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Monogenea

2, University of Oslo, Oslo Norway.

Monogenea comprise a species-rich group of neodermatan platyhelminths characterised by the following features:

1).  All possess a posterior attachment organ, the opisthaptor, which is usually armed with a variety of hooks, bars, suckers and clamps, for attachment to the final host;

2).  They are predominantly ectoparasites of aquatic vertebrates (fish, amphibians and aquatic reptiles), although a number of exceptions to this rule are known. A very small number have invaded internal sites, including the alimentary canal, lungs, kidneys and bladder. Where they infect terrestrial organisms (predominantly amphibians and reptiles), they occupy internal sites such as the bladder, lungs or mouth and nasal cavities;

3).  They have a simple life cycle, infecting only a single host (cf Digenea, in which a minimum of two hosts are present in the life cycle). The larva is usually a small ciliated oncomiracidium, which hatches from the egg and swims to locate and infect another host. In some cases the oncomiracidium has secondarily lost its cilia; however in a large group of monogeneans, the larva is primitively unciliated and creeping.

With a few exceptions (for example the hyperparasitic Udonella, which infects a copepod fish parasite and has an unarmed opisthaptor but nevertheless appears to be a monogenean), there is little controversy over what constitutes a monogenean.  Having said this, molecular evidence suggests that the Monogenea is a paraphyletic group, made up of the Heteronchoinea, generally larger, blood-feeding monogeneans found either on the gills of predominantly marine fish (the Polyopisthocotyleans) or in the bladders of amphibians (the Polystomatids), and the Monopisthocotylea, a diffuse, variously related group of epithelial browsers from the skin and fins of almost all extant fishes.  These two groups are not closely related, the Monopisthocotylea being a sister group to the tapeworms and digeneans, while the Heteronchoinea are sister group to the (Monopisthocotylea + other Neodermata) clade. Further molecular evidence is needed to resolve the exact relationship between Monopisthocotylea, and Heteronchoinea, and it might be expected that additional groups of Monopisthocotylea may remain to be discovered.

Overall diversity within the Monogenea is masked by the existence of a small number of ‘hyperdiverse’ genera, particularly among the Dactylogyridae and the Gyrodactylidae, in which speciation has generated huge numbers of species with relatively little biological diversification except in relation to host identity.  In fact, overall, the Monogenea are a relatively homogenous group with only the polystomatids, parasites of semi-aquatic and terrestrial amphibians and reptiles, showing a significantly different biology (endoparasitic, adapted for periodic reproduction, utilisation of progenesis to boost reproductive output).  The exception to this generalisation would be within the Monopisthocotylea, where a number of families appear to genuinely lack the phylotypic oncomiracidium larva.  This group includes the Udonellidae, the Gyrodactylidae, the Acanthocotylidae and the Enoplocotylidae, in all of which the hatchling seems to be a crawlaway, a miniature adult best considered as a juvenile rather than a larva.  Dispersal in the udonellids, the gyrodactylids and the enoplocotylids is probably achieved by any stage in the life cycle, rather than just by the larva.   More work is needed on the diversity of these families.  It should be remembered that  the Enoplocotylidae has been the subject of only 3 research papers since first discovered in 1912, while Udonellidae have been generally ignored as not monogeneans;  it is undoubtedly the case that there remains substantial true diversity of monogeneans to be discovered, when attention is diverted from the hyperdiverse gyrodactylids and dactylogyrids.

A note on naming…

The naming of the Monogenea/Monogenoidea remains confusing, partly because there is no clear answer to the problem. The dual naming arose during the 1950s and 1960s when there was little interchange between the Soviet science system (within which Bychowsky was the leading scholar of monogenean systematics and phylogeny) and the Western European system.   In fact the name Monogenea, attributed to van Beneden (1858) and Carus (1863), was in common use at least as far back as the 1930s in the West (e.g. Jones, E. I., Parasitology 19, 227-232), although at this stage, most researchers referred to some version of ‘Monogenetic Trematodes’ (trématodes monogénès, monogenetischen Trematoden etc) to reflect the belief, going back to van Beneden (1858) and Carus (1863), that the monogeneans and digeneans were simply orders of the Trematoda. During the 1950s, Llewellyn particularly, following Sproston, began to popularise the name Monogenea, reflecting the growing scepticism that the Trematoda were a natural group, and that the monogeneans were actually more closely related to the cestodes, an idea attributed to Bychowsky (1937).  Bychowsky (1937) also introduced the name Monogenoidea into current use, but considered the extent of the class as more or less the same as the old order Monogenea (or Monogénèses as originally named). This name then came into western usage with the publication of Bychowsky’s (1957) monograph (still, interestingly, translated as ‘Monogenetic Trematodes’).  The partial adoption of this name can, for example, be seen in the papers of Euzet; in 1957 he published two papers referring to ‘Trematoda-Monogenea ‘ (the ordinal appelation), then later in the same year published on ‘Monogenoidea – Monopisthocotylea’, using the Class designation provided by Bychowsky.  Despite this, the name Monogenoidea never gained widespread support outside of the soviet and eastern bloc community of monogenean workers, and by 1974, the ICOPA in Warsaw agreed to the name ‘Monogenea’ as the highest level appelation for the group.  Since that time, one group of workers have persistently used Monogenoidea, pointing out correctly that the ICZN has no authority over higher level names for taxa, and also indicating that Monogenoidea does not carry the ‘baggage’ of Monogenea, a name previously reserved for the group as part of the Trematoda (Boeger & Kritsky, 2001).  However, this latter argument seems to have lost its power as Trematoda has become a widespread appelation for the taxon comprising the Digenea and the Aspidogastrea, without anyone apparently misunderstanding that this is not the original conception of the Trematoda as a class.  An indication of how marginalised the use of ‘Monogenoidea’ has become is shown from the volume edited by Littlewood & Bray (2001) which represents the most recent detailed survey of platyhelminth interrelationships.  Within this book, all other authors with an opinion on the matter, apart from Boeger & Kritsky (2001) use the term ‘Monogenea’, and even Littlewood & Bray (2001), in their introduction to the book, refer to Monogenea in relation to Boeger & Kritsky’s chapter!  The name Monogenoidea therefore seems to have more or less fallen into disuse in all other sectors of the research community.   The argument is in any case a sterile one; the conception was of monogenetic  trematodes, or  Monogénèses, which was freely translated into other languages, and the ending of the name was never really very significant.  If the group do indeed turn out to be paraphyletic (as looks to be the case currently), then the name will (and should) fall into disuse anyway.

A bigger problem turns out to be the naming of the constituent groups of the Monogenea. Traditionally, the orders Monopisthocotylea and Polyopisthocotylea have been used. These remain the most popular choice, and make the distinction of the monogeneans into two distinct groups, one of which is sister group to the tapeworms and Digenea, the other being sister group to (tapeworms + Digenea + Monopisthocotylea) quite straightforward. The problem is that Bychowsky (1957) again modified the subclass naming of the Monogenea, erecting the Oligonchoinea and the Polyonchoinea.  Oligonchoinea corresponds roughly to the Polyopisthocotylea, the Polyonchoinea to the Monopisthocotylea . Bychowsky’s boundaries did not entirely match those of Odhner hence the name change, whereas the modern conception of the two groups is much closer to Odhner’s system. Bychowsky’s classification should be deprecated, because of the potential for confusion of Polyonchoinea with Polyopisthocotylea, when actually they refer to diametrically opposite groups.   Unfortunately, Boeger & Kritsky (2001) again utilise the Bychowsky classification, almost in isolation, without any real justification.  The only point where their naming does become justified concerns the taxon Polyopisthocotylea + Polystomatidea. There is good evidence that these two groups are not the same, although they share a common ancestor.  The use of the name Heteronchoinea to accommodate Polyopisthocotylea and Polystomatidea, and the sister group of the Monopisthocotylea therefore appears a sensible innovation.

References
Boeger, W.A. & Kritsky, D.C. (2001).  Phylogenetic relationships of the Monogenoidea. In Interrelationships of the Platyhelminthes (Littlewood & Brayeds). Systematics Association Special Volume 60.  Taylor & Francis, London & New York.
Bychowsky, B.E. (1937). Ontogenesis and phylogenetic interrelationships of parasitic flatworms (in Russian).  Izvestiia Nauk SSSR, Ser Biologiya 4, 1354-1383.
Bychowsky, B.E. (1957). Monogenetic Trematodes, their Systematics and Phylogeny.  Akademi Nauk USSR pp 1-627.
Carus, J.V. (1863). Vermes.  In Peters, W.C.H., Carus, J.V. & Gerstaecker, C.E.A. (eds.). Handbuch der Zoologie, 422-484.
Littlewood, D.T.J., & Bray, R.A.  (2001). Interrelationships of the Platyhelminthes.  Systematics Association Special Volume 60.  Taylor & Francis, London & New York.
Van Beneden, P.J.  (1858). Memoire sur les vers intestinaux.  J.B. Bailliere, Paris

 

Monogenean Pictures