The Systematic Position of the Inglisonematinae Mawson, 1968 (Nematoda)

Proc. Helminthol. Soc. Wash. 51(1), 1984, pp. 69-72

M. R. BAKER Department of Zoology, University of Guelph, Guelph, Ontario NIG 2W1, Canada

ABSTRACT: New information concerning the female reproductive system, cephalic end, and esophagus supports the classification of the Inglisonematinae Mawson, 1968, in the Heterakoidea, rather than the Seuratoidea as originally proposed. Many primitive heterakoids (Heterakidae) possess a prominent vagina that is markedly elongated posteriorly and divided into distinct muscular and sac-like uterine portions. This arrangement does not occur in other Ascaridida, but it is observed in paratypes of Inglisonema mawsonae Schmidt and Kuntz, 1971 (Inglisonematinae). The esophagus and cephalic extremity of Inglisonematinae are morphologically similar to early fourth-stage larvae of Heterakidae (esophagus club-shaped and lacking valves, cephalic lips inconspicuous). In contrast in late fourth-stage and adult Heterakidae esophageal valves and three distinct cephalic lips are present. It is hypothesized that the Inglisonematinae evolved by paedomorphosis from heterakoids, with Heterakis (Heterakinae) as a possible ancestral group. It is proposed that Inglisonematinae be classified as a family in the Superfamily Heterakoidea.

The Subfamily Inglisonematinae Mawson, markedly close to the Family Heterakidae. They 1968 includes only three species in two genera: also considered these groups closely related since Madelinema angelae Schmidt and Kuntz, 1971; in the Inglisonematinae the "reduced lips, lack Inglisonema typos Mawson, 1968; /. mawsonae of interlabia and oesophageal teeth are reminis- Schmidt and Kuntz, 1971. These species form a cent of the Meteterakinae Inglis, 1958." This was clearly homogeneous group restricted to birds of considered sufficient grounds to place Ingliso- the Far East (Taiwan, Philippines) and Australia. nematinae in the Heterakoidea with family rank The classification of the group to superfamily has and distinguished from Heterakidae by esopha- been controversial because the caudal structures geal characters, and from Ascaridiidae by ce- of males are typical of the Heterakoidea (Schmidt phalic and male caudal characters. Although this and Kuntz, 1971), whereas the cephalic and correlation of cephalic structures between Ingli- esophageal morphology are typical of the Seu- sonematinae and Meteterakinae is not accepted ratoidea (Chabaud, 1978). (see below), the placement of the Inglisonema- Chabaud (1978) classified the Inglisonemati- tinae in the Heterakoidea is supported by new nae in the Family Schneidernematidae (Seuratoi- information concerning cephalic, esophageal, and dea) indicating that they represent a somewhat female reproductive structures. intermediate stage in the evolution of the Het- erakoidea from Cosmocercoidea ancestors. Material Examined However, other studies (i.e., Baker, 198la) sug- Paratype females of Inglisonema mawsonae (USNM gest that Heterakoidea most likely evolved di- Helm. Coll. No. 71750) were borrowed from the Na- rectly from the Cosmocercoidea without seura- tional Parasite Collection, U.S. Department of Agri- toid-like ancestors. In particular the presence of culture, Beltsville, Maryland 20705. esophageal valves in the more primitive heterakoids (i.e., Heterakidae) and cosmocercoids, Results contrasted with their absence in seuratoids, is strong evidence that these three groups are not Female reproductive system related in the evolutionary sequence Cosmocer- Female reproductive structures have not been coidea-Seuratoidea-Heterakoidea. It is unlikely considered of systematic value for the Hetera- that forms bearing esophageal valves (Cosmo- koidea and related groups. However, many Het- cercoidea) gave rise to forms lacking these struc- erakoidea, including some of the most primitive tures (Seuratoidea) which in turn gave rise to representatives (Heterakidae), have evolved a forms bearing valves (Heterakoidea). morphologically unusual vagina that is unique Schmidt and Kuntz (1971) pointed out that for the Order Ascaridida and therefore may be the male caudal ends of Inglisonematinae are a character indicating heterakoid affinities.

Figure 1. Inglisonema mawsonae Schmidt and Kuntz, 1971. Vagina of paratype female, lateral view.

Primitively, a short, muscular vagina gives rise brevicaudata and H. dispar develop only in the to two opposed uteri near midbody. This is char- late fourth larval stage after considerable growth acteristic of most Cosmocercoidea and several in body size. From these observations it is hy- species of Heterakis (Heterakinae). During evo- pothesized that the Inglisonematinae evolved lution of heterakoids there has been a tendency from the Heterakidae as a group that retained toward the marked elongation of the vagina, early fourth larval stage morphology of the an- which becomes directed posteriorly and divided terior end into the adult sexually mature stage into a muscular anterior portion and thin-walled (paedomorphosis). The following observations sac-like posterior portion. This uterine portion support this hypothesis. may or may not be divided into two thin tubes. (1) Bain (1970) has noted that during the fourth This arrangement is observed in several different larval stage of S1. brevicaudata the body grows species of Heterakidae, i.e., Heterakis bosia Lane, four times in size and there is an early devel- 1914, Odonterakis fariae (Travassos, 1913) opment of the genital organs. This precocity of (Heterakinae), Africana chabaudi Baker, 1981 development is apparently true for the superfam- (Spinicaudinae), and Meteterakis spp. (Meteter- ily as a whole (Bain, 1970), indicating a possible akinae) (see Lane, 1914; Travassos, 1945; Inglis, predisposition to paedomorphosis. 1958; Baker, 1981b). (2) Adult Inglisonematinae are relatively small. The female reproductive structures of Ingli- For example, Inglisonema typos, the largest sonematinae have not previously been de- known species, reaches a maximum size of 3.7 scribed. The vagina in a 2.8-mm-long gravid mm for males and 4.4 mm for females (Mawson, paratype female of /. mawsonae is 600 /urn in 1968). This may be compared to Heterakidae, length (Fig. 1). It is posteriorly directed from the which are generally well over 5.0 mm in length. vulva (located 1,100 /^m from anterior extrem- Thus, adult Inglisonematinae are comparable in ity), muscular in the anterior 370 /mi, and thin- size to fourth-stage Heterakidae. walled in the posterior 230 /mi- The uteri are If the Inglisonematinae indeed evolved by pae- opposed at their origin, with one ovary located domorphosis, then it may be expected that in near the anus, the other just posterior to the characters not affected by the paedomorphic de- esophagus. This therefore corresponds closely to velopment (i.e., sexual structures) a close resem- the elongated vagina of evolved heterakoids. blance may be found with the "parental" group. Thus, it is instructive to note the close resem- Cephalic and esophageal structures blance between Inglisonematinae and the genus The cephalic end and esophagus of the Ingli- Heterakis (Heterakinae). In particular, the full sonematinae have been well described (Mawson, array of male caudal characters (caudal alae, size 1968; Schmidt and Kuntz, 1971). The esophagus and arrangement of caudal papillae, location of is club-shaped, muscular, and lacking valves. The caudal sucker bearing a single papilla in its pos- mouth is triangular and three inconspicuous lips terior rim, morphology of the spicules) is re- lacking cuticular flanges are present. In contrast markably similar. Heterakis is a cosmopolitan the esophagus of all Heterakidae bear large valves genus that is also parasitic mainly in birds. and the mouth is bordered by three distinct lips It is quite possible that the Inglisonematinae each of which bears a cuticular flange. These dif- are a relatively recently evolved group since they ferences are of considerable systematic impor- occur in a restricted geographical range. The tance in the modern classification of the Order unique dispersive ability of birds has tended to Ascaridida (Chabaud, 1978). However, when the produce a wide distribution for most bird par- cephalic and esophageal morphology of the few asites. described fourth larval stage Heterakidae are The classification of Inglisonematinae in the compared to adult Inglisonematinae, a clear re- Heterakoidea is therefore supported. Although semblance emerges. Early fourth-stage Strongy- they are probably phylogenetically close to the luris brevicaudata Mueller, 1849 (Spinicaudinae) Heterakinae, it is proposed that they hold the and Heterakis dispar (Schrank, 1790) (^Heter- rank of family as suggested by Schmidt and Kuntz akis papillosa (Bloch, 1782)) (Heterakinae) have (1971). This is convenient from a diagnostic point club-shaped esophagi lacking valves and ce- of view as the Inglisonematidae can be distin- phalic ends closely resembling adult Inglisone- guished easily from all other Heterakoidea except matinae (Uribe, 1922; Bain, 1970). The esoph- Ascaridiidae by their lack of esophageal valves. ageal valves that are observed in adult S. It is distinguished from the Ascaridiidae by the

Copyright © 2011, The Helminthological Society of Washington 72 cephalic morphology (lips inconspicuous as op- monwealth Agricultural Bureaux, Farnham Royal, posed to the presence of three massive lips). England. 71 pp. Inglis, W. G. 1958. A revision of the nematode genus Literature Cited Meteterakis Karve, 1930. Parasitology 48:9-31. Lane, C. 1914. Suckered round-worms from India Bain, O. 1970. Cycle evolutifde 1'Heterakidae Stron- and Ceylon. Indian J. Med. Res. 2:655-669. gyluris brevicaudata (Nematoda). Mise en evi- Mawson, P. M. 1968. Inglisonema typos gen. nov., dence de deux mues dans 1'oeuf. Ann. Parasitol. sp. nov. (Nematoda: Seuratoidea: Inglisonemati- Hum. Comp. 45:637-653. nae, sub fam. nov.) from an Australian bird. Par- Baker, M. R. 198la. Austraplectana n. gen. (Cos- asitology 58:71-73. mocercidae, Austraplectaninae n. sous-fam.), Schmidt, G. D., and R. E. Kuntz. 1971. Nematode nematode parasite d'amphibiens Australiens. Bull. parasites of Oceanica. XI. Madelinema angelae Mus. Natn. Hist. Nat, 4 Ser., Sect. A 3:111-116. gen. et sp. n. and Inglisonema mawsonae sp. n. . 1981b. Africana chabaudi n. sp. (Nematoda, (Heterakoidea: Inglisonematidae) from birds. J. Heterakidae) in a Brazilian iguana. Bull. Mus. Natn. Parasitol. 57:479-484. Hist. Nat., 4 Ser., Sect. A 3:783-737. Travassos, L. 1945. Heterakisfariae Travassos, 1913 Chabaud, A. G. 1978. Keys to genera of the Super- (Nematoda: Subuluroidea) Mem. Inst. Oswaldo families Cosmocercoidea, Seuratoidea, Heterakoi- Cruz 42:551-557. dea and Subuluroidea. In R. C. Anderson, A. G. Uribe, C. 1922. Observations on the development of Chabaud and S. Willmott, eds. CIH Keys to the Heterakis papillosa Bloch in the chicken. J. Par- Nematode Parasites of Vertebrates. No. 6. Com- asitol. 8:167-176.

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