The evolutionary expansion of the Spirurida

International

Pergamon

Journalfor Parasitology, Vol. 24. No. 8, pp. 1179-1201, 1994 Copyright 8 1994 Australian Society for Parasitology Elswier Science Ltd Printed in Great Britain. All rights reserved 002&7519/94 $7.00 + 0.00

0020-7519(94)0012%6

THE EVOLUTIONARY ALAIN

EXPANSION

OF THE SPIRURIDA

and ODILE BAIN

G. CHABAUD

Laboratoire de Biologie Parasitaire, Protistologie et Helminthologie, 61 Rue Buffon, 7523 1 Paris cedex 05, France A. G. and Bain 0. 1994. The evolutionary expansion of the Spirurida. International Journal for Parasitology 24: 1179-1201. The possible origins of the 12 superfamilies of the Spirurida are

Abstract-Chabaud

considered, based on comparative morphology, host and geographic distributions. The available evidence suggests a complex origin of these nematodes, some families being derived from the Seuratoidea, and others from the Cosmocercoidea (Ascaridida). The spirurid radiation is an old one and seems to have occurred primarily in the Secondary or early Tertiary eras. Since then, expansion has occurred with host capture as a prominent mechanism. The Dracunculoidea Procamallanidae and Camallanidae are probably derived from the Chitwoodchabaudiidae and the Rictularioidea from the Schneidernematidae. The Seuratidae may have given rise to the Gnathostomatoidea, the Physalopteroidea, the Thelazioidea, the Habronematoidea, the Spiruroidea and the Acuarioidea. The filarioid nematodes appear to have several origins with the Diplotriaenoidea derived from the Spiruroidea, while constituents of the Aproctoidea derived from the Cystidicolinae, the Seuratoidea and the Spiruroidea. The Filarioidea are thought to have arisen from the Spiruroidea and the Thelazioidea. The evolution of tissue parasitism as a secondary phenomenon is considered in various groups. INDEX KEY WORDS: Spirurida; Nematoda; phylogeny; evolution

INTRODUCTION

The Adenophorean nematodes are simple organisms and their morphological evolution, although rich and diverse in each order or superfamily, follows uniform, characteristic, and well defined processes. In the parasites of vertebrates, the evolution of the cephalic structures, the migration of the male cloaca1 papillae, the progressive increase in complexity of the organs of attachment (synlophe, cordons, etc.), the genital anatomy of the female and even biological peculiarities invariably follow the same pattern and provide sound morphological and biological data for establishing their phylogeny. Furthermore, the morphology of the larval stages provides valuable information when the larvae of specialised species are morphologically similar to the adults of primitive species. When the phylogeny of a parasitic group is sufficiently well established, analysis of the host range and of the geographical distribution enables formulation of an hypothesis on the evolutionary history of these parasites which can be compared with the palaeontological data available for the hosts. Valuable publications on this subject relating to different groups of nematode parasites of vertebrates are by Durette-Desset (1985) on the Trichostrongylina, Quentin (1971), Hugot (1988) on the Oxyurida and Sprent (1992) on the Ascaridoidea.

The Spirurida are not particularly amenable to this kind of analysis because their origin appears to be very ancient and many are parasites of birds, the fossil record for which is poorly known. Chitwood (1950) was very cautious about their origin. He wrote: “If we were to suggest any group as being similar to possible ancestors of the Spirurida, it would be the Cylindrocorporidae (Rhabditoidea) “. Here Chitwood who was always the most exacting and meticulous of authors, and who can usually be used as an example of precision, appears to us, to be wrong. He grouped the Strongylina and the Ascaridina in the order Rhabditida and isolated the Spirurida in a separate order. As will be shown below, it is impossible to understand the Spirurida if one does not admit that they arose from the Ascaridida. In order to establish the historical evolution of the nematode parasites of vertebrates, we postulated the following concepts: (1). The Oxyurida excepted, the nematode parasites of vertebrates readily adapt to a new host, sometimes quite unrelated to the original one. When the parasite becomes established in this new host, the consequence is isolation, which, sooner or later, entails morphological or biological speciation. It is the “capture phenomenon”.

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A. G. CHABAl JD and 0. BAIN

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(2). The evolutionary explosion of a group of vertebrates gives rise to many new ecological niches. Consequently, the period of the explosion of a group of nematodes often coincides with the period of the evolutionary explosion of the hosts. (3). An “ancient host” is an animal differing little from fossil forms dating from an ancient geological epoch, e.g. a present-day tenrecoid, didelphid, dermopteran and even a chiropteran differs little from corresponding animals present at the beginning of the Tertiary. The nematode parasites of these hosts may evolve little or not at all when its host remains unchanged. The relict vertebrates (crocodiles, tortoises, ratites) are often parasitised by relict nematodes. A “modern host” has no clearly related fossil forms except from a relatively recent geological epoch, e.g. the first ruminants resembling the modern Bovidae appeared only in the Miocene. The nematode parasites of these hosts are very often of an evolved type. SUPERFAMILY

CAMALLANOIDEA

Frocamallaninae morphological and biological evolution. The phylogeny of the Camallanidae was established principally by Campana-Rouget (1961a,b) studying the morphogenesis of buccal structures from the third larval stage in the copepod to the adult in the fish. The larvae have bipartite caliciform buccal capsule. In the Procamallaninae, the posterior portion disappears; the anterior portion remains caliciform and can aquire spiral thickenings. In the Camallaninae, the posterior portion remains in the primitive species; the anterior portions is separated into paired lateral valves. Petter (1979a) performed a systematic analysis of the evolution of the cephalic structures and the evolution of the male caudal extremity. Five types were differentiated: type 1, assumed primitive, with many papillae, the postcloacal ones distributed along different axes, the dorsal ones corresponding to the 1, 4, and 8 papillae of the Cosmocercoidea (cf. Chabaud & Petter, 1961); type 2, close to type 1, with fewer precloacal papillae (Spirocamallanus, Asiatic type); type 3, with wide caudal alae, 3 precloacal pairs of papillae; 2 large juxtacloacal pairs and 5 postcloacal pairs; this type was called the “marine” type; type 4 and type 5 without caudal alae and with papillae irregularly distributed on the latero-ventral axes (type 4) or regularly distributed (type 5) (Neotropical fish type). In the present paper, we have modified slightly the

conception of Petter (1979a) because we believe that type 5 arose from type 3 and not from type 2. Petter (1979a) pointed out that the genus which is from Spiroc~al~anus, derived Procamallanus by acquiring spiral thickenings, occurred at three different times and is actually a convergent group: a, in marine fishes, b, in African amphibians, c, Neotropical fishes, with a small branch identifiable by the morphology of one of the spicules. Host range and geographical

distribution. Pro-

camallaninae are absent from the Holarctic region. They are numerous in four different faunas: 1, freshwater fishes and amphibians from Africa; 2, freshwater fishes from Asia; 3, marine fishes; 4, freshwater fishes from South America. Africa: The number of Procamallanus species is small. P. laeviconchus, parasitic in many fishes, mainly Siluriformes, has a primitive morphology (caudal papillae) and a very wide distribution. In Madagascar, one particular species is a parasite of eels. In amphibians, two species are characterised by their small size and by the tail of the female, which is armed with small spines resembling the morphology of the larva and which is assumed to be a primitive character. The genus ~nchoc~allanus is absent. One species of Sp~rocamallanus, parasitic in amphibians, is close to the species of Procamallanus quoted above and 4 species parasitic in Siluriforms have a “marine type” morphology. Asia: The Procamallaninae are many and diverse, but the number of species is uncertain because of many synonymies. There are about 10 species of primitive Procamallanus, close to the African species, parasitising mainly Siluriformes and Channiformes, 2 or 3 species of ~n~ho~arna~~anusin the same hosts, and 5 to 20 species of Sp~ro~~allanus (type 2) parasitic in freshwater fishes from different families. South America: The fauna is rich and diversified, mainly in the Siluriformes and the Cypriniformes (Characidae). There are no primitive Procamallanus but only type 3 species and one type 5 species. Spirocamallanus spp. are numerous and belong to types 3, 4 or 5. Marine fishes: Many species are widespread, in all oceans and in many families of fishes. They are Procamallanus or Spirocamallanus which both have a type 3 tail extremity. Origin and expansion. For a long time, the Camallaninae were classified close to the Cucullanidae. Actually they are very different. Puylaert’s

Evolution of the Spirurida

(1970) discovery of the Chitwoodchabaudiidae (Seuratoidea), parasitic in African amphibians, showed the existence of a relict family which may be close to the ancestors of the Camallanina. The above analysis of the Procamallaninae, may indicate a Gondwanan origin, probably in the Ostariophysi (Siluriformes and Cypriniformes) which are the hosts of the primitive species. Novacek & Marshall (1976) believe that the Preostariophysan fishes emerged on the Gondwanan continent. The differentiation of the Ostariophysi occurred in South America in the early Cretaceous, after the opening of the Atlantic ocean. In the middle Cretaceous, they split into Siluriformes and Cypriniformes and spread over South America and north-west Africa which, at this time, were united. The splitting of the two continents occurred during the Turonian. At the late Cretaceous and early Paleocene, West Africa became linked to the Arabo-African block and the Siluroids and Characoids dispersed throughout Asia. Our data show that there are no primitive species in South American freshwater fishes. The type 3 species (marine type) arose from the species of marine fishes which adapted to freshwater. Type 5 species can be easily traced from them. Type 4 species are more difficult to interpret, but at all events, they cannot be considered as primitive species. The origin of the Procamallaninae therefore may be found either in Africa or in Asia. Petter (1979a) chose the second hypothesis because “on y observe (en Asie Tropicale) une radiation evolutive des formes primitives. 11sont done dD prendre naissance posterieurement 8 l’apparition des Ostariophysaires, au moment de la diversification des Siluroides en Asie”. We believe rather an African origin, because the independent branch in the amphibians shows these parasites to have had a strong evolutionary development in Africa, and because the type 3 species, which also shows a strong evolutionary development, is African and not Asian. We hypothesise that the site of the Procamallanidae was in West Africa, after the splitting of South America i.e. in the late Cretaceous. According to this hypothesis, the Procamallaninae arose during the Turonian, in the West African freshwater Ostariophysi. They became adapted to the African amphibians and diversified in tropical Asia in the late Cretaceous and Paleocene. They would have reached the South American freshwaters late, by the intermediary of African species adapted to marine fishes, which secondarily became readapted to freshwater.

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Camallaninae Morphological

and biological evolution. As indicated above, the morphological analysis was performed by Petter (1979b). Paracamallanus, the most primitive genus has, behind the buccal valves, a large chitinoid buccal cavity which atrophied during the course of evolution. However this is a process which has occurred in each of the several evolutionary lineages. Thus, the genus Paracamallanus is polyphyletic, containing all the primitive species, some of which show peculiarities indicating future evolutionary developments. The posterior part of the buccal capsule became progressively reduced in the species parasitising Indo-Malaysian freshwater fishes, Claridae, Siluridae, Channidae, Anabantidae and Mastacembelidae and intermediates between the genera Paracamallanus and Camallanus can be found. The species considered as being the most evolved are those with the posterior buccal capsule reduced to a thin chitinoid ring, as seen in Camallanus from Cypriniformes and Amphibians in tropical Asia, freshwater fishes of other regions, and in marine fishes. Denticulations on the longitudinal crests of the capsule are found in one or two small evolutionary lineages which became differentiated in IndoMalaysian freshwater fishes. The number of longitudinal crests increased during the course of evolution. It is 9-11 in the majority of Paracamallanus and Camallanus in Indo-Malaysian freshwater fishes, while it is always greater than 12 and sometimes reaches 30-40 in Camallanus in Cyprinifonnes and marine fishes. As a general rule, the length of the trident-shaped, chitinoid process increased in the course of evolution; several small evolutionary lineages which developed in tropical Asia, show, on the contrary, a tendency to become atrophied. The precloacal papillae are multiplied in the most specialised species. The left spicule has tended to disappear in the course of evolution, while the right spicule acquired a spur in the species adapted to tetrapods. Host range and geographical distribution. The genus Paracamallanus is mainly a parasite of Siluriformes and Channiformes in tropical Asia. The genus Camallanus has spread all over the world in freshwater and marine fishes and in amphibians in Asia, Africa and North America. The genus Oncophora is a parasite of Scombridae in different oceans. The genus Serpinema is a parasite of turtles in tropical Asia, Holarctic and Neotropical areas

A. G. CHABAUD

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and in Australia. The genus Camallanides is a parasite of snakes in tropical Asia. Origin and expansion. A paleobiogeographical analysis was made by Petter (1979b) and her conclusions are summarised as follows: The most primitive species Fish parasites: (Paracamallanus) are found mainly in tropical Asia in Siluriformes and Channiformes. The most primitive Camallanus are also found in this area. Also, a large number of species belong to many small divergent evolutionary branches. The more evolved South Asiatic Camallanus are parasites either of Cypriniformes, or of marine fishes. Therefore the may have originated in the Camallanidae Siluriformes of the Indo-Malaysian area, from Procamallaninae ancestors, and diversified when the Channiformes developed. Later, a branch adapted to the Cypriniformes and another (which appears to be the root of the genus Oncophora) adapted to marine fishes. The branch parasitising the Cypriniformes spread over North Asia and the entire Holarctic area and became adapted to many freshwater fishes. The only species described from South America is very specialised and may derive from a marine species. In Africa, the fauna is an impoverished copy of the Indo-Malaysian fauna and may have been introduced with the hosts, when Africa was invaded by tropical Asiatic fishes. Amphibian parasites: The most primitive species (buccal cavity with a smaller number of crests) are parasites of Ranidae and Bufonidae from the IndoMalaysian area. They may have spread over Africa and North America with their hosts. Reptile parasites: Adaptation of Serpinema to the turtle family Emydidae must have occurred prior to the dispersion of these hosts, because the Emydidae are parasitised throughout their range. Hence infection of other turtles families appears to be secondary. Camallanides spp. which are parasitic in different families of snakes are known only from the Indo-Malaysian area. These data as a whole lead us to think that the Camallaninae originated from the Procamallaninae in the Indo-Malaysian area and evolved in the Siluriformes, therefore, probably in the early Tertiary. SUPERFAMILY

DRACUNCULOIDEA

Morphological and biological evolution. The Camallanoidea live in the gut of their hosts, although some species of Procamallanus (P. mehrii, P. attui) are found in the body cavity or swimblad-

and 0. BAIN der. By contrast, the Dracunculoidea are adapted to tissue habitation and this adaptation has induced a significant number of morphological modifications of which the main ones are: (a) In primitive species, the shape and the length of the body are comparable to the other nematode parasites of vertebrates; the body may become longer and more slender (filariform) or globular and mammilated in evolved species. (b) Sexual dimorphism is slight in primitive species and becomes marked in specialised species; the growth of the female continues after copulation. (c) The buccal cavity is well developed and provided with denticles in primitive species. It becomes reduced to a ring or is atrophied in the course of evolution. (d) The glandular oesophagus is variable. Each of the 3 sectors contains fundamentally one nucleus, but in some species they may multiply while other species retain only the muscular oesophagus. (e) The atrophied anus is not functional and may disappear completely. (f) Evolution of the female genital apparatus is marked by a change from oviparity to viviparity and from didelphy to monodelphy (with transitional forms which possess one atrophied uterine branch). The ovejector and the vulva become atrophied and in extreme cases, the vulva disappears and the larvae are freed by the bursting of the body wall. (g) In a few primitive species, the ancestral position and number (21) of the cloaca1 papillae of the male is preserved, but more often the papillae are atrophied and scanty. (h) The spicules become progressively reduced to 2 short, subequal needles and may disappear or be replaced by a copulatory plate, probably originating from the posterior wall of the rectum. (i) In both sexes, the caudal extremity may preserve the three terminal vestigial spines of the larval stages, become simple and pointed or become rounded. One particular character of the Dracunculoidea provides the main argument for those authors who support the monophyletic origin of the superfamily. This is the cephalic papillae, and mainly the internal labial cycle of papillae, which are well developed and are not atrophied even in the most evolved species. Furthermore, the ventral and dorsal internal labial papillae migrate towards the median axis. The 2 ventral internal labial papillae and the two dorsal internal labial papillae may be in contact and thus form a pair of median papillae otherwise unknown in the Spirurida. The evolution of the different characteristics

Evolution of the Spirurida described above is not homogeneous. In very specialised groups, some characters remain primitive. It appears impossible to outline a general evolution from primitive species to more evolved and more modern species. Thus, it is necessary to analyse separately each family or subfamily, the links between them being difficult to elucidate. Host range and geographical distribution. Many new taxa have been discovered recently because many of these nematodes are difficult to find during necropsy and our knowledge is probably very incomplete. Seven families are distinguished by Moravec & Koie (1987) but we prefer to include the family Daniconematidae in the Skrjabillanidae. Anguillicolidae: The family includes only a few species of the genus Anguillicola parasitising the swimbladder of eels in China, Japan and Australia. Their introduction to Europe occurred a few years ago (DuPont & Petter, 1988). Skrjabillanidae: The 2 species included in Daniconematinae are a species of Daniconema which differs from Skrjabillaninae by the absence of a buccal cavity and of caudal alae and a species of Mexiconema, described by Moravec, Vidal & Salgado Maldonado (1992), which may be easily included in the Guyanematidae. The Skrjabillanidae include some genera parasitising the swimbladder or the peritoneal cavity of palaearctic freshwater fishes (eels, Cypriniformes and pikes). Guyanemidae: The host range is wide, including some freshwater fishes (Petter & Dlouhy, 1985) and also marine fishes and selacians. All the described species are from the New World, mainly Neotropical and also from Scorpaeniformes of British Columbia (Adamson & Roth, 1990) and from selacians. Philometridae: The family includes 3 very different subfamilies. The Philonematinae are essentially holarctic parasites of Salmoniformes. Philometrinae is an important and diversified subfamily parasitising various freshwater and marine fishes in all oceans. The subfamily Phlyctainophorinae includes only one aberrant genus parasitic in the subcutaneous tissues of selacians (Adamson, Deets & Bentz, 1987). Micropleuridae: The only genus in this family is a characteristic parasite of crocodiles and turtles, known from species in India and Brazil. Moravec & Little (1988) hesitating by classifying the genus Granufinema in the family; we prefer to interpret it as a primitive Dracunculidae. Dracunculidae: The Dracunculidae includes the genera Protenema, parasitic in Necturus (Amphibia, Proteidae)‘ in Minnesota, Granulinema parasitic in

1183

selacians living in the sea or in freshwater in Louisiana, Dracunculus in reptiles and mammals and Avioserpens in birds. These last 2 genera are cosmopolitan. Origin and expansion. To perpetuate the life cycle, the eggs or the larvae of the parasite must be expelled from the host. The localisations in the digestive tract ipso facto allow this expulsion and the same applies for localisations in hollow organs such as the urinary system, the pulmonary system, the gallbladder, the mammary glands, the lachrymal glands, and the swimbladders of some fish. Tissue localisation in birds allow also the expulsion of eggs or larvae through the air sacs. In the reptiles, the lungs extend posteriorly and facilitate localisation in these tissues. The expulsion of eggs is more difficult in fishes, amphibians and mammals. In general, Camallanina larvae develop only in free living copepods. Thus, the life cycle necessitates a migration of the mature female nematodes to the skin and the formation of an abscess which opens when the parasitised host is in an aquatic environment. The life cycle may seldom evolve by an adaptation of the larvae to the blood and the transmission by haematophagous arthropods as occurs in the Spirurina (Onchocercidae). For example, in Molnaria intestinalis and Skrjbbillanus scardinii, parasite of Palaearctic Cyprinidae, the larvae, carried by the blood stream, localise subcutaneously and aggregations of larvae are ingested by a Branchiuran, an ectoparasitic crustacean of the genus Argulus (see Tikhomirova, 1975). In ZchthyoJlaria canadensis, parasitic in Lycodes (eelpout) the larvae are blood dwelling (Appy, Anderson & Khan, 1985) as well as in Lockenloia sanguinis which is an enigmatic Dracunculoidea parasitic in sharks in Florida (Adamson & Caira, 1991). Apart from these particular adaptations, the fundamental life cycle necessitates the expulsion of the first stage larvae from the vertebrate host in order that they may be ingested by a copepod and allow larval development. The consequence of these events is that the Dracunculoidea are restricted in their expansion to a few favourable hosts. In conclusion, we believe that although the origin of the Dracunculoidea appears to be very ancient, the extension of the superfamily is still strictly limited in its host range and geographical distribution. There are a small number of species and a large number of genera. This observation is characteristic of ancient lineages including relict species rather than species arising from an explosive evolution of a recent branch.

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A. G. CHABAUD

Contrary to the general rule, the more primitive genera have a host range and a geographical distribution narrower than the more specialised genera. Furthermore, the tissue parasites, living in a more stable environment than the parasites of the gut, may be more stable themselves. The speed of evolution may be slower and the probability of survival greater. SUPERFAMILY GNATHOSTOMATOIDEA Morphological and biological evolution. The single family Gnathostomatidae includes 3 subfamilies which have in common 2 massive and trilobate pseudolabia but are actually very different and do not represent a single evolutionary lineage but rather the vestiges of ancient groups. Their general anatomy is primitive but the cephalic anatomy which is used for attachment is specialised. Spiroxyinae: The single genus Spiroxys has neither cephalic bulb nor cephalic appendages. Ancyracanthinae: The single genus Ancyracanthus has long cephalic appendages arising from the pseudolabia. Gnathostomatinae: The three genera have a strongly striated cephalic bulb, without hooks in Tanqua, with hooks in Echinocephalus and Gnathostoma, the latter being characterised by hooks also on the body and the rounded caudal extremity of the male. Thus it is possible to accept a roughly progressive filiation from Tanqua to Echinocephalus and to Gnathostoma. Host range and geographical distribution. Spiroxys

comprises species in amphibians, snakes and freshwater turtles. It is known from the USA, Mexico, Algeria, India, Japan, Australia and China. Ancyracanthus comprises two species from Brazil, one in freshwater turtles and one in fishes. Tanqua, is known from lizards and snakes with a Gondwanan distribution (South America, Africa, India, Sri-Lanka, Hainan (China), South East Asia and Australia). Echinocephalus comprises several species parasitising sharks and rays all over the world. Gnathostoma comprises about 12 more or less cosmopolitan species, mainly in aquatic Carnivora. Origin and expansion. The Gnathostomatoidea are particular nematodes and it is difficult to propose a precise hypothesis for their origin. We think, with Bartlett & Anderson (1985), that the first intermediate hosts are copepods and that the various invertebrates in which their larvae are found are paratenic hosts, which relates them to primitive Spirurida. Thus, in spite of the diverse morphology of the 3 families, some common biological phenomena

and 0. BAIN appear, the first moult in the egg and larval migrations in the final host, which may indicate that they are intermediate between the Ascaridida and the Spirurida, e.g. the Seuratoidea. In this superfamily, the genus Echinonema, parasitic in Australian marsupials (redescribed and reclassified by Inglis (1967)) appears to be somewhat related to the Gnathostomatoidea. Thus it is possible to hypothesise that the Gnathostomatoidea arose from an Echinonematine ancestor [a subfamily recognised by Quentin (1971), as a member of the Seuratidae] of which Echinonema is the only relict. The whole indicates a very ancient origin, confirmed by the host range which comprises mainly the amphibians, the reptiles and the selacians. Gnathostoma is the only relatively modern genus parasitic in mammals. It appears to have arisen directly from genera such as Tanqua parasitic in Gondwanan reptiles or such as Echinocephalus secondarily adapted to the marine environment in selacians. Thus the Gnathostomatoidea appear to be one of the most archaic Spirurida, and probably differentiated as early as the Jurassic epoch. SUPERFAMILY

PHYSALOPTEROIDEA

Morphological and biological evolution. The single family Physalopteridae is characterised by the presence of two massive but not trilobate pseudolabia. It comprises 3 subfamilies: Thubunaeinae: The Thubunaeinae are devoid of a cephalic collarette. As a general rule, the primitive disposition of the cloaca1 papillae (21 papillae with 1, 4, 8 lateral paired) is preserved. Proleptinae: In the Proleptinae, the cephalic collarette is present. The caudal alae of the male merge into the lateral borders of the body and the area rugosa is limited to the zone anterior to the anus. Physalopterinae: The Physalopterinae are also provided with a cephalic collarette. The caudal alae of the male are united on the ventral surface of the body and the caudal bursa is ornamented. The morphology of the Physalopteridae is therefore homogeneous, their evolution being indicated by discrete characters: the cephalic collarette, the increasing number of cephalic teeth, the shape of the male tail showing a tendency to become closed, the pattern of the cloaca1 papillae which become gathered around the cloaca and the multiplicity of the uterine branches. Host

range

Thubunaeinae

and geographical distribution. The parasitizes relatively modern reptiles

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Evolution of the Spirurida

(lizards and snakes) from the New World, Africa, Madagascar and Asia. One species, occurring in neotropical amphibian, has no particular affmities. The Proleptinae are marine parasites but the different genera occur in distinct hosts. Proleptus and Paraleptus are parasites of selacians, less often of teleosteans. Heliconema parasites anguilliform fishes. These genera are cosmopolitan, Bulbocephalus with a very modified cephalic extremity occurs in teleosteans from Asia. The Physalopterinae occur throughout the world in modern reptiles to mammals. Pseudabbrevjata known from a single species parasite of an African lizard is the most primitive genus since it has a buccal capsule. ~k~ab~optera with only a single pair of labial teeth parasitizes reptiles. Abbreviata possessing externo-lateral teeth is principally a parasite of reptiles but it occurs also in amphibians, rodents and primates. Physalopteru with the larger number of teeth on the lips occurs mainly in birds of prey but also in many varied mammals. The other genera, have a more restricted host range, (for example, Pseudophysalopteru occurs in soricoid insectivores) or a more restricted geographical distribution (Turgidu in neotropical mammals or Pentadentoptera in palaearctic rodents). Origin and expa~ion. The Proleptinae which are morphologically closer to the Physalopterinae are parasites of very ancient animals: the selacians and the anguilliform fishes. On the contrary, the Thubunaeinae which have a more primitive morphology are parasites of more modem animals: lizards and snakes. Thus, there is a contradiction between the morphological data and the host range. We propose the following hypothesis: an initial evolutionary line adapted to freshwater selacians from ancestors similar to those of Gnathostomatoidea (i.e. from Ascaridida), then became adapted to marine fish, and finally evolved in the same way as the Physalopterinae. A second evolutionary line, the Thubunaeinae, would have become adapted to modern reptiles at the beginning of the Tertiary and by successive hostswitching become adapted to numerous birds and mammals, through the Tertiary. One particular character of the Physalopteridae is that the phenomenon of capture entails only slight modifications of morphology. Among phasmidian nematodes, the morphology of the parasite usually indicates the order of its vertebrate host. Due to homogenous morphology, the same identification has often been made for parasites from distant geographical areas. A more precise analysis

shows that actually almost each species (except the bird parasites) has a strictly limited geographical distribution. Thus, the expansion of the Physalopterinae may be more recent than generally accepted, perhaps in the late Eocene, when the drift of the continents was largely complete. SUPERFAMILY

RICTULARIOIDEA

Morphological and biological evolution. An analysis of morphological evolution was performed by Quentin (1969) on the single family Rictulariidae. Three elements are of consequence. Cephalic morphology: The initial apical mouth opening became progressively dorsal. The symmetrical hexaradial arrangement of the structures became bilaterally symmetrical. The 6 small labial lobes of the larval stages became atrophied and replaced by two lobes, a well developed ventral one, and a reduced dorsal one bearing only 2 papillae of the internal cycle. Cloaca1 papillae: The primitive Ascaridina type with 1, 4, 8 lateral pairs, became progressively the Spirurida type, with papillae arranged in 2 longitudinal files, then a specialised type with pedunculated papillae gathered around the cloaca. Pectate elements: The number of combs or spines inserted on the latero-ventral axes of the body, which is characteristic of the family, increased progressively in the course of evolution. Other characters like the vulvar location or the spicule length are less important. The above character analysis leads to the seperation of 2 different genera: Rictularia: The mouth opening is wholly dorsal, which entails an atrophy of the ventral oesophageal teeth. This is the last stage of evolution. The other characters (primitive pattern of the cloaca1 papillae, small number of the pectate elements) belong on the contrary to an archaic type. Thus, the genus appears to have followed an evolutionary direction distinct from the other genera. Pterygodermatites: The progressive and parallel evolution of all the characters leads us to believe that the branch is homogenous. Quentin (1969) recognised 5 sub-genera: Paucipectines: Mouth opening apical, cloaca1 papillae primitive, 29-39 pairs of prevulvar spines. Neopaucipectines: Mouth opening subapical, cloaca1 papillae primitive, 34-38 pairs of prevulvar spines. Pterygodermat~tes: Mouth opening subdorsal, peribuccal denticles of irregular size, 40-46 pairs of prevulvar spines. Mesopectines: Mouth opening subdorsal, peribuccal

1186

A. G. CHABAUD and 0. BAIN

denticles forming a regular crown, caudal papillae along two subventral rows, 37-51 pairs of prevulvar spines. ~ultipecti~es: Mouth opening subdorsal, peribuccal denticles replaced on the ventral border by a sclerotic apophysis, caudal papillae pedunculate and grouped around the anus, 47-58 pairs of prevulvar spines. More recently Chabaud & Bain (198 1) described a third genus Quentius which, considering its cephalic structures, is more primitive than the others but which presents hypertelic characters as it is often the case with relict species (a dorsal cuticular ala, an inflated posterior extremity of the body, complex oesophageal teeth etc.) Host range and geographical distribution. QueRtius parasitizes a marsupial from Columbia. Rictularia parasitizes rodents (Sciuridae, Gliridae, Muridae, Arvicolidae) and bats in the Holarctic region. Paucipectines is mainly a parasite of rodents (Sciuridae, Cricetidae and Arvicolidae) from the Neotropical and Holarctic regions. Neopaucipectines occurs in European bats, Ethiopian rodents and Oriental femurs. Pterygodermatites occurs mainly in insectivores and bats from the Mediterranean area. ~esopect~~es occurs in rodents (Gerbillidae and Muridae), carnivores (Viver~dae) and primates from Africa and Asia. ~u~tipectines is cosmopolitan in the Mustelidae, Felidae and Canidae. Origin and expansion. Quentin (1969) pointed out that in the intermediate host, the rictulariid larvae are small, stout, and strongly bent along the dorsal axis, This is unusual for the Spirurida and resembles that of the subulurid infective larva. Also, the chitinoid stoma1 structure with 3 aesophageal teeth resembles that of the Subuluroidea. Thus, the Rictularioidea form a particular group among the other Spirurida. As with others, their origin must be among the Ascaridida, though atkities with the Subuluroidea support the hypothesis for a common ancestor between the two superfamilies, for which an ancestor of the Schneidernematidae is suggested. Quentin (1969) believed that 2 different evolutionary trends occurred. The genus Rictularia could have originated in the North of the American continent and remained localised in the northern hemisphere then spread into Eurasia. The original hosts were probably the Sciuridae and the Gliridae. The parasites in Muridae, Talpidae and Chiroptera are morphologically more evolved and these hosts are probably secondary, i.e. “capture hosts”. Pterigodermatites: The common stem is represented by the sub-genus Paucipectines comprising species

showing the most primitive characters, the geographical distribution of which includes Siberia and the American continent. The South American species derive from the North American ones. Their introduction into South America may have coincided with the migration of the Cricetidae from North America to South America during the PlioPleistocene. Thus, in South America, the Cricetidae are the natural hosts, and the marsupials and Chiroptera the “capture hosts”. Four branches diversified from the Paucipectines group and have spread all over the world, except Australia, in the different hosts named above. From species occurring in rodents, evolution occurred from North to South in America on the one hand, and in Africa and Asia on the other hand. The host-switchings occurred to more ancient animals which were already present before the rodents arrived. According to Quentin (1969), on the basis of the data available at the time, parasites of Sciuridae and Gliridae evolved relatively late, i.e. Oligocene. This is somewhat surprising since the other archaic Spirurida seem to be much more ancient. The discovery of Quentius, the most primitive of the genera, from a neotropical marsupial calls for a new interpretation. The passage from the South to the North could not have occurred during the Tertiary, the connections being severed during that period. It may be inferred that the Rictularioidea did arise as early as the Cretaceous in the American marsupials. They were maintained in these hosts, at least until the Oligocene. At this time, ancestors similar to Quentius, were probably captured by the rodents from the North of the Nearctic region and began the evolution described above. SUPE~AMILY

THELAZIOIDEA

The Thelazioidea comprises Spirurida with a round or hexagonal mouth opening, not compressed laterally, which according to Chitwood & Wehr (1934), groups the primitive forms together. The comprises the primitive superfamily therefore Spirurina, but does not necessarily indicate genuine relationships. Consequently the 3 families must be analysed separately. Rhabdochonidae ~orpholog~cai and biological evolution. ~abdo~hona, the basic genus, comprises numerous homogen-

eous species which parasitise the gut of freshwater fishes. Their morphology becomes specialised when the ecological niche differs i.e. extraintestinal loca-

Evolution of the Spirurida tion, adaptation to marine fishes, adaptation to vertebrate other than fishes. Evolution is characterised by the loss of cloaca1 papillae, particularly the precloacal ones, loss of the cephalic teeth, atrophy of the buccal capsule, lengthening of the pharynx, and anterior or posterior migration of the vulva, entailing monodelphy. range and geographical distribution. Host Rhabdochona is parasitic in freshwater fishes

throughout the world, except Australia. There are numerous species mainly in the Palaearctic and Oriental regions (Moravec, 1975). Fellicola, Johnstonmawsonia, Vasorhabdochona, Heptochona, Hepatinema, Pancreatonema follow, to

variable degrees, the evolutionary trend described above. They became adapted either to marine fishes or to extraintestinal locations: liver, pancreas, gall bladder, blood stream, body cavity. Freitasia with an exceptionally long pharynx, became adapted to terrestrial reptiles in Cuba. Trichospirura comprises two closely related species, one in the pancreatic ducts from an American primate, the other in the salivary ducts of a Malaysian tupaid. A female specimen was also found in the gut of a microchiropteran. Origin and expansion. The origin of the genus ~abdochona is particularly difficult to trace since no

species of Seuratoidea are clearly related to it. The most original feature being the very long pharynx (= protorhabdion), we suppose that the genus derived more or less directly from some freshwater Cosmocercoid but that the direct ancestors have disappeared. The origin of the other genera is clear. Due to host switching, they became adapted to new environments such as extra intestinal locations, the marine environment and even to another vertebrate order (Chabaud & Krishnasamy, 1975). The main difficulty is dating the radiation of the genus Rhabdochona. The mo~holo~cal evolution of the genus has not been traced and the different subgenera have no phyletic significance. The species are very numerous in the Palaearctic and Oriental regions, numerous in Africa, scanty in the Nearctic and mainly in the Neotropical areas and absent in Australia. The abundance of species does not necessarily indicate the geographical origin of a lineage. The phenomenon of capture appears to be a more reliable point from which to try to determine their origin. From this point of view, the species of Trichospir~ra are interesting because of their host

1187

range - the platyrhinians, the Tupaiidae and the Chiroptera - this may date them to the Paleocene. Furthermore, the capture phenomenon, known in Rhabdochona, occurs mainly in the Neotropical region or in Southern Asia. Thus, the origin of the family is probably Gondwanan. Australia being the only area from which they are absent, the origin of the lineage could be the late Cretaceous. Thelaziidae morphological and biological evolution. The 2 sub-

families Oxyspirurinae and Thelaziinae correspond to two different biological evolutionary stages, even though the adults in both cases, live in the same location, the orbital cavity of their hosts. The eggs of the Oxyspirurinae are swallowed, reach the faeces and are ingested by cockroaches in which they complete the usual spirurine life cycle. In the Thelaziinae (at least in the species parasitic in mammals, the life cycle of which is known), the larvae hatch and occur free in the lachrymal fluid. Ingested by sucking flies, they develop in the usual fashion but the infective stages migrate to the mouth parts and are deposited on the eye during feeding by the fly. Thus, their biology is intermediate between the intestinal spirurine life cycle and the tilarioid life cycle. The morphology of the 2 subfamilies also corresponds to 2 different stages. The Oxyspirurinae are primitive (6 lips in the larva, buccal cavity sometimes divided into 2 parts and often armed with teeth, oesophagus divided into 2 parts, pointed tail in both sexes...). In- the Thelaziinae, the primitive pattern of the head papillae is preserved, but the other characters have acquired a filariid-like morphology, i.e. bucccal cavity atrophied, short rounded tail. Host range and geographical distribution. The Oxyspirurinae comprise numerous species parasitic in various birds and is therefore cosmopolitan. The Thelaziinae also comprise several genera parasites of birds but some related species are parasites of mammals (cattle, equids, suids, Camivora, primates). Origin and expansion. The simplified morphology of an adult Thelazia is actually due to the atrophy of complex structures. In Oxyspirura, differentiation of buccal cavity into two parts is primitive. For the Thelaziidae as well as for the Rhabdochonidae, the adaptation to parasitism could have occurred directly from the Cosmocercoidea. The genus Skrjabinelazia (Seuratoidea) may provide indications on this evolutionary process. Skrjabinelaz~a is closely related to ~axvachonia but the

1188

A. G. CHABAUD and 0. BAIN

latter is provided with an oesophageal bulb and therefore is classified in the Cosmocercoidea. Skrjabinelazia, considered for a long time as a member of the Thelaziidae, is actually a Seuratoid and links the Cosmocercoidea with the Spirurida (Chabaud, 1973). Due to the host range, which comprises birds and domestic mammals, the Thelaziidae are cosmopolitan and it is very difficult to determine the date of their origin. Pneumospiruridae

Unlike the Thelaziidae which became adapted to the orbital cavity, the Pneumospiruridae became adapted to the pulmonary system. Thus morphological evolution does not lead to convergence with the filarioid type, but towards the metastrongylid type. The cephalic structures and the sensory apparatus often preserve primitive features, but the cuticle is enclosed in a tegumental sheath and often there is a double gubernaculum. The family has been classified with the lung strongylids by Dougherty (1952) and many other authors. This was possible, since Chitwood did not separate the Strongylida from the AscarididaSpirurida. Although the life cycle remains unknown, the opinion of Gerichter (1948) is convincing and we classify the Pneumospiruridae in the Thelazioidea. The main genus Metathelazia, comprises many species throughout the world. Each one presents various original characters which indicate a relictual group. The host range which comprises insectivores, primates and carnivores confirms the concept of an ancient group dating from the Eocene. SUPERFAMILY

SPIRUROIDEA

Morphological and biological evolution. Chitwood & Wehr (1934) established the phylogenetic value of cephalic structures and sensory apparatus. Chabaud (1959a,b; 1965) classified the families and the genera taking into account a process of gradual involution of the cephalic structures. This classification was verified by a study of the morphogenesis of the buccal structures during larval development by Quentin (1971). These analyses indicate that the Gongylonematidae is the most primitive family. The Spiruridae has a common origin with the Spirocercidae. The aberrant genera such as Physocephalus or Mastophorus can be classified easily since the larval cephalic structures correspond to those of the adults of less specialised genera. The Hartertiidae are separated from the other Spiruroidea because the

larvae have a particular cephalic structure (Quentin, 1971). Host range and geographical distribution. With the exception of Hartertia, the Spiruroidea and the superfamilies considered below do not parasitize the intestines but dwell in the mucosa of the anterior part of the digestive tract. Gongylonema comprises numerous species from birds and mammals, closely related to each other; Paraspirura is the only species parasitic in a reptile (Agamidae from Kenya). Apart from a single species, Spiralatus baeri, which is parasitic in an endemic bird from Madagascar, the SpirocercinaeAscaropsinae group is parasitic in mammals, mainly Carnivora, but also Insectivora, Suidae, Bovidae, rodents, Many distinctive genera of etc. Spirocercinae are parasitic in endemic mammals of South America (Chabaud & Bain, 1981). Hartertiidae are parasitic in birds with a particular genus in Australia; the others occur mainly in African bustards. Origin and expansion. The primitive cephalic structures, particularly in larvae, are similar to those of the Thelazioidea. The cloaca1 papillae of the male often have a distinctive pattern which is found also in the Habronematoidea: 4 precloacal pairs, 2 large postcloacal pairs and 4 very small pairs (plus the phasmids) gathered at the distal part of the tail. This pattern may derive from certain Seuratoid - like nematodes, for example the genus Seuratum. The host range includes no reptiles (with a single exception) or amphibians. Gongylonematidae, the most primitive family, comprises closely related species, parasitic in birds and in mammals. Almost all the species of the more evolved families are parasitic in mammals. We know that the group was present and evolved in South America during the Tertiary. Thus we can hypothesise that the Spiruroidea arose during the late Cretaceous (perhaps from the dinosaurian Thelazioidea) and became diversified in the numerous mammals feeding on coprophagous or detritiphagous insects. SUPERFAMILY

HABRONEMATOIDEA

Hedruridae

The single genus Hedruris is parasitic in amphibians and turtles in Europe, Asia and in North and South America. Like most relict species, there is a coexistence of specialised characters (posterior extremity of the body provided with novel organs of

Evolution of the Spirurida attachment) and primitive characters (cephalic structures). The larval morphology which was described by Petter (197 1) does not clarify the origin of the genus; the undivided oesophagus and the 4 lips are distinct as early as the second stage larva. The lateral labia support the 8 sensory papillae but they are covered by median labia which are hypertrophied in the adult stage. Thus, the origin of the genus remains enigmatic. One may suppose a common ancestor with the Gnathostomatoidea, i.e. related to Seuratoidea of the Echinonema group. Indeed, the important development of the median lips which is characteristic of Hedruris appears to be a secondary acquisition since the cephalic papillae are located on the lateral lips. Thus the classification of the genus amongst the Habronematoidea is doubtful. In any case, the origin of the genus, like that of the Gnathostomatoidea must be very ancient, as early as the Jurassic epoch. Cystidicolidae

The analysis of the Cystidicolidae is difficult because its morphological evolution involves essentially the cephalic structures. In spite of many recent descriptions, these structures remain insufficiently known. Many authors present SEM pictures which can perhaps be interpreted by themselves, but as corresponding drawings are lacking, they remain enigmatic to other investigators. Morphological and biological evolution. The buccal cavity, initially discrete, lengthens progressively and becomes armed through sclerotisation of the walls. The cloaca1 papillae are homogeneous and are of a primitive-type (4 precloacal pairs and 6 postcloacal, more or less regularly disposed along the tail). The papillae multiply in some more evolved genera. However, the cephalic structures appear to give a better indications of the evolution of the family. The evolutionary trend of the cephalic structures (Chabaud, 1958) is characterised by a progressive invagination and atrophy of the submedian labia, and later of the pseudolabia, similar to the process followed by the Habronematinae parasitic in birds and mammals. The morphological analysis and the nomenclature proposed by Ko (1986) for the genus Ascarophis is: “the pseudolabia are continuous medially with anterior extensions of the lateral walls of the buccal cavity. On the anterior surface of each pseudolabium is an elevated structure called a pseudolabial protuberance. The submedian labia each possess a thick-

1189

ened margin. Internal to each submedian labium, there is a flap-like structure with a thickened free margin and which may appear bilobed”. In agreement with Petter (1979~) we suggest the following evolutionary sequence: (1) Head flat, with only the pseudolabia protruding, 4 cephalic papillae, 4 external labial papillae and 4 well developed internal labial papillae: Prospinitectus (see Petter, 1979~). (2) The 4 submedian labia and the 2 pseudolabia create a protruding platform. The 4 cephalic papillae, the 4 external submedian labial papillae and sometimes the internal labial papillae are inserted on the platform: Cristitectus (see Petter, 1970, Quintero, Estevez, Alvarez & Sammertin Duran, 1992). (3) The labial papillae disappear. The submedian labia become reduced: Collarinema and Cyclozone with large pseudolabia and Parascarophis with reduced pseudolabia. (4) The submedian labia become invaginated and form, in the mouth cavity, submedian protuberances, which create a more or less quadrangular mouth opening. These submedian protuberances produce blade-like formations (= sublabia); each one becomes divided into 2 teeth and then into denticles: Ascarophis, Caballeronema, Capillospirura, Spinitectoides, some marine species of Spinitectus such as S. beaveri and S. oviflagellis (see Margolis, 1977, Appy

& Dadswell, 1978, Appy & Anderson, 1982, Petter, 1984, Ko, 1986) (5) The sublabia can be replaced by rod-like median formations: Pseudoproleptus, or by cuticular blade-like formations: Cystidicoloides (see Petter, 1984) (6) The buccal cavity can become sclerotised either partially: Salvelinema (see Margolis & Kabata, 1967) or completely: Metabronema (see Rasheed, 1965) (7) The disappearance of the sublabia leaves an oval mouth opening provided with blades: Sterliadochona, with teeth: Cystidicola, or without teeth: freshwater Spinitectus (see Jilek & Crites, 1982) Host range and geographical distribution. Prospinitectus is parasitic in Scombridae from the Far East, Cristitectus in congers from Europe, Cyclozone in sturgeons from the Caspian Sea, Collarinema in Gadidae from Europe, Parascarophis in Atlantic selacians, Capillospirura in sturgeons from the Ancient and New World, Ascarophis in marine fishes from all over the World, Spinitectus

with stong pseudolabia from freshwater fishes all over the World, Spinitectus with small pseudolabia in marine fishes or in freshwater fishes of marine

1190

A. G. CHABAUD and 0. BAIN

origin, Caballeronema in teleosteans from the Pacific, Spinitectoides in Gadidae from Europe, Pseudoproleptus in freshwater fishes from Africa or IndoMalaysia, Cystidicoloides in freshwater fishes from South America, Salvelinema in swimbladder of Salmonidae, Metabronema in marine fishes from Australia or the Philippines, Sterliadochona in Holarctic freshwater fishes, Cystidicola in the swimbladder of Salmonidae. Origin and expansion. The morphological evolution proposed above does not fit perfectly with the host range. Indeed, the supposedly most primitive forms are not necessarily those which parasitise the most ancient fishes. Amongst the 6 genera classified here as being the most primitive, 4 genera are parasitic in ancient hosts (selacians, sturgeons and congers) but 2 other genera are parasitic in Scombridae and Gadidae which are modern fishes. Furthermore, one may suppose that such ancient parasites have a cosmopolitan distribution. Actually, 2 genera, Ascarophis and Spinitectus, appear to be localised in a restricted area. Apparently, this is not due to lack of data because recent data confirm their previously known geographical distributions. Cystidicolidae have some characters in common with the Rhabdochonidae, which, according to our above hypothesis, date from the late Cretaceous. However, the characteristic hosts of Cystidicolidae appear to be much more ancient, and probably derive from the early Secondary. Furthermore, the passage from freshwater species to marine species, which is a general phenomenon in the Spirurida, cannot be clearly established for the Cystidicolidae. Thus the origin of the Cystidicolidae is uncertain. Their roots are certainly ancient, but the constraints of an heteroxenous life cycle i.e., an extreme dilution in the aquatic environment, may result in the absence of an explosive radiation and the extinction of many lineages. During the centuries, they appear to have conquered, independently, restricted host groups or geographical areas, this process occurring at various dates, some ancient, some modern. Habronematidae Morphological

and biological evolution. Considering the cephalic structures of the larvae, it appears that evolution entails an invagination of the lips into the buccal capsule. Two lineages can be differentiated, one with the invagination on the lateral axis, the other with the invagination on the median axis (Chabaud, 1958). The first lineage begins with the genus Odontospirura and ends with

the genus Draschia. The subfamilies Histiocephaline and Parabronematinae, which are characterised by a more or less complex ornamentation of the posterior border of the lips, used for the fixation of the worm to the mucosa, arose from this lineage at different times. The second lineage begins with the genus Chitwoodspirura and comprises successively the genera Sicarius, Gendrespirura, Excisa, Procyrnea, Cyrnea, Metacyrnea and Habronema. Host range and geographical distribution. In the first lineage, Odontospirura is parasitic in American comprise many genera ratites. Histiocephalinae parasitic in various birds. Parabronematinae are parasitic in elephants from Africa and from Asia, in the okapi and in different ungulates. Draschia is parasitic in equids. In the second lineage, Chitwoodspirura is parasitic in African primates and Gendrespirura in pholidotes from Africa and Asia. The other genera are parasitic in various birds, except for Habronema parasitic in equids. Thus, in this family, a good correlation exists between morphological evolution and the relative antiquity of the hosts. The biology of the species parasitic in equids is remarkable because the infective stages actively leave the mouth parts of the fly vector, leading, according to the interpretation of Chandler, Alicata & Chitwood (1941) and Bain (198 l), to the filarioid type of life cycle. According to Anderson (1957) however, this is a phenomenon of convergence. Origin and expansion. The most primitive cephalic structures in the Habronematidae are similar to those of the Cystidicolidae. Thus the Habronematidae may have arisen from the Cystidicolidae. Odontospirura, the most primitive genus is parasitic in ratites, a relictual group which expanded long before the other birds, probably in the early Tertiary. The expansion of the Habronematidae may have occurred at the same time as that of the birds and mammals during the Tertiary, from ancient mammals such as the pholidotes and primates to the modem mammals such as the equids which are the hosts of the most specialised genera Draschia and Habronema. Tetrameridae Morphological

and biological evolution. The cephalic structures of the Tetrameridae are similar to those of the Habronematidae and the 2 families have close relationships, but the Tetrameridae live in the

Evolution of the Spirurida tissues. The posterior extremity of the body, where the vulva is located, is the only part opening into a hollow organ (digestive tract, urogenital tract). The 3 subfamilies are very different: The females of Tetramerinae live in the glands of Lieberkuehn in the proventriculus of birds; the males live on the surface of the mucosa. The Geopetitiinae live inside peritoneal cysts connected with the digestive tract by a thin peduncle. The Crassicaudinae are parasitic in the urogenital tract or the placenta of cetaceans. The mo~hologi~al evolution of the T~tramerinae is charaeterised by a dilatation of the body of the females. The body, at first is coiled (~~c~~~~~ef~~~. The spirals swell and form an almost closed spiral [M~crotetr~mere~~ and finally are joined together to farm a sphere (T~~r~~eres). The genus ~~cro~#~ei~ cfearly demonstrates a link between the Habronematinae and the Tetramerinae (Quentin & Wertheim, 1975). In the Geopetitiinae (single genus Geopetitia) the body of the female narrows just before the dilated posterior extremity which is inserted into the gut of lumen. The Crassi~udinae have a gigantic body (several metres long) which allows the production of millions of eggs. Host range and geogru~hic~~ ~~str~b~t~o~.The Tetramerinae and the Geopetitiinae have an heteroxenous life cycle and are parasitic mainly in insectivorous birds with apparently little specificity. The Crassicaudinae are parasitic in cetaceans. Due to their host range, the genera are cosmopolitan. Origin and expansion. The origin of the Crassicaudinae should be sought in the Cystidicolidae and the origin of the Tetrameridae and Geopetitiinae in the Habronematidae. The host range includes no relictual animals. ~icroha~e~ia itself is parasitic in Lanius, a modem bird, and does not provide any indication. Thus, the date of the origin of all these forms appears to be impossible to define.

SUPERFAMILY ACUARIOIDEA The Acuarioidea is an exceptionally homogeneous group, consequently its systematics are based almost entirely on the increasing complexity of the cephalic cordons. They could have arisen from ancestors closely related to the Cystidicolidae, in which the pseudolabial protuberance may be the origin of the characteristic pair of lateral teeth. They are parasitic in the gizzard of birds and show a strong tendency towards dweIling in the tissues.

1191

Their most frequent location is between the tunics of the gizzard and they show strong convergence with Habronematinae of birds which share the same location. Thus they are of little interest in this paper. The single example of a phenomenon of capture is provided by the genus ~t~merinema which has invaded insectivorous mammals and except for a cephalic inflation, has no distinctive characteristics. The date of the origin of this superfamily, as well as that of the Tetrameridae, cannot be determined. It is likely to be relatively modern, i.e. the Miocene. SUPERFAMILY DIPL~T~AENO~EA The single family Diplotriaenidae includes 2 subf~ilies, the Dicheilonematinae and Diplotriaeninae. They inhabit the air-sacs of reptiles and birds where they lay thick-she~ed eggs which are eliminated in the faeces. Their life cycle is identical to that of Spiruroidea.

Morphological and biological evolution. Atrophy as a consequence of tissue dwelling is not marked. The cephalic mo~holo~ of the infective stage, with 2 median reliefs, as seen in Serrratospiculzdm tendo, resembles that of primitive adult Spirurids and the infective stage of numerous Spiruroidea (Bain & Vassiliades, 1969). The cephalic armature, which is absent in Ver~terne~, is reduced to weak lateral elevations in Monopeta~onema, and it develops progressively forming lateral epaulettes (Hastospiculum, Dicheilonema). The lateral teeth are very well developed in ~astospi~lum, reduced in Di~heilone~ and they disappear in ~erratos~iculum. The oesopha~s remains very large and divided. The male posterior extremity is of a primitive type (Versternema) or becomes rounded and loses a few postcloacal papillae. Host range and geogra~hieu~ distribution. ~~to~p~~ cuds spp. are fundamen~lly parasites of varanids

in Africa, Asia, and Australia, but are found also in snakes from South America, and less frequently, in other reptiles. The other genera are parasites of birds; Versternema is parasitic in the ostrich, ~onopeta~one~ principally in Halcyonidae, and the other genera are cosmopolitan parasites of large insectivorous birds, One species of Diche~lone~ is parasitic in Struthio, another one in Rhea. Origins and expansion. The hosts of origin seem to be the Ratites because they harbour the most primitive genus ~e~s~erne~ in Africa, and 2 species of

1192

A. G. CHABAUD

Dicheilonema, one in Africa, one in America.

The transfer to the reptiles seems to have occurred once because the parasites of varanids from the Old World are very closely related to those of snakes from the New World. The transfer to the reptiles might have occurred at the time of Gondwana, at the end of the Secondary. Diplotriaeninae Morphological and biological evolution. This sub-

family is very homogeneous and is characterised by the presence of lateral cuticular formations in the form of protrusible trident like structures on either side of anterior end of the oesophagus and opening by pores on either side of oral opening. Only three genera are known: Chabaudiella with tridents simply represented by a pair of lateral cuticularised structures, blade-like at the apex and trilobed at base, Diplotriaena with one pair of lateral trident structures and Quadriplotriaena with 2 pairs of lateral digitiform structures. The male caudal extremity is more evolved than that of Dicheilonematinae; it is short and rounded. The right spicule is initially of simple shape and tends to twist spirally. Host range and geographical distribution. Chabaudiella is parasitic in Passeriformes in South America. Diplotriaena comprises numerous species

in

insectivorous

birds

throughout

the

world.

Quadriplotriaena occurs in various birds from North

America and Russia. Origin and expansion. Larval morphology shows great similarities with the primitive Spiruroidea, which are presumed to lie at the origin of the whole group. Chabaudiella, the most primitive genus, might have derived from forms close to Monopetalonema by the process of invagination of the teeth on the lateral axes, a process continued in Diplotriaena. Quadriplotriaena seems to derive from forms close to Chabaudiella. Whatever the genus, the host list contains only modern vertebrates. Chabaudiella is known from South America where some Monopetalonema are also found. It may be that the Diplotraeninae arose in South America during that Tertiary, but the parasitism in birds which are vagile has allowed their worldwide expansion, despite the isolation of South America during that epoch. SUPERFAMILY

APROCTOIDEA

Morphological and biological evolution. The groups together nematodes markedly altered by their tissue

and 0. BAIN habitat; they are examples of the phenomenon of convergence and are probably polyphyletic. The Desmidocercidae have a well developed buccal cavity with 2 lateral teeth which disappear in Desmidocerca. Spicules are unequal. The Aproctidae includes the Tetracheilonematinae which have 2 pseudo-labia with 4 prominent submedian lobes, bearing a very well developed sensorial apparatus. The first larval stage has a simple pointed tail. The Aproctinae are divided into 2 groups, Pseudaprocta-Lissonema with large cloaca1 papillae, equal spicules, deirids, large eggs, and long first stage larvae with a pointed tail of the Seuratoid type, and the Aprocta group with a few, small cloaca1 papillae, spicules slightly unequal, no deirids, small egg, short larva with a rounded, spiny tail of the Spiruroid type. Only one life cycle is known, that of a species of Aprocta; its infective larva is of the Spirurid type, with a divided oesophagus; the glandular part is atrophied in the adult stage (Quentin et al., 1976). Host range and geographical distribution. The Desmidocercidae are cosmopolitan parasites of fisheating birds. The Tetracheilonematinae are only known in the Tinamidae (South America) and, perhaps, in some African birds. Pseudaprocta is cosmopolitan in Passeriformes. Lissonema is specifically parasitic in birds with “soft feathers” (Berlioz, 1950) as opposed to Aprocta which is parasitic in other groups of birds (Bain & Mawson, 1981). Origin and expansion. The Desmidocercidae have a cephalic structure which seems close to that of the Cystidicolidae, a notion which is in accord with their host range. The Tetracheilonematinae represents a small isolated group, related to Lissonema. The group Pseudaprocta - Lissonema might have arisen directly from the Seuratoidea rather than Aprocta which itself shows affinities with the most primitive Spiruroidea. These different groups of Aproctoidea are parasites of modern birds and might date from the midTertiary. SUPERFAMILY

FILARIOIDEA

The superfamily is characterised by the fact that the female worms lay microfilariae; consequently it has a specialised biology. This evolutionary step seems to have appeared several times. A small group presently placed with these worms lays eggs and has

Evolution of the Spirurida probably a biology of the Spirurid type. In addition, some genera are only sligh~y modified by their tissue inhabiting life whereas others have undergone a generalised atrophy of body structures except those of the genital apparatus. These factors give rise to heterogeneity within the superfamily. Filariidae Morphological and biological evolution. The genera Filaria and Suifilaria have a long divided oesophagus and lay eggs. The genera Pseudafilaria, Parafilaria and Stephano~laria have a short undivided oesophagus and lay microfilariae. Pseudo~~aria has 6 internal

labial papillae; they are transfo~ed into cuticular points in the infective larva of Stephano~lar~a and Para~laria or into blades in adult Para$laria. In Stephanofilaria, all papillae may be transformed into spines and may multiply to form crowns (Boomker, Bain, Chabaud & Krick, in press). The cuticle of the primitive forms have striae of the Thelazia type which become elaborated with spines (Stephano$laria) or bosses (Parafilaria). Host range and geographical distribution. Pilaria

and Suz~laria are parasites of primitive rodents (Hystrix, Pedetes), Tub~identates, Hyracoidea, Suidae and Bovidae in Africa, of Carnivora in Africa, the Holarctic and Neotropical regions; Pseudofilaria is parasitic in Bovidae and Giraffidae in Africa, Parafilaria is a parasite of the domestic horse and of Bovidae in Europe, Asia and Africa, and of elephants in Asia. Stephanofilaria is parasite of domestic Bovidae, elephants in Asia, hippopotamus and rhinoceros in Africa. Origin and expansion. The genus Filaria is a typical Spiruroidea and it is unfortunate but irreversible, that the Filarioidea is named after it. Its hosts indicate an origin during the Eocene in Africa, with more recent captures from species parasitic in Carnivora. The other three genera as a whole are linked to the Ungulates, and more precisely to the ancient ones (elephants, rhinoceros, giraffe, hippopotamus). They seem to date from the Oligocene or Miocene, presumably in Africa. The morphology of the primitive forms presents analogies with the actual Thelaziinae; they might have a common origin. Onchocercidae

The morphology of the third stage larva of the Oncho~er~idae appears to be very consistent: head round, not ornamented, buccal capsule present, flattened laterally, oesophagus with differentiated glan-

1193

dular portion, female genital p~ordi~ in the anterior half of the body. All the groups seem to originate from the Spirurina (Spi~oidea or Habronematoidea, or a common ancestor); nevertheless the extent of convergence in the Onchocercidae makes analysis particularly uncertain and transmission by means of a microfilaria may have occurred several times and at several periods. Due to the great impoverishment of morphology in the family, it is not possible to present hypotheses on the precise origin of each group, contrary to what has been done previously. In particular, the groups in which the filariae from birds are abundant are not analysed, although very important data have been added recently (Bartlett & Greiner, 1986; Bartlett & Anderson, 1990). The capacity of dispersion for these hosts and the absence of fossils make hypotheses on evolution even more precarious than with filariae from terrestrial vertebrates. To present a view on onchocercid evolution, it appeared advisable to select some groups which seem to date from different periods, such as one very ancient group (Oswaldofilariinae), one group of which the origin is ancient and the expansion occurred during the Tertiary (~ipetalonema fine), and 2 modern groups (Setariinae, genus ~chocerca). (1) ~waldo~ariinae:

This subfamily includes 7 genera parasitic in reptiles. Life cycles occur in culicids (1 cycle completed in India, 4 in South America). Third stage larvae have a long tail and 2 caudal lappets. Morphological and biological evolution. The subfamily is characterised by the vulva opening posterior to the oesophagus though this may migrate in some species to the posterior end of the body (Sola~~aria, Gonojilaria). As usual in the Filarioidea, morpholo~cal evolution is regressive: the oesophagus is long (Os~aZdo~laria) and becomes shorter (Be~Iar~a, Piratuba), the buccal capsule is large (Oswa~do~~aria) and becomes less conspicuous (Conispiculum), deirids are present (Oswaldo$Zaria) and later atrophied. The caudal papillae, composed initially of 10 or 9 pairs (Oswaldofilaria of crocodiles and Iguanidae) tend to multiply (Oswaldojilaria from Teiidae and Scincidae) and to be arranged irregularly (Piratuba, Conispiculum) . A particular change is shown by the female and male copulatory organs: the vagina is complex and spicules unequal and dissimilar in different species including the primitive Oswa~do~laria; the vagina is simple and spicules similar in the evolved Conisp~~u~um and Piratubu; intermediary forms are represented by Piratuboides.

1194

A. G. CHABAUD and 0. BAIN

Host range and geographical distribution. Oswaldo~~ur~ is parasitic in crocodiles from South

America and Africa, Lacertilians (I~anidae, Teiidae, Scincidae) from South America and Agamidae from Australia. The genus EeJlaria, close to the former, is found in Gekkonidae from Africa and Madagascar, and Iguanidae in the West Indies. Piratuboides is known in Scincidae in the Neotropical region and Varanidae in the Australian region. SolaJlaria is parasitic in Gerrhosauridae from Madagascar, Conispiculum and Gonojilaria in Agamidae from Asia, Piratuba in Iguanidae and Teiidae from South America. Origm and exp~sion. The genus Oswaldo~~aria is the most primitive morphologically and it presents a Gondwanan distribution with 5 Neotropical species, 4 Australian species and 1 Ethiopian species. The 2 species of OswaldojZaria parasitic in crocodiles, 1 from South America, the other from Africa, are closely related, but they are not different morphologically from the species in Saurians. Thus, the genus might have appeared when Gondwana was not yet divided and the Saurians had already diversified, dated by Renous (1982), during the late Jurassic. Piratuboides and Befiaria are each present in remote regions and could have appeared at the same time. The 4 other genera are endemic to a geographical region derived from Gondwana, showing that their evolution occurred after the break-up of this continent (Bain, Kouyate & Baker, 1982). No new region, particularly the Asiatic region, has been invaded; this seems to indicate that the possibility of expansion by the subfamily was rapidly extinguished. (2) Dipetalonema group: Morphological and biological evolution. The oesophagus and buccal capsule are initially well developed and tend to be reduced, as observed generally in Filarioidea. Life cycles occur in a variety of haematophagous arthropods. Bain, Baker & Chabaud (1982) distinguished 4 lineages, based on morphology; they each contain primitive and evolved forms. (1) An Australian lineage which has an area rugosu made of small cuticular longitudinal rods irregularly arranged (not transverse rows as in the 3 other lineages). The thick spicules are unequal (Breinlia) and become equal by the shortening of the left spicule (Johnstonema). The caudal papillae tend to gather on the median ventral line. (2) A South American lineage with 2 caudal lappets in both sexes, sheathed microfilariae, oesophagus clearly divided and buccal capsule well cuticularised, made of three segments in the relictual

species Sk~abino~laria. Except in this species, the cephalic plate is stretched laterally, the gnbernaculum is present. The spicules evolve: in ~asypa~laria the blade of the left spicule is reduced; in Dipetalonema s. s., the blade of the left spicule lengthens and the spicular ratio increases; in parallel, the vagina becomes more complex (Bain, Diagne & Muller, 1989). (3) A Mansonella branch (named the Tetrapetalonema branch before the description of Mansonella ozzardi was completed by Orihel & Eberhard, 1982): This branch is characterised by a slender undivided oesophagus and 4 caudal lappets in the adult and infective stages. A tubular buccal capsule is found in one species (S~dnema sum& it is atrophied in the other species. The right spicule is spoon-shaped (Sandnema, Tupainema); the blade becomes flattened and spatulated (several species of the sub-genera Esslingeria in African primates, in Caviomorpha, and Tetrapetalonema, such as T. panamensis (see Esslinger, 1979)), and later looks filiform (several Tetrapetalonema and Esslingeria species of primates); in M. (M.) ozzardi and allied species the right spicule has a subterminal heel. The left spicule is twice as long as the right spicule [M. (T.) panamensis and closely related species] and becomes thread-like, and the spicular ratio increases (species from African and South American Primates, Filarissima). Microtiariae are rather thick and settle in the small cutaneous lymphatics of blood vessels (E. streptocerca, T. panamensis and allied species, cf. Hawking, 1973; Petit, 1985) and become slender and circulate in the blood system (other species). The terminal caudal papillae tend to be atrophied and the caudal lappets unite. The cuticle and the epitheliomuscular sheath become more complex, essentially to help the male’ and female worms to grasp during mating (Bain & Chabaud, 1988); body swellings appear in the anterior region, made by giant coelomocytes, and the body is flattened dorso-ventrally. (4) An Acanthocheilonema branch which does not have the characters of the above lineages: The right spicule is spoon-shaped (Acanthocheilonema, Macdonaldius) and becomes cone-shaped (Molinema) or develops a subterminal heel (Ackertia, Monanema, Cercopithifilaria). The left spicule has a handle and a blade which remain distinct but the blade becomes elaborate (CercopithtjiZaria, Monanema, etc.). As in Mansonellu, body-swellings appear in the more evolved species but they are formed with some hy~rtrophi~ muscles (Cercop~th~~~aria). Host range and geographical distribution. One genus, Macdonaldius, is parasitic in Lacertilians and

Evolution of the Spirurida snakes from South America. All other genera are found in the principal groups of mammals. Lineage 1 is parasitic in marsupials in the Australian region, in a lemurid, Muridae and Sciuridae in the Oriental region. Lineage 2 is present in South American marsupials, Xenartha and Primates. Lineage 3 is parasitic in Insectivora, Tupaiidae and primates in the Oriental region, Ursidae in the Palaearctic region, Anthropoid primates and humans in the Ethiopian region, of primates, including humans, Carnivora, Caviomorpha and Sciuridae in Neotropical region. Lineage 4 is parasitic in Insectivora, Carnivora, rodents (Hystricidae and Muridae), Bovidae in the Ethiopian region, marsupials and Muridae in Australia, pholidotes and Sciuridae in the Oriental region, Carnivora (Canidae, Ursidae) and Cervidae in the Palaearctic region. Origin and expansion. The group Dipetalonema is of a very ancient origin; it arose during the epoch of Gondwana with the marsupials and Insectivora and extended after its break-up giving rise to 4 principal lineages. (a) An Australian lineage parasitic in marsupials and represented by Breinlia (group B of Spratt & Varughese, 1975) and the derived genus Johnstonema. Breinlia migrated secondarily into the Oriental region where species are parasitic in heterogeneous forest mammals: a lemurid, several Rat&s spp. and sciurids. (b) A paleo-endemic South American lineage represented by the relict genera Skrjabinofilaria, and possibly Cherylia, in marsupials, by Orihelia and Dasypajilaria in Xenartha. We suppose that these genera belong to the primitive Gondwana fauna which has been conserved in South America due to its isolation as early as the Late Cretaceous (as it was for Breinlia in Australia). Dipetalonema s s. derives from these paleo-neotropical forms (similarities are particularly evident with the parasites of Xenartha) but is specific to the South American Platyrhinians; it arose and diversified when primates arrived from Africa during the late Eocene (Hoffstetter, 1981), offering a wide range of new niches. (c) An Acanthocheilonema lineage which seems to have its origin in Africa in the Insectivora and Carnivora during the late Paleocene, with the most primitive genus Acanthocheilonema. It later invaded the Oriental and Holarctic regions, and very recently South America, with some captures in endemic marsupials (A. pricei in Didelphis). Molinema, Ackertia, and possibly Cruortjilaria on the one hand, Yatesia on the other hand, might be forms of

1195

African origin introduced at the end of Eocene during the migration of the African rodents (Phiomorpha) into South America (Hoffstetter, 1981; Durette-Desset, 1971; Quentin, 1973). Macdonaldius in American reptiles is interpreted as a capture which could have occurred during that period. Cercopithifilaria derives rather clearly from Acanthocheilonema; it is the most evolved form of the lineage (greatly reduced buccal cavity even in the infective larva). Its biology is characteristic, with dermal microfilariae and transmission by hard-ticks. CercopithiJilaria exhibits, according to our interpretation, a unique means of expansion because, it is the opposite to the norm in the nematode parasite of vertebrates. It seems to depend upon the vector and not the definitive host. The survival of hard-ticks, the great capacity for passive transportation, the life cycle with several hosts, make them the ideal “reservoirs de virus”; this has resulted in a great expansion by the nematodes which utilise them and is demonstrated by the “zoologically incoherent” host range. The genus is found in the Ethiopian region in Carnivora, Primates, Hystricidae and Bovidae, in the Palaearctic region in Cervidae, dogs and bears (C. japonica) (see Uni, 1983)) in North America in Lagomorpha, in South America in dogs, marsupials (C. didelphis) and Dasypodidae (the species venezuelensis with dermal microfilariae for which the genus Strianema Eberhard, Orihel Jc Campo-Aasen, 1993 was erected is a representative of Cercopithzjilaria), in Australia in Muridae and marsupials (C. johnstoni), and probably in Asia in Sciuridae (C. laemmleri).

(d) The Mansonella lineage. Sandnema sunci, the sole species of the lineage which has a buccal capsule and of which the spicules are not very different from those in Acanthocheilonema supports the hypothesis of a common ancestor, at the epoch of Gondwana. Nevertheless the branch Mansonella might have evolved separately, because the infective stage is particular with four caudal lappets. It seems to have arisen in the Oriental region from forms parasitic in Insectivora, of which S. sunci in Soricoidea in Asia is a good example, and to have developed in the Insectivora and primates: S. digitata is recorded from a monkey and Tupainema from Tupaidae (cf Eberhard & Orihel, 1984). Later the lineage diversified in the African primates (of which only the species of Esslingeria from Anthropoids remain), and migrated into South America at the end of Eocene in the same time as the hosts, (the monkeys) and the Caviomorpha. In South America, primitive forms with spatulated right spicules are found in

1196

A. G. CHABAUD and 0. BAIN

these two groups of hosts (such as T. panamensis and Campo-Aasen & Orihel, 1984, respectively) and evolved forms with an elongated filiform right spicule - such as M. (T.). marmosetae and Filarissima, respectively. A small lineage having the right spicule with a subterminal heel, Mansonella s. s., had adapted to various hosts, Carnivora, Sciuridae and humans. M. akitensis Uni, 1983 from the black bear might belong to this line. It is to be noted that the South American fauna is particularly complex: post-Eocene faunas originating from Africa have been added to the ancient endemic fauna, and more recently Pleistocene faunas arrived from North America. At each period, numerous captures occurred in various mammals even in the most ancient ones, the didelphid marsupials. (3) Setariinae: Morphological and biological evolution. The buccal capsule has a well developed anterior segment but it is not salient (Papillosetaria). The development of peribuccal cuticular ring occurs in Setaria thomasi, S. congolensis, S. javensis from Tragulidae and Suidae, becoming complex in Setaria from Bovidae, Cervidae and Equidae. Deirids are present, with specific shapes. The body is extremely long in S. E. rotundicapita Eberhard,

loveridgei. Host range and geographical distribution. Papillosetaria is parasitic in Tragulidae from SouthEast Asia; Setaria is found in diverse Ungulates,

Suidae, Tragulidae in Asia and Africa, Bovidae in Africa, Asia and in the Holarctic region, in Cervidae in the Holarctic region and in South America, with one species in African and domestic Equidae, and one in Procaviidae from Africa. Origin and expansion. If Papillosetaria can be interpreted as an ancestral form of Setaria (see Bain & Shoho, 1978), one notes that the most primitive species are parasitic in 2 groups of very primitive Ungulates, the Suidae and Tragulidae, whose affinities were recognised long ago. As the majority of the primitive species are found in Asia, the subfamily probably diversified in the Oriental region. Some particularities of the infective larva (thick body) and larval development (multiplication of the glandular cells of the oesophagus, as observed in S. labiato-papillosa) resemble features found in habronematids, and it was suggested that the Setariinae should form a small lineage separating from the habronematids later than the other Onchocercidae (Bain, 198 la). Another hypothesis has also to be considered since an archaic filaria from Bradypodidae, Chabjilaria,

presents morphological similarities with Setaria (vulva very anterior, large oesophagus, same type of area rugosa, left spicule very complex as in S. equina, see Bain, Purnomo & Dedet, 1983). The Setariinae could have originated much earlier, in the period of Gondwana, and in ancient hosts, with filarial forms resembling those currently present in Xenartha. More generally, the Neotropical filarial fauna contains forms which represent the diverse groups of the Onchocercidae; these might have originated during the Gondwanan period, their ancestors having disappeared except in the South American region because it was isolated during most of the Tertiary. (4) Onchocerca: The genus includes 28 species (Bain, Wahl & Renz, 1993). Morphological and biological evolution. The most instructive character is given by the caudal papillae; a perfect spirurid plan is shown by 0. raillieti with 10 pairs of which 4 are precloacal, 2 are postcloacal, and the 4 last constitute a subterminal group. In the other species a regression of the precloacal papillae is observed (0. gutturosa) and their grouping close to the cloaca (0. volvulus), the transformation of some subterminal papillae into cuticular points (0. dukei, 0. ochengi, 0. tarsicola, 0. gutturosa) and later their reduction in number (0. jakutensis). Sometimes the terminal papillae migrate towards the cloaca (0. armillata, 0. reticulata). The oesophagus is divided (Onchocerca from Equids, 0. Jiexuosa, 0. armillata, etc), and later the glandular part is reduced (0. ramachandrini, 0. dewittei, etc). The vulva is situated at about the end of the muscular oesophagus, where the female genital primordium occurs in the infective larva (0. raillieti and other Onchocerca from Equids, 0. flexuosa, 0. armillata). The vulva then migrates further from the head (0. tarsicola, 0. jakutensis and 0. garmsi from Cervidae). In addition, the genus Onchocerca exhibits one distinctive feature which is the complexity of the female cuticle; these very long and thin worms, which often inhabit tissues where pressure is important (tendons and ligaments) must have a very resistant flexible cuticle. The cuticle is striated (0. cervipedis) but, in most species, it differentiates into 2 layers, a mid layer which is divided transversely by “striae” and an external layer which is regularly thickened by transverse half rings (“ridges”); these are rectilinear and become contorted. The epitheliomuscular sheath undergoes a particular development; the lateral chords are narrow and muscles well developed (most of the Onchocerca species) but the chords may become hypertrophied, playing the role of storage organs, and muscular fields become atro-

1197

Evolution of the Spirurida phied (0. volvulu~, 0. oehengi, 0. gibsoni, etc.) (Bain, 1981b). Host range and geogruphicaz distribution. Only one species is parasitic in humans. All the others are parasites of Ungulates: wild Equidae and domestic horse, Suidae and Camelidae, Bovidae and Cervidae. Origin and expansion. The evolution of the genus Onchocerca is particular because the geographical

distribution of the parasites seems more important than the zoological relationships of the hosts. For example the Suidae and the Camelidae, the modem repre~ntatives of which appeared long before those of the Equidae, do not harbour the most primitive Onchocerca species. In the Holarctic region, several species parasitic in Bovidae and Cervidae are closely related. In Africa, one distinguishes 2 lines in wild Bovidae, one rather primitive in forested regions, and one evolved line in the savanna region, this being the nodular line from which the human parasite, 0. volvulus, was derived by capture. The origin of the genus and its principal evolution might have taken place in Africa where the most primitive species (0. r~~i~iet~ and the greatest number of species, belonging to varying groups, are represented. This evolution seems to have occurred during a recent epoch, may be when the Equidae reached Africa, during the early Pleistocene. SUMMARY AND CONCLUSION The order Spirurida includes nematodes which are morphologically and biologically homogeneous, but

whose origins appear to be quite heterogeneous. The adaptation of the free living Rhabditi~ to parasitism in vertebrates may have occurred on different occasions. Parasitism by some species of Cyhndrocorporidae or Cephalobidae (see Anderson & Bain, 1982) is apparently very recent. Nevertheless the Ascaridida-Spirurida group is so homogeneous that it appears to have originated from a few lineages (perhaps a single lineage) which became adapted, a long time ago, to parasitism in vertebrates. In the primitive species of this lineage, the most distinctive and the most constant character is the pattern of the cloaca1 papillae, the pairs 148 being lateral and the other pairs ventral. Thus, the ancestors may be related to genera such as Cephaloboide~ {see Chabaud & Petter, 1961) which were at the origin of the Cosmocercoidea, then the Seuratoidea, and later different groups of Spirurida (Chabaud, Campana-Rouget & Brygoo, 1959; Inglis, 1967). In the above analysis we have attempted to determine the origin of the 12 superfamilies representing the Spirurida. The Chitwoodchabaudiidae could be at the origin of (a) The Dracunculoidea as early as the Triasic or the Jurassic (~icrop~euru) in the crocodiles and the turtles. (b) The Procamallanidae at the Iate Cretaceous (Procamall~~~s in African Ostariophysy). (c) The Camallanidae, from the Procamallanidae, at the early Tertiary (Procamallanus) in the IndoMalaysian siluriforms. The Schneidernematidae could be at the origin of (a) The Rictularioidea. A relictual species

DRACUNCULOIDEA I

I

cH~~~~A~~~ CAMALLANOIDEA

SCHNEIDERNEMATIDAE -

COSMOCERCOllXA-

RICTULARIOIDEA

SEURAT&A GNATHOSTOMATOIDEA / EcmNo-A\n”AE \

PHY SALOPTEROlDEA

/ SEURATIDAE \ SEURATINAE-

THELZIOIDEA ~RO~TO~~ SP~~O~EA ACUARIOIDEA

Fig. 1. Hierarchical relationships of Spirurid families and superfamilies indicating hypothesised phylogenetic relationships.

1198

A. G. CHABAUD and 0. BAIN

(~eniju~ in an American marsupial) could indicate an origin as early as the late Secondary, but the expansion of the group occurred later in the Oligocene from the North of the holarctic area (Paucipectines and Rictularia in ancient rodents such as the Sciuridae and Gliridae). The Seuratidae-Echinonematinae could be at the origin of (a) The Gnathostomatoidea in the Secondary (EchinocephaIus in selacians, Tanqua in Gondwanan reptiles). (b) The Physalopteroidea, from the Gnathostomatoidea, perhaps in the Jurassic (Prolept~ in selacians) and later in the Tertiary, but from more primitive forms (~hu~unuea in modem reptiles). The Seuratidae-Seuratinae could be at the origin of (a) The Thelazioidea with 3 distinct groups: (i) The Rhabdochonidae, perhaps descending directly from the Cosmocercoidea, could have arisen in freshwater fishes, in Gondwana, in the late Cretaceous; (ii) the Pneumospiruridae, from thelaziid-like ancestors, parasitise the most primitive mammals from the Eocene; (iii) the Thelaziidae are relatively recent. They are known only from modern birds and mammals. Several groups appear to have arisen from a Seuratoid which could be more ancient. It is supposed that they arose in now extinct groups. Living forms such as the genera Skrjabinelazia (Seuratoidea) and Maxvachoniu (Cosmocercoidea) give indications of these ancestors. (b) The Habronematoidea are equally diversified: (i) The Hedruridae represent a small relictual group parasitic in amphibians and turtles, the origins of which probably date from the Secondary. They could have an ancient link with the Gnathostomatoidea instead of with the ~abronematoidea; (ii) the Cystidicolidae may have a common origin with the Rhabdoehonidae but appear to be more ancient since many of their hosts are archaic fishes. Freshwater fishes were probably the first hosts but presently they are known mainly from marine fishes. They may have originated at the beginning of the Secondary and pursued their evolution during the Tertiary; (iii) the Habronematidae originated from some Seuratoid ancestor at the beginning of the Tertiary as is shown by the genus ~dontosp~ru~a, parasitic in a ratite; (iv) the Tetrameridae have originated from the Habronematoidea at the mid-Tertiary. (c) The Spiruroidea appearing at the late

Cretaceous (Palusp~~ura), became diversified in birds and mammals during the Tertiary epoch. (d) The Acuarioidea, a relatively modem group, evolved in birds. The filarioid worms seem also to have various origins. (e) Diplotriaenoidea became separated from the Spiruroidea, the ancient forms are parasitic in ratites and date from the beginning of the Tertiary; they evolved later in other birds. (f) Aproctoidea: the Desmidocercinae may be derived from the Cystidicolinae. Pseudaprocta Lissonema with the Tetracheilonematinae might be derived directly from the Seuratoidea, while Aprocta might be derived from the primitive Spiruroidea. The whole of the Aproctoidea is relatively modern. (g) Filarioidea: in Filariidae the genus F&via is a true Spiruroid and might have arisen during the Eocene in Africa. The other genera have originated from Thelazioidea and date from the Oligocene-Miocene in Africa. In the Onchocercidae, all the groups seem to have originated from the Spirurina (Spiruroidea or Habronematoidea or a common ancestor), but transmission by microfilaria seems to have evolved on various occasions and at several periods. The selected examples show that their origin may be very ancient because many groups present a Gondwanan dist~bution, but their evolution has continued during the Tertiary in mammals and birds. Thus these analyses indicate that the Spirurida originated from various groups of Seuratoidea or perhaps sometimes from their ancestors the Cosmocercoidea, i.e. from Ascaridida. Frequently, this adaptive evolution occurred during an ancient epoch, during the Secondary or the early Tertiary and the expansion occurred by successive captures, the nematode becoming adapted to new hosts as new niches became vacant. These captures were often accompanied by important morphological and biological modifications, which in each branch, occurred in a rather uniform manner. A remarkable peculiarity of most of the Spirurida is their strong organotropism: they tend to leave the digestive tract to invade the tissues. The tissue dwelling parasites are often more primitive than those living in the gut. We think that in the Aphasmidians, or in the Coccidia, this tissue dwelling biology is actually primitive. On the contrary, for the Phasmidians, we suppose that the tissue parasites, living in a more stable environment, and sheltered from competition can be transmitted without further evolution inside their hosts.

Evolution of the Spirurida The timing of this revue is opportune because the information obtained using classical zoological approach will soon be tested with data obtained by modern techniques. We have tried to expose the affinities and the mode of expansion of each group with a degree of precision which is obviously excessive for animals with no available fossil record. This arrogance barely conceals our uncertainties, but appears to us more useful than prudence. Jeanne1 (1942), on the basis of Coleopteran setae, was correct in supporting the theory of continental drift when geophysicists fiercely opposed it. Without pretending to a similar prophetic acuteness, we are at least encouraged to trust morphological data. Acknowledgements-We

are very grateful to Professor Irene Landau and to Dr Ian Beveridge for the revision and the translation of the manuscript. REFERENCES Adamson M. L., Deets G. B. & Bentz G. W. 1987. Description of male and redescription of female Phlyctainophora squali Mudry and Dailey, 1969 (Nematoda: Dracunculoidea) from elasmobranchs. Canadian Journal of Zoology 65: 3006-3010.

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Anderson R. C. 1957. The life cycles of dipetalonematid nematodes (Filarioidea: Dipetalonematidae): the problem of their evolution. Journal of Helminthology 31: 203-224. Anderson R. C. & Bain 0. 1982. Keys to genera of the superfamilies Rhaditoidea, Dioctophymatoidea, Trichinelloidea and Muspiceoidea. In: Commonwealth Institute of Helminthology Keys to the Nematode Parasites of Vertebrates, No. 9 (Edited by Anderson R. C.,

Chabaud A. G. & Wilhnott S.). pp. l-26 Commonwealth Agricultural.Bureaux, Famham Royal, U.K. Anderson R. C. 1992. Nematode Parasites of Vertebrates. Their Development and Transmission C.A.B. International. Wallingford, U.K. Appy R. G. & Dadswell M. J. 1978. Parasites of Acipenser brevirostrum LeSueur and Acipenser oxorhynchus Mitchill (Osteichthyes: Acipenseridae) in the Saint John River Estuary, N. B., with a description of Caballeronema pseudoargumentosus sp.n. (Nematoda: Spirurida). Canadian Journal of Zoology 56: 1382-1391. Appy R. G. & Anderson R. C. 1982. The genus Capillospirura Skrjabin, 1924 (Nematoda: Cystidicolidae) of Sturgeons. Canadian Journal of Zoology 60: 194202.

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Ichthyoflaria

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