Evolution of monogenean parasites across vertebrate hosts illuminated by the phylogenetic position of Euzetrema Combes, 1965 within the Monopisthocotylea

The Monogenea, which is divided into two clades, namely the Monopisthocotylea and Polyopisthocotylea, is a highly diversified group of platyhelminth parasites that infest mainly actinopterygian and chondrichthyan fishes but also, to a lesser extent, freshwater sarcopterygian hosts. Euzetrema knoepffleri Combes, 1965 (Monogenea: Iagotrematidae), which is specific to the salamander Euproctus montanus Savi, 1838 is among the rare monopisthocotylean parasites infesting tetrapod hosts. We sequenced the complete 18S rRNA gene of this parasite to infer its phylogenetic position within the Monopisthocotylea. Our results provide a new insight for coevolutionary scenarios between monopisthocotyleans and gnathostomatan hosts. Indeed, the basal position of E. knoepffleri within a subgroup of the Monopisthocotylea which comprises two clusters that both include parasites of the Actinopterygii and Chondrichthyes, suggests a very old association between the Iagotrematidae and tetrapods. Furthermore, if we take into account a recent view of Gnathostomata evolution where bony and cartilaginous fishes are regarded as a monophyletic group, it could be argued that the Iagotrematidae arose very early, during the fish–tetrapod transition, as did the Polystomatidae, the only monogenean family of the Polyopisthocotylea that infests sarcopterygian hosts.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 727–734.     

The mode of hatching of the monogenean Entobdella soleae, a skin parasite of the common sole (Solea solea).

Observations have been made on the hatching behaviour of the larva of the monogenean Entobdella soleae and on the effects of various enzymes on the opercular cement of the egg. These observations indicate that hatching is brought about by a proteolytic hatching fluid which is produced by two pairs of ventral head glands and spread over the inner surface of the opercular joint by rotation of the larva about its longitudinal axis. After hatching there is no trace of the ventral head glands. Similar glands are present before hatching in the oncomiracidium of E. hippoglossi.     

Euzetrema caucasica sp. n. (Monogenea, Polyopisthocotylidea), a parasite of the Caucasian salamander]

A new species of monogeneans, Euzetrema caucasica sp. n., from the urinary bladder of Mertensiella caucasica (Waga, 1876) is described. The new species differs from E. knoepffleri Combes, 1965 by greater sizes of the disc, median and marginal hooks and anterior suckers. Certain suggestions are made on the biology and life cycle of Euzetrema.     

Structure of photoreceptors ofpolystoma integerrimum (platyhelminths,monogenea)

Summary The structure of the eyespots of the free-swimming larva ofPolystoma integerrimum (Monogenea, Polystomatidae) was studied by electron microscopy. Each eyespot is rhabdomeric in type, with one cup-shaped supportive cell and one sensory cell. The supportive cell is characterized by concentric rows of platelets, separated by 120 nm. This entirely new structure in a platyhelminth acts like a concave mirror of a telescope in concentrating the light. Moreover, at each interface of lamellae of platelets, light is amplified. InPolystoma, the light concentration occurs by reflection whereas it occurs by refraction in all other platyhelminths studied up to now. Among the monogenean Trematodes, all the Polystomatidae appear to present this reflecting system.     

Entobdella soleae--pointers to the future

The biology of the monogenean skin parasite Entobdella soleae and its relationship with its host, the common sole (Solea solea), are probably better known than those of any other monogeneans. The author describes his early involvement with this parasite and the special features of parasite and host that make this relationship so suitable for parasitological studies. Aspects of the biology of E. soleae that have been investigated are briefly mentioned, but most of the paper is concerned with areas of the parasite's biology that remain a challenge to determine. Unresolved areas are as follows: (1) the identity of the factor (or factors) in host skin mucus that stimulates hatching of the parasite's eggs; (2) whether or not the larvae of the parasite are attracted to their host; (3) the nature of factors controlling the contrasting behaviour of adult parasites on the upper and lower surfaces of the host; (4) how nutrients are supplied to the remote regions of the haptor; (5) whether the host has any control via its immune system over parasite invasion success and survival; (6) how the parasite copes with the migratory habits of some sole populations, assuming that such populations are infested with the parasite. The intimacy of this parasite/host relationship is its most remarkable feature, the reflection of which, not surprisingly, is the greatly restricted host range of the parasite. E. soleae has been reported from only three host species, all highly specialised bottom-dwelling members of Solea. It is all the more surprising that relatives of E. soleae, such as Neobenedenia melleni, retain the ability to parasitise an enormous range of hosts. How this versatility is achieved remains to be seen.     

The rate of development and longevity of the monogenean skin parasite Entobdella soleae

Using soles (Solea solea) infected experimentally with oncomiracidia of the monogenean skin parasite Entobdella soleae, it was found that the parasite begins to assemble eggs at about 85 days post infection and may survive for as long as 6 1/2 months at 12 +/- 1 degrees C. Growth of the anterior hamuli continues throughout life but the growth rate decreases with time. The oldest (largest) parasites recovered from laboratory soles were similar in size to the largest parasites collected in the wild.     

The larval ocelli of Golfingia misakiana (Sipuncula, Golfingiidae) and of a pelagosphera of another unidentified species

 The inverse cerebral ocelli of the pelagosphera larva of Golfingia misakiana and of another unidentified larva are composed of two or three sensory cells and one supportive pigmented cell. The sensory cells bear an array of microvilli as well as a single cilium with poor undulation of its membrane; the photoreceptive organelles are regarded as the rhabdomeric type. A striking feature of these cells is the cores, which extend within the microvilli from the tip into the midregion of the cell. It is suggested that these structures are identical with the submicrovillar cisternae found in the cerebral inverse eyes of larvae of Polychaeta. The findings allow the conclusion that in the pelagosphera of the Sipuncula, contrary to the teleplanic veliger larvae of Gastropoda, a lengthy pelagic cycle is not correlated with the development of a ciliary photoreceptor. Additionally, it is assumed that the pigment cup ocelli in larvae of Sipuncula are homologous with the cerebral inverted pigment cup ocelli of larvae of Polychaeta. Accepted: 19 March 1997     

Ultrastructure of the photoreceptors of Allostoma sp. (Plathelminthes,Prolecithophora)

The four eyes of the prolecithophoran Allostoma sp. are disposed in two pairs in a dorsolateral position at the periphery of the brain and beneath its capsule. They are rhabdomeric pigment-cup ocelli. Each eye in the anterior pair consists of one pigment cell and one receptor cell; each in the posterior pair is made up of a larger, single pigment cell and two photoreceptor cells. A lens in front of the pigment cell's aperture is formed by electron-dense, refractive, finger-like protrusions which arise from unpigmented cytoplasmic extensions of the pigment-cup margin. Degenerative signs are sometimes visible in the lens.     

Fine structure of the eyes of Pseudoceros canadensis (Turbellaria,Polycladida)

Summary The cerebral and epidermal ocelli of the Müller's larva and the cerebral and tentacular eyes of the adult turbellarian Pseudoceros canadensis were studied by electron microscopy. The right cerebral ocellus of the larva consists of one cup-shaped pigmented cell and three sensory cells that bear microvilli. The left cerebral eye of the larva has the above named cells plus a sensory cell with many cilia. Evolutionary significance is attributed to the presence of both ciliary and microvillar photoreceptors in an eye of a flatworm. The one epidermal ocellus of the larva is composed of two cells: a cup-shaped pigmented one bearing flattened cilia, the presumed photoreceptors, and a cell above the cup that adds a few nonciliary lamellae to the stack of ciliary ones from the pigmented cell. The adult eyes contain only microvillar receptors; cilia were not observed.     

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.     

Presumptive photoreceptor structures of the trochophore of Harmothoë imbricata (Polychaeta)

The behaviour of the Harmothoë trochophore changes with age, the larva being phototropic initially and later photonegative.

The trochophore possesses two ocelli midway between the prototroch and the apex in a mid‐lateral position. They appear first at the eighth day of development and grow to be kidney‐shaped structures. There is a pigment cup derived from a single cell that encloses a rhabdomeric type of photoreceptor apparatus that is also derived from a single (or rarely two) cell.

In the late trochophore (14 days old) an organ of different origin and formation but of presumed photoreceptor type begins to develop among nerve cell bodies below the apex of the animal. This structure consists of an array of membranes developed from both cilia and microvilli. The cilia are of 9 + 2 configuration.     

Feinstruktur pigmentierter und unpigmentierter Photoreceptoren bei Proseriata (Plathelminthes)

The fine structure of rhabdomeric photoreceptors of Cirrifera aculeuta, Monocelis fusca and Nematoplana coelogynoporoides is described. The existence of one receptor cell and one pigmented or unpigmented mantle cell is thought to be a basic feature of the Neoophora at least. The existence of a pigment shield formed by many cells is derived, in addition to one receptor and one unpigmented mantle cell, in the eyes of Monocelis fuscu.     

First evidence of unpigmented rhabdomeric photoreceptors in a Microstomum species (Plathelminthes, Macrostomorpha, Microstomidae) and ultrastructure of photoreceptor-like ciliary aggregations

Microstomum spiculifer possesses a pair of intracerebral photoreceptors each consisting of a single rhabdomeric sensory cell and two cup or mantle cells. The mantle cells are devoid of pigment. In addition, four so-called ciliary aggregations, presumed to have a light-sensing function, are present. Each ciliary aggregation represents a specialized cell with an internal cavity filled with axonemes of modified cilia. Rhabdomeric photoreceptors consisting of one to three sensory cells and a single pigmented or unpigmented mantle cell are widespread within taxa of the Plathelminthes Rhabditophora. On the contrary, the existence of two mantle cells forming the eye cup is only known for M. spiculifer and a few other species of the Macrostomida. Therefore, at least two hypotheses are possible: (1) two cup cells are a basic characteristic of the Rhabditophora and a reduction from two to one cup cell has occurred secondarily or (2) the stem species of the Rhabditophora possessed rhabdomeric eyes with one cup cell, and two mantle cells have evolved within the Macrostomorpha. The existence of ciliary aggregates has been documented for several taxa of the Plathelminthes Rhabditophora. From their distribution it can not be concluded whether these differentiations are either a basic feature of the Rhabditophora or have evolved several times convergently. Accepted: 26 September 1999     

Ultrastructure of prostomial photoreceptors in four marine polychaete species (annelida)

The photoreceptors of four polychaete species were investigated by transmission electron microscopy: Eteone longa and Anaitides mucosa (Phyllodocidae), Scolelepis squamata (Spionidae), and Heteromastus filiformis (Capitellidae). Four different types of light-sensitive organs could be distinguished: 1) a simple, unpigmented rhabdomeric type; 2) a simple ocellus composed of a sensory and a pigmented cell; 3) complex eyes with a lens consisting of secretory granules; 4) a simple, unpigmented type with modified cilia. In spite of its simpler organization the fourth type is listed last, because its function as a photoreceptor seems dubious. The first type (unpigmented rhabdomeric receptor) occurs in all four species investigated. It is the only type of photoreceptor in Heteromastus. Additionally, the two phyllodocids Eteone and Anaitides possess another kind of receptor (type 4) in close proximity to the type 1 receptor. Simple ocelli (type 2) are found in Scolelepis. A pair of complex eyes (type 3) is present in both Eteone and Anaitides, but they show important differences in the two species. First, the eyes in Eteone exhibit ciliary rudiments within the sensory processes, but such rudiments are absent in the eyes of Anaitides. Secondly, the sensory cells in Anaitides possess pigment granules, whereas in Eteone they do not. Thirdly, the lens in Eteone is composed of secretion granules of equal electron density, whereas in Anaitides the lens granules show increased electron density centrally. Lens material appears to be secreted from a single corneal cell in Eteone, and from several corneal cells in Anaitides. In both species these corneal cells are located distally outside the lens.     

Photoreceptors in species of the Macrostomida (Plathelminthes): ultrastructural findings and phylogenetic implications

The submicroscopic anatomy of intracerebral and pericerebral photoreceptors in six species of the Macrostomida is described. Cylindromacrostomum notan-dum, Paramyozonaria simplex and Macrostomum hystricinum marinum possess two rhabdomeric intracerebral photoreceptors each consisting of two pigmented cup cells and three (C. notandum and P. simplex) or two sensory cells (M. hystricinum marinum). In C. notandum and P. simplex two of the sensory cells are equal in size, while the third one is much smaller. This organisation is hypothesised as an autapomorphy of the Dolichomacrostomidae. Photoreceptors with two mantle cells are also known for Microstomum spiculifer. Since only one cup cell exists in representatives of nearly all other high-ranked taxa of the Rhabditophora, it is concluded that the characteristic ”two cup cells in rhabdomeric photoreceptors” has evolved in the stem lineage of the taxon Macrostomida or Macrostomorpha, respectively. In Myozona purpurea and Psammomacrostomum turbanelloides rhabdomeric intracerebral photoreceptors of a special type were encountered. These light-sensing organs consist of numerous cells forming an ellipsoid. The surface membranes of these cells are elongated to form filiform extensions which are tightly intertwined with each other. Pericerebral ciliary aggregations consisting of cells with an internal cavity into which axonemata of modified cilia project were observed in all species mentioned above and in Bradynectes sterreri as well. Such putative light-perceiving organs are widespread within taxa of the Plathelminthes Rhabditophora and have been hypothesised either as homologous characteristics or as analogous ones. With increasing examples being described it becomes likely that pericerebral ciliary aggregations are an apomorphic ground pattern characteristic of the Rhabditophora. Accepted: 22 January 2001     

Ultrastructural investigations of presumed photoreceptive organs in two Saccocirrus species (polychaeta,saccocirridae)

In addition to the pigmented ocelli, four different types of photoreceptor-like organs without shading pigment have been found in Saccocirrus papillocercus and S. krusadensis. The sensory cells of these presumed ocelli are either ciliary or rhabdomeric with ciliary rudiments. With the exception of the multicellular type-2 ocelli they are bicellular consisting of a sensory cell and a supportive cell. In each ocellus the supportive cell forms a thin cup-shaped envelope around the sensory elements. In the type-2 ocellus, 7 supportive cells form an ovoid cavity leaving openings through which dendritic processes of an equal number of sensory cells enter the cavity. The pigmented ocelli possess an ocellar cavity communicating with the exterior through a pore in the eyecup, ciliary rudiments in both sensory and supportive cell, and additional non-photoreceptive sensory cells in the opening of the eyecup. The sensory organs show characteristic differences between the two species, such as presence or absence of a particular type of ocellus (type 2 is absent in S. krusadensis, type 3 in S. papillocercus), number of cilia in type-4 ocelli, density of microvilli, number of non-photoreceptive sensory cells in the pore of the pigmented ocellus, etc. These differences provide important characters which can be used for discrimination either of species or of subgeneric taxa in Saccocirrus. The phylogenetic significance of the different photoreceptive organs is discussed.     

Development and differentiation of the eye in Platynereis dumerilii (Annelida,Polychaeta)

The nereid polychaete, Platynereis dumerilii, possess two pairs of post-trochophoral eyes with one vitreous body each. The development of these eyes has first been observed in 2-day-old larvae. Whether the eye anlagen arise from stem cells or from undifferentiated ectodermal tissue was not determined. At first, the anlagen of the anterior and the posterior eyes adjoin each other. They separate in late 3-day-old larvae. The first separated eye complexes consist each of two supporting and two sensory cells. The supporting cells synthesize two different kinds of granules, the pigment granules of the pigment cup and the prospective tubules of the vitreous body. These tubules accumulate in the distal process of the supporting cell. The vitreous body is formed by compartments of the supporting cells filled with the osmiophilic vitreous body tubules. The short, bulbar photosensory processes bear microvilli that emerge into the ocular cavity. At the apex of each sensory cell process, a single cilium (or occasionally two) arises. The sensory cells contain a different kind of pigment granule within their necks at the level of the pigment cup. The rate of eye development and differentiation varies. New supporting cells are added to the rim of the eye cup. They contribute to the periphery of the vitreous body like onion skins, and sensory cells move between supporting cells. The older the individual compartments of the vitreous body are, the more densely packed is their content of vitreous body tubules. Elongation of the sensory and supporting cell processes of the older cells increases the volume of the eye. The eyespots of the trochophore are briefly described as of the two-celled rhabdomeric type with a single basal body with ciliary rootlet.     

A simple visual system without neurons in jellyfish larvae

Earlier detailed studies of cnidarian planula larvae have revealed a simple nervous system but no eyes or identifiable light sensing structures. Here, we describe the planula of a box jellyfish, Tripedalia cystophora, and report that these larvae have an extremely simple organization with no nervous system at all. Their only advanced feature is the presence of 10-15 pigment-cup ocelli, evenly spaced across the posterior half of the larval ectoderm. The ocelli are single cell structures containing a cup of screening pigment filled with presumably photosensory microvilli. These rhabdomeric photoreceptors have no neural connections to any other cells, but each has a well-developed motor-cilium, appearing to be the only means by which light can control the behaviour of the larva. The ocelli are thus self-contained sensory-motor entities, making a nervous system superfluous.     

Retinal ultrastructure may mediate polarization sensitivity in larvae of the Sunburst diving beetle, Thermonectus marmoratus (Coleoptera: Dytiscidae)

A number of invertebrates are known to be sensitive to the polarization of light and use this trait in orientation, communication, or prey detection. In these animals polarization sensitivity tends to originate in rhabdomeric photoreceptors that are more or less uniformly straight and parallel. Typically, polarization sensitivity is based on paired sets of photoreceptors with orthogonal orientation of their rhabdomeres. Sunburst diving beetle larvae are active swimmers and highly visual hunters which could potentially profit from polarization sensitivity. These larvae, like those of most Dytiscids, have a cluster of six lens eyes or stemmata (designated E1 through E6) on each side of the head capsule. We examined the ultrastructure of the photoreceptor cells of the principal eyes (E1 and E2) of first instar larvae to determine whether their rhabdomeric organization could support polarization sensitivity. A detailed electron microscopical study shows that the proximal retinas of E1 and E2 are in fact composed of photoreceptors with predominantly parallel microvilli and that neighboring rhabdomeres are oriented approximately perpendicularly to one another. A similar organization is observed in the medial retina of E1, but not in the distal retinas of E1&2. Our findings suggest that T. marmoratus larvae might be able to analyze polarized light. If so, this could be used by freshly hatched larvae to find water or within the water to break the camouflage of common prey items such as mosquito larvae. Physiological and behavioral tests are planned to determine whether larvae of T. marmoratus can actually detect and exploit polarization signals.