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The Life Cycles of Dipetalonematid Nematodes (Filarioidea, Dipetalonematidae): The Problem of Their Evolution

Published online by Cambridge University Press:  05 June 2009

Roy C. Anderson
Affiliation:
Department of Parasitology, Ontario Research Foundation, Toronto, Canada From the Department of Parasitology, London School of Hygiene and Tropical Medicine

Extract

The evolution of the life cycles of the members of the family Dipetalonematiidae Wehr, 1935 (Filarioidea) is considered in the light of existing knowledge of spirurid nematodes. The hypothesis that the life cycles of the dipetalonematids originated from life cycles similar to those of Draschia megastoma, Habronema muscae and H. microstoma is considered to be incorrect. Alternatively, it is pointed out that in the primitive subfamily Thelaziinae Baylis and Daubney, 1926 there are forms with typical spiruroid life cycles (Rhabdochona ovifilamenta), forms with life cycles approaching those of the dipetalonematids (Thelazia spp.), and forms with life cycles intermediate between these two (Oxyspirura spp.). It is suggested that intestinal species similar to Rhabdochona gave rise to the more specialized spiruroids and forms that left the gut (Oxyspirura, Thelazia) gave rise to the dipetalonematids.

The dipetalonematids are believed to have originated from nematodes resembling the species of Thelazia and having life cycles like those of T. rhodesii, T. skrjabini and T. gulosa. Some of these worms established themselves in subcutaneous tissues. Like Parafilaria multipapillosa, they released their eggs through a break in the skin of the definitive host, thus causing a skin lesion that attracted various haematophagous arthropods which finally became involved as intermediate hosts in the life cycle. Certain species like the members of Parafilaria and Stephanofilaria (?) came to rely upon intermediate hosts that were unable to break the skin of the definitive host (Musca) and cutaneous lesions became permanent features of their life cycles. Other species became dependent upon intermediate hosts that could puncture the skin (mosquitoes, simuliids etc.) and skin lesions became unnecessary to the life cycle. The larvae of these worms then began to spread into the tissues of the skin, as found in Stephanofilaria, Onchocerca, and some species of Dipetalonema, and the infective larvae developed the ability to penetrate into the wound made by the intermediate host and perhaps, in some cases, the intact skin. Ultimately the larvae of some species habitually entered, or were deposited into, the blood stream and the adult worms were then free to colonize the vertebrate body as their larvae would then be available to the intermediate host no matter where the latter fed on the body of the definitive host; this group of worms gave rise to the many members of the family Dipetalonematidae.

The family Filariidae Claus, 1883 is briefly reviewed in the light of the above hypothesis. It is pointed out that many species, e.g. Diplotriaeninae Skrjabin, 1916, live in the air sacs of reptiles and birds and probably have life cycles similar to that of Diplotriaenoides translucidus, i.e. the eggs pass through the lungs, up the trachea and out in the faeces. It is thought that these forms may represent a separate line of evolution from that which gave rise to the Dipetalonematidae. Certain genera (Lissonema, Aprocta), occurring in the orbits of birds, probably have life cycles like Thelazia or Oxyspirura. Many other genera occurring in superficial muscles and subcutaneous tissues (Squamofilaria, Ularofilaria, Tetracheilonema, Pelecitus, Monopetalonema) may release their eggs through some sort of skin lesion. Studies on these forms are urgently needed as the details of their life cycles may shed fresh light on the origins of the more specialized filarioids.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1957

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References

Anderson, R. C., 1956.—“Ornithofilaria fallisensis n. sp. (Nematoda: Filarioidea) from the domestic duck with descriptions of microfilariae in waterfowl.” Canad. J. Zool., 32, 125137. (W.L. 5998C).CrossRefGoogle Scholar
Anderson, R. C., 1956.—“The life cycle and seasonal transmission of Ornithofilaria fallisensis Anderson, a parasite of domestic and wild ducks.” Canad. J. Zool., 34, 485525.CrossRefGoogle Scholar
Anderson, R. C., 1957.—“Observations on the life cycles of Diplotriaenoides translucidus Anderson and members of the genus Diplotriaena.” Canad. J. Zool., 35, 1524.CrossRefGoogle Scholar
Baer, J. G., 1951. —Ecology of animal parasites. Univ. Illinois Press, UrbanaGoogle Scholar
Baumann, R., 1946.—“Beobachtungen beim parasitaren Summerblüten der Pferde.” Wien. tierärztl. Mscht., 32, 5255. (W.L. 23007).Google Scholar
Buckley, J. J. C., 1937.—“On a new species of Stephanofilaria causing lesions in the legs of cattle in the Malay Peninsula.” J. Helminth., 15, 233242. (W.L. 11224C).CrossRefGoogle Scholar
Buckley, J. J. C., 1955.—“Symposium on loiasis. V. The morphology of the larval stages in the vector: some of the problems involved.” Trans. R. Soc. trop. Med. Hyg., 49, 122126. (W.L. 21671).Google Scholar
Chabaud, A. G., 1954.—“Sur le cycle évolutif des spirurides et de nématodes ayant une biologie comparable.” Ann. Parasit. hum. comp., 29, 4288. (W.L. 899a).CrossRefGoogle Scholar
Chabaud, A. G., 1954a.—“Sur le cycle évolutif des spirurides et de nématodes ayant une biologie comparable.” Ann. Parasit. hum. comp., 29, 206249.CrossRefGoogle Scholar
Chabaud, A. G., 1954b. —“Sur le cycle évolutif des spirurides et de nématodes ayant une biologie comparable.” Ann. Parasit. hum. comp., 29, 358425.CrossRefGoogle Scholar
Chabaud, A. G., 1955.—“Essai d'interpretation phylétique des cycles évolutifs chez les nématodes parasites de vértebres. Conclusions taxonomiques.” Ann. Parasit. hum. comp., 30, 83126.CrossRefGoogle Scholar
Chabaud, A. G., 1955a.—“Remarques sur la symétrie céphalique des nématodes et hypothèses concernant l'évolution de cette symétrie chez les phasmidiens parasites.” Bull. Soc. zool. Fr., 80, 314323. (W.L. 5401).Google Scholar
Chabaud, A. G., 1956. —“Remarques sur le cycle évolutif des filaires du genre Diplotriaena et redescription de D. monticelliana (Stossich. 1890). ” Vie et milieu, 6, 342347. (W.L. 22540a).Google Scholar
Chabaud, A. G. and Choquet, M. T., 1953.—“Nouvel essai de classification des filaires (superfamille de Filarioidea).” Ann. Parasit. hum. comp., 28, 172192. (W.L. 899a).CrossRefGoogle ScholarPubMed
Chandler, A. C., Alicata, J. E. and Chitwood, M. B., 1941. —“Life history (Zooparasitica). II. Parasites of vertebrates” (An introduction to nematology). (Chitwood et al.), Sect. II, Part II. pp. 267301.Google Scholar
Chitwood, B. G., 1932.—“A review of the nematodes of the genus Hastospiculum, with descriptions of two new species.” Proc. U.S. nat. Mus., 80, 19. (W.L. 16944).CrossRefGoogle Scholar
Chitwood, B. G., 1940. —“Nemic embryology. ” (An introduction to nematology). (Chitwood et al.). Sect. II, Part I, pp. 216225.Google Scholar
Chitwood, M. B., 1940. —“Postembryonic development. ” (An introduction to nematology). (Chitwood et al.), Sect. II, Part I, pp. 227240.CrossRefGoogle Scholar
Chitwood, B. G. and Chitwood, M. B., 1950. —An introduction to nematology. Sect. I. Anatomy. Monumental Printing Co., Baltimore.Google Scholar
Chitwood, B. G. and Wehr, E. E., 1934.—“The value of cephalic structures as characters in nematode classification, with special reference to the superfamily Spiruroidea.” Z. Parasitenk., 7, 273335. (W.L. 23536b).Google Scholar
Christenson, R. O., 1950. —“Nemic ova”. (An introduction to nematology). (Chitwood et al.). Sect. I. Anatomy. pp. 175187.Google Scholar
Datta, S., 1939.—“Microfilarial pityriasis in equines (lichen tropicus.)” Vet. J., 95, 213222. (W.L. 22518).Google Scholar
Desportes, C., 1942.—“Forcipomyia velox Winn. et Sycorax silacea Curtis, vecteurs d'Icosiella neglecta (Diesing), filaire commune de la grenouille verte.” Ann. Parasit. hum. comp., 19, 5368. (W.L. 899a).CrossRefGoogle Scholar
Dikmans, G., 1934.—“Observations on stephanofilariasis in cattle.” Proc. helm. Soc. Wash., 1, 42. (W.L. 16747a).Google Scholar
Dikmans, G., 1934a.—“Nematodes as the cause of a recently discovered skin disease of cattle in the United States.” N. Amer. Vet., 15, 2225. (W.L. 15224).Google Scholar
Dikmans, G., 1948.—“Skin lesions of domestic animals in the United States due to nematode infestation.” Cornell Vet., 38, 323. (W.L. 6888).Google ScholarPubMed
Dubinin, V. P., 1949. —(Experimental studies on the developmental cycles of the parasitic worms of some vertebrate animals of the Volga Estuary.) (Russian text.) Mag. Parasit., Moscow, 9, 145151. (W.L. 16035b).Google Scholar
Fain, A., and Herin, V., 1955.—“Filarioses des bovidés au Ruanda-Urundi. III. Etude parasitologique.” Ann. Soc. belge. Méd. trop., 35, 535554. (W.L. 926).Google Scholar
Fielding, J. W., 1927.—“Further observations on the life history of eye worm of poultry.” Aust. J. exp. Biol. med. Sci., 4, 273281.(W.L.2245a).CrossRefGoogle Scholar
Fielding, J. W., 1928.—“Additional observations on the development of the eye worm of poultry.” Aust. J. exp. Biol. med. Sci., 5, 18.CrossRefGoogle Scholar
Fülleborn, F., 1908.—“Über Versuche an Hundefilarien und deren Übertragung durch Mücken.” Arch. Schiffs-u. Tropenhyg., 12, 313351. (W.L. 1804).Google Scholar
Gordon, R. M., and Crewe, W., 1953.—“The deposition of the infective stage of Loa loa by Chrysops silacea, and the early stages of its migration to the deeper tissues of the mammalian hosts.” Ann. trop. Med. Parasit., 47, 7485. (W.L. 1063).Google Scholar
Herin, V., and Fain, A., 1955.—“Filarioses des bovidés au Ruanda-Urundi. II. Etude histopathologique.” Ann. Soc. belge. Méd. trop., 35, 523533. (W.L. 926).Google Scholar
Herin, V., Thienpont, D. and Fain, A., 1955.—“Filarioses des bovidés au Ruanda-Urundi. I. Etude clinique.” Ann. Soc. belge. Méd. trop., 35, 505521.Google Scholar
Ihle, J. E. W., and Ihle-Landenburg, M. D., 1933.—“Over een dermatitis squamosa et crustosa circumscripta bij het rund in Nederlandsch-Indie, genaamd cascada. II. Stephanofilaria dedoesi (N.gen., N.sp.) een nematode uit de huid van het rund.” Ned. ind. Bl. Diergeneesk., 45, 279284. (W.L. 15011).Google Scholar
Jensen, R. and Seghetti, L., 1956.—“Elaeophoriasis in sheep.” J. Amer. vet. med. Ass., 127, 499505. (W.L. 11022).Google Scholar
Kershaw, W. E., 1948.—“Observations on Litomosoides carinii (Travassos, 1919) Chandler, 1931. I. The development of the first-stage larva.” Ann. trop. Med. Parasit., 42, 377399. (W.L. 1063).CrossRefGoogle ScholarPubMed
Klesov, M. D., 1949. —[The biology of the nematode Thelazia rhodesii (Desmarest 1827)]. [Russian text. ] C. R. Acad. Sci. U.R.S.S., 66, 309311. (W.L. 7450).Google Scholar
Klesov, M. D., 1950. —(Contribution to the biology of two nematodes of the genus Thelazia Bosc., 1819, parasites of cattle.) [Russian text.] C. R. Acad. Sci. U.R.S.S., 75, 591594.Google Scholar
Kobayashi, H., 1928.—“On the life history of Oxyspirura mansoni and the pathological changes in the conjunctiva and the ductus lacrymalis, caused by this worm, with further observations on the structure of the adult worm.” J. Med. Ass. Formosa, 29, 491532. (W.L. 11337).Google Scholar
Krastin, N. I., 1949. —[Elucidation of the life cycle of Thelazia rhodesii (Desmarest, 1827) parasitic in the eyes of cattle.] [Russian text. ] C. R. Acad. Sci., U.R.S.S., 64, 885887. (W.L. 7450).Google Scholar
Krastin, N. I., 1949a. —[Epizoology of thelaziasis in cattle and biology of Thelazia rhodesii (Desmarest, 1827). ] [Russian text], J. agric. Sci. Series G., 26, 68. (W.L. 22749b).Google Scholar
Krastin, N. I., 1950. —A study of the developmental cycle of the nematode, Thelazia gulosa (Railliet and Henry, 1911) a parasite of the eyes of cattle. [Russian text]. C. R. Acad. Sci. U.R.S.S., 70, 549551. (W.L. 7450).Google Scholar
Levine, N. D. and Morrill, C. C., 1955.—“Bovine stephanofilaria dermatitis in Illinois.” J. Amer. vet. med. Assoc., 127, 528530. (W.L. 11022).Google Scholar
Leroux, P. L., 1950.—“What is Filaria martis Gmelin, 1790, the type species of the genus Filaria Mueller, 1787 on which the term filariasis (vel filariosis) is based ?” Trans. R. Soc. trop. Med. Hyg., 44, 34. (W.L. 21671).Google Scholar
Losev, L. A., Erokhin, I. P., and Nikanorov, A. F., 1937. —(Parafilariosis of horses in the territories of the lower Volga). [Russian text]. Papers on Helminthology, 30 year Jub. K. I. Skrjabin, pp. 333345.Google Scholar
Lower, H. F., 1954.—“A morphological interpretation of post-embryonic insect development.” Arch. Zool. exp. gen., 91, 5172.(W.L. 1915).Google Scholar
Manson, P., 1878.—“On the development of Filaria sanguinis hominis and on the mosquito considered as a nurse.” J. Linn. Soc., (Zool.) 14, 304311. (W.L. 11296).Google Scholar
Manson-Bahr, P. H., 1940. —Manson's Tropical Diseases. Cassell & Co.Google Scholar
McFadzean, J. A. and Smiles, J., 1956.—“Studies of Litomosoides carinii by phase-contrast microscopy: the development of the larva.” J. Helminth., 30, 2532. (W.L. 11224c).CrossRefGoogle Scholar
McKee, A. J., 1938.—“Microfilaria found in the skin.”(Extracts from paper before Ann. Meet. State Vet. Med. Ass. Texas, Houston), Jan. 13–14. Vet. Med., 33, 115. (W.L. 22520).Google Scholar
Neveu-Lemaire, M., 1936. —Traité d'helminthologie médicale et vétérinaire. Paris.Google Scholar
Pande, P. G., 1936.—“On the identity of the nematode worm recovered from hump sore of cattle in India.” Ind. J. vet. Sci., 6, 346351. (W.L. 9941h).Google Scholar
Peel, E. and Chardome, M., 1946.—“Sur des filaridés de chimpanzés Pan paniscus et Pan satyrus au Congo Belge.” Ann. Soc. belge Méd. trop., 26, 117156. (W.L. 926).Google Scholar
Roubaud, E. and Descazeaux, J., 1921.—“Contribution à l'histoire de la mouche domestique comme agent vecteur des habronémoses des equidés. Cycle évolutif et parasitisme de l'Habronema megastoma (Rudolphi, 1819) chez la mouche.” Bull. Soc. Path. exot., 14, 471506. (W.L. 5310).Google Scholar
Roubaud, E. and Descazeaux, J., 1922.—“Deuxiéme contribution à l'étude des mouches, dans leurs rapports avec l'évolution des Habronémes d'equidés.” Bull. Soc. Path. exot., 15, 9781001.Google Scholar
Schwabe, C. W., 1951.—“Studies on Oxyspirura mansoni, the tropical eyeworm of poultry. II. Life history. Pacif. Sci., 5, 1835. (W.L. 15920a).Google Scholar
Strong, R. P., 1934. —“Onchocerciasis, with special reference to the central American form of the disease. ” No. 6. Contrib. Dept. trop. Med. Inst. trop. Biol. Med. (Harvard Univ. Press). pp. 3132.Google Scholar
Sumners, W. A., 1943.—“Experimental studies on the larval development of Dirofilaria immitis in certain insects.” Amer. J. Hyg., 37, 173178. (W.L. 600a).Google Scholar
Skrjabin, K. I. and Shikhobalova, N. P., 1948. —(Filariae of animals and man.) [Russian text]. Moscow.Google Scholar
Underwood, J. R., 1934.—“Equine dhobie itch, a symptom of filariasis.”A report on 56 cases. Vet. Bull. U.S. Army, 28, 227236. (W.L. 22517d).Google Scholar
Vaills, L., 1936.—“Filariose et microfilariose autochtones chez le chien. Formes cliniques. Considerations.” Rev. vet., Toulouse, 88, 133141. (W.L. 19315).Google Scholar
Wehr, E. E., 1935.—“A revised classification of the nematode superfamily Filarioidea.” Proc. helm. Soc. Wash., 6, 9597. (W.L. 16747a).Google Scholar
Weller, T. H., 1938.—“Description of Rhabdochona ovifilamenta n.sp. (Nematoda: Thelaziidae) with a note on the life history.” J. Parasit., 24, 403408. (W.L. 11428).Google Scholar
Yokagawa, S., 1938.—“Investigations on the mode of infection of Wuchereria bancrofti.” Jap. J. med. Sci. V. Path., 3, 167181. (W.L. 10881r).Google Scholar
Yokagawa, S., 1939.—“Studies on the mode of transmission of Wuchereria bancrofti.” Trans. R. Soc. trop. Med. Hyg., 32, 653668. (W.L. 21671).Google Scholar
Yokagawa, S., 1939a.—“Transmission of W. bancrofti.”(Correspondence). Trans. R. Soc. trop. Med. Hyg., 33, 363364.Google Scholar
Yokagawa, S., 1939b.—“Investigations on the mode of infection of Wuchereria bancrofti.”(Second report). Jap. J. med. Sci. V. Path., 4, 197204. (W.L. 10881r).Google Scholar