosis and (d) the disappearance of RFamide-dependent immunocytochemical signals in sensory neurons during this process. However, a difference occurs during the development of the anterior end, insofar as apoptotic cells and settlement appear earlier in planulae induced with bacteria. Thus, basically, Cs⁺ may be used as an artificial inducer, mimicking the natural process. However, differences in the appearance of apoptotic cells and in settlement raise the question of how enormous developmental plasticity in hydrozoans actually can be, and how this is related to the absence of malignant devolution in hydrozoans.     

Ontogenetic changes in responses to settlement cues by Anemonefish

Population connectivity for most marine species is dictated by dispersal during the pelagic larval stage. Although reef fish larvae are known to display behavioral adaptations that influence settlement site selection, little is known about the development of behavioral preferences throughout the larval phase. Whether larvae are attracted to the same sensory cues throughout their larval phase, or exhibit distinct ontogenetic shifts in sensory preference is unknown. Here, we demonstrate an ontogenetic shift in olfactory cue preferences for two species of anemonefish, a process that could aid in understanding both patterns of dispersal and settlement. Aquarium-bred na?ve Amphiprion percula and A. melanopus larvae were tested for olfactory preference of relevant reef-associated chemical cues throughout the 11-day pelagic larval stage. Age posthatching had a significant effect on the preference for olfactory cues from host anemones and live corals for both species. Preferences of olfactory cues from tropical plants of A. percula, increased by approximately ninefold between hatching and settlement, with A. percula larvae showing a fivefold increase in preference for the olfactory cue produced by the grass species. Larval age had no effect on the olfactory preference for untreated seawater over the swamp-based tree Melaleuca nervosa, which was always avoided compared with blank seawater. These results indicate that reef fish larvae are capable of utilizing olfactory cues early in the larval stage and may be predisposed to disperse away from reefs, with innate olfactory preferences drawing newly hatched larvae into the pelagic environment. Toward the end of the larval phase, larvae become attracted to the olfactory cues of appropriate habitats, which may assist them in identification of and navigation toward suitable settlement sites.     

Is the Schwabe Organ a Retained Larval Eye? Anatomical and Behavioural Studies of a Novel Sense Organ in Adult Leptochiton asellus (Mollusca,Polyplacophora) Indicate Links to Larval Photoreceptors

The discovery of a sensory organ, the Schwabe organ, was recently reported as a unifying feature of chitons in the order Lepidopleurida. It is a patch of pigmented tissue located on the roof of the pallial cavity, beneath the velum on either side of the mouth. The epithelium is densely innervated and contains two types of potential sensory cells. As the function of the Schwabe organ remains unknown, we have taken a cross-disciplinary approach, using anatomical, histological and behavioural techniques to understand it. In general, the pigmentation that characterises this sensory structure gradually fades after death; however, one particular concentrated pigment dot persists. This dot is positionally homologous to the larval eye in chiton trochophores, found in the same neuroanatomical location, and furthermore the metamorphic migration of the larval eye is ventral in species known to possess Schwabe organs. Here we report the presence of a discrete subsurface epithelial structure in the region of the Schwabe organ in Leptochiton asellus that histologically resembles the chiton larval eye. Behavioural experiments demonstrate that Leptochiton asellus with intact Schwabe organs actively avoid an upwelling light source, while Leptochiton asellus with surgically ablated Schwabe organs and a control species lacking the organ (members of the other extant order, Chitonida) do not (Kruskal-Wallis, H = 24.82, df = 3, p < 0.0001). We propose that the Schwabe organ represents the adult expression of the chiton larval eye, being retained and elaborated in adult lepidopleurans.     

Development and organization of the Drosophila olfactory system: An analysis using enhancer traps

Drosophila uses different olfactory organs at different developmental stages. The larval and adult olfactory organs are morphologically dissimilar and have different developmental origins: the antenno-maxillary complex (AMC), which houses the larval olfactory organ, is histolyzed during metamorphosis; the third antennal segment—the principal adult olfactory organ—derives from an imaginal disc. A screen for genes expressed in both larval and adult olfactory organs, but in relatively few other tissues, has been carried out. Seven enhancer trap lines showing reporter gene expression in both the larval AMC and in certain subsets of the adult antenna are described. The antennal staining pattern of one line shows a striking change over the first few days of adult life, with a time course comparable to that of the development of sexual maturity. A pronounced sexual dimorphism in antennal staining pattern is seen in another line. Some staining patterns resemble the patterns of certain classes of antennal sensilla; others show expression restricted to only a small number of cells. Some lines also show expression associated with other chemosensory organs at either the larval or adult stage, including the maxillary palps, labellum, and anterior wing margin. One line, which also shows staining in the male reproductive tract, is male sterile. The significance of these results is considered in terms of (1) the molecular organization of the olfactory system; (2) the recruitment of olfactory genes for use in two developmental contexts; (3) the sharing of genes among different sensory modalities; (4) the role of olfaction in sexual behavior; and (5) posteclosional changes in the olfactory system. © 1992 John Wiley & Sons, Inc.     

Precursor structures and evolution of tympanal organs in Lepidoptera (Insecta, Pterygota)

 The patterns of scolopal organs and their innervation were studied by the methylene blue method in larvae, pupae and adults of an Yponomeuta species (Yponomeutidae) and of tympanate adult representatives of the Noctuoidea, Geometridae, Drepanidae and Pyraloidea. The studies were focused mainly on the mesothorax, the metathorax and some anterior abdominal segments. In the abdominal tympanal organs of Geometridae, Drepanidae and Pyraloidea, the auditory scolopidia are homologous with the lateral scolopal organs of the first abdominal segment; however, the hearing organs as such evolved independently in the three taxa. The studies confirm that the tympanal organ in the Noctuoidea is derived from the caudal dorsolateral region of the metathorax including its dorsal scolopal organ and the B-cell. The adult scolopal organs are present already in the larvae and are maintained nearly unchanged during metamorphosis to the adult. Only in the Noctuoidea are the three sensory cells of the larval scolopal organs, which become part of the tympanal organs, reduced to one (in Notodontidae) or two (in other Noctuoidea) during metamorphosis. A hypothetical scenario of the evolution of the tympanal organs is outlined. Accepted: 12 March 1997     

Development of the olfactory and vomeronasal organs in Discoglossus pictus (Discoglossidae,Anura)

Using histological techniques and computer‐aided three‐dimensional reconstructions of histological serial sections, we studied the development of the olfactory and vomeronasal organs in the discoglossid frog Discoglossus pictus. The olfactory epithelium in larval D. pictus represents one continuous unit of tissue not divided into two separate portions. However, a small pouch of olfactory epithelium (the “ventromedial diverticulum”) is embedded into the roof of the buccal cavity, anteromedial to the internal naris. The lateral appendix is present in D. pictus through the entire larval period and disappears during the onset of metamorphosis. The disappearance of the lateral appendix at this time suggests that it is a typical larval organ related to aquatic life. The vomeronasal organ develops during hindlimb development, which is comparatively late for anurans. The development of the vomeronasal organ in D. pictus follows the same general developmental pattern recognized for neobatrachians. As with most anurans, the vomeronasal glands appear later than the vomeronasal organ. After metamorphosis, the olfactory organ of adult D. pictus is composed of a series of three interconnected chambers: the cavum principale, cavum medium, and cavum inferius. We suggest that the ventromedial diverticulum at the anterior border of the internal naris of larval D. pictus might be homologous with the ventral olfactory epithelium of bufonids and with the similar diverticulum of Alytes. J. Morphol. 2013. © 2012 Wiley Periodicals, Inc.     

Establishing character correspondence for sensory organ traits in flies: sensory organ development provides insight for reconstructing character evolution

In Diptera and in other insects sensory organ patterns play an important role in the construction of phylogenies based on morphological characters. In this paper I explore the developmental basis for sensory organ pattern transformations between and within species. Knowledge of the properties of sensory organ development provides a foundation to judge the correspondence relationships between sensory organs. This is used to explore what components of notum bristle patterns are equivalent across the Schizophora. By investigating patterning processes in leg development, and their conservation across holometabolous insects, I show ways of relating specialised leg vestiture between species. Sensory organ patterns on the legs are diversified under homeotic gene control, potentially adding patterns of homeotic variation between legs to the list of informative traits for phylogenetic analysis. Correspondence relationships between wing and haltere sensory organ fields are resolved by exploring homeotic gene action in detail.     

A new sensory organ in “primitive” molluscs (Polyplacophora: Lepidopleurida), and its context in the nervous system of chitons

Introduction

Chitons (Polyplacophora) are molluscs considered to have a simple nervous system without cephalisation. The position of the class within Mollusca is the topic of extensive debate and neuroanatomical characters can provide new sources of phylogenetic data as well as insights into the fundamental biology of the organisms. We report a new discrete anterior sensory structure in chitons, occurring throughout Lepidopleurida, the order of living chitons that retains plesiomorphic characteristics.

Results

The novel “Schwabe organ” is clearly visible on living animals as a pair of streaks of brown or purplish pigment on the roof of the pallial cavity, lateral to or partly covered by the mouth lappets. We describe the histology and ultrastructure of the anterior nervous system, including the Schwabe organ, in two lepidopleuran chitons using light and electron microscopy. The oesophageal nerve ring is greatly enlarged and displays ganglionic structure, with the neuropil surrounded by neural somata. The Schwabe organ is innervated by the lateral nerve cord, and dense bundles of nerve fibres running through the Schwabe organ epithelium are frequently surrounded by the pigment granules which characterise the organ. Basal cells projecting to the epithelial surface and cells bearing a large number of ciliary structures may be indicative of sensory function. The Schwabe organ is present in all genera within Lepidopleurida (and absent throughout Chitonida) and represents a novel anatomical synapomorphy of the clade.

Conclusions

The Schwabe organ is a pigmented sensory organ, found on the ventral surface of deep-sea and shallow water chitons; although its anatomy is well understood, its function remains unknown. The anterior commissure of the chiton oesophagial nerve ring can be considered a brain. Our thorough review of the chiton central nervous system, and particularly the sensory organs of the pallial cavity, provides a context to interpret neuroanatomical homology and assess this new sense organ.