The origins and evolutionary expansion of the Strongylida (Nematoda)

THE EVOLUTIONARY EXPANSION OF PARASITES

The Nematodes

InrerwrionaI

Pergamon

Journalfor

Para.simlogy,

Vol. 24. No. 8, pp. 1139-l 165, 1994 Australian Society for Parasitology Elsevier Science Ltd Printed in Great Britain 0020-7519194 $7.00 + 0.00

0020-7519(94)00130-8

THE ORIGINS AND EVOLUTIONARY EXPANSION STRONGYLIDA (NEMATODA) M.-C. DURETTE-DESSET,*

I. BEVERIDGE?

OF THE

and D.M. SPRATTJ

*Laboratoire de Biologie Parasitaire, Protistologie, Helminthologie MusCum National d’Histoire Naturelle, Paris, France tDepartment of Veterinary Science, University of Melbourne, Parkville, Victoria, Australia $C.S.I.R.O., Division of Wildlife and Ecology, Canberra, ACT., Australia Abstract-Durette-Desset M.-C., Beveridge I. & Spratt D.M. 1994. The origins and evolutionary expansion of the Strongylida (Nematoda). InternationalJournalfor Parasitology24: 1139-l 165. The Strongylida are thought to have arisen from free-living rhabditoid nematodes, but the relationships between the major groupings within the Strongylida, the Strongylina, the Metastrongylina, Trichostrongylina and the Ancylostomatina are far from clear in spite of the abundance of morphological data now available for analysis. Evolutionary mechanisms including co-evolution, host switching, host dispersal, use of intermediate hosts, various sites of localisation within the definitive host and modifications of life-cycle strategies appear to have been utilised in the expansion of the Strongylida, with different mechanisms predominating in different families or superfamilies. Co-evolution appears to have been a major mode of evolution in the Strongylina, in contrast to the Trichostrongylina. which have used host dispersal and host-switching to great advantage. The phylogeny of the Ancylostomatina shows little association with host evolution, but does match the feeding preferences of the hosts. The Metastrongylina have utilised intermediate hosts and life cycle modifications including a shift to extra-intestinal sites as major means of diversification, in contrast to the other sub-orders. The review, while indicating much progress in our understanding of the phylogeny of the Strongylida, also reveals that enormous gaps still exist, and emphasises the tentative nature of many of the phylogenetic hypotheses tendered to date. INDEX KEY WORDS: Strongylida; phylogeny; evolution.

INTRODUCTION

The Strongylida or bursate nematodes represent one of the major radiations of the nematode parasites of vertebrates. Originating as terrestrial free-living forms, they invaded amphibians, possibly as early as 350 million years ago since this is when amphibians first appeared, and have subsequently evolved to parasitise reptiles, birds and mammals (including man) on all continents of the globe. This expansion has been based on the exploitation of numerous alternative life history strategies, remarkable morphological divers& cation on an essentially simple body plan, has utilised coevolutionary mechanisms as well as host-switching and has been influenced also by patterns of host dispersal. The contributions of these basic mechanisms of parasite evolution are examined below in an attempt to account for the diversification of this extraordinarily successful group of nematodes. ORIGINS OF THE STRONGYLIDA There is little dispute that the parasitic nematode

order Strongylida evolved from terrestrial free-living ancestors related to contemporary rhabditids, as

indicated by the morphology of the stoma and oesophagus, the life-cycle stages and the rays of the copulatory bursa of male strongylid nematodes which are unquestionably homologous with the caudal papillae of male rhabditids (Osche, 1958; Chabaud, Pulyaert, Bain, Petter & Durette-Desset 1970). Indeed, as Dougherty (1951a) observed, there is “a complete intergradation from accidental to obligate parasitism in the basically free-living families of rhabditoids.” How parasitism evolved and how the mijor groups within the Strongylida developed is however still a matter for speculation. The origins of parasitism appear to lie with the ability of larval nematodes to penetrate the skin of a host as oral routes of infection are probably secondary developments (Dougherty, 1951a; Chabaud, 1955; Durette-Desset, 1985; Adamson, 1986). In support of this hypothesis may be cited the existence of genera such as Micronema which are free-living rhabditids and which occasionally penetrate the skin of vertebrates to cause disease, while numerous parasitic rhabdiasoid nematodes (Rhabdias, Strongyloides) penetrate the skin of their vertebrate hosts yet

1139

1140

M.-C. DURETTE-DESSET et al.

maintain free-living generations, demonstrating a curious, even aberrant transitional stage in the evolution to obligate parasitism in vertebrates. The principal super-families within the order Strongylida are the Strongyloidea, Trichostrongyloidea, Metastrongyloidea, Ancylostomatoidea and Diaphanocephaloidea (Chabaud, 1974). Recently, Durette-Desset & Chabaud (1993) have elevated 4 of these super-families to subordinal status in order to clarify evolutionary relationships within the Trichostrongylina, now composed of 3 super-families, Trichostrongyloidea, Molineoidea and Heligmosomoidea. They also recognised the Strongylina, Metastrongylina and Ancylostomatina, the latter including the Ancylostomatoidea and Diaphanocephaloidea. The most recent system has been adopted here (Table 1). RELATIONSHIPS BETWEEN SUB-ORDERS There is now general agreement that the Metastrongylina, which are restricted to mammals, probably evolved from ancestors within the Trichostrongylina, though the precise evolutionary pathway remains undetermined. By contrast, relationships between the Trichostrongylina and other sub-orders are less clear. Relationships between suborders and super-families have been based primarily on the buccal capsule, which is considered to be atrophied in the Trichostrongylina (see DuretteDesset, 1985) and enlarged in the Strongylina and Ancylostomina, and on the female genital system which is primitively amphidelphic (Dougherty, 1951a). Several authors have provided an overview of relationships within the Strongylida but the most detailed are those of Dougherty (1951b) and Schulz (1951) and are summarised by Skrjabin, Shikhobalova, Schulz, Popova, Boev & Delyamure (1952). A principal criticism of Schulz’s system (1951) has been its apparent reliance on the group of hosts rather than the morphological features of the nematodes (Chabaud, 1965) although this criticism can also be applied in some measure to Dougherty’s work. Dougherty (1951a) for example concluded that the Strongyloidea arose from the Cloacininae, because the latter nematodes allegedly possess 6 lips, (though in fact very few do), and because they parasitise marsupials. They were it seems therefore primitive. He also suggested (1949) that the Metastrongyloidea arose from the Cloacininae via the lung worm genus Heterostrongylus in didelphoid marsupials. In these instances, the assumed primitive nature of the host appears to have determined the phylogenetic position given to the nematodes.

Recently, morphological structures used to infer phylogeny such as the buccal capsule, the female reproductive system, the male reproductive system and the pattern of bursal rays have been described and analysed in considerable detail (see Durette-Desset, 1985; Lichtenfels, 1980a,b for reviews) and Lichtenfels (1979) tabulated the principal features of each superfamily. No attempt appears to have been made to utilise the new data in a re-evaluation of relationships of the sub-orders within the order Strongylida, and no attempt has been made to investigate whether cladistic methods, which appeared after the publications of Dougherty (1951a) and Schultz (1951), help to clarify their phylogenetic relationships. The establishment of a suitable out-group for cladistic analysis is relatively simple, with the free living rhabditid nematodes being the obvious choice. In fact, Dougherty (195 la) analysed several morphological features of the Strongylida in relation to a presumed rhabditoid ancestor but did not do so in a systematic fashion. Using the Rhabditida as an outgroup it is possible to make critical comments on the use of morphological features in past systems and to suggest which ones might elucidate the phylogenetic relationships between the sub-orders. However, a detailed cladistic analysis of the relationships of the suborders is beyond the scope of this paper. If cladistic methods are applied to the new data, using the rhabditids as out-groups, then it is apparent that relatively few synapomorphies exist (Table 2) and that some features used to align sub-orders in the past are plesiomorphic, and therefore invalid. Buccal capsule

The buccal capsules present in the trichostrongylin families Herpetostrongylidae, Ornithostrongylidae and Amphibiophilidae, all arising close to the base of the trichostrongylin phylogenetic tree (see Durette-Desset, 1983) can be considered primitive or plesiomorphic since they most closely resemble the form found in parasitic rhabditoids such as Eutomelas Travassos, 1930, including the presence of teeth at the base. The buccal capsule can therefore be considered to be secondarily reduced in the remaining trichostrongylin and metastrongylin families providing a synapomorphy between them, with the notable exception of the trichostrongylin subfamily Globocephaloidinae in which it is greatly enlarged. In the Strongyloidea, Ancylostomatoidea and Diaphanocephaloidea, a greatly enlarged buccal capsule compared with the out- group can be considered synapomorphic, as can the development of a complex dorsal gutter in the Diaphanocephaloidea and in many Strongyloid and Ancylostomatoid

1141

Phylogeny of the Strongylida Table I-Taxa

within the order Strongylida, based on Lichtenfels (1980a, b), Durette-Desset (1983) and Anderson (1978) with modifications of Beveridge (1987) and Durette-Desset & Chabaud (1993)

Order

Sub-order

Super-family

Families

Sub-families

Strongylida

Strongylina

Strongyloidea

Strongylidae

Strongylinae Cyathostominae Chabertiinae Oesophagostominae Cloacininae Phascolostrongylinae

Chabertiidae Cloacinidae

Ancylostomatina

Trichostrongylina

Ancylostomatidae

Diaphanocephaloidea

Diaphanocephalidae

?

Amidostomatidae

Amidostomatinae Epomidiostomatinae

Trichostrongyloidea

Dromaeostrongylidae Trichostrongylidae

Libyostrongylinae Cooperiinae Graphidiinae Ostertagiinae Trichostrongylinae Haemonchinae

Molineoidea

Amphiobiophilidae

Amphibiophilinae Johnpearsoniinae Dictyocaulinae Mertensinematinae Molineinae Ollulaninae Anoplostongylinae Nematodirinae

Dictyocaulidae Molineidae

Mackerrastrongylidae

Heligrnosomoidea

Strongylacanthidae Viannaiidae Heligmosomidae Heligmonellidae

Herpetostrongylidae Nicollinidae Ornithostrongylidae

Metastrongylina

Ancylostomatinae Bunostominae -

Ancylostomatoidea

Metastrongyloidea

Metastrongylidae Protostrongylidae Crenosomatidae Angiostrongylidae Filaroididae Skrjabingylidae Pseudaliidae

Mackerrastrongylinae Tasmanematinae Viannaiinae Hydrochoerisnematinae Heligmonellinae Brevistriatinae Pudicininae Nippostrongylinae Herpetostrongylinae Globocephaloidinae Omithostrongylinae Inglamidinae

1142

M.-C. DURETTE-DESSET Table 2-Morphological

et al.

characters of Strongylida used in analysing phylogenetic relationships*

Strongylina

Trichostrongylina

Metastrongylina

Ancylostomatoidea

Diaphanocephaloidea

Buccal capsule enlarged (+)

+

_*

_

+

+

Dorsal gutter present

+ _

_

+

+

Lateral jaws present (+) or absent (-)

_*

_

_

+

Teeth or cutting plates at oral opening present (+) or absent (-)

_*

+

_

Female amphidelphic (a) or prodelphic (p)/monodelphic (m)

P (few a)

a/m

a (few p)/m

a

a/P

Ovejector with long (1) or short (s) sphincters

I

S*

S

S

Synlophe present (+) or absent (-)

_*

_

_

+*

_

_

_*

_

_

_

ixc.

Globocephaloidinae)

(ext. in Hypodontus)

(except in Cyclostrongylus)

Cephalic vesile Cephalic papillae fused (f) or separate (-)

iot all genera)

;xcept Stephanurus)

Bursal forrnulat

2-l-2

1-3-1 2-l-2 2-3 2-2-l 3-2

2-l-2

2-l-2

2-l-2

Dorsal lobe of bursa reduced

-*

+

+

_

_

Life cycle oral infection

+

+

+

+

+

+* (rare)

+

_

+

_

Principal site in host

large intestine or saccular forestomach

monogastric stomach and small intestine

lungs, venous sinuses fascia

small intestine

stomach and small intestine

Host group

Reptiles, birds, mammals

Reptiles, amphibians, birds, mammals

Mammals

Mammals

Reptiles

skin penetration

*Presumed plesiomorphic state tSee Durette-Desset (1983).

Phylogeny of the Strongylida

genera. This structure has been lost secondarily in the Strongyloidea (Lichtenfels, 1980a). The jaw-like structures which characterise the Diaphanocephaloidea in a phenetic sense are autapomorphic (occur in one group only) and therefore are not particularly informative phylogenetically. The occurrence of similar structures in the Globocephaloidinae (Trichostrongylina) is presumably a phenomenon of convergence (homoplasy). The female genital system

A transition series can be constructed in the development of the reproductive system, beginning with the form seen in rhabditoids, proceeding to the amphidelphic system with distinct vestibule, sphincters and infundibula found in the Amidostomatidae, Trichostrongylina, certain Metastrongylina and in the Ancylostomatoidea. Further development with a more posterior vulva and the advent of monodelphy has been traced within the Trichostrongylina by DuretteDesset (1985) and in the Metastrongylina by Dougherty (1949). Lichtenfels (1980a) has investigated its further development within the Strongyloidea, with elongation of the vagina vera (Strongylus), posterior shift of the vulva and the development of a prodelphic condition (Type I ovejector) then the evolution of a kidney-shaped or J-shaped ovejector (Type II ovejeo tor). Within the Diaphanocephaloidea, uteri are amphidelphic, but in some species they are prodelphic and in one species, elongation of the vagina has occurred in a manner similar to the Strongyloidea (Schad, 1962). Variations also occur in other suborders. Mecistocirrus (Trichostrongylina) has an elongated vagina (Durette-Desset, 1983), similar in proportions to that seen in many Strongyloidea, while within the trichostrongyloid species Cheiropteronema globocephala from bats, females occur with vaginae of differing lengths and with amphidelphic, prodelphic and opisthodelphic ovejectors (Durette-Desset & Vaucher, 1988). The plesiomorphic condition thus remains in the Ancylostomatoidea and Diaphanocephaloidea. A basic tenet of Dougherty’s (1951a) arrangement was that the Trichostrongylina and Ancylostomatina as well as the Amidostomatidae are related because of similar reproductive systems in the female. From a cladistic viewpoint, all share a primitive or plesiomorphic genital system which is phylogenetically uninformative. Cephalic structures

The cephalic papillae were emphasised in phylogenetic reconstruction by Chitwood (1950), Dougherty (1949, 1951a,b) and Chabaud (1965). The plesiomorphic state, with several (3) circles of sensory papillae

1143

is found in primitive Trichostrongyhna and in the Metastrongylina. Reduction in the cephalic papillae, an apomorphic development, occurs in the Strongyloidea. Additional apomorphic features which unite the 3 Trichostrongylin super-families are the presence of a cephalic vesicle. A cephalic vesicle is absent in the Amidostomatidae. Synlophe

A synlophe or set of cuticular body ridges used in attachment to the gut wall is present in most genera of the Trichostrongylina, providing a synapomorphy linking them. It is absent in the Amidostomatidae and in the remaining sub-orders. In considering these features, it is evident, as may be expected, that each sub-order is characterised by a mixture of plesiomorphic and apomorphic characters. If only the apomorphic characters are used, the resultant arrangement of taxa would differ somewhat from those currently accepted (Fig. 1). The Ancylostomatoidea, Strongyloidea and Diaphanocephaloidea would be derived from a common ancestor since they share an enlarged buccal capsule RRABDITIDA : RHABDIASIDAE STRONGYLOIDIDAE

/

METASTRONGYLOIDBA

MOLINEOIDEA HELIGMOSOMOIDEA

\

/j

TRICHOSTRONGYLOIDEA

P

V’ ‘U

AMIDOST~MAT~~~E

I

DIAPRANOCEPWLIDAE ANCYLOSTOMATTDAE

SYNGAMIDAE DELETROCEPHALIDAE STRONGYLIDAE CHABERTDDAE

%

CLOACINIDAE

Fig. 1. Speculative view of relationships between principal sub-families, families and super-families within the Strongylida, indicating the Rhabditid families Rhabdiasidae and Strongyloididae as likely ancestral groups. Due to uncertainties in relationships and to different taxonomic systems employed by various authors, a speculative view of relationships between taxa of equivalent rank was not considered possible.

1144

M.-C. DURETTE-DESSET

and a dorsal gutter. This is in contrast to the systems of Dougherty (195 1a) and Schulz, (195 1). The similarities between the Ancylostomatoidea and Strongyloidea noted here suggest a close relationship; their separation in previous systems based on the morphology of the female genital system is overcome by considering that the condition in the Ancylostomatoidea is plesiomorphic and therefore, in a cladistic sense, is not informative. The Trichostrongylina likewise also form a group of 3 closely related super-families derived from a common ancestor with the Strongyloidea Ancylostomatoidea. The Metastron~lina is derived from the Trichostrongylina by reduction of the bursa and the adoption of particular life histories. The position of the ~idostomatidae is uncertain. Amidostomatids share certain morphological features with the Trichostrongylina, and were included as a family within the Trichostrongyloidea by DuretteDesset (1983) but lack a cephalic vesicle and synlophe. Every morphological feature considered here is plesiomorphic in the Amidostomatidae. Similarities with the Ancylostomatoidea have been suggested (Schultz, 1951), but similarities based on the female genital system are plesiomorphic, and Amidostomatids clearly lack the enlarged, deviated buccal capsule of the Ancylostomatoids. They may however represent a relictual group dating from the major separation of the Trichostrongylina and the Strongyloidea Ancylostomatoidea, or may be considered ancestors to these parasitic lineages. Durette-Desset & Chabaud (1993) in their consideration of the major taxa within the Strongylida refrained from assigning the Amidostomatidae to any particular group, underlining the uncertainties surrounding their taxonomic as well as their phylogenetic position. The review presented here represents a superficial examination only, but suggests that the application of cladistic methods to mo~hological data now available could resolve some of the problems that have impeded our understanding of the relationships of these groups to the present. The information presented does not clarify the relationships with host groups; that is with the reptiles, birds and mammals, but does suggest some possible associations. One would postulate on the available evidence that the Strongylida arose in amphibians from a rhabditoid ancestor, with Rhabdias and Strongyloides perhaps representing aberrant relics from that transition. The Amidostomatidae, in birds, may represent a relict of the early strongyhd parasites. The Trichostrongy~ina invaded reptiles, birds and mammals, giving rise to 3 major lineages, the Trichostrongyloidea, Mohneoidea and Heligmosomoidea and ultimately to the

et al.

Me~stron~lina in mammals. The Diaphano~phaloidea possibly arose from an ancestor close to the Strongylina with enlargement of the buccal capsule and the development of lateral jaws, retaining primitive features such as double cephalic papillae, and became specialised parasites of snakes, rarely lizards. The Strongylina and Ancylostomatoidea either arose from a common ancestor with the Trichostrongylina in birds then infected mammals, or arose from a common ancestor with the Trichostrongylina already present in mammals, with enlargement of the buccal capsule, fusion or loss of cephalic papillae and development of a more specialised female reproductive system, in the case of the Stron~loidea. The Ancylostomatoidea have an origin close to that of the Strongyloidea as indicated by the buccal capsules and dorsal gutters, but have retained a more primitive female reproductive system, and occur only as parasites of mammals. Obviously, these suggestions are highly speculative, and additional analyses are required before any firm hypotheses can be advanced, but they do reflect the current state of knowledge of the evolution of the order Strongylida and avoid past emphases placed on the host group as an indicator of phylogenetic affinities of the parasites.

Origins The origins of the Strongyloidea are obscure, and given the lack of morphological characters available for analysis and the apparent strict host specificity of families within the Strongyloidea (Lichtenfels, 1979), it is tempting to deal with the strongyloids on the basis of the host groups in which they occur. The deletrocephalids and syngamids, parasitic primarily in birds, are apparently close to the origin of the suer-family. They possess a number of primitive morphologi~l features which can be used in support of this view, and the hosts of the deletrocephalids, as well as the strongylid Codiostomum, are ratite birds, a group paraphyletic with remaining birds (Cracraft, 1988). This hypothesis of a possible origin associated with ratites is of interest because of a close parallel with the evolution of the families Trichostrongylidae and Dromaeostrongylidae (Trichostrongyloidea) also arising apparently in ratite birds (DuretteDesset & Chabaud, 1981). Very few genera of Strongyloidea are known from reptiles. The 2 genera inhabiting tortoises, Chap~iella and Sa~ricoZa, possess a number of features of the male reproductive system as well as the buccal capsule which align them with the strongyloids of

Phylogeny of the Strongyiida

horses (Beveridge, 1987). They nevertheless retain a relatively primitive female genital system (Lichtenfels, 1980a). Dougherty (1951a) and Chabaud & Tcheprakoff (1977) considered that the genus arose by host switching from mammals, while Lichtenfels and Stewart (1981) preferred to consider them a primitive group. Although the Chelonia are an ancient group, the land tortoises are derived from aquatic forms (Gaffney & Meyland, 1988) and have apparently acquired their strongyloid parasites on land, since no strongyloids are known from aquatic chelonians. The origins of these genera therefore remain uncertain. The majority of strongyloid genera occur in mammals. While the host specificity of the major families: the Strongylidae in perissodactylsiproboscoideans, the Chabertiidae in artiodactyis and the Cloacinidae in Australian marsupials is clear, implying a long association with their hosts, tying the origins of the nematodes with the period of origin of the host group is not necessarily reliable due to evidence of switching of some nematodes between host groups. In the case of the marsupials, tying the origin of the Cloacinidae to the origins of the marsupials would be clearly incorrect since although the marsupial~utherian split is currently dated at about 135 mya (Richardson, 1988) [though the range provided in a variety of studies is from 71 to 170 mya (see Hope, Cooper & Wainwright, 1990)], the Strongyloidea of marsupials are restricted to the herbivorous families which appeared at most 40 mya based on Palaeontological evidence (Stirton, Tedford & Woodbourne, 1968), a date which is supported by microcomplement fixation data (Baverstock, Krieg & Birrell, 1990) though DNA-DNA hybridisation studies suggest an earlier date of 58 mya (Westerman, Janczewski & O’Brien, 1990). In both instances, the estimates are much lower than 135 mya. The lack of any other possible origin for the strongyloids in marsupials led Beveridge (1982, 1987) to speculate that the Cloacinidae may have arisen by a host-switch from a ratite bird, representatives of which are common in Australia. The same may conceivably have occurred in the other families, with the Chabertiidae derived from Deletrocephalus in rheas and the Strongylidae from Codiostomum in ostriches. However, with the current lack of evidence, the idea remains highly speculative and more information is needed before a firm hypothesis can be advanced. Phylogenetic relationsh~s and host ranges (Fig. 2)

The most detailed examination of the phylogeny of the Strongyloidea is that of Lichtenfels (1979,

1145

1980a, 1986). Lichtenfels (1979, 1980a) recognised two major families, the Stron~lidae (24 genera) occurring in perissodactyls, elephants and hyraxes, with a few in Australian marsupials and the Chabertiidae (39 genera) in artiodactyls, Australian marsupials, rodents and primates. Two small families, Deletrocephalidae and Syngamidae occur primarily in birds with a few species in mammals. The Deletrocephalidae and Syngamidae possess a number of morphological features which can be considered primitive, including a globular buccal capsule and hexagonal mouth opening. They were considered to lie close to the origins of the Strongyloidea. The basic features of Lichtenfels’ (1979, 1980a) analysis were subsequently coaxed (Beveridge, 1987) using additional characters of the male reproductive system, although minor modifications were made to unite the genera from Australian marsupials in a single family group. Other minor changes suggested by Beveridge (1987) were that the strongyles of horses and elephants formed 2 parallel lines of evolution, while the relationship between Stephanurus and the Deletrocephalidae was further supported. Dvoinos (1982) also considered the equine strongyloid genera to be monophyletic but considered the Cyathostominae with cylindri~l buccal capsules to be primitive, in contrast to Lichtenfels (1979, 1980a) and Beveridge (1987) who considered the globular buccal capsules of the Strongylinae as primitive. The latter view is supported by developmental data with certain Cyathostominae (Cylicostephanus Iongibursatus and 1958) and Cylicocyclus sp.) (see Popova, Chabertiidae (Oesophagostomum venulosum) having sub-globular buccal capsules in the fourth larval stage, but cylindrical buccal capsules in the adult (Goldberg, 1951).

Among the major Strongyloid families, host specificity is relatively narrow, as noted above, suggesting a broad co-evolutionary pattern of host-parasite relationships. The suggestions that the marsupial inhabiting genera are monophyletic, the equid-parasitic genera are monophyletic (Dvoinos, 1982; Beveridge, 1987) and possibly those of proboscideans (Beveridge, 1987) (though several genera remain to be examined morphologically), lends further weight to this hypothesis. Co-evolution has also been significant at the generic level, as illustrated by studies on Oeso~hagostomum and its reiatives. Chabaud & Durette-Desset (1973) studied the evolution of oesophagostomes in African suids, rodents and in

1146

M.-C. DURETTE-DESSET

et al. Pharyngostrongylinea

b

Zoniolatminea Coronostrongylinea

MARSUPIALS MARSUPIALS MARSUPIALS

ClOI%Ci”i”ae

Macropostrongylinea

MARSUPIALS

Lahiostrongylinea

MARSUPIALS

Cloacininea

MARSUPIALS

CLOACINIDAE p

Macqostrongylinea / Phascolostrongylinae

\

Phascobstrongylinea t

Hypadontinea

Bourgelatiinea / Oesophsgostominae

y

MARSUPIALS

MARSUPIALS MARSUPIALS

RODENTS PRIMATES SUIDS

Oesophagostominea

PRIMATES UNGULATES RODENTS

Bourgelatoidinea

TRAGULIDS

CHABERTIIDAE

(

PRIMATES RODENTS RUMINANTS

Chahertiinae

Archeostrongylinae Stephanurinae

RODENTS SUIDS RODENTS UNGULATES BIRDS, FELIDS ELEPHANTS

SSYNGAMIDAE Syngaminae -

DELETROCEPHALIDAE

RATITES

ELEPHANTS OSTRICH

strongy1inae ,Murshidiinea

I

ELEPHANTS, SUIDS PERISSODACTYLS PERISSODACTYLS ELEPHANTS RHINOCEROS HYRACOIDS EQUIDS

\\

’

Cyathostominae -Cyathostomt”ea

EQUIDS UNGULATES WRTLES

Fig. 2. Relationships between tribes of the Strongyloidea, based on Lichtenfels (1980a) and Beveridge (1987).

primates, concluding that the genus Daubneya in primitive suids (Hylochoerus, Phacochoerus) in Africa and gave rise to (1) Oesophagostomum in more recent suids @US, Pomatochoerus), (2) the subgenera Hysteracrum, Proteracrum and Bosicola in ruminants and (3) the related sub-genera Lerouxiella in African rodents and Conoweberia and Zhlea in primates (Fig. 3). Glen & Brooks (1985) using cladis-

tic methods, arrived at a phylogenetic tree for the same taxa which differed at only one node from that of Chabaud and Durette-Desset (1973), even though characters used differed, the character polarisation differed and the methods of analysis differed between the 2 studies (Fig. 3). The results of both studies supported the hypothesis of broad co-evolution within the artiodactyls but with switching of

1147

Phylogeny of the Strongylida

DAUBNEYA

DAUBNEYA

Suids

0. (HYSTERACRUM)

0. (OESOPHAGOSTOMUM)

Suids

0. (PROTERACRUM) 0. (HYSIERACRUM)

Ruminants

0. (OESOPHAGOSTOMUM)

0. (PRO’IERACRUM)

Bovidae

0. (BOSICOLA)

0. (BOSICOLA)

BOVidae

0. (LEROUX~LLA~

RodeatS

0. (CONOWEBERIA)

Primates

0. (LEROUX~L~) 0. (CONOWEBE~)

0. (IHLEA) 0. (IHLEA)

Fig. 3. Comparison of relationships between the strongyloid genus Daubneya and the sub-genera of Oesophagostomum with their hosts as determined using non-cladistic methods (right hand diagram) (from Chabaud & Durette-Desset, 1973) or cladistic methods (left hand diagram) (from Glen & Brooks, 1985). some species to Brooks (1985)

rodents and primates. Glen & of also studies the species ~ono~eber~~, Ihleu and ~r~~x~e~~a cladistically (Fig. 4), concluding that the resultant parasite phylogeny could best be explained in terms of co-evolution (8

of 12 speciation events). They used their data to infer that the centre of evolution of the group had been Africa with dispersion of 2 parasite groups (bzjk~~-a~le~t~~ and b~ffnehar~i-rai~lieti-~~~turn~ to south-east Asia in primates. IhIeu ste~hanosto~~m

C. ZUKOWSKYI

Africa

C. BIFURCUM

Africa

C. BRUMPn

Africa

C. ACULEATUM

Africa - Southeast Asia

L. XERI

Africa

L. SUSANNAE

Africa

C. BLANCHARDI

SoutheastAsia

c. RAILLIETI

Southeast Asia

C. OVATUM

Southeast Asii

C. PACHYCEPHALUM

Africa

Primates

Rodents

I. S~~OSOMUM

Ptilllab%

Primates

Africa ” South America Primates south America

Fig. 4. Comparison Conoweberia,

of relationships between species of the oesophagostome sub-genera determined by cladistic methods, (from Glen 8c Brooks, 1985) and the geographic distributions of their hosts.

Ihlea and Lerouxiella,

1148

M.-C. DURETTE-DESSET

and I. ventri had dispersed from Africa to South America with primate hosts. However, Lichtenfels (1986) has correctly pointed out that in both of these studies the Chabertiine genera Cyclodontostomum, Castorstrongylus and Ransomus in rodents and Ternidens and Colobostrongylus in primates have not been included, and it is just possible that the oesophagostomine genera in rodents and primates are polyphyletic and may have developed in parallel from chabertiine ancestors, Lerouxiella from Castorstrongylus or Ransomus and Conoweberia from Ternidens or Colobostrongylus, in much the same way as in the ruminants the genera Proteracrum and Bosicola could have evolved from Chabertia. This possibility of multiple parallel lines of evolution remains to be explored. The evolution of the strongyloid parasites of elephants possibly begins with the genera with large buccal capsules (Equinurbia, Decrusia and Choniangium) and proceeds, in parallel with other groups to genera with cylindrical buccal capsules, containing numerous species, namely Murshidia and Quilonia. Chabaud (1957) considered that the latter genera might have evolved either in elephants or in rhinoceroses, but the preliminary data of Beveridge (1987) on spicule sheath morphology favour an origin in elephants, with, consequently, host switching to sympatric rhinoceroses and warthogs (Chabaud, 1957). Species diversity is greatest in the African elephant (23 species of Murshidia and Quilonia), with only 6 species in the Indian elephant, a situation consistent with the known evolutionary history of the elephants which originated and reached their greatest diversity in Africa, while dispersing from Africa across Laurasia (Stahl, 1985). Thus, the fragmentary evidence we have for the evolution of these genera supports a co-evolutionary pattern with subsequent host switching. The general predominance of co-evolutionary relationships has also been demonstrated in electrophoretic studies in strongyloids in Australian marsupials. Allozyme electrophoresis of Hypodontus macropi revealed 6 cryptic species, with at least 4 of the speciation events matching those of the hosts. The remaining speciation events could be interpreted either as co-evolution or host switching, due to differences in opinions on the evolutionary relationships of the hosts (Chilton, Beveridge & Andrews, 1992). A similar study of Macropostrongyloides spp. revealed a basic pattern of co-evolution with one case of host-switching into a sympatric but distantly related species of kangaroo (Beveridge, Chilton & Andrews, 1993). Given the overall pattern of a mixture of co-evolu-

et al.

tion and host switching at the family, species and cryptic species levels, a careful investigation of other genera or tribes is clearly warranted. Within the Trichostrongyloidea, it has been noted that parasite expansion occurs primarily at the same time as rapid host expansion (Durette-Desset, 1982). This phenomenon is difficult to assess with the strongyloids of equids and elephants because the hosts are essentially relicts of formerly speciose groups of mammals. The ruminants are a group which is still widespread and in which the oesophagostomes are a dominant component of the parasite fauna. The best example of the role of host expansion is that of the macropodid marsupials which harbour 38 genera of strongyloids. Although many host taxa are now extinct, there are still some 47 extant species of kangaroos and wallabies, representing various evolutionary grades within the Macropodoidea. A reliable estimate of the number of strongyloid species, which currently stands at 171 (Spratt, Beveridge & Walter, 1991) cannot yet be given since significant components of the fauna are undescribed, but the time scale of the parasite radiation can be dated approximately since most of the genera of the family Macropodidae, containing the large kangaroos, have evolved in the last 10 mya, with the oldest forms dating to 20 mya (Flannery, 1989). Thus this extraordinary radiation is a recent one and the variety of cephalic structures found within the Cloacinidae indicates the evolutionary plasticity of cephalic features. The radiation of the kangaroo strongyloids was not simply due to the presence of a host group evolving rapidly in isolation; it is also associated with evolutionary changes in the gastro-intestinal anatomy of the kangaroos (Beveridge, 1982). The primitive kangaroos, now represented only by the musky rat-kangaroo, Hypsiprymnodon moschatus, were monogastric and fermentative digestion occurred in the short caecum and colon, a site inhabited by the strongyloid genus Corollostrongylus. Other genera of nematodes restricted to this site in recent kangaroo species are Hypodontus and Macropicola. During their evolution, the kangaroos developed a large saccular fore-stomach, and this became the principal site of fermentative digestion (Hume, 1982). The Cloacininae invaded the stomach and then underwent an extensive radiation within it. In this case, the evolution of the gastro-intestinal tract of the hosts has been of major importance in the evolution of the parasites. A similar involvement of changes in the digestive tract of elephants and horses may well have influenced the evolution of their nematode inhabitants, and it is presumed in the

Phylogeny of the Strongylida

case of the horses that this evolutionary change in the caecum dates from the evolution of the first horses in the Eocene (Stahl, 1985, p. 493). Chabaud (1957) and Chabaud & Durette-Desset (1981) have drawn attention to the fact that in such vast digestive organs, competition between nematode species is unlikely, allowing a greater diversification than would be possible if resources were limiting. In the case of the wombats (Vomatidae) only 5 species of strongyloid nematode are known (Spratt et al., 1991), all from the colon, which is an organ of relatively vast size. The wombat radiation was not as expansive as that of the kangaroos with only 3 extant species, hinting at the importance of host radiation in the development of a complex nematode fauna. Within the Australian strongyloid radiation, a further exploitation of the anatomical peculiarities of a host is provided by the genera Cyclostrongylus and Spirostrongylus which occur coiled around elongate papillae in the oesophagus of wallabies of the subgenus Notamacropus and Wallabia. As an aid in attachment, these nematodes have developed simple body ridges, analogous with the synlophe of many trichostrongyloid nematodes. There have been few attempts to investigate the role of host dispersal in the evolution of the strongyloid nematodes. Glen & Brooks (1985) have provided evidence for the dispersal of the oesophagostomes of primates from Africa to southeast Asia and to South America. Similarly, Smales (1992) has suggested that the genus Ancistronema, present in hydromyine rodents in Australia and possibly in Malaysia, arose in rodents in south-east Asia and evolved when hydromyine rodents dispersed and entered Australia from Asia some 5-15 million years ago (Watts & Aslin, 1981). The Strongylidae and Chabertiidae may have been dispersed widely by host movement within Laurasia, with both perissodactyls and artiodactyls migrating across the Bering Strait region. The effect of these migrations on the cestode parasites of various mammals has been discussed by Rausch (1982), and on various trichostrongyloids by Durette-Desset (1985), but its implications for the strongyloids have not been considered in detail. The large strongyloid radiation in marsupials may have stemmed from host-switching from an unrelated host such as a ratite (Beveridge, 1982), though Cameron (1964) suggested that the morphological similarities recognised at that time between the strongyloids of kangaroos and elephants suggested that kangaroos may once have occurred in southern Africa. This hypothesis has never been substantiated

1149

with palaeontological evidence, though the reverse possibility, namely that some form of primitive placental mammals once occurred in Australia seems likely (Clemens, Richardson & Baverstock, 1989). Life cycles

Strongyloids appear not to have utilised life-cycle modifications as a major evolutionary mechanism, their life cycles, with a few exceptions being relatively uniform. The members of the super-family are essentially monoxenous, though Syngamus and Stephanurus have earthworms as paratenic hosts (Anderson, 1992). Similarly, infection of the definitive host is exclusively oral, with the primitive route of infection, the percutaneous route existing only in Stephanurus (see Anderson, 1992). Migration to the extra-intestinal or respiratory tissues of the host are uncommon, with extensive somatic migrations occurring only in Stephanurus and Strongylus (see Anderson, 1992). The tissue migration of Stephanurus seems to be somewhat chaotic rather than carefully programmed (Waddell, 1969), as is the case with phases of the parasitic life cycles of Strongylus edentatus and S. equinus (see Anderson, 1992 for summaries). These life cycles appear not to be phylogenetically informative, other than in the sense that all species with tissue migrations can be considered primitive on morphological grounds. ANCYLOSTOMATINA:

ANCYLOSTOMATOIDEA

Origins

The origins of the Ancylostomatoidea were not considered by Lichtenfels (1980b) in a recent review of the super-family, though he did comment on their hypothesised evolution from the trichostrongylin family Amidostomatidae, a view supported by Schulz (1951) and Chabaud (1965). This association is based on the morphology of the female reproductive system and hence on plesiomorphic characters. The only apparent apomorphies available are the enlargement of the buccal capsule and the presence of a dorsal gutter, a feature present in some genera of all Strongyloid families and also present in the Ancylostomatinae. Deviation of the buccal capsule the Strongyloidea and the occurs in both Ancylostomatoidea. The Ancylostomatoidea possess teeth or cutting plates at the mouth opening, though in each subfamily, Ancylostominae and Bunostominae, there are genera which lack teeth. Lichtenfels (1980b) placed these genera as the most primitive within each sub-family and they present therefore a convenient link with the Strongyloidea. A further piece of possible evidence derived from life

1150

M.-C. DURETTE-DESSET

cycle studies, is that the buccal capsule of the fourth larval stage of nematodes such as Uncinariu stenocephala is globoid but symmetrical and resembles that of fourth stage strongyloid nematodes (Gibbs, 1961). Phylogenetic relationships and host ranges (Fig. 5)

The evolution of the Ancylostomatoidea has occurred exclusively in mammals but in contrast to the Strongyloidea, there is no apparent relationship between nematode and host groups (Lichtenfels, 1980b). The Ancylostomatoidea may have appeared initially with the early omnivorous mammals, the Ancylostomatinae subsequently developing in the carnivores and the Bunostominae within herbivores, with the primitive members of each sub-family occurring in omnivores (Lichtenfels, 1980b). The evolution of the Ancylostomatoidea has attracted relatively little attention, which is surprising given the quality of most generic descriptions. Life cycles

The life cycles of hook-worms are of interest since both oral and percutaneous routes of infection are possible. Percutaneous infection is the most common route in genera of the Bunostominae infecting ruminants, while in species of Uncinaria and Ancylostoma in carnivores, oral infection is as important or more important. The genus Uncinaria provides an excellent example of how ancylostomatoid nematode life cycles can be adapted to differing environmental conditions. U. stenocephala in dogs is transmitted primarily by ingestion of the third-stage infective larva by the definitive host (Gibbs, 1961). However, in seals, which evolved from terrestrial carnivores, the life cycle of U. lucasi has been greatly modified to accommodate a host which spends most of its life at sea, transmission being primarily trans-colostral (for summary see Anderson, 1992). Newly born seals ingest larvae from the mammary gland of the mother and heavy, often fatal infections develop in pups. Eggs shed in faeces develop to the third stage on the beach and penetrate the skin of potential hosts. Only in female seals is the life cycle completed. The life cycle of U. lucasi demonstrates the extraordinary plasticity of life cycles within the Ancylostomatidae. ANCYLOSTOMATINA:

DIAPHANOCEPHALOIDEA

The Diaphanocephalids have received relatively little attention since the major revision of Schad (1962). They are a group of singular interest, occurring in the intestine of snakes (rarely lizards) and characterised morphologically by paired, lateral,

et al.

jaw-like structures on either side of the mouth resembling found in the opening, those trichostrongylin sub-family Globocephaloidinae. As pointed out above, this feature is essentially autapomorphic and therefore provides few clues to phylogenetic affinity. The shape of the oesophagus, general structure of the bursa, genital cone and spicules closely resemble some genera of the Strongylidae, and the Ancylostomatidae. If it could be shown that these were indeed synapomorphies, then a strong case could be made, together with the enlarged buccal capsule, for a close association between Strongyloidea, the Ancylostomatoidea and Diaphanocephaloidea. Of possible significance is the fact that in certain species of Kalicephalus, for example K. appendiculatus, the head is deviated slightly dorsally, recalling the situation found in the Ancylostomatoidea and in some Strongyloidea (Corollostrongylus). The female genital system is usually amphidelphic and therefore resembles the form found in Ancylostomatoidea and some Trichostrongylina. However, species also exist, such as K. appendiculatus and K. costatus which are prodelphic, and in one species, K. longispicularis, the ovejector is prodelphic and elongated (Schad, 1962), resembling the Type 1 ovejector of the Strongyloidea (see Lichtenfels, 1980b). Thus a re-analysis of morphological features could clarify the relationships of the Diaphanocephaloidea. Life cycles are direct (see Schad, 1962) in all species which have been investigated. TRICHOSTRONGYLINA

Origins

The Trichostrongylina has a common origin with the other strongylid suborders and arose from an ancestor, close to the rhabditoids. The hypothetical ancestor of the Trichostrongylina, inferred from contemporary forms would have possessed 6 lips, a dorsal oesophageal tooth, 3 complete circles of cephalic papillae, a well developed dorsal lobe to the bursa and an amphidelphic female. The proposed ancestral forms of the most known families and subfamilies occur in hosts which have a Gondwanan distribution, and, by contrast, only 4 families currently occur in the Holarctic (Trichostrongylidae, Molineidae, Heligmosomidae and Heligmonelidae). Thus, most modem trichostrongylin families were probably present as early as the beginning of the Tertiary and either were parasites of amphibians and reptiles, or, occurred in monotremes, marsupials and insectivores, mammals which were present at the end of the Secondary and which have modern represen-

1151

Phylogeny of the Strongylida tatives. Beyond these generalisations and inferences, the precise origins of the Trichostrongylina are unclear and require further investigation. Phylogenetic relationships and host ranges

The phylogeny of the Trichostrongylina has been investigated by Durette-Desset & Chabaud (1977, 1981) and Durette-Desset (1971, 1983, 1985) (Fig. 6) and is based on 4 principal sets of characters, cephalic structures, the female reproductive system, the male bursa and the synlophe. In the first three instances, the Rhabditida have been used as an outgroup to define the polarity of evolutionary change; in the case of the synlophe, ontogeny, that is comparison of the synlophe of the fourth larval stage with that of the adult, has been used (DuretteDesset, 1985). Evolutionary changes within the Trichostrongylina are characterised by: (1) loss of the buccal capsule; (2) development of the ovejector and monodelphy; (3) reduction of the dorsal lobe of the bursa and migration of ray 4 towards ray 3; and (4) appearance of the synlophe and cephalic vesicle. Details of the morphological features used and the phylogenies constructed were reviewed by DuretteDesset (1985) and are not repeated here. Three principal super-families were recognised in the Trichostrongylina by Durette-Desset & Chabaud (1993) these being the Trichostrongyloidea, the Molineoidea, and the Heligmosomoidea.

Trichostrongyloidea

The primitive family Dromaeostrongylidae is of Gondwanan origin, since it is present both in the Neotropical and Australian regions. The genus Paramidostomum, parasitic in Brazilian birds, is morphologically close to Batrachostrongylus (Molineoidea-Amphibiophilidae) in amphibians, but is distinguished from it by bursal ray 2. The remaining genera are Australian. Dromaeostrongylus, parasitic in emus ressembles the genus Libyostrongylus in African ratites, the latter belonging to the while Peramelistrongylus in Trichostrongylidae, dasyurid and peramelid marsupials is linked by Proflarinema in phalangerid marsupials to the genus Filarinema which has diversified in the macropodids. The large family Trichostrongylidae is divided into 3 related pairs of subfamilies. In the first (Libyostrongylinae-Cooperiinae), the most primitive forms (Libyostrongylus, Paralibyostrongylus) occur in African ratites and ancient mammals in Africa, and appear to have originated in this region. Derived from these genera are Pseudostertagia in Antilocapra and Obeliscoides and Teporingonema in Nearctic and Neotropical lagomorphs, which appear to indicate a migration of the nematode lineage to the New World via Bering Strait. Transfer from lagomorphs to ruminants in the Old World has given rise to the Cooperiinae. In the second group (Graphidiinae-Ostertagiinae),

ARTHROCEPHALINEA Arthrocephalus Arthrostoma Placoconus UNCINARIINEA Undnarla Bioccastrongylus

Carnivora

ANCYLOSTOMATINEA Ancylostoma Galoncus

Carnlvora, Edentata Rodentla, Suldae Primates

GLOBOCEPHALINEA Globucephalw

ACHEILOSTOMINEA Acheilostoma Tetragomphius BUNOSTOMINEA Bunostomum Brachydonus Necator Galgeria Monodontus Cameronecator Grammocephalw

Fig. 5. Relationships of genera of the Ancylostomatoidea 1980b.)

Carnlvora Plnnlpedia Rodentia

Suldae, Prlmates Rodentla Carnlvo~a Marsupialla Carnlvora Rodentia Carulvora Rodentla Pl-hnp

Perissodactvla Probascoid
with their hosts. (Redrawn from Lichtenfels,

NERP~TOSTRONGYLIDAE~ VIANNAIIDAE ORNtTNOSTRONGYLlOAE c,

,_

!-,

BAEVISTR~ATINAE

PUDIC~NAE

ORNlTHOSTRONGYLtNAS IN~~lOtNAE

GLOSOC~PHALOIDINAE NEffPETOSTR~GY~NAE

-. - -

--

_~

- - - -

- -

PRIMATES

RODENTS RODF.NTS

- _.

.-

- - -

(1383).

INSECTIVDRES, RODENTS, LAGOMORPHS

RODENTS. TUPAUDS

RODENTS BIRDS, CH1RCFl-E~ ROIZNTS

MARSUPIALS,

~~L~,A~~~*ALS

MCWWMES, MARWPIALS

MONOTREMES iviARSWlALS

-

AMPHIBIANS, REXTLES, CARNIVORES, lN5ECIWCJR%?, RODl?NTS CHIROFIERA, PKIMAm, PHOLIEUiXS, ~~1D~AT~ CfflRorn, XENAKFHA, TUPAIIDS

FEUDS

AMPHIBIANS, RWTILES UNGULATES, IWNIPEDS

MERTENSINEMATINAE DtCTYOCAULlNAE OLLU~NtNAE

LAGOMOWHS.

REIWLES, LAGOMORWIS

LAGQMORPHS

BA’IHYERGIDS

AMPHIRIANS AM~BI~S,

“NGULATES, RUMINANl3

RUMINANTS,

RATlTE%RODENlF, HYRACORZ

JONNPEARSONliNA& AMPRlSlOPHtLiNAS

TRlCHOS~~6YLlNAS HAEMONCHINAE

GRAPHlDtlNAE OSTERTAGtlNAE

URYOS7RONGYLlNAS COOPERIINAE

Fig. 6. ~clationships of the famiIies and subfamilies of the ~ricbostrong~~~na and their hosts. Based on Durette-Desset

HELtGWONELLlDAE

NtCOLLlNlOAE

-

d

t

+

-

OlCl‘YOCAULtDAE 4

A~~HtRiOPHlLlOA~

TRtCHOSTRONGYLIDAE

DRO~ASOSTRONGYLIDAE

3

ii

3 m

!z

e

6

Phylogeny of the Strongylida the most primitive nematodes (Gruphidium) occur in Palearctic lagomorphs. Hyostrongylus has evolved in the Ethiopian region in lagomorphs, tragulids, okapi, suids (now cosmopolitan in domestic pigs) and primates. Only Purostertugiu is found in the New World, in peccaries, but the fossil record indicates that peccaries were once cosmopolitan. These data suggest that the Graphidiinae arose in the Old World. Transfer to recent ruminants, Bovidae and Cervidae, gave rise to the Ostertagiinae with 2 groups of genera, Murshullugiu, Cumelostrongylus, Ostertugiu, Longistrongylus from a Gruphidium like ancestor and Teladorsugia, Spiculopterugiu from a Hyostrongylus like ancestor. In the third group (Trichostrongylinae-Haemonchinae), the most primitive genus, Trichostrongylus, is a cosmopolitan parasite of lagomorphs and ruminants. The subfamily probably arose in the New World, where all of its constituent genera are found. Most of the trichostrongyles of lagomorphs are known from the New rather than the Old World. The Haemonchinae appear to have evolved initially in caviomorph rodents in America, then in lagomorphs and ruminants, and spread to the Old World. Thus in each of the 3 groups within the Trichostrongylidae, there is evidence either of evolution in an initial group of birds or mammals, followed in succession by invasion of lagomorphs and then ruminants, or of an origin in lagomorphs and then invasion of rodents and ruminants. Molineoideu

The Amphibiophilidae, with 2 sub-families, Amphibiophilinae and Johnpearsoniinae, are primarily parasitic in amphibians and reptiles in South America, Africa, Malaysia and Australia, with the Amphibiophilinae containing Amphibiophilus in Ethiopian amphibians, Butruchostrongylus in Oriental amphibians and Wunuristrongylus in Australian lizards. The Johnpearsoniinae contains Butruchonema in Malaysian and Peruvian amphibians, in Australian amphibians and Johnpeursoniu (Durette-Desset, Ben Slimane, Cassone, Barton & Chabaud, 1994). Their origin is presumably Gondwanan. From a morphological viewpoint, the remaining 3 families of the Molineoidea seem to be derived from an ancestor close to Amphibiophilus. Within the Dictyocaulidae, members of the Mertensinematinae, parasitic in the gut of amphibians and reptiles from the Neotropical, Paleartic and Oriental regions appear to have a Gondwanan origin. Morphologically and biologically (viviparity) they are intermediate between the primitive

1153

molineids (Amphibiophilidae) and the Dictyocaulinae, the large lungworms of ruminants. The Molineidae consists of 4 sub-families. In the Molineinae, which is considered to be derived directly from the Amphibiophilidae, several genera, which are either monospecific or contain few species, occur in reptiles and amphibians: Trichoskrjubinia in chelonians, Typhlopsiu in South-American lizards and Schulzia and Poekilostrongylus in neotropical amphibians. The cosmopolitan genus Oswuldocruzia appears to have arisen later, with the Bufonidae and has radiated with this host family. The remaining genera of the sub-family are parasitic in eutherian mammals, principally in the Old World. Among them, the genus Molineus, which appears to be primitive, occurs in Carnivores in most regions of the world, and has secondarily invaded the New World monkeys. With Molineus as its origin, 2 lineages have arisen, the first in Pholidotes and Tubulidentates in the Ethiopian and Oriental regions, and a second lineage in the insectivorous Tenrecoids with the genus Brygoonema at its base. From Brygoonemu have developed genera in insectivores (Tenrecoidea, Soricoidea) which have secondarily invaded primates. Other genera derived from Brygoonema include parasites of Tupaiidae and of Old World and (by extension) Australian Chiroptera (Molinostrongylus). A single genus Shattuckius, parasitic in Solenodon in the Antilles is the only representative of the sub-family in this region. The Ollulaninae is represented by a single genus Ollulunus, a cosmopolitan parasite of Felidae. It therefore represents a small evolutionary expansion from Molineidae parasitic in reptiles and amphibians, restricted to the Carnivora. The Anoplostrongylinae as characterised by Durette-Desset & Chabaud (1977) have a neotropical origin since they are almost exclusively parasites of Xenarths and neotropical bats, with a single genus in the Old World. The Nematodirinae are derived directly from the Molineinae. They occur in ruminants and lagomorphs, but unlike the trichostrongylids, the Nematodirinae of ruminants are not derived morphologically from those in lagomorphs. Similarities between the synlophes of Nematodirinae in lagomorphs and those of the neotropical Anoplostrongylinae as well as the existence of the genus Lamanemu parasitic in Lumu in Peru, suggest that the sub-family arose in the New World from primitive Molineinae. From this origin, two lineages are derived. The first in ruminants, conserved a primitve synlophe. According to Rossi (1983), the genus Nematodirus arose in North-American camelids

1154

M.-C. DURETTE-DESSET

from an ancestor similar to Lumanema. From camelids, Nematodirus spread to nearctic Odocoleinae (Cervidae) and Caprinae (Bovidae) and entered the paleartic region with these hosts. Nematodirella, parasitic in ruminants and camelids is derived directly from Nematodirus. The second lineage infected lagomorphs, with Rauschiu and Nematodiroides in leporids and Murielus in ochotonids. The Mackerrastrongylidae is restricted to Australia and new Guinea. The most primitive members are grouped in the sub-family Tachynematinae and are parasitic in monotremes. Members of the genus Zuglonema from the New Guinea echidna, Zaglossus, form a transition with the sub-family Mackerrastrongylinae, parasitic exclusively in dasyuroid and perameloid marsupials in Australia. The Strongylacanthidae, present in palearctic rhinolophid bats, may be derived from the Molineidae. Its origin is difficult to determine. Heligmosomoidea

Each of the major lineages within this super-family is characteristic of a particular biogeographic region. Remarkably, one finds at the origin of each of the major lineages genera with a synlophe composed of 3 ventral or left-ventral cuticular ridges; these genera are Woolleya (Australian region), Viannniu (Neotropica1 region) and Suncinema (Old World). The first major lineage comprising the families Nicollinidae and Herpetostrongylidae is principally Australian. The Nicollinidae are fundamentally parasites of monotremes, with a single genus Nicollina in echidnas. The genus Copemania, in dasyuroid marsupials, is interpreted as a capture from monotremes. The Herpetostrongylinae is divided into 2 sub-families, Globocephaloidinae and Herpetostrongylinae. The origin of the Globocephaloidinae, parasitic in macropodid marsupials, is difficult to determine, since species lack synlophes. The Herpetostrongylinae is found in Australian and Oriental reptiles and has diversified greatly in dasyurid, peramelid, phalangerid, petaurid and macropodid marsupials. Several hypotheses on the evolution of the sub-family in marsupials have been proposed (Durette-Desset, 1982; Humphrey-Smith, 1983; Cassone, Durette-Desset & Presidente, 1986). The most primitive genus is Woolleya in dasyuroid marsupials from which have arisen Dessetostrongylus and Put&ialina in the same host group. Also derived from Woolleya is the genus Beveridgiella in peramelid and myrmecobiid marsupials. From Dessetostrongylus are derived 3 genera, Sutaro-

et al.

strongylus, Austrostrongylus and Paraustrostrongylus

parasitic in herbivorous marsupials of the families Phalangeridae, Petauridae, Potoroidae and Macropodidae. The genus Nasistrongylus, parasitic in the nasal cavities of the dasyurid genus Antechinus is placed in the Herpetostrongylinae in spite of some morphological pecularities. The second major lineage, from the Neotropical region, consists of 2 families, Viannaiidae and Ornithostrongylidae. In the Viannaiidae, Viunnaia, parasitic in marsupials is the most primitive genus, with 3 left-ventral ridges. Hoinejjia and Travassostrongylus, derived from Viunnaiu, constitute an evolutionary radiation within the South-American marsupials. A second evolutionary development, also derived from Viannaia, invaded families of caviomorph rodents: Caviidae, Hydrochoeridae, Chinchillidae and Cuniculidae. The Ornithostrongylidae has more derived characters than the Viannaiidae. One subfamily, the Inglamidinae is represented by a single species from a Chilean cricetid. It probably represents a capture from an ancestor in reptiles or amphibians. The Ornithostrongylinae are parasitic in birds and bats in South America with several representatives in the same host groups in the Ethiopian and Oriental regions. The genus Allintoshius occurs in South American bats and in Malaysia in Tupaia, but it is difficult to determine whether it is derived from parasites in birds. In the New World, Vexillata occurs in geomyid rodents. The third lineage arose in the Ethiopian, Oriental then Holarctic regions, and has only recently reached the Australian and Neotropical regions. It comprises 2 families, the Heligmosomidae and Heligmonellidae. Primitive Heligmosomidae have a synlophe with 3 left-ventral ridges. The most primitive genus, Suncinema, is found in soricoid insectivores of the Ethiopian and Oriental regions. In the Holarctic, this didelphic genus gave rise to the monodelphic Longistriata, also parasitic in soricoids, then to Ohbayashinema in ochotonid lagomorphs. Also derived from Suncinema is the genus Citellinema in squirrels (Spermophilus spp.) and related genus Citellinoides in nearctic myomorph rodents. Citellinema gave rise to the genera Heligmosomoides and Heligmosomum, distinguished by their monodelphy. The primitive species of these genera are found in Arvicolidae in Eurasia. Subsequent speciation and host migration from West to East occurred, with entry to North America via Bering Strait. The palearctic genera Heligmoptera and Dessetia, parasitic in Spalacidae, derive from them. The Heligmonellidae are divided into 4 sub-fami-

Phylogeny of the Strongylida lies, Heli~onellinae, Pndicinae, Brevistriatinae and Nippos~on~linae. The p~itive cosmopolit~ subfamily Heli~onellinae occurs in a variety of ancient mammal groups: Talpoidea in the holarctic region, Old World and Neotropical lagomorphs and phiomorph and caviomorph rodents in the Old World. The sub-family has an Afro-asian origin (Heligmonella), with Tricholinstowia representing a small evolutionary development within talpoid insectivores. Squirrels in Morocco were infected secondarily by means of the genus Xericola. The sub-family was transferred to South America at the same time as the phiomorph rodents. The Pudicinae and Brevistriatinae constitute 2 equivalent lineages within the family, the first in the New World, the second in the Old World and both are derived directly from the Heligmonellidae. The Pudicinae diversified in caviomorph rodents (Capromyidae, Echimyidae, Erethizontidae, Dasyproctidae, Myocastoridae, Caviidae) from forms close to the genus Paraheligmonella. The cladistic analysis of DuretteDesset & Justine (1991) indicates that the Pudicinae are divisible into 2 supra-generic groups. The first infected squirrels with the genus Sciurodendrium which appears to be the most evolved genus of the Pudicinae, based on an increase in the number of ridges and reduction of the dorsal lobe. The second group evolved with the appearance of comaretes and discontinuous ridges. The Brevistriatinae have diversified in the Old World, principally in Sciuromorphs then in Hystricidae and Gliridae from forms close to Xericola. The most highly evolved genus, Fissicauda, was passed, by capture, from Sciuridae to the Tragulidae and Muridae. The Nippostrongylinae constitute the most highly evolved sub-family, and are parasites of recent rodents, essentially Muridae and Arvicolidae, but they have secondarily invaded the Cricetidae of the New World. They probably appeared in Murids in Asia, where the most primitive genus, Ur~entostrong~~lus,mo~hologically close to Heligmone~la, occurs. The Nippostrongylinae diversified primarily in the Asian region. Then, associated with migration of the Muridae, they invaded eastern Africa with the genus Neoheligmonella and Australia with the genus Odilia. In the Palearctic region, the Nippostrongylinae passed from the Muridae to the Arvicolidae, giving rise to the genus Carolinensis. This genus passed with its host to the Nearctic region and gave rise to the genus Hassa~strongyZ~s. In a secondary evolutionary development, the Asiatic genus Ni~~ostrongy~us, closely related to Orientostrongy~us, and infecting the genus Rattus, reached Australia in these hosts. In West Africa, the genus Heligmonina appeared from

1155

forms close to ~eo~eIigmoneZla. In the Nearctic region, the Nippostron~linae were passed from the Arvicolidae to the Cricetidae which spread to South America. In South America, arising from Hassalstrongylus, several genera and numerous species of Nippostrongylinae have developed. Evolutionary mechanisms

Analysis of the host spectrum and the biogeographic distribution of super-families demonstrates that each parasite group is characteristic of a particular host group and/or geographical region. In addition, hosts of a given parasitic group are not necessarily closefy related phylogenetically, for example the host spectrum of the Molineidae. Certain hosts may be parasitized by more than one evolutionary line, for example the lagomorphs by Trichostrongylidae, Molineidae and Heligmonellidae, the ruminants by Trichostrongylidae, Dictyothe caviomorph caulidae and Nematodirinae, rodents by Viannaiidae and Pudicinae and a given parasitic lineage may occur in the same host group in geographical regions quite distant from one another, for example the Amphibiophilidae in amphibians. Thus within the Tri~hostron~lina, there are very few examples of parallel evolution between the host and the parasite at the level of family or sub-family. The best example of co-evolution is with the Herpetostrongylidae. The evolution of the group has occurred in Australian marsupials except for 2 genera parasitic in reptiles, one in varanids in Malaysia and the other in varanids and pythons in Australia. The most primitive parasites occur in primitive marsupials, the Dasyuroidea; the most evolved parasites marsupials, occur in the more recent the Phalangeroidea, particularly in the Macropodidae. The Perameloidea harbour some he~etos~ongylids but are parasitized p~~ipally by another family, the Macke~astron~lidae. Thus the initial evolution of the Herpetostrongylidae occurred in all probability during the first half of the Tertiary when marsupials were radiating but, in this example, morphological characteristics do not indicate whether parasites of marsupials are derived from forms in reptiles from which they radiated in marsupials or if reptiles captured the parasites of marsupials. Analysis of the various families and sub-families of the Trichostrongylina reveals that host-switching or capture is a more frequent phenomenon than coevolution. Captures occur, or become more evident, if they occur when the host group is either undergoing a substantial evolutionary radiation or is actively dispersing, The evolutionary expansion of the para-

1156

M.-C. DURETTE-DESSET ef al.

sites can occur simul~neously with the evolution of the newly acquired host group (convolutions or may invade a host group following the latter’s diversification, in which case little or no co-evolutionary relationships will be detected. These situations depend on host evolutionary expansion and dispersal and are considered below by means of examples. The Molineinae occur in anurans, reptiles, and mammals. Morphological analysis suggests that the Molineinae of mammals are derived from forms similar to those in anurans and reptiles. The mammalian host spectrum is extremely diverse but, except for Australian and South American mammals, it represents the major groups of eutherian mammals which appeared and had their period of expansion at the beginning of the Tertiary. These contemporary hosts have remained morphologically similar to their Eocene ancestors. We presume therefore that the ancestors of the parasites found today in these hosts have also changed little and can be considered as living relicts and that their origin dates from the Eocene. Sometimes, we can infer more precisely the period of appearance of a parasite genus. The Ornithostrongylidae is composed of 2 sub-families. The more primitive, the Inglamidinae, is represented by a single genus rnglam~dum, which occurs in a Chilean cricetid rodent and has conserved very primitive characters. Cricetids did not arrive in South America before the upper Pliocene and the presence of the primitive genus Inglamidum in these hosts can be understood only if it represents a switch from a more ancient host group. The genus, in fact, belongs to an ancient lineage and further investigations will probably reveal further primitive members of the same family in Neotropical amphibians, reptiles or marsupials. The similarity between the cephalic structures of rnglamidum and those of parasites in amphibians, reptiles or marsupials suggests that the Ornithostron~lidae had its origin near the end of the Secondary, but the genus In~lam~dum itself can be dated more precisely from the upper Pliocene. Most host groups have at one time or another undergone relatively important geographical migrations. The history of these movements is particularly well known in mammals, the host group in which Trichostrongylina have had their greater success, and host dispersal has been an important factor in parasite evolution. Caviomorph rodents harbour 2 distinct families, the Viannaiidae and the Heli~onellidae. In the Viannaiidae, the most primitive forms occur in Neotropical marsupials. In the Heli~onellidae, the most primitive forms (sub-family Heligmonellinae)

occur in talpoid insectivores of the Old World. The latter family spread to phiomo~h rodents in Africa with the genus HeligmonelIa. Hoffstetter & Lavocat (1970) suggested that the phiomorph rodents migrated from Africa to South America during the upper Eocene and lower Oligocene, giving rise to the Caviomorphs. Paraheligmonella, very similar to and derived from Heligmonella, occurs in South American caviomorphs of the families Echimyidae and Capromyidae. Evolution of the Heligmonellidae in South America subsequently gave rise to the Pudicinae, the most primitive representatives of which occur in caviomorph families other than those parasitized by Viannaiidae, namely, Erethizontidae, Echimyidae, Capromyidae, Myo~storidae and Dasyproctidae. During the same period, the upper Eocene, the Viannaiidae spread from the marsupials to the caviomorph families, Hydrochoeridae, Chinchillidae and Cuniculidae. Trichostrongylina of squirrels (Sciuridae) belong to 2 subfamilies, Pudicinae in South America, with the single Sciurodendrium and Brevistriatinae in Africa and Asia. These subfamilies are morphologically very similar and are derived from heligmonelline-like ancestors. However, they parasitized squirrels at 2 different times, during the Oligocene in the Old World with the Brevistriatinae and during the upper Pliocene in South America with the Pudicinae. Squirrels supposedly originated in Asia in the lower Oligocene. Squirrels subsequently migrated to North America where they arrived in the Miocene and, in the upper Pliocene, crossed into South America by way of the isthmus of Panama. The Brevistratinae diversified in Old World Hystricidae, Sciuridae then Gliridae during the Oligocene, based on dating of host radiations. The date of appearance of the single genus Sciurodendrium, a Pudicinae derived from forms in Caviomorph rodents is, however, at the most five million years ago when squirrels entered South America. We believe that sciurids were devoid of Trichostron~lina when they moved into South America for 2 reasons: (a) Trichostrongylina are rare in Holarctic Sciuridae and those that exist belong to a recent family which appeared after the dispersal of the sciurids, and (b) ancient evolutionary lines such as the Heligmonellidae, to which the Pudicinae and the Brevistriatinae belong, are restricted to tropical and subtropical regions. The Cricetidae are among the oldest existing myomorph rodents. Their cricetodont ancestors diversified in the Oligocene. Present day cricetids resemble cricetodonts and accordingly, we expect their parasites not to have changed significantly since

Phylogeny of the Strongylida the Oligocene. Trichostron~lina, in present-day cricetids are rare except in South America, and seem to date from the Miocene since they belong to genera parasitizing recent rodents such as the Muridae and the Arvicolidae. The only way we can explain this observation is that, during the Oligocene when the Cricetidae appeared and diversified, Trichostrongylina were in a period of evolutionary stasis, Cricetids were infected much later by a subfamily of the Heligmonellidae, the Nippostrongylinae, from other rodent families. Since the most primitive forms of Nippostrongylinae occur in South-East Asian Muridae and resemble Heligmonellinae, we suggest that they arose from a heligmonelline-like ancestor and that this occured in South-East Asia, where murids appeared and diversified in the upper Miocene. During the lower and middle Pliocene, Nippostrongylines spread throughout the world with the Muridae, and later, other groups of myomorph rodents, whether older or more recent than the murids, were invaded. Australia, Africa and North America, each received a branch of this parasitic lineage. The passage of the sub-family into North America occurred by the holarctic route, that is the Nippostrongylinae passed from murids to Palearctic and then Nearctic arvicolids. During the upper Pliocene, a second radiation occurred in Australian and African murids. In North America, cricetids were infected by the parasites of Nearctic arvicolids and they introduced them into South America by way of the isthmus of Panama, where they and their parasites later underwent a major radiation. The Arvicolidae are also parasitized by Heligmosomidae. They probably arose in soricoid insectivores since the most primitive forms occur in these hosts. Thus the family would have its origin around the Eocene. Its evolution continued in ground squirrels and lagomo~hs and later, the family passed to the Arvicolidae during their period of expansion in the late Pliocene. Kowalski (1961) and Thaler (1962) agree that the Arvicolidae arose from cricetids near the end of the Pliocene but are uncertain as to the region of origin which may be North America, Mongolia or Central Europe. A Central European origin suits our data best since the most primitive Trichostrongylina from the Arvicolidae occur in this region, and the further the species in question is away from Central Europe, the more numerous are the cuticular ridges. Thus, 2 genera have gradualiy evolved with their host group, and one has spread across Bering Strait into North America. Unlike the the Heligmosomidae never Nippostrongylinae, reached South America. The few non-arvicolid

1157

rodents that they are able to infect occur in the central Palearctic region. ~ongst these species one, ~eligmosomoides polygyru~ parasitic in European murids of the genera, Apodemus and h&s is particularly interesting. Two sub-species of H. polygyrus occur in the Nearctic region. Morphological studies suggest that subspeciation occurred in the transfer from Mus musculus to a Cricetid, Reithrodontomysin North America and a second subspeciation occurred in the latter form in the Arvicolid, Phenacomys. The presence of 2 subspecies of H. polygyrus in North America cannot be explained unless the second subspecies was introduced from Europe with the domestic mouse in the last 4 centuries. This would seem to suggest that in this group, radiation is still taking place. In the Trichostrongylina, therefore phylogenetic history depends on a number of evolutionary processes other than co-evolution. A parasitic lineage may become isolated from its ancestral forms, passing from one host group to another and the isolation may be followed by speciations of variable importance, the phenomenon of host switching or capture (Chabaud, 1965). Capture may be of minor importance, as is the case in He~igmosomoide~, of Holarctic which are essentially parasites Arvicolidae, but isolated species are also known in cricetid, sciurid and murid rodents. Alternatively, captures may be followed by major radiations. For example, genera of the Heligmonellinae are parasites of phiomorph rodents, but some became adapted to caviomorph rodents and gave rise to the sub-family Pudicinae. Due to the phenomenon of capture, the Nippostrongylinae spread throughout the entire world. The evolutionary history involves 2 successive captures. The first, from murid to arvicolid rodents and the second from arvicolid to cricetid rodents. In the Tric~ostron~lina host switching mainly occurs between phylogenetically unrelated hosts. For example, parasites of rodents are derived from parasites of birds in the Ornithostrongylidae, from marsupials in the Viannaiidae, from talpoid insectivores in the Heligimonellidae and from soricoid insectivores in the Heligmosomidae. A parasitic lineage may undergo radiation when new host groups appear and radiate, offering new ecological niches. These niches may arise from the radiation of new host groups when they appear or when they migrate. Thus, cricetids were not parasitized by trichostrongylins when they appeared in Asia during the Oligocene, but much later, in North America during the Pliocene, and developed their own endemic trichostrongylin fauna during migration to and radiation in South America. Hosts may

M.-C. DURETTE-DESSET

1158

be uninfected due to loss of their parasites. For example, sciurids apparently lost their brevistriatine parasites during their migration into North America and were subsequently reinfected in South America by the Pudicinae of caviomorph rodents. Sometimes captures occur repeatedly, following the appearance of various host groups. For example, the Heligmosomidae, originally parasites of soricoid insectivores, transferred to lagomorphs, then to ground squirrels and then to myomorph rodents. Sometimes captures occur independently of the time of appearance of host groups. Thus, certain Nippostrongylinae, originally parasitic in Old World murids, transferred to arvicolids, which predate the murids in the fossil record and then transferred to Nearctic and Neotropical cricetids which predate both the murids and the arvicolids. Life cycles

The life cycles of Trichostrongylina were reviewed by Humphery-Smith (1984, unpublished Ph. D. thesis, University of Queensland) and DuretteDesset (1985). The Trichostrongylina are monoxeneous. The first 2 moults occur in the external environment and the first 3 larval stages are free living. The infective third stage larva either actively penetrates the skin of the host or is ingested by the host. Oral infection appears after skin penetration during the course of evolution. The appearance of oral transmission allowed the Trichostrongylina to expand and diversify greatly in herbivorous mammals such as the lagomorphs, ruminants and myomorph rodents and in particular the Arvicolidae. The evolutionary implications of trichostrongyline type of life cycles are firstly that the free-living larval stage facilitates dispersal and secondly that during the centuries, greater dispersal offers more opportunities from host-switching between phylogenetically

et al.

diverse hosts. In order to be an acceptable host, the new host need only support development and reproduction of the parasite. METASTRONGYLINA: Origins

There is general consensus that the Metastrongylina arose from the Trichostrongylina, but the precise evolutionary origins and pathways have not been determined. Metastrongyloidea occur as adults exclusively in metatherian and eutherian mammals. Anderson (1982, 1988a) argued that lungworms had a terrestrial origin and that heteroxenity and subsequently paratenesis evolved under terrestrial conditions. Such parasites could have adapted to aquatic conditions with their hosts, provided that a high degree of specificity had not yet evolved. Adaptation to aquatic intermediate and paratenic hosts in the food chain of the definitive host would ensure survival. Anderson (1982, 1988a) considered that this accounted for the presence of lungworms in pinnipeds and cetaceans, that monoxenous parasites could not make this transfer and that consequently they were absent in strictly aquatic vertebrates, although some do occur in aquatic mammals which use terrestrial rookeries. Phylogenetic relationships and host ranges

The Metastrongyloidea is a relatively small (approximately 45 genera) super-family of parasitic nematodes which, like the Ancylostomatoidea, is confined to mammals. Anderson (1978) combined the economy of Dougherty’s (1949, 195 1b) classification system with the detailed morphological information of the system proposed by Soviet helminthologists (Boev, 1975; Kontrimavichus, Delyamure & Boev, 1976) to recognise 7 families in the Metastrongyloidea, 5 clearly defined, 2 less well

PSEUDALIIDAE

ODONTDCETES, VIVERRIDS

SKRJABINGYLIDAE

MUSTELIDS

FILAROIDIDAE ANGIOSTRONGYLIDAE

Fig. 7. Relationships

METASTRONGYLOIDEA

PRIMATES,CARNIVORES,PINNIPEDS MARSUPIALS,INSECTIVDRES, CARNIVORES,RODENTS

CRENOSOMATIDAE

INSECTIVORES.CARNIVORES. MARSUPIALS,PINNIPEDS

PROTOSTRONGYLIDAE

RUMINANTS, LAGOMORPHS

METASTRONGYLIDAE

SUIDS

of families of the Metastrongylina Lichtenfels, 1986.)

and their hosts. (Redrawn

from

Phylogeny of the Strongylida so. A diagrammatic representation of the relationship between the families was published by Lichtenfels (1986) and has been copied here (Fig. 7). The Metastrongylidae are confined to species of Metastrongylus occurring in the lungs of Suidae. They are characterised by 6 primitive lips fused into 2 large lateral trilobed labia, thick-shelled sculptured eggs containing a larva and an atypical bursa. The Protostrongylidae occur in the lungs, musculature or central nervous system of Bovidae, Cervidae, Antilocapridae and secondarily Leporidae. They are characterised by oviparity in the female and a highly developed bursa and complex accessory structures (telamon, gubernaculum and spicules) in the male. The Crenosomatidae occur in the bronchi of insectivores and carnivores, the nasal sinus of marsupials and the bronchi and veins of pinnipeds. They possess a spectrum of primitive morphological features, an amphidelphic, median vulva and ovejector with prominent sphincters, ovoviviparity and a highly developed bursa. The Angiostrongylidae are well represented geographically in marsupials, insectivores, carnivores and rodents and possess morphological features intermediate between the more primitive Protostrongylidae and Crenosomatidae and the more advanced Filaroididae. The 6 primitive lips are highly developed in some genera in marsupials (Didelphostrongylus, Heterostrongylus) and insectivores (Madangiostrongylus) but are greatly reduced in other genera in marsupials (Filostrongylus, Marsupostrongylus), insectivores (Stefanskostrongylus), rodents (Rodentocaulus) and carnivores (Aelurostrongylus). Similarly, males have a typical bursa in some genera (Gallegostrongylus, Angiostrongylus) but there is a tendency towards bursal reduction in others (Madafilaroides, Andersonstrongylus). Females are oviparous or ovoviviparous, prodelphic, possess a posterior vulva and the ovejector generally lacks a prominent sphincter. The Filaroididae occur in marsupials, primates and carnivores including pinnipeds. Males lack a true bursa although remnants of lateral and ventral rays may be well defined, aligning the family with the Angiostrongylidae. Females are ovoviviparous, the vulva is generally near the anus and the ovejector sometimes muscular and with a well-developed sphincter. The Skrjabingylidae occur exclusively in the frontal sinuses of Mustelidae. The bursa is uniquely modified to form lateral fleshy lobes. Females are ovoviviparous, amphidelphic, have a median vulva and an ovejector with a prominent sphincter. Finally, the Pseudaliidae occur exclusively in the lungs, circulatory system and cranial sinus of toothed whales (Odontoceti), with the sole exception of the genus

1159

Stenuroides in Viverridae (Arnold & Gaskin,

1975). Males have a reduced bursa with highly modified fusion of some rays. Females are ovoviviparous, prodelphic, have a posterior vulva and an ovejector without a prominent sphincter. Evolutionary mechanisms

Dougherty (1949) considered morphological modifications within the Metastrongyloidea in some detail and concluded that few families (Metastrongylidae, Filaroididae, Pseudaliidae and Protostrongylinae) had evolved closely with their particular host groups. Among the major metastrongyloid families, host specificity in the definitive host is narrow, suggesting a strong co-evolutionary pattern of host-parasite relationships. However, whether this specificity is physiological or ecological will be determined only with future acquisition of experimental evidence. Joyeux & Gaud (1943, 1946) recognised Protostrongylus rufescens var. rufescens in sheep and goats and P. rufescens var. cuniculorum in rabbits and hares, and suggested that these races cannot crossinfect the reciprocal hosts. This work requires confirmation by careful experimental study. Dunsmore and Spratt (unpubl. data), working in Australia under quarantine conditions were able to infect laboratory and wild rabbits as well as sheep with the putative P. rufescens var. cuniculorum during studies to augment myxomatosis in the biological control of rabbits in Australia, confirming doubts raised by Dougherty (1951b) concerning the validity of the 2 putative varieties. The appearance of heteroxenity and paratenesis in the transmission of nematode parasites of terrestrial vertebrates allowed parasitic nematodes to transfer to aquatic ecosystems by way of intermediate and paratenic hosts being eaten by fish (Anderson, 1988b). Nematode parasites invaded the marine environment a second time via the marine mammals. Many monoxenous forms could not make the transition and presumably became extinct. The species which did succeed were mainly the heteroxenous forms, although pinnipeds which use terrestrial rookeries have retained some of the monoxenous nematodes. As a consequence, “. . the fauna of marine mammals is, like that of fishes, a restricted fauna with unmistakable affinities to groups in terrestrial hosts” (Anderson, 1988b). In the Metastrongyloidea, species of Filaroides (ParaJilaroides) occur in both otariid and phocid seals. Species of Filaroides (Filaroides) occur widely in modern carnivores, especially mustelids and canids. Otariids and phocids evolved from terrestrial carnivores (Repenning, 1980; Wyss & Flynn, 1993;

1160

M.-C. DURETTE-DESSET

Arnason & Ledje, 1993) and although their ancestry may differ, their lungworms may have had a common origin in terrestrial carnivores before the appearance of pinnipeds. Similarly, the genus Otostrongylus (Crenosomatidae) occurs exclusively in Phocidae but allied genera (Crenosoma, Troglostrongylus) occur commonly in mustelids, ursids, felids and procyonids demonstrating another link between pinnipeds and terrestrial carnivores. Transmission of the pseudaliid lungworms of toothed whales (Odontoceti) has not been determined. Anderson (1982) stated that this nematode group has peculiar characters which suggest they are archaic forms which have persisted in whales in the absence of competing forms which could not persist in the aquatic ecosystem. The peculiar characters were not identified, but from a morphological viewpoint pseudaliids have a number of advanced rather than primitive features (reduced bursa with fusion of rays, prodelphic, posterior vulva, ovejector without prominent sphincter). Anderson (1982, 1984) argued that the single genus of pseudaliid in the frontal sinuses of the mongoose (Viverridae) perhaps represents the lone survivor of a lungworm group formerly widespread in terrestrial carnivores. He suggested that the pseudaliids have been replaced in terrestrial mammals by more recently evolved lungworms such as Angiostrongylidae and Filaroididae, the pseudaliids persisting, free of competition, only in the toothed whales (Odontoceti). This argument implies that the Angiostrongylidae and the Filaroididae became too specialised in terrestrial hosts or their descendants (Pinnipeds) to be able to spread to new hosts upon re-entry into the aquatic environment. Only those nematode groups arising from ancestors which infected the host percutaneously developed tissue parasitism and the use of intermediate hosts (Adamson, 1986). A percutaneous mode of transmission is considered primitive in nematode parasites of vertebrates and this was replaced by oral transmission in some groups (Chabaud 1955; Durette-Desset, 1985; Adamson, 1986). Nevertheless, larvae ingested orally underwent a migration through the lungs and trachea before returning to the intestine. This tracheal migration exposed larvae to a variety of host habitats. In the Metastrongyloidea, when maturation of nematodes occurred at an earlier stage in their tissue migration, this permitted colonisation of deep tissue sites, such as air passages, blood vessels and sinuses (Adamson, 1986). Intra-host competition probably led to extinction of some parasite lineages during radiation in the tissues of the host. Competition for sites in lungs

et al.

would be strong. Anderson (1982) suggested that the Skrjabingylidae represent an ancient remnant group which survived by isolating itself in the frontal sinuses of the host, leaving the lungs to colonisation by more recent groups like the Angiostrongylidae and Filaroididae. One exceptional possibility in metastrongyloids is that of a paratenic host replacing an intermediate host. Filaroides (Parafilaroides) decorus develops to the infective third-stage larva in coprophagic fish (Dailey, 1970). This subgenus of lungworms in pinnipeds appears closely related to the subgenus Filaroides in mustelids and canids which use terrestrial gastropods as intermediate host (Anderson, 1978). Anderson (1984) suggested that the coprophagic fish paratenic host had, during evolution, replaced the invertebrate intermediate host and become a true intermediate host in its own right. Paratenesis increases the number of hosts encountered by a parasite. A parasite may be advantaged during this phase and recommence development in the paratenic host converting it to an intermediate host through precocious development, as occurs in Ascaridoidea, or colonising the paratenic host and in the process acquiring a new definitive host. This latter phenomenon is most likely to occur in lungworms using vertebrate paratenic hosts (Crenosomatidae) resulting in “capture” of a parasite from one vertebrate to another unrelated vertebrate and subsequent speciation (Chabaud, 1965). Life cycles

Most adult “lungworms” are associated with the respiratory system, primarily the lungs (Marsupostrongylus spp.), but others are associated with lymph and blood vessels of the body (Parelaphostrongylus tenuis, Angiostrongylus spp.), or with nasal sinuses (Skrjabingylus spp.) and cranial sinuses (Stenurus spp.). Some bypass the lungs altogether (Skrjabingylidae, Angiostrongylus costaricensis). Generally however, species living in the lungs deposit unembryonated eggs, embryonated eggs or first-stage larvae and those living distant from the lungs deposit unembryonated eggs which are carried to the lungs in blood. Unembryonated eggs embryonate in the lungs, larvae hatch and first-stage larvae escape from the lungs via the bronchial escalator, are swallowed and passed from the definitive host via the alimentary tract and faeces. The earliest nematode parasites of vertebrates were monoxenous and probably infected the host by a percutaneous route (Ftilleborn, 1920). Isolation or “seclusion” of free-living stages from the perils of the

Phylogeny of the Strongylida external environment resulted in development of cuticle retention by infective larval forms, development of non-parasitic stages within an environmentally resistant egg or development within an intermediate host (Chabaud, 1954). Metastrongyloids are the only group of bursate nematodes exhibiting heteroxenity and it is assumed that they acquired intermediate hosts after having been monoxenous parasites like the Trichostrongylina and the Ancylostomatoidea (Anderson 1982). Possible evidence of this may be found in the persistence of monoxenous cycles in Osierus osleri of canids (Urquhart, Jarrett & O’Sullivan, 1954; Dorrington, 1965, 1968; Polley & Creighton, 1977; Dunsmore & Spratt, 1979), ~iiuro~des hirthi of canids (Georgi, 1976; Georgi, Fleming, Hirth & Cteveland, 1976; Georgi, Georgi & Cleveland, 1977) and Andersonstrongyhs cuptivensis of mustelids (Webster, 1980) with first-stage infective larvae being passed to new hosts via regurgitative feeding, coprophagy or both, respectively. However, Anderson (1982) considered heteroxenity as basic and primitive in the Metastrongyloidea and that monoxenity was a secondarily acquired feature, i.e. the intermediate host was subsequently lost during the course of evolution. Anderson (1982, 1988a) recognised 3 types of heteroxenity within lungworms: 1. The primitive mode of transmission where the intermediate host is an essential item in the diet of the definitive host (lungworms of insectivores, rodents, small carnivores). 2. The mode of transmission where there is dependence upon consumption of large quantities of herbage and where the intermediate host is ingested accidentally with the food of the definitive host (lungworms of ruminants and lagomorphs). 3. The mode of transmission where a vertebrate paratenic host, which feeds on gastropods and is itself part of the diet of the definitive host, is located between the intermediate and definitive hosts. Members of the super-family generally utilise gastropods, primarily terrestrial forms, as intermediate hosts although several exceptions are known. Metastrungylus spp. of suids utilise earthworms as intermediate hosts (Schwartz & Alicata, 1934; Alicata, 1935; Dunn, 1955; Bhattacharyya, Sinha & Sarkar, 1971), Filaroides (Pura~laroides) decorus in sea lions utilises coprophagic fish (Dailey, 1970) and third-stage larvae of ProtostrongyZus stilesi ingested in alpine snails by pregnant bighorn ewes, cross the placenta and enter the liver of the foetus, moving to

1161

the lungs and maturing to adults after birth of the lamb (Hibler, Lange & Metzger, 1972). The use of transport hosts (paratenesis) subsequently evolved in order to adapt heteroxenous life cycles to the evolving food habits of radiating carnivorous vertebrates (Anderson, 1982). Metastrongyloids of carnivores in particular have utilised these life-cycle modifications as an evolutionary mechanism. They make broad use of vertebrate paratenic hosts (e.g. amphibians, reptiles, rodents) placed, as in the Spirurida, between the intermediate and definitive hosts, to ensure that infective larvae are brought into the food-chain of the definitive host. Anderson (1982) considered this feature crucial for survival of nematode parasites during the evolution of the Carnivora, acting as an ecological rather than a physiological requirement in transmission. CONCLUSION

By any measure, the Strongylida must be deemed an extremely successful group of parasites. They occur in all major groups of tetrapods, but have had their greatest success in the mammals. It is clear that in order to achieve this success, the Strongylida have taken advantage of a range of mechanisms, including co-evolution and host-switching; they have taken advantage of host migrations and have adopted intermediate hosts as well as invading parts of the mammalian body outside the gastro-intestinal tract. In each order, 1 or 2 mechanisms, appeared to predominate. Thus, in the Strongylida co-evolutionary relationships appear to have been a major influence of host-parasite relationships, while in the Trichostrongylina, host-switches and host dispersal have been major determinants of the evolution of this group. The phylogeny of the Ancylostomatoids shows little correlation with host taxonomic position, but does match feeding preferences of hosts, while in the ~etastrongyloidea, life-cycle modifications are a dominant evolutionary phenomenon with the extensive use of intermediate and paratenic hosts, and’ the invasion of numerous extra-intestinal sites. In spite of their prominence, their economic importance and their significance in human health, this review also illustrates the uncertainties that remain in our knowledge of the order and in how it has achieved its obvious success as a parasitic group and emphasises the tentative nature of many of the phylogenetic hypotheses which have been tendered to date. Clearly, many intriguing questions still remain to be answered about the evolution of these nematodes and how they have achieved the degree of diversification evident to us today.

1162

M.-C. DURETTE-DESSET

REFERENCES Adamson M. L. 1986. Modes of transmission and evolution of life histories in zooparasitic nematodes. Canadian Journal of Zoology 64. 1375-1384.

Alicata J. E. 1935. Early development stages of nematodes occurring in swine. Technical Bulletin No. 489. United States Department of Agriculture, Washington, DC. Anderson R. C. 1978. Commonwealth Institute of Helminthology Keys to the Nematode Parasites of Vertebrates. No. 5. Keys to genera of the superfamily

Metastrongyloidea (Edited by Anderson R. C., Chabaud A. G. & Wilhnott S.) pp. 140. Commonwealth Agricultural Bureaux, Famham Royal, U.K. Anderson R. C. 1982. Host-parasite relations and evolution of the Metastrongyloidea (Nematoda), Deuxieme Symposium sur la specificite parasitaire des parasites de vertebres, 13-17 Avril, Memoires du Museum National d’Histoire Naturelle, Nouvelle Serie. Ser. A, Zoologie 123: 129-133. Anderson R. C. 1984. The origins of zooparasitic nematodes. Canadian Journal of Zoology 62: 317-328. Anderson R. C. 1988a. Nematode transmission patterns. Journal of Parasitology 74: 3045.

Anderson R. C. 1988b. Nematodes, how did they become parasitic? Wardle Award Address. Canadian Society of Zoologists Bulletin 19: 10-l 3. Anderson R. C. 1992. Nematode Parasites of Vertebrates, Their Development and Transmission. C.A.B. International, Wallingford. Amason U. & Ledje C. 1993. The use of highly repetitive DNA for resolving cetacean and pinniped phylogenies. In Mammal Phylogeny - PlacentaIs (Edited by Szalay F. S., Novacek M. J. & McKenna M. C.), pp. 75-80. Springer, Berlin. Arnold P. W. & Gaskin D. E. 1975. Lungwonus (Metastrongyloidea: Pseudaliidae) of harbour porpoise, Phocoena phocoena (L. 1758). Canadian Journal of Zoology 53: 713-735.

Baverstock P. R., Krieg M. & Birrell J. 1990. Evolutionary relationships of Australian marsupials as assessed by albumin immunology. Australian Journal of Zoology 37: 273-287.

Beveridge I. 1982. Evolution of the Strongyloid nematodes of Australian marsupials. Memoires du Museum national d’Histoire naturelle, Paris, Nouvelle Serie, Ser. A. Zoologie 123: 87-91. Beveridge I. 1987. The systematic status of Australian Strongyloidea (Nematoda). Bulletin du Museum national d’Histoire naturelle, Paris 4 eme ser. 9: 107-126.

Beveridge I. Chilton N. B. Kc Andrews R. 1993. Sibling species within Macropostrongyloides baylisi (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology 23: 21-33.

Bhattacharyya H. M. Sinha P. K. & Sarkar P. B. 1971. Studies on the incidence of Metastrongylus salmi in West Bengal with observations on its life cycle. Indian Veterinary Journal 48: 993-996.

Boev S. N. 1975 [Principles of Nemacology (Edited by Ryzhikov K. M.), Vol. XXV. Protostrongylidae] Izdatel’stvo “Nauka”, Moscow, USSR. [In Russian.]

et al.

Cameron T. W. M. 1964. Host specificity and the evolution of hehninthic parasites. Advances in Parasitology 2: l-34. Cassone J., Durette-Desset M.-C. & Presidente P. J. A. 1986. Nouvelle hypothese sur l’evolution des Herpetostrongylinae (Nematoda, Trichostrongyloidea) parasites de Marsupiaux Australiens. Bulletin du Museum national d’Histoire naturelle, 4&me ser. 8: 267-283. Chilton N. B., Beveridge I. & Andrews R. H. 1992. Detection by allozyme electrophoresis of crytic species of Hypodontus macropi (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology 22: 271-279.

Chabaud A. G. 1954. Sur le cycle Cvolutif des Spirurides et de Nematodes ayant une biologie comparable. Valeur systematique des caracttres biologiques. Annales de Parasitologie humaine et comparee 29: 42-88.

Chabaud A. G. 1955. Essai d’interpretation phyletique des cycles tvolutifs chez les Nematodes parasites de VertCbrCs. Annales de Parasitologie humaine et comparee 30: 83-126.

Chabaud A. G. 1957. Revue critique des nematodes du genre Quilonia Lane, 1914 et du genre Murshidia Lane, 1914. Annales de Parasitologie humaine et comparee 32: 98-131.

Chabaud A. G. 1965. Ordre des Strongylida. In: Trait& de Zoologie Vol 4 (Edited by Grasse P.-P.), pp. 869-931. Masson, Paris. Chabaud A. G. Puylaert F., Bain 0.. Petter A. J. & Durette-Desset M.-C. 1970. Remarques sur l’homologie entre les papilles cloacales des Rhabditides et les totes dorsales des Strongylida. Compte Rendus hebdomadaires des seances de ljicademie des sciences 271: 1771-1774. Chabaud A. G. & Durette-Desset M.-C. 1973. Description dun nouveau nematode oesophagostome, parasite d’Hyemoschus au Gabon, et remarques sur le genre Oesophagostomum. Bulletin du Museum national d’fiistoire naturelle, Parts, 3 eme ser., Zoologie 123: 1415-1424.

Chabaud A. G. 1974. Class Nematoda. Keys to subclasses, orders and superfamilies. In: Commonwealth Institute of Helminthology Keys CO the Nematode Parasites of Vertebrates, No. 1. General Introduction (Edited by

Anderson, R. C., Chabaud A. G. & Willmott S.), pp. 617. Commonwealth Agricultural Bureaux, Famham Royal, U.K. Chabaud A. G. & Tcheprakoff R. 1977. Sur Chapiniella diazi n.sp., strongylide parasite de Testudo denticulaca au Venezuela. Bulletin du Museum national dHistoire naturelle. Paris, 3 eme ser., Zoologie 326: 765-769.

Chabaud A. G. & Durette-Desset M.-C. 1981. Parasitisme par plusieurs esptces congeneriques. Bulletin de la Societe zoologique de France

103: 459464.

Chitwood, B. G. 1950. Cephalic structures and stoma. In: An Introduction to Nematology (Edited by Chitwood B. G. & Chitwood M. B.), pp. 5677. University Park Press, Baltimore. Clemens W. A., Richardson B. J. & Baverstock P. R. 1989. Biogeography and phylogeny of the Metatheria. In: Fauna of Australia, Vol 1B (Edited by Walton D. W. & Richardson B. J.) pp. 527-548. Australian Government Publishing Service, Canberra.

Phylogeny of the Strongylida J. 1988. The major clades of birds. In: The Phylogeny and Classification of the Tetrapods, Vol. 1:

Cracraft

Amphibians, Reptiles, Birds. (Edited by Benton M. J.) Systematics Association Special Volume No. 35A, pp. 339-361. Clarendon Press, Oxford. Dailey M. D. 1970. The transmission of Parafilaroides decorus (Nematoda: Metastrongyloidea) in the Californian sea lion (Zalophus californianus). Proceedings of the Helminthological Society of Washington 31: 215-222.

Dorrington J. E. 1965. Preliminary report on the transmission of Filaroides osleri (Cobbold, 1879) in dogs. Journal of the South African Veterinary Medical Association 36: 389. Dorrington J. E. 1968. Studies on Filaroires osleri infestation in dogs. Onderstepoort Journal of Veterinary Research 35: 225-285.

Dougherty E. C. 1949. The phylogeny of the nematode family Metastrongylidae Leiper, (1909): a correlation of host and symbiote evolution. Parasitology 39: 222-234. Dougherty E. C. 1951b. A further revision in the classification of the family Metastrongylidae Leiper (1909) (Phylum Nematoda). Parasitology 41: 91-96. Dougherty E. C. 1951a. Evolution of that groups in the phylum Nematoda, with special reference to host distribution. Journal of Parasitology 31: 353-378. Dunn D. R. 1955. The culture of earthworms and their infection with Metastrongylus spp. British Veterinary Journal 111: 97-101. Dunsmore J. D. & Spratt D. M. 1979. The life history of Filaroides osleri in wild and domestic canids in Australia. Veterinary Parasitology

5: 275-286.

Durette-Desset M.-C. 1971. Essai de classification, des Nematodes Heligmosomes. Correlations avec la paltobiogeographie des h&es. Memoires du Museum national d’Histoire naturelle, Paris, nouvelle serie, ser. A. Zoologie 69: 1-126. Durette-Desset M.-C. & Chabaud A. G. 1977. Essai de classification des nematodes Trichostrongyloidea. Annales de Parasitologic humaine et comparee 52: 539-558.

Durette-Desset M.-C. & Chabaud A. G. 1981. Nouvel essai de classification des Nematodes Trichostrongyloidea. Annales 297-312.

de

Parasitologie

humaine

et

comparee

56:

Durette-Desset M.-C. 1982. Relations hbtes-parasites chez les Trichostrongyloides. Memoires du Museum national d’Histoire naturelle, Paris, Ser. A, Zoologie 123: 93-101. Durette-Desset M.-C. 1983 Commonwealth Institute of Helminthology Keys to the Nematode parasites of Vertebrates. No. 10. Keys to genera of the superfamily

Trichostrongyloidea. (Edited by Anderson R. C. & Chabaud A. G.) pp. l-68. Commonwealth Agricultural Bureaux, Farnham Royal, U. K. Durette-Desset M.-C. 1985. Trichostrongyloid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24: 239-306.

Durette-Desset M.-C. & Vaucher C. 1988. Trichostrongyloidea (Nemodata) parasites de Chiropttres neotropicaux. II. Nouvelles don&es sur le genre Cheiropteronema Sandground, 1929. Revue Suisse de Zoologie 95: 889-899.

1163

Durette-Desset M.-C. & Justine J.-L. 1991. A cladistic analysis of the genera in the subfamily Pudicinae (Nematoda, Trichostrongyloidea, Heligmonellidae). International Journal for Parasitology

21: 579-587.

Durette-Desset M.-C. & Chabaud A. G. 1993. Nomenclature des Strongylida au-dessus du groupe - famille. Annales de Parasitologie humaine et comparee 68: 11l-l 12. Durette-Desset M.-C., Ben Slimane B., Cassone J., Barton D. P. & Chabaud, A. G. 1994. Johnpearsonia gen. nov. and Johnpearsoniinae subf. nov. (Molineoidea, Nematoda) from Bufo marinus, with comments on the primitive trichostrongyle parasites of amphibians and reptiles. Parasite 1: 153-160. Dvoinos G. M. 1982. [Systematics and phylogeny of nematodes of the superfamily Strongyloidea Weinland, 1858, parasitic in horses.] In: Parazity i parazitozy cheloveka i zhivotnyka, pp. 106114. Naukava Damka, Kiev, U.S.S.R. [In Russian.] Flannery T. F. 1989. Phylogeny of the Macropodoidea; a study in convergence. In: Kangaroos, Wallabies and Ratkangaroos, pp. 146. (Edited by Grigg G., Jarman P. & Hume I.). Surrey Beatty & Sons, New South Wales. Ftillebom F. 1920. ijber die Anpassung der Nematoden an den Parasitismus und den Infectionsweg bei Askaris und anderen Fandenwtirmern des Menschen. Archiv fur Schtffs-und Tropen-Hygiene, Pathologie Exotischer Krankheiten 24: 34&347.

und Therapie

Gaffney E. S. & Meyland P. A. 1988. A phylogeny of turtles. In: The Phylogeny and Classification of the Tetrapods, Volume I: Amphibians, Reptiles, Birds (Edited by Benton M. J.) pp. 157-219. Systematics Association Special Volume No. 35A. Clarendon Press, Oxford. Georgi J. R. 1976. Filaroides hirthi: experimental transmission among beagle dogs through ingestion of first-stage larvae. Science 194: 735. Georgi J. R., Fleming W. J., Hirth R. S. & Cleveland D. J. 1976. Preliminary investigation of the life history of Filaroides hirthi Georgi and Anderson, 1975. The Cornell Veterinarian 66: 309-323.

Georgi J. R., Georgi M. E. & Cleveland D. J. 1977. Patency and transmission of Filaroides hirthi infection. Parasitology 15: 251-257.

Gibbs H. C. 1961. Studies on the life cycle and developmental morphology of Dochmotdes stenocephala (Railliet, 1884) (Ancylostomatidae: Nematoda). Canadian Journal of Zoology 39: 325-348. Glen D. R. & Brooks D. R. 1985. Phylogenetic relationships of some strongylate nematodes of primates. Proceedings of the Helminthological Society of Washington 52: 227-236. Goldberg A. 1951. The life history of Oesophagostomum venulosum, a nematode parasite of sheep and goats. Proceedings of the Helminthologieal Society of Washington 18: 3647.

Hibler C. P., Lange R. E. & Metzger C. 0. 1972. Transplacental transmission of Protostrongylus spp. in bighorn sheep. Journal of Wildlife Diseases 8: 289. Hoffstetter R. & Lavocat R. 1970. Decouverte dans le Deseadien de Bolivie du genre Pentalophontes appuyant les affinitts africaines des Rongeurs Caviomorphes.

1164

M.-C. DURETTE-DESSET

Compte Rendus hebdomadaires des seances de I’Acaddmie des sciences 271: 172-175.

Hope R., Cooper S. & Wainwright B. 1990. Globin macromolecular sequences in marsupials and monotremes. Australian Journal of Zoology 37: 289-313. Hume I. D. 1982. Digestive Physiology and Nutrition of Marsupials. Cambridge University Press, Cambridge. Humphery-Smith I. 1983. An hypothesis on the evolution of Herpetostrongylinae (Trichostrongyloidea: Nematoda) in Australian marsupials, and their relationships with Viannaiidae, parasites of South American marsupials. Australian Journal of Zoology 31: 931-942. Joyeux C. & Gaud J. 1943. La pneumonie vermineuse des ovins au Maroc. Bulletin de la Socit% de pathologie exotique 36: 232-235.

Joyeux C. & Gaud J. 1946. Recherches hClminthologiques marocains. Etudes sur la pneumonie vermineuse. Archives de I’lnstitut Pasteur. Maroc 3: 383-461.

Kontrimavichus V. L., Delyamure S. L. & Boev S. N. 1976. [Principles of Nematology] Vol XXVI. (Edited by Ryzhikov K. M.) Metastrongyloidea of Domestic and Wild Animals.] Izdatel’stvo “Nauka”, Moscow, U.S.S.R. [in Russian] Kowalski K. 1961. L& micromammiftres du Plioctne et du Pleistodne inf&ieur de la Pologne. Colloques Znternationaux du Centre National de Recherche No. 104: 409416.

Scientifique

Lichtenfels J. R. 1979. A conventional approach to a new classification of the Strongyloidea, nematode parasites of mammals. American Zoologist 19: 1185-l 194. Lichtenfels J. R. 1980a Commonwealth Znstirute of Helminthology Keys to the Nematode Parasites of Vertebrates. No. 7. Keys to genera of the superfamily

Strongyloidea (Edited by Anderson R. C., Chabaud A. G. & Willmott S.) pp. 14. Commonwealth Agricultural Bureaux, Farnham Royal, U.K. Lichtenfels J. R. 1980b. Commonwealrh Institute of Helminthology Keys to the Nematode Parasites of verfebrutes. No. 8. Keys to genera of the superfamilies

Ancylostomatoidea and Diaphanocephaloidea (Edited by Anderson R. C., Chabaud A. G. & Willmott S.) pp. l-264. Commonwealth Agricultural Bureaux, Farnham Royal, U.K. Lichtenfels J. R. & Stewart T. B. 1981. Three new species of Chapiniella Yamaguti. 1961 (Nematoda: Strongyloidea) from tortoises. Proceedings of the Helminthological Society of Washington 48: 137-147.

Lichtenfels J. R. 1986. Phylogenetic inference from adult morphology in the Nematoda; with emphasis on the bursate nematodes, the Strongylida; advancements (1982-1985) and recommendations for further work. In Parasitology - Quo Vadit? Proceedings of the Sixth International Congress of Parasitology (Edited by Howell

M. J.), pp. 269-279. Australian Academy of Science, Canberra. Osche G. 19.58. Die Bursa- und Schwanzstrukturen und ihre Aberrationen bei den Strongylina (Nematoda); morphologische Studien zur Problem der Pluri und Paripotenzerscheinungen. Zeitschrift ftir Morphologie und tikologie der Tiere 46: 571635.

et al.

Polley L. & Creighton S. R. 1977. Experimental direct transmission of the lungwonn Filuroides osleri in dogs. Veterinary Record 100: 136137. Popova T. I. 1958. Essentials of Nematodology. Vol. 7. Strongyloids of animals and man. Trichonematidae (Edited by Skrjabin K. I.) Akademia Nauk, S.S.S.R. [English translation by Israel Program for Scientific Translation, 19651 Rausch R. L. 1982. Cestodes in mammals: the zoogeography of some parasite-host assemblages. MPmoires du MusPurn national d’histoire naturelle, Paris, SCr. A. Zoologie 123: 179-l 83. Repenning C. A. 1980. Warm-blooded life in cold ocean currents. Following the evolution of the sea. Oceans 13: 18-24. Richardson B. J. 1988. A new view of the relationships of marsupials. Australian Australian and American Mammalogy 11: 71-73. Rossi P. 1983. Sur le genre Nemarodirus Ransom, 1907 (Nematoda: Trichostrongyloidea). Annales de Parasitologie humaine et comparPe 58: 557-581.

Schad G. A. 1962. Studies on the genus Kalicephalus (Nematoda: Diaphanocephalidae) II. A taxonomic revision of the genus Kalicephalus Molin, 1861. Canadian Journal of Zoology 40: 1035-l 165.

Schulz R. S. 1951. Filogenez nematod podotryada strongilyat i perestroika systemy Metastrongyloidea. Doklady Akademii Nauk SSSR 8: 293-296.

Schwartz B. & Alicata J. E. 1934. Life history of lungworms in swine. Technical Bulletin No. 456 United States Department of Agriculture, Washington, D.C. Skrjabin K. I., Shikhobalova N. P., Schulz R. S., Popova T. I., Boev S. N. & Delyamure S. L. 1952. Key to the parasitic nematodes. Vol. 3. Strongylata (Edited by Skrjabin K. I.). Akademiya Nauk S.S.S.R. [English translation by Israel Program for Scientific Translations, 19611. Smales L. R. 1992. A survey of the helminths of Rattus sordidus, the canefield rat, together with a description of Ancistronema coronatum ng., n. sp. (Nematoda: Chabertiidae). Systematic Parasitology 22: 73-80. Spratt D. M.. Beveridge I. & Walter E. L. 1991. A catalogue of Australasian monotremes and marsupials and their recorded helminth parasites. Records of the South Australian Museum, Monograph Series 1: l-105. Stahl B. 1985. Vertebrate History: Problems in Evolution. (Second edition) Dover Publications: New York. Stirton. R. A.. Tedford R. A. & Woodboume M. 0. 1968. Australian Tertiary deposits containing terrestrial mammals. Universiry of California Publications in Geological Science 77: l-30.

Thaler L. 1962 Campagnols primitifs de 1’Ancien et du Nouveau Monde. Colioques Znternationaux du Centre National de Recherche Scientijque No. 104 387-398.

Urquhart G. M., Jarrett W. R. H. & O’Sullivan J. G. 1954. Canine tracheobronchitis due to infection with Filaroides osleri. Veterinary Record 66: 143-145.

Waddell, A. H. 1969. The parasitic life cycle of the kidney worm Srephanms dentafua D&sing. Australian Journal of Zoology 17: 607-618.

Phylogeny of the Strongylida Watts C. H. S. & Aslin H. J. 1981. The Rodents of Australia. Angus & Robertson, Sydney. Webster W. A. 1980. The direct transmission of Andersonstrongylus captivensis Webster, 1978 (Metastrongyloidea: Angiostrongylidae) in captive skunks Mephitis mephitis (Schreber). Canadian Journal of Zoology 58: 12001203.

1165

Westerman M., Janczewski D. N., O’Brien S. J. 1990. DNA-DNA hybridisation studies and marsupial phylogeny. Australian Journal of Zoology 31: 315-323. Wyss A. R. & Flynn J. J. 1993. A phylogenetic analysis and definition of the Camivora. In Mammal Phylogeny Placentals (Edited by Szalay F. S., Novacek M. J. & McKenna M. C.), pp. 33-50, Springer, Berlin.