A cladistic analysis of the Trichostrongyloidea (Nematoda)

A cladistic analysis of the Trichostrongyloidea (Nematoda)

M.C. Durette-Desset a, *, J.P. Hugot b, P. Darlu c, A.G. Chabauda

aMuseÂum national d'Histoire naturelle, Paris, Laboratoire de Biologie Parasitaire, associeÂ au CNRS et Ecole Pratique des HautesEtudes, 61, rue Bu�on, 75231 Paris Cedex 05, France

bMuseÂum national d'Histoire naturelle, Paris, Institut de BiosysteÂmatique (FR CNRS 1541), 55, rue Bu�on, 75231 Paris Cedex 05,France

cINSERM U 155, EpideÂmiologie GeÂneÂtique, UniversiteÂ Denis Diderot, case 7041, 2, Place Jussieu, 75251 Paris Cedex 05, France

Received 4 November 1998; received in revised form 11 February 1999; accepted 1 March 1999

Abstract

A morphologically based cladistic analysis of 40 genera included within the Trichostrongyloidea(Amidostomatidae, Dromaeostrongylidae and Trichostrongylidae) is proposed. Two genera were used as outgroups,one from the Strongylina and the other from the Ancylostomatina. Seven genera do not appear in the matrixbecause some signi®cant morphological characters remain unknown for these genera. Nonetheless, except forMoguranema which is excluded as incertae sedis, a likely systematic position could be assigned to them based on themorphological characters that are known.The classi®cation which best ®ts the consensus tree is composed of three families. In adding the genera not

included in the tree, we obtain: (i) Trichostrongylidae with three sub-families, Amidostomatinae (four genera),Filarinematinae (three genera) and Trichostrongylinae (®ve genera); (ii) Haemonchidae with two sub-families:Ostertagiinae (eight genera) and Haemonchinae (®ve genera); (iii) Cooperiidae with three sub-families:Libyostrongylinae (®ve genera), Obeliscoidinae n. subfam. (®ve genera) and Cooperiinae (ten genera).Dromaeostrongylus and Ortleppstrongylus, whose females have a caudal spine, are excluded from theTrichostrongyloidea and are placed in the Molineoidea. The hypotheses relating to the evolutionary history of theTrichostrongyloidea are: the origin of the superfamily could have occurred during the upper Cretaceous period. Thetwo most ancient sub-families (Amidostomatinae and Filarinematinae) would be of Gwondwanan origin andevolved during the Paleocene period within Neotropical aquatic birds and within the Australian marsupials. TheTrichostrongylinae would have arisen during the Eocene period within birds and then adapted to diverse archaicmammals in the Neotropical region on one hand and in the Nearctic region, on the other hand and lastly adaptedto the Lagomorpha and subsequently to the Ruminantia. In both families originating from the Trichostrongylidae,the adaptation to the Lagomorpha may have taken place during the Oligocene but in a di�erent way. In theHaemonchidae, the Ostertagiinae may have passed directly from the Neartic region to Europe. In the Cooperiidae,the adaptation to Lagomorpha may have occurred either within the Libyostrongylinae which may have remained inthe Ethiopian region since the Paleocene, or, more likely, by the passage of the Obeliscoidinae from the Nearcticregion to the Asian, through the Bering strait.In all cases, the adaptation of the Trichostrongyloidea of Lagomorpha to Ruminants apparently took place

during the Miocene, mainly in the Palearctic and the Ethiopian regions. # 1999 Australian Society for ParasitologyInc. Published by Elsevier Science Ltd. All rights reserved.

Keywords: Nematoda; Trichostrongyloidea; Cladistic analysis; Mammals; Birds; Paleobiogeography

International Journal for Parasitology 29 (1999) 1065±1086

0020-7519/99/$20.00 # 1999 Australian Society for Parasitology Inc. Published by Elsevier Science Ltd. All rights reserved.

PII: S0020-7519(99 )00028-4

* Corresponding author. Tel.: +33 1 4079 3509; fax: +33 1 4079 3499; e-mail: [email protected]

1. Introduction

The genera within the superfamily Trichostron-gyloidea have been di�cult to classify becauseseveral comprise of just a few species and a num-ber are monotypic. Generally, genera are mor-phologically very di�erent, thus ordering theminto suprageneric taxa is not easy and leads to amultiplication of taxonomic subdivisions. Also,the validity of the Trichostrongyloidea as a natu-ral group has been questioned. The presence ofthe Amidostomatidae within the Trichostrongy-loidea, for instance, still remains a topic ofdebate [1±3]. The type genus Trichostrongylus isatypical and is di�cult to associate with a speci®clineage. Consequently, a cladistic analysis of theTrichostrongyloidea may be helpful in resolvingsome of these di�culties. To some extent, suchan analysis was conducted by Hoberg andLichtenfels [4]), but we disagree with their con-clusions for the reasons stated in Section 4.

2. Materials and methods

2.1. Delineation of the ingroup and outgroups

The order Strongylida which comprises allnematodes with a caudal bursa, is currently sub-divided into four suborders, Ancylostomatina,Strongylina, Trichostrongylina andMetastrongylina [5]. The Strongylina and theAncylostomatina have a well-developed buccalcapsule and can be separated from the Tricho-strongylina and the Metastrongylina, which havea buccal capsule that is reduced or absent. TheTrichostrongylina can be distinguished from theMetastrongylina because their ®rst larval stagehas a valvular oesophageal bulb and a simpleconical tail ending in a simple sharp spine,whereas in the Metastrongylina the oesophagushas a bulb without a valve and a tail with acurled tip. The Trichostrongylina are subdividedinto three super-families. The Heligmosomoidea,which can be distinguished from the Trichostron-gyloidea and the Molineoidea, by having abilaterally asymmetrical synlophe. The Trichos-trongyloidea can be distinguished from the Moli-

neoidea because their adult females have nospine on the tail.

Prior to 1993, the super-family Trichostrongy-loidea was composed of 14 families [6]. Sub-sequently, Durette-Desset and Chabaud [5]elevated the super-family Trichostrongyloidea tothe sub-order Trichostrongylina with three super-families, the Trichostrongyloidea, the Molineoi-dea and the Heligmosomoidea. The present studydeals with the cladistic analysis of the Trichos-trongyloidea which, according to Durette-Dessetand Chabaud [5], is comprised of only 2 families,the Dromaeostrongylidae and the Trichostrongy-lidae. In this work, the Amidostomatidae areconsidered to belong within the Trichostrongyloi-dea. The genera Oesophagostomum (Hysteracrum)(Strongylina) and Bioccastrongylus (Ancylosto-matina) are used as outgroups because the sub-orders to which they belong are considered to besister groups, the reduction of the buccal capsuleof the Trichostrongylina being a secondaryphenomenon [7, 8]. Seven genera within the Tri-chostrongyloidea are excluded because descrip-tions of some of their characters such as thebuccal structure, synlophe or caudal bursa areunknown. These genera are Moguranema Yama-guti, 1941, Pseudamidostomum Boulenger, 1926,Graphinema Guerrero and Chavez, 1984, Hoa-zinstrongylus Pinto and Gomes, 1985, Biogastra-nema Rohrbacher and Ehrenford, 1954,Minutostrongylus Le Roux, 1936 and LeiperiatusSandground, 1930.

Moguranema parasitises Mogura (Talpidae) inJapan. Described as being devoid of a caudalspine on the female it may therefore be a memberof the Trichostrongyloidea. It appears to be anarchaic genus with a corona radiata but the pos-ition of the genus remains enigmatic. Pseudami-dostomum parasitises aquatic birds. It is closelyrelated or identical to Epomidiostomum. Graphi-nema which parasitises Lama in South America isa member of the Trichostrongylinae. Hoazin-strongylus, which parasitises the relictual birdHoazin in Amazonia may be classi®ed in theObeliscoidinae due to the pattern of the caudalbursa. Biogastranema which parasitises Lagomor-pha in the USA seems to be closely related toObeliscoides. Minutostrongylus, which parasitises

M.C. Durette-Desset et al. / International Journal for Parasitology 29 (1999) 1065±10861066

Taurotragus (Bovidae) in Africa, is a member ofthe Cooperiinae and Leiperiatus which parasitisesHippopotamus belongs to the Haemonchinae.

Two other genera Dromaeostrongylus Lubimov,1933 and Ortleppstrongylus Durette-Desset, 1970,previously classi®ed in the Trichostrongyloideaare now transferred into the Molineoidea becausetheir females have a spine on the tail.

Although the systematics of the Ostertagiinaeremain confused, for the purposes of this study,we have retained the six genera de®ned by Dur-ette-Desset [9] plus Graphidium and Hyostrongy-lus.

2.2. Characters

1. Caudal spine. According to Osche [10] andChabaud [8], the female caudal spine in theStrongylida is a plesiomorphic larval charac-ter. This caudal spine is present in one of theoutgroups, Bioccastrongylus (Ancylostomina).The absence of the caudal spine in the Tri-chostrongyloidea is the apomorphic state ofthe character.

2. Buccal capsule. The large bucal capsule whichis present in both the outgroups, Oesophagos-tomum (Hysteracrum) (Strongylina) (Fig. 1)and Bioccastrongylus (Ancylostomina)(Fig. 20), is reduced or absent in the Tricho-strongyloidea. The reduction of the buccalcapsule in the Trichostrongyloidea is theapomorphic state of the character.

3. Bulbous vesicle. Some of the Trichostrongyloi-dea are characterised by the presence of a syn-lophe, i.e. the whole of the longitudinalcuticular ridges on the outer surface of thebody. The synlophe functions in locomotionor in the attachment of the worm to the hostintestinal villi. We suppose that the function-ing of the synlophe is controlled by variationof the osmotic pressure. This osmotic pressurecould depend on the cuticular dilatations ofthe head, termed ``bulbous vesicle'' and``cephalic vesicle''. When the synlophe ispoorly-developed, there is no cephalic vesiclebut the cephalic cuticle is swollen around the

cephalic papillae (Fig. 2) and forms a bulbous

vesicle, which is an apomorphic character.

4. Cephalic vesicle. When the synlophe is well-

developed, the cephalic vesicle is a complex

organ with a swollen anterior pericephalic sec-

tion and a thin, cervical posterior section. The

cephalic vesicle is completely separated from

the body cuticle (Fig. 3). This character is

apomorphic.

5. Peribuccal epaulets. The genus Epomidiosto-

mum, closely related to the genus Amidosto-

mum in all characters, possesses a modi®ed

cephalic extremity forming peculiar peribuccal

epaulets (Fig. 4) which is an autapomorphy

for the genus.

6. Oesophageal cuticular thickening. The cuticular

thickening of the anterior part of the oesopha-

gus with a large dorsal tooth is the equivalent

of a buccal capsule (Fig. 5). This character is

an autapomorphy for the genus Filarinema.

7±19. Buccal aperture and cephalic characters.

7. The rhabditid type of head is the plesio-

morphic state for the character. The minute,

rounded buccal aperture with oesophageal cu-

ticular thickening and no tooth (Fig. 6) is an

autapomorphy for the genus Pseudostertagia.

8. The large trilobate buccal aperture with ®ve

teeth in the anterior part of the oesophagus

(Fig. 7) is an autapomorphy for the genus

Boehmiella.

9. The rounded triangular buccal aperture with

neither lips nor teeth and a rounded triangular

ring (Fig. 8) is an autapomorphy for the

genus Peramelistrongylus.

10. The rounded buccal aperture with no lips, a

rounded ring and a prominent dorsal tooth


Pro®larinema.

11. The large hexagonal buccal aperture con-

nected with a thick, notched, hexagonal ring


Travassosius.

12. The large triangular buccal aperture uncon-

nected to the thick notched hexagonal ring


Graphidium.

M.C. Durette-Desset et al. / International Journal for Parasitology 29 (1999) 1065±1086 1067

Figs. 1±11 Caption opposite.


13. The buccal aperture with no cuticular ring,surrounded by three lips (Fig. 12) is an apo-morphic character.

14. The buccal aperture with no cuticular ring orlips (Fig. 13) is an apomorphic character.

15. The trilobed buccal aperture, unconnectedwith the short cuticular ring (Fig. 14) is anapomorphic character.

16. The trilobed buccal aperture, with a smallcuticular ring and separated from theexterno±labial papillae by a di�erentiatedarea (Fig. 15) is an apomorphic character.

17. The hexagonal buccal aperture, connectedlaterally with a notched hexagonal ring(Fig. 16) is an apomorphic character.

18. The rounded buccal aperture distant from alight notched ring (Fig. 17) is an apomorphiccharacter.

19. The peribuccal cuticular ring reinforcements(Fig. 18) are an apomorphic character.

20. Position of the excretory pore. In both rhab-ditids and Trichostrongylina larvae, theexcretory pore is situated at the level of thenerve ring. In some genera, during ontogen-esis, the posterior part of the oesophagusstretches displacing the excretory pore poster-iorly. The extreme posterior position of theexcretory pore is an apomorphic character.

21±22. Shape of the deirids. In most of the Stron-gylina, the deirids are rounded or spine-shaped. 21. The presence of hooked-shapeddeirids (Fig. 19) is an apomorphic state of thecharacter.

22. The presence of ®sh-hook shaped deirids(Fig. 20) is an autapomorphy for the genusBioccastrongylus.

23. Longitudinal vulvar opening. This is an apo-morphic character.

24. Perivulvar protuberances. These characters(Fig. 21) are adaptions which facilitate the ®x-ation of the caudal bursa of the male duringmating. This is an apomorphic character.

25. Elongated vestibule. This is an autapomorphyfor the genus Mecistocirrus.

26. Monodelphy. This is an autapomorphy forthe genus Impalaia.

27±30. Patterns of rays 2 and 3. Accordingto the nomenclature of Durette-Desset andChabaud [3]: In the majority of the Strongylinaand the Ancylostomina, rays 2 and 3 are small,straight, subequal and joined to each other(Fig. 22). From this plesiomorphic arrange-ment, four evolutionary lines have beenobserved within the Trichostrongyloidea, eachline representing a di�erent apomorphy(Fig. 23).

27. Rays 2 and 3 with a very long commontrunk (Fig. 24).

28. The distal ends of rays 2 and 3 are curvedtowards each other. Rays 2 are smaller thanrays 3. Rays 3 are directed posteriorly, thencurve abruptly anteriorly. The distancebetween the extremities of rays 2 and 3 issmaller than that of rays 3 and 4 (Fig. 25).

29. The distal ends of rays 2 and 3 are well sep-arated. Rays 2 are smaller than rays 3. Thedistance between the extremities of rays 2and 3 is greater than that of rays 3 and 4.The common trunk between rays 2 and 3 isabsent (Fig. 26).

30. The distal ends of rays 2 and 3 are close toeach other. Rays 2 are slightly smaller thanrays 3 (Fig. 27).

31. Relative lengths of rays 4 and 8. In the Stron-gylida, the extremities of papillae 1, 4 and 8open dorsally whereas the others open ven-

Figs. 1±11: Cephalic extremities. Fig. 1: Oesophagostomum (Hysteracrum), lateral view [25]; Fig. 2: Teladorsagia, lateral view, orig-

inal (T. hamata from Oryx gazella, South Africa); Fig. 3: Cooperia, lateral view, original (C. oncophora from Bison bison, Canada);

Fig. 4: Epomidiostomum (A), lateral view (B), apical view, after Quentin, original (Epomidiostomum sp. from Anas sp. Togo); Fig.

5: Filarinema (A), lateral view (B), apical view [26]; Fig. 6: Pseudostertagia (A), lateral view (B), apical view, original (P. bullosa

from Antilocapra americana, Canada); Fig. 7: Boehmiella: (A), lateral view (B), apical view [27]; Fig. 8: Peramelistrongylus (A), lat-

eral view (B), apical view [28]; Fig. 9: Pro®larinema (A), lateral view (B), apical view [28]; Fig. 10: Travassosius (A), lateral view

(B), apical view, original (T. americanus from Castor canadensis, Canada); Fig. 11: Graphidium (A), lateral view (B), apical view,

original (G. strigosum from Oryctolagus cuniculus, France).


Figs. 12±23 Caption opposite.


trally, at some distance from the bursal mar-gin. During the course of evolution, rays 4and 8 have extended and reach the edge ofthe caudal bursa. Rays 4 and 8 being rela-tively short therefore represents the plesio-morphic state (Fig. 28). The apomorphicstate is represented either by caudal bursaewith rays 4 and or rays 8 long.

32. Asymmetry of the dorsal lobe. This characteris an apomorphy frequent in the Strongylida(Fig. 29).

33±34. Division of the papilla `Ò''.33. The papilla `Ò'' is basically unpaired. The

division into two parts (Fig. 30) is an apo-morphy.

34. The papilla `Ò'', divided into three parts(Fig. 31) is an autapomorphy for the genusParostertagia.

35. Sclerotised rays 4. This is an autapomorphyfor the genus Cnizostrongylus (Fig. 32).

36. Extradorsal rays. This is an autapomorphyfor the genus Peramelistrongylus (Fig. 22).

37±47. Caudal bursa pattern of rays 2±6. In themajority of the Strongylina and the Ancylos-tomatina, the ventral rays 2 and 3 are closeto each other and are well separated from thelateral trident, composed of rays 4, 5 and 6.This is the plesiomorphic pattern. In almostall Strongylida, during the course of evol-ution, the ventral lobes (rays 2 and 3) developprogressively, while the dorsal lobe (rays 8±10) is greatly reduced, the lateral lobes (rays4±6) being intermediate. The plesiomorphicbursal pattern is therefore of type 2±3 with

rays 3 smaller than rays 5 (Fig. 22). Fromthis plesiomorphic type, observed in Oesopha-gostomum, Bioccastrongylus and Peramelis-trongylus, ®ve transition series are recognisedin the Trichostrongyloidea. (Fig. 33): hyper-trophy of the ventral lobes separates rays 2and 3 and hence the bursae characteristic ofall trichostrongylids, type 1±4 are obtained;the type 1±1±3, logically intermediarybetween types 2±3 and 1±4, when the lat-eral lobes hypertrophy; rays 3 then turns ven-trally come forward and type 1±1±3 isachieved (Fig. 26). Within this type, the rela-tive development of rays 3 and 5 is variable:in Graphidioides, rays 3 are larger than orequal to rays 5; in Travassosius, rays 3 aresmaller than rays 5. This character (37±39)has therefore been coded ``?'' for the twogenera.(37±39): Dorsal movement of rays 3 hasgiven the type 1±4. With this pattern, threeevolutionary lines have sucessively appeared.

37. Rays 3<rays 5 which is the plesiomorphicstate (Fig. 28).

38. Rays 3=rays 5 which is an apomorphicstate of the character (Fig. 34).

39. Rays 3>rays 5 which is another apomorphicstate of the character (Fig. 35).

40. Rays of the lateral trident are not joined.Either, rays 6 are separated from rays 5(types 1±3±1 and 2±2±1) or rays 5 and 6 areseparated from rays 4 (types 2±1±2 and 1±2±2). These arrangements are apomorphicstates of the character.

Figs. 12±23. (Figs. 12±18: Cephalic extremities). Fig. 12: Trichostrongylus (A), lateral view (B), apical view, original (T. retortaefor-

mis from Oryctolagus cuniculus, France); Fig. 13: Hoazinstrongylus (A), lateral view, [29]. (B), apical view, original (H. amazonensis

from Opisthocomus hoazin, Brasil); Fig. 14: Graphidioides (A), lateral view (B), apical view, [30]; Fig. 15: Cooperia (A), lateral view

(B), apical view, original (Cooperia sp. from Bison bison, Canada); Fig. 16: Ashworthius (A), lateral view (B), apical view [31]; Fig.

17: Ostertagia (A), lateral view (B), apical view, original (Ostertagia sp. from Oreamnos americanus, Canada); Fig. 18:

Mecistocirrus (A), lateral view (B), apical view, original (M. digitatus from Bos indicus, Mexique); (Figs. 19 and 20: Deirids). Fig.

19: Hyostrongylus, ventral view [32]; Fig. 20: Bioccastrongylus, lateral view [33]; Fig. 21: Perivulvar protuberances in a transversal

section, Cnizostrongylus [34]; (Figs. 22 and 23: Caudal bursa patterns of rays 2 and 3). Fig. 22: Peramelistrongylus, right lobe, ven-

tral view [28]; Fig. 23: Diagram of the relative disposition of rays 2 and 3 of the caudal bursa. From the plesiomorph disposition

with rays 2 and 3 subequal and joined to each other, four evolutionary lines appear: (A) character (27), rays 2 and 3 with a very

long common trunk (Haemonchinae). (B) character (28), distal ends of rays 2 and 3 curved towards each other (Cooperiidae except

Cooperioides). (C) character (29), distal end of rays 2 and 3 quite separate (Trichostrongylidae). (D) character (30), distal ends of

rays 2 and 3 close to each other (Ostertagiinae and Cooperioides).


41. Rays 3 and 6 have moved dorsally which has

given the type 1±3±1 (Fig. 36). This character

is an apomorphy.

42 and 43: rays 6 have moved dorsally which

has given the type 2±2±1 with the primitive

character rays 3<rays 5.

42. This type is the plesiomorphic state of the

character (Fig. 37).

43. In the following stage, rays 5 moved dorsally

towards rays 6 which has given the type 2±

1±2 (Fig. 38). This type is an apomorphic

state of the character.

44. Caudal bursa pattern type 2±1±2 in whichrays 5 and 6 are joined (Fig. 40). This dispo-sition is an apomorphic state.

45. Caudal bursa pattern type 1±2±2 and rays3>rays 5 (Fig. 39). This is an autapomorphyfor the genus Mecistocirrus.

46. Caudal bursa pattern type 2±2±1 in whichthe ventral lobes are hypertrophied and rays3>rays 5 (Fig. 41). This type is an apo-morphic state of the character.

47. Hypertrophy of the dorsal lobe with rays 6adjacent to rays 5 is a reverse disposition oftype 2±3 (Fig. 42).

Figs. 24±32: Caudal bursa patterns of rays 2 and 3, right lobe of caudal bursa, ventral view. Fig. 24: Ashworthius [35]; Fig. 25:

Paralibyostrongylus [35]; Fig. 26: Travassosius, original (T. americanus from Castor canadensis, Canada); Fig. 27: Marshallagia,

original (M. marshalli from Ovis canadensis, Canada); Fig. 28: Amidostomum [36]; Fig. 29: Haemonchus [35]. Figures 30±31: Genital

cone with shape of papilla ``zero''. Fig. 30: Hyostrongylus [35]; Fig. 31: Parostertagia [12]; Fig. 32: sclerotized rays of caudal bursa,

Cnizostrongylus, right lobe of caudal bursa, ventral view [34].


48. Synlophe [see page 6, character (3)]. Thesynlophe is absent in the nematodes. Thepresence of a synlophe in some Trichostron-gylina is therefore considered as the apo-morphic state of the character.

2.3. Cladistic analyses

The phylogenetic relationships within the Tri-chostrongyloidea were determined using PAUP

3.1.1 [11]. Characters were coded as binary charac-

ters (0: absent; 1: present, except for character (1)

coded 1 for absent). Two characters, caudal bursa

pattern of rays 2 and 3, and caudal bursa pattern

of rays 2 to 6 can be described under more than

two discrete states, 4 and 12, respectively. For

these characters, transformations from one state

to an other could be coded assuming that any state

can be transformed into any other state with equal

cost. However, this crude character coding leads

to improbable transformations. For such complex

Figs. 33. Diagram of the caudal bursa patterns of rays 2 to 6. From the plesiomorph caudal pattern of type 2±3 with 3<5

observed in the outgroups and Peramelistrongylus, ®ve apomorphic evolutionary lines have been distinguished: (A) Characters

(37)±(39): the Trichostrongylidae of type 1±4 with 3<5 (Amidostomatinae), 3=5 (Filarinematinae), 3>5 (Trichostrongylinae) and

of type 1±1±3 (Trichostrongylinae). (B) Character (41): the Libyostrongylinae of type 1±3±1. (C) Characters (46), (47): the

Cooperiinae of type 2±2±1 with 3>5 except Megacooperia of type 2±3 with 3<5. (D) Characters (44), (45): the Obeliscoidinae and

the Haemonchinae of type 2±1±2 with rays 5 and 6 joined except Mecistocirrus of type 1±2±2 and 3>5. (E) Characters (42), (43):

the Ostertagiinae of type 2±2±1 with 3<5 then of type 2±1±2 with rays 5 and 6 separated.


traits, morphological reasoning can suggest morerealistic character state transformations, as shownFigs. 23 and 33. These `ùser-de®ned'' transform-ations can be taken into account through factoris-ation, which changes multistate characters intoequivalent data sets entirely coded as binary. Inthe data matrix (Table 1), these two characters are

recoded from column 27 to 30 and from 37 to 47,respectively, following the schemes given inFigs. 23 and 33. Missing characters were coded asan ``?''. Characters (37), (38) and (39) are alsocoded ``?'' for Graphidioides and Travassosius sincetheir states cannot be accurately coded, asexplained below.

Figs. 34±42: Caudal bursa pattern (rays 2 to 6), right lobe of caudal bursa, ventral view). Filarinema [26]; Fig. 35: Trichostrongylus,

original, (T. retortaeformis from Oryctolagus cuniculus, France); Fig. 36: Libyostrongylus [35]; Fig. 37: Hyostrongylus [35]; Fig. 38:

Graphidium, original (G. strigosum from Oryctolagus cuniculus, France); Fig. 39: Mecistocirrus, original (M. digitatus from Bos indi-

cus, Mexique); Fig. 40: Tapironema [37]; Fig. 41: Chabaudstrongylus [38]; Fig. 42: Megacooperia [39].


All characters were equally weighted. The ana-lyses were performed using various heuristicsearches and branch swapping algorithms, all ofthem leading to the same results.

The phylogenetic trees were built followingtwo di�erent assumptions depending on thedirection of character state transformation: (i) byassuming that all character changes are revers-ible, changes from 0 to 1 and from 1 to 0 being

equally parsimonious. This is the `ùnorderedoption''. Trees are then rooted by outgroups(Bioccastrongylus and Oesophagostomum (Hyster-acrum); and (ii) by assuming that the ancestralstates are 0 and the derived state 1, changesbeing assumed to be irreversible, only changesfrom 0 to 1 being allowed. This is the `ìrrevers-ible option'' which can be restrictively relaxed forsome characters.

Figs. 43. Phylogenetic tree of the Trichostrongyloidea (Nematoda) based on morphological characters. The tree was constituted

using parsimony method (PAUP 3.1, Swo�ord, 1993), with two outgroups and character state changes being polarized as explained

in the text. The localisation of character changes are represented along the branches by the number of the character. Bold numbers

are homoplasies. Fil: Filarinematinae; Ami: Amidostomatinae; Tri: Trichostrongylinae; Ost: Ostertagiinae; Hae: Haemonchinae;

Lib: Libyostrongylinae; Obe: Obeliscoidinae; Coo: Cooperiinae.


3. Results

The number of equally parsimonious treesobtained by using the unordered option andkeeping the characters of the Figs. 23 and 33 asunordered multistate characters, is larger than10 000. However, when these two characters are

recoded following their user-de®ned charactertransformations, the unordered option being stillactive, this number is reduced to 164, each treerequiring 59 steps (CI=0.81). By removing themost homoplasious character (48), [presence orabsence of synlophe] which changes four timesalong the trees, then the unordered option leads

Table 1

Matrix of characters used in the clastitic analysis of the Trichostrongynloidea

111111111122222222223333333333444444444

123456789012345678901234567890123456789012345678

Oesophagostomum 100000000000000000000000000000000000000000000000

Bioccastrongylus 000000000000000000000100000000000000000000000000

Peramelistrongylus 110000001000000000000000000000000001000000000000

Pro®larinema 110000000100000000000000000010000000110000000000

Filarinema 110001000000000000000000000010000000110000000000

Amidostomum 110000000000000000000000000010000000100000000000

Paramidostomum 110000000000000000000000000010000000100000000001

Epomidiostomum 11001000000000000000000000001000000?100000000000

Pararhabdonema 110000000000010000000000000100100000000110000001

Teporingonema 110000000000000000000000000100100000000100010001

Tapironema 110000000000000000000000000100100000000100010001

Libyostrongylus 110000000000000000000001000100100000000110000001

Paralibyostrongylus 110000000000000000000001000100100000000110000001

Cnizostrongylus 110000000000000000000001000100100010000110000000

Gazellostrongylus 110000000000000100000000000100100000000100000101

Cooperioides 110100000000000100000000000001100000000100000101

Chabaudstrongylus 110100000000000100010000000100100000000100000101

Cooperia 110100000000000100010000000100100000000100000101

Impalaia 110100000000000100010000010100100000000100000101

Paracooperia 110100000000000100000000000100100000000100000101

Paracooperioides 110100000000000100000000000100100000000100000101

Megacooperia 110100000000000100000000000100100000000100000111

Laurostrongylus 110000000000000000000000000100100000000110000000

Parostertagia 110000000000100000000010000010100100111000000001

Trichostrongylus 110000000000100000000010000010100000111000000000

Pseudostertagia 110000100000000000000000000100100000000100000101

Obeliscoides 110000000000001000000000000100100000000100010001

Graphidium 110000000001000000001000000001100000000101100001

Graphidioides 110000000000001000000000000010100000???000000001

Travassosius 110000000010000000000000000010100000???000000001

Boehmiella 110000010000000000001000001000110000000100010001

Haemonchus 110000000000000010001000001000110000000100010001

Mecistocirrus 110000000000000010101000101000100000000100011001

Ashworthius 110000000000000010101000001000100000000100010001

Hyostrongylus 111000000000000001001000000001101000000101000001

Teladorsagia 11100000000000000100100000000110100?000101000001

Spiculopteragia 111000000000000001001000000001101000000101000001

Marshallagia 111000000000000001001000000001101000000101100001

Camelostrongylus 111000000000000001001000000001101000000101100001

Ostertagia 111000000000000001001000000001101000000101100001

Longistrongylus 111000000000000001001000000001101000000101100001


to six parsimonious trees with 54 steps. Theother homoplasious characters are (15), (17) [or(32)], (28), (30), (31), (43) and (44). Characters(28) and (43) show reversal, characters (15), (30),(31) and (44) convergent changes, and characters(17) and (32) reversal or convergent changesdepending on the tree and the optimalised option(accelerated or delayed changes).

The irreversible option leads to 176 trees(length 62 steps; CI=0.79). However, oncecharacter (17) is constrained to have less chanceto reverse than character (32) and once oneallows for character (28) to reverse (two hy-potheses which are discussed below), then onecan extract 12 parsimonious trees (60 steps;CI=0.80) which di�ers only because of the nu-merous changes of the most homoplasious char-acter (48) (synlophe), changing at least fourtimes. When the character (48) (synlophe) isremoved, then one ®nds a single most parsimo-nious tree (54 steps; CI=0. 87: Fig. 43) whichis identical to one among the 164 parsimonioustrees given by the unordered option. Convergentcharacters are (15), (30), (31), (32), (43), (44),and (28) is a reversal.

3.1. New classi®cation

The tree obtained shows the evolution of thegroup based mainly on the morphological evol-ution of the caudal bursa characters (Fig. 43).The most archaic Strongylida possess a ventrallobe of the caudal bursa (rays 2 and 3) which issmall and quite separate from the lateral one(rays 4, 5 and 6). This plesiomorph disposition(Type 2±3 with rays 3 smaller than rays 5) isobserved in the outgroups (Strongylina andAncylostomatina) and only in the genus Perame-listrongylus in the Trichostrongyloidea. Duringthe course of evolution, the ventral rays becameseparated but the lateral trident has remainedunseparated (Type 1±4 or 1±1±3). This corre-sponds to characters (37)±(39) which character-ises therefore the family Trichostrongylidae andopposes it to the two other families (Haemonchi-dae and Cooperiidae) where the rays of the lat-eral trident are always separated [character (40)].

In the tree obtained, the family Trichostrongy-lidae is not clearly divided into branches which ispredictable due to the fact that it groups the gen-era which have the most plesiomorphic charac-ters and do not have derived characters.However, it is very heterogeneous as has beenrecognised in all previous classi®cations.

The super-family Trichostrongyloidea com-prises taxa of the greatest veterinary importanceand changes of nomenclature would be very dis-turbing. For this reason, we decided not tostrictly follow the conclusions of the cladistic treeand avoid, as much as possible, the creation ofsupra generic new taxa. We propose the follow-ing classi®cation:

i To avoid creating a new family for the solegenus Peramelistrongylus, including it in theTrichostrongylidae with the other parasitesof Australian marsupials, since the caudalbursa evokes that of the genus Pro®larinema.

ii To retain the sub-family Amidostomatinaeeven if the genera share only plesiomorphicparticularities (rays 4 and 8 not reaching theedge of the caudal bursa, buccal capsule lessreduced than the other Trichostrongyloidea,ventral lobe of the caudal bursa smaller thanthe lateral one i.e 3<5).

iii To retain the sub-family Filarinematinae,even if the genera do not share apomorphiccharacters. Rays 4 and 8 do not reach theedge of the caudal bursa but the buccal cap-sule is reduced and the ventral lobe is moredeveloped than the above case i.e. 3=5.

iv To characterise the sub-family Trichostrongy-linae (which gathers together the other generain which the rays of the lateral trident remainjoined) by two apomorphic characters: rays 4and/or rays 8 reaching the edge of the caudalbursa (31), and ventral lobe of the caudal bursahypertrophied (3>or=5) (39) and (40),except for the genus Travassosius.

Taking into account the above remarks, thenew classi®cation proposed is the following.


Trichostrongyloidea (Leiper, 1908, subfam.)Trichostrongylina: female tail without cau-

dal spine (1); buccal capsule reduced or atro-phied in relation to that of Strongylina orAncylostomina (2); synlophe absent or bilater-ally symmetrical.

Parasites mainly of birds, Australian marsu-pials, caviomorph rodents, lagomorphs andartiodactyls.

Trichostrongylidae (Leiper, 1908, subfam.)Leiper (1912)

Trichostrongyloidea with distal ends of rays2 and 3 well separated; rays 2 smaller thanrays 3; distance between the extremities ofrays 2 and 3 greater than that of rays 3 and 4;common trunk between rays 2 and 3 absent(29); caudal bursa with rays of the lateral tri-dent grouped (37)±(39)].

Amidostomatinae Travassos (1919)Trichostrongylidae: caudal bursa of type 1±

4; rays 3 smaller than rays 5 (37); rays 4 shortand thick and rays 8 short, not reaching edgeof bursa. Amidostomum, Epomidostomum andParamidostomum are very similar, but thecephalic structures are di�erentiated in Epomi-dostomum (5). Parasites of aquatic birds. Cos-mopolitan.

Type-genus: Amidostomum Railliet andHenry, 1909. Other genera: EpomidostomumSkrjabin, 1915; Paramidostomum Freitas andMendonc° a, 1949; Pseudamidostomum Boulen-ger, 1926.

Filarinematinae (Skrjabin and Schikhoba-lova, 1937, tribe)

Trichostrongylidae; caudal bursa of type 1±4; rays 3 and 5 of equivalent length (38); rays4 short and thick; or in Peramelistrongylus,caudal bursa of a di�erent type, recognisableby extra-dorsal rays (36). Parasites of Austra-lian marsupials.

Type-genus: Filarinema MoÈ nnig, 1929.Other genera: Peramelistrongylus Mawson,1960; Pro®larinema Durette-Desset and Bever-idge, 1981.

Trichostrongylinae Leiper, 1908Trichostrongylidae, caudal bursa of type 1±

4 with rays 3 larger than rays 5 (39); rays 4and/or rays 8 reaching the edge of the caudal

bursa (31); buccal aperture with 3 lips, without

peribuccal ring (13); vulvar opening longitudi-

nal (23). Parasites of birds and mammals, or

caudal bursa of type 1±1±3; rays 3 larger thanor equal to rays 5 (except for the genus Tra-

vassosius). Parasites of Castoroidea, Cavio-

morphs and Lama.

Type-genus: Trichostrongylus Loos, 1905.

The genus is very polymorphic with numerous

species and, in the future, must be subdivided.

Other genera: Graphidioides Cameron, 1923;

Graphinema Guerrero and Chavez, 1984; Par-

ostertagia Schwartz and Alicata, 1933 which

has several autapomorphic characters (Hoberg

and Lichtenfelds [12]); Travassosius Khalil,

1922.

Haemonchidae (Skrjabin and Schulz, 1937,

tribe)

Trichostrongyloidea with rays of the lateral

trident not grouped (40); rays 4 and/or rays 8

reaching the edge of the caudal bursa (31);

hook-shaped deirids (21). Parasites of mam-

mals.

Ostertagiinae (Skrjabin and Schulz, 1937,tribe) Lopez-Neyra, 1947

Haemonchidae; rays 2 smaller than rays 3,

slightly separated at mid-length, extremities

close to each other (30); caudal bursa of type

2±2±1 and rays 3 smaller than rays 5 (42), or

with 2±1±2 pattern and rays 5 and 6 separated

(43); head with cephalic bulb (3) except for the

genus Graphidium; rounded buccal aperture,

separated from slight, rounded and notched

ring (18) except for the genus Graphidium (12);

bi®d papilla 0 (33) except for the genus Gra-

phidium. Parasites of artiodactyls (except for

the genus Graphidium and some species of the

genus Hyostrongylus).

Type-genus: Ostertagia Ransom, 1907.

Other genera: Camelostrongylus Orlo�, 1933;

Graphidium Railliet and Henry, 1909; Hyo-strongylus Hall, 1921; Longistrongylus Le

Roux, 1931; Marshallagia Orlo�, 1933; Spi-

culopteragia, Orlo�, 1933; Teladorsagia

Andreeva and Satubaldin, 1954.

Haemonchinae (Skrjabin and Schulz, 1937,

tribe) Skrjabin and Schulz, 1952


Haemonchidae; caudal bursa of type 2±1±2;

rays 5 and 6 joined or parallel (44) except forthe genus Mecistocirrus; rays 2 and 3 with

long common trunk (27); buccal aperture hex-

agonal and laterally connected with a notched

hexagonal ring (17) [except for the genusBoehmiella (8)]. Parasites of artiodactyls

(except for the genus Boehmiella).

Type-genus: Haemonchus Cobb, 1898. Other

genera: Ashworthius Le Roux, 1930; Boeh-

miella Gebauer, 1932; Leiperiatus Sandground,1930; Mecistocirrus Railliet and Henry, 1912.

Cooperiidae (Skrjabin and Schulz, 1937,

tribe)

Trichostrongyloidea with rays of the lateral

trident not grouped (40); rays 4 and/or rays 8

reaching the edge of the caudal bursa (31);

rays 3 directed posteriorly then abruptly cur-

ving anteriorly; distal ends of rays 2 and 3curved pincer-like (28), except for the genus

Cooperioides. Parasites of ratites and mam-

mals.

Libyostrongylinae Durette-Desset and Cha-baud, 1977

Cooperiidae; caudal bursa of type 1±3±1;

rays 3 equal to or smaller than rays 5 (41).

Parasites of ostriches, archaic Ethiopian ver-

tebrates and Malagasian mammals.

Type-genus: Libyostrongylus Lane, 1923.

Other genera: Cnizostrongylus Chabaud, Dur-

ette-Desset and Houin, 1967; Laurostrongylus

Durette-Desset and Chabaud, 1992; Parali-byostrongylus Ortlepp, 1939; Pararhabdonema

Kreis, 1945.

Obeliscoidinae subfam. nov.

Cooperiidae; caudal bursa of type 2±1±2;rays 5 and 6 joined or parallel (44). Two gen-

era are Neotropical, one of which is poorly

known, atypical in morphology and is a para-

site of birds. The other is parasitic in perisso-dactyls (tapir). The two other genera of this

sub-family are parasites of Nearctic and

Holarctic lagomorphs.

Type-genus: Obeliscoides Graybill, 1924.Other genera: Biogastranema Rohrbacher and

Ehrenford, 1954; Hoazinstrongylus Pinto and

Gomes, 1985; Tapironema Durette-Desset, Sut-

ton and Chabaud, 1997; Teporingonema Har-ris, 1985.

De®nition: Trichostrongyloidea. Cooperii-dae. Head without cephalic vesicle, with orwithout corona radiata; synlophe present orabsent; caudal bursa with 2±1±2 pattern; rays5 and 6 joined or parallel; didelphic or mono-delphic. Parasites of Neotropical birds, tapirand lagomorphs. Type-genus: ObeliscoidesGraybill, 1924.

Cooperiinae (Skrjabin and Schulz, 1937,tribe) Skrjabin and Schikhobalova, 1952

Cooperiidae; caudal bursa pattern generallyof type 2±2±1 and rays 3 bigger than rays 5(46); or, for the genus Megacooperia of type2±3 and rays 3 smaller than rays 5 (47); buccalaperture trilobed with di�erentiated areabetween externo±labial papillae; without buc-cal ring (16) except for the genus Pseudosterta-gia which has no di�erentiated area (7);cephalic vesicle bipartite except for the generaGazellostrongylus and Pseudostertagia (4).Parasites of artiodactyls.

Type-genus: Cooperia Ransom, 1907. Othergenera: Chabaudstrongylus Durette-Desset andDenkeÂ , 1978; Cooperioides Gibbons, 1978;Gazellostrongylus Yeh, 1956; Impalaia MoÈ n-nig, 1923; Megacooperia Khalil and Gibbons,1976; Minutostrongylus Le Roux, 1936; Para-cooperia Travassos, 1935; ParacooperioidesBoomker, Horak and de Vos, 1981; Pseudos-tertagia (Orlo�, 1933).

3.2. Changes

In comparison with the classi®cation proposedby Durette-Desset [6], which was amendedslightly by Durette-Desset and Chabaud [5], theprincipal systematic changes which result fromthe cladistic analysis are the following (Table 2).The family Dromaeostrongylidae (Skrjabin andSchulz, 1937, tribe), is reduced to its type-genus.Previously classi®ed in the Trichostrongyloidea,it is transferred into the Molineoidea, close tothe Amphibiophilidae. The family Amidostomati-dae is included in the Trichostrongyloidea(whereas the Strongylacanthidae seems closer tothe Ancylostomatina than the Trichostrongylina).


The family, reduced to a sub-family, is a memberof the family Trichostrongylidae. The genusParamidostomum, previously classi®ed in theDromaeostrongylidae, is placed in the Amidosto-matinae. The genera Filarinema, Pro®larinema,and Peramelistrongylus, previously classi®ed inthe Dromaeostrongylidae, are placed in the Tri-chostrongylidae, sub-family Filarinematinae(Shrjabin and Schikhobalova, 1937 tribe). TheGraphidiinae (Trichostrongylidae) has been sup-pressed. The genera Graphidium and Hyostrongy-lus are transferred to the Ostertagiinae and thegenus Parostertagia to the Trichostrongylidae.The Cooperiidae is separated into three sub-families: the Obeliscoidiinae nov. subfam., withthe genera Obeliscoides, Biogastranema, Hoazin-strongylus, Tapironema and Teporingonema. TheLibyostrongylinae are now limited to genera thatoccur in the Ethiopian region. The genus Pseu-dostertagia is placed in the Cooperiinae.

4. Discussion

4.1. Di�erences between our results and thecladistic analysis of Hoberg and Lichtenfels

We disagree with the cladistic analysis pro-posed by Hoberg and Lichtenfelds [4] for the fol-lowing reasons:

i They restricted their attempt solely to theTrichostrongylidae and we consider it is im-possible to understand the phylogenetic re-lationships within the family whendisconnected from the other taxa in the Tri-chostrongyloidea;

ii Their analysis deals with the position of thegenera in sub-families as previously proposedby Durette-Desset and Chabaud [13]. In doingthis, they failed to test the validity of the subdi-visions, for which a large amount of new datahas been obtained during recent years;

iii The de®nition of the genera included in theiranalysis utilises mainly the description of therespective type-species, and therefore ignorespart of the morphological information avail-able;

iv Finally, we disagree with their assumptionsconcerning the evolution of individual char-acters, mainly that of the synlophe.

Hoberg and Lichtenfelds [4] concluded that thesynlophe disappeared during the course of evol-ution. This seems to be contrary to what isknown. In the Molineoidea and the Heligmoso-moidea, the synlophe became more and morecomplex during the course of evolution. Onto-genetic studies lead to the same conclusions, thatis, the adult synlophe is always more complexthan that of the fourth stage larva in the samespecies [14]. In addition, in cases where the num-ber of the ridges decreases (e.g. Pudicinae), sev-eral ridges merge to form a ``comareÃ te''. Thesynlophe can be present on a limited portion ofthe body (i.e the portion in contact with the hostmucosa), but there is no case in which the syn-lophe has disappeared secondarily. In somespecialised parasites, which live in mammaryglands (i.e. the genus Mammanidula, Sadovskaja,1952), the synlophe, although of no use, does notdisappear, but consists of numerous small subeq-ual ridges.

According to Hoberg and Lichtenfels [4], theCooperiinae which have a synlophe, are ancestralto the Libyostrongylinae and the Trichostrongyli-nae. This hypothesis is in opposition to the hostspectrum. Within the Cooperiidae, the archaicgenera, parasitic in ratites and archaic mammalsoccur in one sub-family, the Libyostrongylinae.The genus Trichostrongylus is probably seconda-rily parasitic in ruminants. We previously inter-preted the origin of this genus as parasitic in theLagomorpha [3]. However, the analyses con-ducted herein indicate an a�nity with the Ami-dostomatinae, and the initial hosts are thereforelikely to be birds. Given this, the genus Trichos-trongylus cannot have arisen from the Cooperii-nae.

4.2. Host range and geographical distribution

The Amidostomatinae are parasites of birds,frequently of aquatic and herbivorous birds suchas members of the Anseriforma. Paramidostomumparasitises an endemic bird from Argentina


Table 2

Former and new classi®cation of the genera belonging to the Trichostrongyloidea

Former classi®cation New classication

Genus

Family Sub-family Family Sub-family

*Amidostomum Amidostomatidae Amidostomatinae Trichostrongylidae Amidostomatinae

*Ashworthius Trichostrongylidae Haemonchinae Haemonchidae Haemonchinae

*Bioccastrongylus Ancylostomatidae Ancylostomatinae Outgroup Ancylostomatoidea

Biogastranema Trichostrongylidae Haemonchinae Cooperiidae Obeliscoidinae

*Boehmiella Trichostrongylidae Haemonchinae Haemonchidae Haemonchinae

*Camelostrongylus Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Chabaudstrongylus Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

*Cnizostrongylus Trichostrongylidae Libyostrongylinae Cooperiidae Libyostrongylinae

*Cooperia Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

*Cooperioides Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

Dromaeostrongylus Dromaeostrongylidae Dromaeostrongylinae Molineoidea Dromaeostrongylinae

*Epomidiostomium Amidostomatidae Epomidiostomatinae Trichostrongylidae Amidostomatinae

*Filarinema Dromaeostrongylidae Dromaeostrongylinae Trichostrongylidae Filarinematinae

*Gazellostrongylus Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

*Graphidioides Trichostrongylidae Trichostrongylinae Trichostrongylidae Trichostrongylinae

*Graphidium Trichostrongylidae Graphidiinae Haemonchidae Ostertagiinae

Graphinema Trichostrongylidae Trichostrongylinae

*Haemonchus Trichostrongylidae Haemonchinae Haemonchidae Haemonchinae

Hoazinstrongylus Cooperiidae Obeliscoidinae (?)

*Hyostrongylus Trichostrongylidae Graphidiinae Haemonchidae Ostertagiinae

*Impalaia Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

*Laurostrongylus Cooperiidae Libyostrongylinae

Leiperiatus Trichostrongylidae Haemonchinae Haemonchidae Haemonchinae (?)

*Libyostrongylus Trichostrongylidae Libyostrongylinae Cooperiidae Libyostrongylinae

*Longistrongylus Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Marshallagia Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Mecistocirrus Trichostrongylidae Haemonchinae Haemonchidae Haemonchinae

*Megacooperia Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

Minutostrongylus Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae (?)

Moguranema Trichostrongylidae Haemonchinae ? ?

*Obeliscoides Trichostrongylidae Libyostrongylinae Cooperiidae Obeliscoidinae

*Oesophagostomum Chabertiidae Oesophagostominae Outgroup Strongyloidea

Ortleppstrongylus Trichostrongylidae Cooperiinae Molineoidea Molineinae

*Ostertagia Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Paracooperia Trichostrongylidae Cooperiinae Cooperiidae Cooperiinae

*Paracooperioides Cooperiidae Cooperiinae

*Paralibyostrongylus Trichostrongylidae Libyostrongylinae Cooperiidae Libyostrongylinae

*Peramelistrongylus Dromaeostrongylidae Dromaeostrongylinae Trichostrongylidae Filarinematinae

*Paramidostomum Dromaeostrongylidae Dromaeostrongylinae Trichostrongylidae Amidostomatinae

*Pararhabdonema Trichostrongylidae Libyostrongylinae Cooperiidae Libyostrongylinae

*Parostertagia Trichostrongylidae Graphidiinae Trichostrongylidae Trichostrongylinae

*Pro®larinema Dromaeostrongylidae Trichostrongylidae Filarinematinae

Pseudamidostomum Amidostomatidae Epomidiostomatinae Trichostrongylidae Amidostomatinae (?)

*Pseudostertagia Trichostrongylidae Libyostrongylinae Cooperiidae Cooperiinae

*Spiculopteragia Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Tapironema Cooperiidae Obeliscoidinae

*Teladorsagia Trichostrongylidae Ostertagiinae Haemonchidae Ostertagiinae

*Teporingonema Cooperiidae Obeliscoidinae

*Travassosius Trichostrongylidae Trichostrongylinae Trichostrongylidae Trichostrongylinae

*Trichostrongylus Trichostrongylidae Trichostrongylinae Trichostrongylidae Trichostrongylinae

Genera marked with an asterisk were used to construct the tree.


within the family Anhimidae. This bird has avegetarian diet and has a�nities with the Anseri-forma. Peramelistrongylus, which parasitises per-ameloid marsupials is classi®ed in theFilarinematinae for practical reasons only. TheFilarinematinae are parasitic in Australian pha-langeroid marsupials. The Trichostrongylinae arebasically parasitic in birds. Phenetic analyses ofmolecular data have also demonstrated that thegenus Trichostrongylus in birds occurred in theouter-most branch compared with species thatparasitise lagomorphs and ruminants [15, 16].Secondarily they adapted to di�erent hosts. Tra-vassosius is a parasite of beavers, Graphidioides ofcaviomorphs and Graphinema of llamas. Trichos-trongylus is parasitic in birds, lagomorphs, herbi-vorous mammals and ruminants, Parostertagia inpeccaries.

The Haemonchidae parasitise strictly herbivor-ous mammals. In the Ostertagiinae, Graphidiumparasitises lagomorphs from the European region.Hyostrongylus, another parasite of Lagomorpha inAfrica, also occurs in various mammals such asGorilla and some Tragulidae, Suidae, Gira�daeand Bovidae. All other Ostertagiinae are parasitesof Tylopoda and Ruminantia, more speci®callyBovidae and Cervidae. In the Haemonchinae,Boehmiella is a parasite of Nearctic Sciuromorphaand of Myocastor, a migrant from the Neotropicsto the Holarctic region. Haemonchus, Ashworthiusand Mecistocirrus are cosmopolitan, because theyparasitise cattle, but derive from the Palearctic andEthiopian fauna, as demonstrated by the abundantspecies described from wild Bovidae and Cervidae.

In the Cooperiidae, each of the three subfami-lies has di�erent hosts. The hosts for the Libyo-strongylinae are archaic Ethiopian vertebrateswith the ostrich for Libyostrongylus, Malagasiancricetids for Cnizostrongylus and Laurostrongylusand Madagascan lemurids for Pararhabdonema.Paralibyostrongylus has a host spectrum includ-ing archaic Ethiopian rodents (Thryonomys,Bathyergus, Atherurus), hyracoids, Lagomorphaand Gorilla. The Obeliscoidinae are from Amer-ica. Hoazinstrongylus parasitises a relictual Ama-zonian bird. Tapironema is a parasite of tapir inFrench Guyana and in a Neotropical cricetid,probably by host transfer. The other two genera

are parasitic in Lagomorpha. Teporingonema inRomerolagus, which is a relict in the Nearcticregion, and Obeliscoides in the Holarctic region.The Cooperiinae have an homogeneous hostspectrum essentially composed of African Bovi-dae, with only one genus cosmopolitan in cattle.Impalaia is often observed in Camelidae. Thereare two exceptions: Pseudostertagia is a parasiteof Antilocapra in the Nearctic region while Cha-baudstrongylus is a parasite of Tragulidae inAsia and Africa. Consequently, the range of theCooperiidae is interesting because it includestwo groups: one African and the other Ameri-can. Ratites or other birds are present amongthe hosts of the two oldest families which prob-ably means that these hosts were present whenthe family originated and dispersed, both fromAmerica and from Africa.

4.3. Biogeographical hypotheses

The evolutionary history of the Trichostrongy-loidea can be re-constructed in part from thespecies which are found in relictual hosts or inhosts which appeared during an ancient geologi-cal period and have evolved only slightly sincethose times [17, 18]. The primitive morphologicalcharacters observed in these parasites suggestthat they have evolved very slowly. It seems thata parasitic group adapts to a host group at thetime of an evolutionary radiation of the host,allowing us to place a date on the origin of theparasites based on the paleontological record ofthe vertebrate hosts [14, 19].

Basing our knowledge on the numerous relictsin the Trichostrongyloidea and with consider-ation of the paleogeographical data, we proposethe following hypotheses (Table 3):

i the Trichostrongyloidea originated duringthe upper Cretaceous period, when Australiaand South America had separated from Ant-arctica. This would explain the occurrence ofthe ancestral sub-family Amidostomatinaeand of Peramelistrongylus in Australian mar-supials or in aquatic birds. The parasites ofthese birds are probably at the origin of theother Trichostrongyloidea;


Table

3

Hypotheses

forthephylogenyoftheTrichostrongyloidea

incorrelationwiththepaleobiogeographyoftheirhostsduringtheTertiary

period

Australia

NeotropicalRegion

NearcticRegion

Asia

Europe

Africa

Upper

Miocene

SciuridsÐ

Pecora

Pecora

Pecora

Pecora

Haem

.Haem

onch.

Haem

.Haem

onch.

Haem

.Haem

onch.

Haem

.Haem

onch.

Haem

.Ostertagiin.

Haem

.Ostertagiin.

Middle

Miocene

Pecora

Pecora

Pecora

Trich.Trichostr.

Trich.Trichostr.

Trich.Trichostr.

Coop.Cooperiinae

Haem

.Ostertagiin.

Haem

.Ostertagiin.

Coop.Cooperiinae

Coop.Cooperiinae

Lower

Miocene

Antilocapra

Lagomorpha

CoopCooperiinae

Trich.Trichostr.

Haem

.Ostertagiin.

Coop.Libyostron.

Middle

Oligocene

Caviomorpha

Castoroidea

Tragulina

Tragulina

Archaic

Mammals

Trich.Trichostr.

Trich.Trichostr.

Coop.Cooperiinae

Haem

Ostertagin

CoopLibyostron.

Lower

Oligocene

Tapirs-Lagomorpha

Lagomorpha

Lagomorpha

Trich.Trichostr.

Coop.Obeliscoid.

Trich.Trichostr.

Coop.Obeliscoid.

Haem

.Ostertagiin.

Upper

Eocene

Lagomorpha

Trich.Trichostr.

Coop.Obeliscoid.

Paleocene

Marsupials

Birds

Birds

Ratite

birds

Trich.Filarinem

at.

Trich.Amidostom.

Trich.Amidostom.

CoopLibyostron.

Trich.Trichostr.

Trich.Trichostr.

Amidostom.:

Amidostomatinae;

Coop.:

Cooperiidae;

Filarinem

at.:

Filarinem

atinae;

Haem

.:Haem

onchidae;

Haem

onch.:

Haem

onchinae;

Libyostron.:

Libyostrongylinae;

Obeliscoid.:Obeliscoidinae;

Ostertagiin.:Ostertagiinae;

Trich.:Trichostrongylidae;

Trichostr.:Trichostrongylinae.


ii the Trichostrongylidae di�erentiated from thisinitial stock during the Paleocene period. Tri-chostrongylus which appeared in aquatic birdsbecame cosmopolitan. Hoberg andLichtenfels [4] criticised the hypotheses of Dur-ette-Desset and Chabaud [3] concerning a Neo-tropical origin for the Trichostrongylidaebecause the published ®gure which representedthe phenomenon diagrammatically, inadver-tently showed Dolichotis (a rodent) and not abird. The Neotropics were isolated duringmost of the Tertiary period and rodents wereunable to spread their parasites to other conti-nents. However, if the primitive hosts werebirds, an origin of the Trichostrongylidae inthe Neotropics cannot be rejected.

The American origin of the Trichostrongy-lidae seems to be con®rmed by the fact thatthe archaic genera which remain today areparasites of mammals which appeared duringthe middle Oligocene, either in the Neotropi-cal region (Graphidioides in the Caviomor-pha) or in the Nearctic region (Travassosiusin Castor). The genus Trichostrongylusadapted to Lagomorpha during the upperEocene period in the Nearctic region andlater became cosmopolitan after it adaptedto Ruminantia. The genus Parostertagiaadapted to pecarries in the Nearctic regionduring the lower Oligocene;

iii in the Haemonchidae, Graphidium, which is aparasite of the Lagomorpha in Europe,appears the most primitive genus encoun-tered in the Palearctic region. This suggeststhat the Haemonchidae spread from theNearctic region to Europe during the lowerOligocene period. After Graphidium, the mostprimitive genus is the cosmopolitan Hyos-trongylus, recorded throughout the world indomestic pigs, but there are also some speciesof this genus, which are parasites of Lago-morpha (these hosts reached Africa duringthe lower Miocene [20]), Tragulidae and Gor-illa in the Ethiopian region. As these hostsare generally considered to have appearedduring the upper Oligocene and lower Mio-cene periods, this lineage would probably

have been widespread during the Mioceneperiod, in Cervidae and Bovidae, both inAfrica and Europe. The di�erent families ofPecoran ruminants spread almost simul-taneously and relatively late during the Mio-cene period [21]. A recent extension couldhave occurred towards the New Worldthrough the Bering Strait. In the Haemonchi-nae, Boehmiella could have originated in theNearctic region, during the upper Miocene,when the squirrels entered North America.Secondarily they parasitised Myocastor, acaviomorph which invaded the Holarcticregion recently. Leiperiatus parasitises thehippopotamus. The other three genera Hae-monchus, Ashworthius and Mecistocirrusmainly parasitise domestic cattle, but alsohave species in Cervidae and wild Bovidae inthe Palearctic and Ethiopian regions. Conse-quently, the radiation which resulted in thesegenera could have occurred in these regions,during the Miocene period;

iv in the Cooperiidae, two `àrchaic'' sub-families and one ``modern'' are present.Within the Libyostrongylinae the existence ofLibyostrongylus, a parasite of the ostrich,suggests a very ancient appearance of thissub-family in the Ethiopian region. This hy-pothesis is also supported because most ofthe other recorded genera in the sub-familyare parasites of lemurs or endemic rodents inMadagascar and these hosts can be con-sidered relictual before Madagascar andAfrica separated. Paralibyostrongylus isfound in Africa and parasitises Thryonomys,Bathyergus, Atherurus, Hyrax and Gorilla.These hosts are phylogenetically unrelatedbut they have evolved in this area during theOligocene period.

The presence of Paralibyostrongylus in theLagomorpha could have occurred when rabbitsentered Africa, during the early Miocene [20].This suggests that the Cooperiinae of Ruminantiahave arisen from Ethiopian Libyostrongylinaealthough an origin of the Cooperiinae from theObeliscoidinae is also possible.


The most primitive genus of the Obeliscoidinae,Hoazinstrongylus, occurs in America in a relictualNeotropical bird. Tapironema in tapirs is inter-preted as a refuge host from the Nearctic region.Proto-tapirs probably existed in the Paleocene,but the true tapirs, closely related to currentspecies, are found in the Holarctic region duringthe Oligocene [22]. Teporingonema, closely relatedto Tapironema is parasitic in a relictual lago-morph, in the Nearctic genus Romerolagus. TheLagomorpha have a Nearctic origin during theupper Eocene [20]. Obeliscoides which parasitisesthe Lagomorpha in the Nearctic region, has beenrecorded from the Sakhaline Islands, Japan andRussia. It probably entered the Old World whenits hosts moved over the Bering Strait during thelower Oligocene period [20] but because the mor-phology of some Asian species is more primitivethan that of some American species, a morerecent migration, in the opposite direction (Asiatowards America), is likely [23, 24].

In the Cooperiidae, Chabaudstrongylus, themost primitive genus, parasitises the Tragulidaeboth in Africa and Malaysia and has also beenrecorded in the Muntjak, in Vietnam. Thissuggests a passage from the Lagomorpha to theTragulidae, or concerning the parasites fromObeliscoides to Chabaudstrongylus, in Asia,before the impressive evolutionary expansion ofthe Cooperiinae in Africa during the Mioceneperiod. Therefore, the Cooperiinae could havebeen derived from the Obeliscoidinae, and thismay have occurred in America. Pseudostertagia,a parasite of Antilocapra could be interpreted asa relict of this group in America. Given this, weconsider an origin of this sub-family in theNearctic region, followed by a migration throughAsia towards Africa, where they later expandedwithin the Bovidae. The Cooperiinae could havebeen derived from the Libyostrongylinae or theObeliscoiidinae. This latter hypothesis seems tobe the more likely.

Acknowledgements

The authors are grateful to Dr. I. Beveridge,University of Melbourne (Victoria) Australia;

Dr. J. Cabaret, INRA-Tours France; Prof. J.L.Justine, MuseÂ um national d'Histoire naturelle,Paris, France for their comments and Prof. L.Ginsburg for the paleobiogeographic data heprovided. They wish to thank Prof. R. Anderson,University of Guelph (Ontario), Canada andProf. W. Samuel, University of Edmonton,(Alberta) Canada who provided part of the ma-terial used for the descriptions of the head andProf. J.C. Quentin who authorised them to pub-lish his original drawings of Epomidiostomum.They also thank Mrs. R. Tcheprako� for hertechnical collaboration.

References

[1] Travassos L. Revisao da familia Trichostrongylidae

Leiper, 1912. Monograph Inst Oswaldo Cruz 1937;1±

512.

[2] Skrjabin KI, Schikhobalowa NP, Schulz RS, Osnovi

Nematodologii III. Trichostrongylids of animals and

man 1954;1±683 (in Russian).

[3] Durette-Desset MC, Chabaud AG. Essai de classi®cation

des NeÂ matodes Trichostrongyloidea. Ann Parasitol hum

comp 1977;52:539±58.

[4] Hoberg EP, Lichtenfels JR. Phylogenetic systematic

analysis of the Trichostrongylidae (Nematoda), with an

initial assessment of coevolution and biogeography.

Parasitol 1994;80:976±96.

[5] Durette-Desset MC, Chabaud AG. Nomenclature des

Strongylida au-dessus du groupe famille. Ann Parasitol

hum comp 1993;68:111±2.

[6] Durette-Desset MC. Keys to genera of the Superfamily

Trichostrongyloidea. In: Anderson RC, Chabaud AG,

editors. CIH Keys to the nematode parasites of ver-

tebrates. Farnham Royal: Commonwealth Agricultural

Bureaux 1983;10:1±68.

[7] Dougherty EC. Evolution of zooparasitic groups in the

phylum Nematoda, with special reference to host-distri-

bution. J Parasitol 1951;37:353±78.

[8] Chabaud AG. Remarque sur la systeÂ matique des

NeÂ matodes Trichostrongyloidea. Bull Soc Zool, France

1959;84:473±83.

[9] Durette-Desset MC. Nomenclature proposeÂ e pour les

espeÁ ces deÂ crites dans la sous-famille des Ostertagiinae

Lopez-Neyra, 1947. Ann Parasitol hum comp

1989;64:356±73.

[10] Osche G. Der dreihoÈ ckeridge Schamz, ein urspruÈ n-

glisches Mermal im Bauplan der Nematoden. Zool Anz

1955;124:136±48.

[11] Swo�ord D. PAUP Phylogenetic Analysis Using

Parsimony, version 3.1.1. Computer Program distribued

by the Illinois Natural History Survey, Illinois, 1993.


[12] Hoberg EP, Lichtenfels JR. Morphology of the synlophe

and genital cone of Parostertagia heterospiculum

(Trichostrongylidae) with comments on the subfamilial

placement of the genus. Syst Parasitol 1992;22:1±16.

[13] Durette-Desset MC, Chabaud AG. Nouvel essai de

classi®cation des NeÂ matodes Trichostrongyloidea. Ann

Parasitol hum comp 1981;56:297±312.

[14] Durette-Desset MC. Essai de classi®cation des

NeÂ matodes HeÂ ligmosomes. CorreÂ lation avec la paleÂ obio-

geÂ ographie des hoÃ tes. MeÂ m Mus natn Hist nat, Paris,

seÂ rie A 1971;34:1±126.

[15] Hoste H, Chilton NB, Gasser R, Beveridge I. Di�erences

in the second internal transcribed spacer (ribosomal

DNA) between ®ve species of Trichostrongylus

(Nematoda±Trichostrongylidae). Int J Parasitol

1995;25:75±80.

[16] Hoste H, Chilton NB, Beveridge I, Gasser RA.

Comparison of the ®rst internal transcribed spacer of

ribosomal DNA in seven species of Trichostrongylus

(Nematoda: Trichostrongylidae). Int J Parasitol

1998;25:75±80.

[17] Chabaud AG. Evolution of host-parasite adaptation in

nematodes of vertebrates. Int J Parasitol 1971;1:217±21.

[18] Chabaud AG. Spectre d'hoÃ tes et eÂ volution des

NeÂ matodes parasites de VerteÂ breÂ s In: DeuxieÁ me sym-

posium sur la speÂ ci®citeÂ parasitaire des parasites de

VerteÂ breÂ s. Colloque International du CNRS, 13±17 Avril

1981, Paris. MeÂ m Mus natn Hist nat, Paris, seÂ rie A,

1982;123±326.

[19] Quentin J-C. Sur les modaliteÂ s d'eÂ volution chez quelques

ligneÂ es d'Helminthes de Rongeurs Muroidea. Cahiers

O.R.S.T.O.M, seÂ rie Entomol meÂ d Parasitol. 1971;9:103±

76.

[20] Hartenberger JL. Les deÂ buts de la radiation adaptative

des Rodentia (Mammalia). CR Acad Sci Paris, seÂ rie II

1996; 631±637.

[21] Kraus F, Miyamoto MM. Rapid cladogenesis among the

Pecoran Ruminants: evidence from mitochondrial DNA

sequences. Syst Zool 1991;40:117±30.

[22] Piveteau J. MammifeÁ res. Origine reptilienne. Evolution.

In: Masson et al. TraiteÂ de PaleÂ ontologie, 1961;1:1±1138.

[23] Measures LN, Anderson RC. New subspecies of the

stomach worm, Obeliscoides cuniculi (Graybill), of

Lagomorphs. Proc Helminthol Soc Wash 1983;50:1±14.

[24] Fukumoto SI. A new stomach worm, Obeliscoides penta-

lagi n.sp. (Nematoda; Trichostrongyloidea) of Ryukyu

rabbits, Pentalugus furnessi (Stone, 1900). Syst Parasitol

1986;8:267±77.

[25] Chabaud AG, Krishnasamy, M. NeÂ matodes

Oesophagostomes parasites de Tragulus javanicus. Bull

Mus natn Hist nat, Paris, 3eÁ me seÂ rie, 1976;388, Zoologie

270:721±727.

[26] Cassone J, Baccam D. Le genre Filarinema MoÈ nnig, 1929

(Nematoda, Trichostrongyloidea), parasite de

Marsupiaux australiens. Bull Mus natn Hist nat, Paris,

4eÁ me seÂ rie, 1985;7, Section A:349±352.

[27] Durette-Desset MC, Sutton CA. Position systeÂ matique

du genre Boehmiella Gebauer, 1932 (Nematoda,

Haemonchinae). Bull Mus natn Hist nat, 4eÁ me seÂ rie,

1979;1, Section A:241±244.

[28] Durette-Desset MC, Beveridge I. Peramelistrongylus

Mawson, 1960 et Pro®larinema n. gen. NeÂ matodes

TrichostrongyloõÈ des paraissant faire transition entre les

Strongyloidea et le genre atypique Filarinema MoÈ nnig,

1929. Ann Parasitol hum comp 1981;56:183±91.

[29] Pinto MR, Gomes DC. Nematodes of Amazonian birds

with a description of Hoazinstrongylus amazonensis n.

gen. n. sp. (Trichostrongylidae, Libyostrongylinae). Mem

Inst Oswaldo Cruz 1985;80:213±7.

[30] Sutton CA, Durette-Desset MC. Revision of the genus

Graphidioides parasite in neotropical rodents. Syst

Parasitol 1995;31:133±45.

[31] FerteÂ H, Durette-Desset MC. Redescription

d'Ashworthius sidemi Schulz, 1933 et d'A. gagarini

Kostayev, 1969 (Nematoda, Trichostrongyloidea) para-

sites de Cervidae. Bull Mus natn Hist nat Paris, 4eÁ me

seÂ rie, 1989;11, Section A:69±77.

[32] Durette-Desset MC, Chabaud AG, Ashford RW,

Butinski T, Reid GDF. Two new species of the

Trichostrongylidae (Nematoda: Trichostrongyloidea),

parasitic in Gorilla gorilla beringei in Uganda. Syst

Parasitol 1992;23:159±66.

[33] Chabaud AG, Petter AJ, Brygoo ER. Trois NeÂ matodes

parasites de HeÂ rissons malgaches. Bull Soc Zool, France

1961;86:38±51.

[34] Chabaud AG, Durette-Desset MC, Houin R.

Description de Cnizostrongylus kleini n. gen. n. sp.

Trichostrongylide parasite d'un Rongeur malgache. Bull

Soc Zool, France 1967;92:233±8.

[35] Durette-Desset MC, DenkeÂ MA. Description de nou-

veaux NeÂ matodes parasites d'un LieÁ vre africain et comp-

leÂ ments aÁ l'eÂ tude morphologique de quelques

Trichostrongylidae. Bull Mus natn Hist nat Paris, 3eÁ me

seÂ rie, 1978;515, Zoologie 354:331±347.

[36] Wertheim G, Durette-Desset MC. Helminthes de

MammifeÁ res et d'Oiseaux d'Israel VI. la taxonomie et

l'eÂ cologie des NeÂ matodes Trichostrongyloides. Ann

Parasitol. hum comp 1975;50:735±62.

[37] Durette-Desset MC, Chabaud AG, Sutton CA.

Tapironema coronatum n. gen., n. sp.

(Trichostrongyloidea±Cooperiidae±Obeliscoidinae), a

parasite of Holochilus brasiliensis in Argentina and

Tapirus terrestris in French Guyana. Relationships with

the genus Teporingonema. Parasite 1997;4:227±32.

[38] Durette-Desset MC, Chabaud AG. Trois nouveaux

NeÂ matodes parasites du Chevrotain aquatique

Hyemoschus aquaticus au Gabon (collection G Dubost).

Bull Mus natn Hist nat Paris, 3eÁ me seÂ rie, 1974;205,

Zoologie, 135:75±87.

[39] Khalil LF, Gibbons LM. The helminth parasites of suni,

Nesotragus moschatus von Dueben, 1846 from Kenya

with the description of a new genus and two new species

of nematodes (Vermes). Revue afr Zool 1976;90:559±77.


Documents

A cladistic analysis of the Trichostrongyloidea (Nematoda)