Primates and their pinworm parasites: The Cameron hypothesis revisited

Systematic Biology

Volumn 48, Issue 3, 1999, Pages 523-546

  Hugot, J P ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Cameron's hypothesis; Cospeciation; Enterobiinae; Host parasite coevolution; Nematoda; Oxyurid; Pinworm; Primate

Indexed keywords

CATARRHINI; ENTEROBIUS; ENTEROBIUS VERMICULARIS; NEMATODA; OXYURIDAE; PLATYRRHINI; PRIMATES; SCIURIDAE; STREPSIRHINI;

ANIMAL; ARTICLE; CLASSIFICATION; ENTEROBIUS; GENETICS; ISOLATION AND PURIFICATION; PARASITOLOGY; PHYLOGENY; PRIMATE; SCIURIDAE; SPECIES DIFFERENCE;

ANIMALS; ENTEROBIUS; PHYLOGENY; PRIMATES; SCIURIDAE; SPECIES SPECIFICITY;

EID: 0033183797     PISSN: 10635157     EISSN: None     Source Type: Journal    
DOI: 10.1080/106351599260120     Document Type: Article

References (91)

1. ANDREWS, P. 1988. Pages 143-175 in The phylogeny and classification of the Tetrapods, volume 2 (M. J. Benton, ed.). Clarendon Press, Oxford, England.
2. ARTIGAS, P. DE TOLEDO. 1936. Estudios helminthologicos. I. Paraoxyuronema brachytelesi g. n., sp. n., parasita de Brachyteles arachnoides (Geoffr., 1806); Oxyuronemidae, fam. n. Mem. Inst. Butantan 10:77-85.
3. BAER, J. G. S. 1935. Etudes de quelques helminthes de Lémuriens. Rev. Suisse Zool. 42:275-292.
4. BARTON, R. A., A. PURVIS, AND P. H. HARVEY. 1995. Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos. Trans. R. Soc. Lond. 348:381-392.
5. BAYLIS, H. A. 1928. Some further parasitic worms from Sarawak. Annu. Mag. Nat. Hist. 1:606-608.
6. BERNARD, J. 1969. Quelques nématodes parasites nouveaux ou encore non signalés en Tunisie. Arch. Inst. Pasteur Tunis 46:397-411.
7. BROOKS, D. R., AND D. R. GLEN. 1982. Pinworms and primates: A case study in coevolution. Proc. Helminth. Soc. Wash. 49:76-85.
8. BUCKLEY, J. J. C. 1931. On two new species of Enterobius from the monkey Lagothrix humboldtii. J. Helminthol. 9:133-140.
9. CAMERON, T. W. 1929. The species of Enterobius Leach, in Primates. J. Helminthol. 7:161-182.
10. CAMERON, T. W. 1932. On a new species of Oxyuris from the grey squirrel in Scotland. J. Helminthol. 10:29-32.
11. CHABAUD, A. G., E. R. BRYGOO, AND A. J. PETTER. 1965. Les nématodes parasites de lémuriens malgaches. VI. Description de six espèces nouvelles et conclusions générales. Ann. Parasitol. Hum. Comp. 40:181-214.
12. CHABAUD, A. G., AND A. J. PETTER. 1959. Les nématodes parasites de lémuriens malgaches. II. Un nouvel Oxyure: Lemuricola contagiosus Mém. Inst. Sci. Madagascar 13:127-132.
13. CHABAUD, A. G., AND A. J. PETTER. 1961. Evolution et valeur systématique des papilles cloacales chez les nématodes phasmidiens parasites de vertébrés. C. R. Acad. Sci. Paris 252:1684-1686
14. CHABAUD, A. G., A. J. PETTER, AND Y. GOLVAN. 1961. Les nématodes parasites de lémuriens malgaches. III. Collection récoltée par M. et Mme Francis Petter. Ann. Parasitol. Hum. Comp. 36:113-126.
15. CIOCHON, R. L., AND A. B. CHIARELLI. 1980. Concluding remarks. Pages 495-501 in Evolutionary biology of the New World monkeys and continental drift (R. L. Ciochon, and A. B. Chiarelli, eds.). Plenum, New York.
16. COBBOLD, T. S. 1864. Entozoa, an introduction to the study of Helminthology, more particularly to the internal parasites of man. London, Groombridge & Sons. Pages 1-480.
17. DAVIDSON, W. R. 1976. Endoparasites of selected populations of gray squirrels Sciurus carolinensis (Gmelin). Diss. Abstr. Int. B 36:4337.
18. DOLLFUS, R. P., AND A. G. CHABAUD. 1955. Cinq espèces de nématodes chez un atèle [Ateles ater (G. Cuvier, 1823)], mort à la ménagerie du muséum. Arch. Mus. Natl. Hist. Nat. Paris 3:27-40.
19. ECKERLIN, R. P. 1975. Studies on the life-cycle of Strongyloides robustus Chandler, 1942, and a survey of the helminths of Connecticut sciurids. Diss. Abstr. Int. B 35:5716.
20. ERHARDOVA, B. 1958. Parasiticti cervi hlodavcu ceskoslovenska. Cslká Parasit. 5:27-103.
21. ERIKSSON, T. 1996. Autodecay, Version 2.9.5 (Hypercard stack distributed by the author). Botaniska Institutionen, Stockholm Univ., Stockholm, Sweden.
22. GEDOELST, L. 1916. Notes sur la faune parasitaire du Congo Belge. Rev. Zool. Afr. 5:24-27.
23. GORGAS, M. 1967. Vergleichend-anatomische Untersuchungen am Magen-Darm-Kanal der Sciuromorpha, Hystricomorpha and Caviomorpha (Rodentia). Z. Wiss. Zool. 175:237-404.
24. HOFFSTETTER, R. 1982. Les Primates Simiiformes (= Anthropoidea). Compréhension, phylogénie, histoire biogéographique. Ann. Paléontol. Paris 68:241-290.
25. HÖRNING, B. 1963. Zur Kenntnis der Endoparasitenfauna des Eichhörnchens (Sciurus vulgaris) in der Schweiz. Rev. Suisse Zool. 70:25-45.
26. HUGOT, J. P. 1982. Les Oxyuridae d'écureuils. Ràpartition géographique et évolution. Mém. Mus. Natl. Hist. Nat. Paris 123:219-226.
27. HUGOT, J. P. 1983a. Enterobius gregorii (Oxyuridae, Nematoda), un nouveau parasite humain (Note préliminaire). Ann. Parasitol. Hum. Comp. 58:403-404.
28. HUGOT, J. P. 1983b. Redescription de Ctenodactylida tunetae (Pharyngodonidae, Nematoda): un Oxyure atypique de Mammifères. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 5:749-757.
29. HUGOT, J. P. 1984a. Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). I. Parasites de Sciuridae: sous-genre Rodentoxyuris. Bull. Mus. Nat. Hist. Nat. Sect. A Zool. 6:711-720.
30. HUGOT, J. P. 1984b. Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). II. Sous-genre Hapaloxyuris parasite de Primates Callitrichidae. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 6:1007-1019.
31. HUGOT, J. P. 1985. Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). III. Sous-genre Trypanoxyuris parasite de primates Cebidae et Atelidae. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 7:131-155.
32. HUGOT, J. P. 1987a. Sur le genre Enterobius: s. g. Colobenterobius. I. Oxyures parasites de singes Colobinae en région éthiopienne. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 9:341-352.
33. HUGOT, J. P. 1987b. Sur le genre Enterobius: s. g. Colobenterobius. II. Oxyures parasites de singes Colobinae en région orientale. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 9:799-813.
34. HUGOT, J. P. 1988. Les nématodes Syphaciinae parasites de rongeurs et de lagomorphes. Taxonomie. Zoogéographie. Evolution. Mém. Mus. Natl. Hist. Nat. Sect. A Zool. 141:1-153.
35. HUGOT, J. P. 1993. Redescription of Enterobius anthropopitheci (Nematoda, Oxyurida), parasite of the chimpanzees. Syst. Parasitol. 26:201-207.
36. HUGOT, J. P. 1995. Redescription of Xeroxyuris parallela (Linstow, 1908) n. gen., n. cb., parasite of Xerus inauris. Parasite 2:1-7.
37. HUGOT, J. P., AND C. FELIU. 1990. Description de Syphabulea mascomai n. sp. Analyse du genre Syphabulea. Syst. Parasitol. 17:219-230.
38. HUGOT, J. P., S. L. GARDNER, AND S. MORAND. 1996. The Enterobiinae fam. nov. (Nematoda, Oxyurida), parasites of primates and rodents. Int. J. Parasitol. 26:147-159.
39. HUGOT, J. P., S. MORAND, AND S. L. GARDNER. 1995. Morphology and morphometrics of three oxyurids parasitic in primates. Description of Lemuricola microcebi n. sp. Int. J. Parasitol. 25:1065-1075.
40. HUGOT, J. P., S. MORAND, AND R. GUERRERO. 1994. Trypanoxyuris croizati n. sp. and T. callicebi, two vicariant forms parasite of Callicebus spp. (Primate, Cebidae). Syst Parasitol 27:35-43.
41. HUGOT, J. P., AND C. TOURTE-SCHAFFER. 1985. Etude morphologique des deux oxyures parasites de l'Homme: Enterobius vermicularis et E. gregorii. Ann. Parasitol. Hum. Comp. 60:57-64.
42. HUGOT, J. P., AND C. VAUCHER. 1985. Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). IV. Sous-genre Trypanoxyuris parasite de Primates Cebidae et Atelidae (suite). Etude morphologique de Trypanoxyuris callicebi n. sp. Bull. Mus. Nat. Hist. Nat. Sect. A Zool. 7:633-636.
43. INGLIS, W. G. 1961. The oxyurids parasites (Nematoda) of primates. Proc. Zool. Soc. Lond. 136:103-122.
44. INGLIS, W. G., AND G. E. COSGROVE. 1965. The pinworms parasites (Nematoda: Oxyuridae) of the Hapalidae (Mammalia: Primates). Parasitology 55:731-737.
45. INGLIS, W. G., AND C. DIAZ-UNGRÍA. 1960. Nematodes parasitos de vertebrados venezolanis. I. Una revision del genero Trypanoxyuris (Ascaridata: Oxyuriae). Mem. Soc. Cienc. Nat. La Salle 19:176-212.
46. INGLIS, W. G., AND F. L. DUNN. 1963. The occurrence of Lemuricola (Nematoda: Oxyurida) in Malaya: With the description of a new species. Z. Parasitenkd. 23:354-359.
47. INGLIS, W. G., AND F. L. DUNN. 1964. Some oxyurids from Neotropical primates. Z. Parasitenkd. 24:83-87.
48. JABLONSKI, N. G. 1986. An history of form and function in the primate masticory apparatus from the ancestral primate through the strepsirhines. Pages 537-558 in Comparative primate biology, volume 1. Systematics, evolution and anatomy. A. R. Liss, New York.
49. JOHNSON-MURRAY, J. L. 1977. Myology of the gliding membranes of some petauristine rodents (Genera: Glaucomys, Petaurista, Petinomys, and Pteromys). J. Mammal. 58:374-384.
50. KEYMER, I. F. 1983. Diseases of squirrels in Britain. Mammal Rev. 13:155-158.
51. KREISS, H. A. 1944. Beiträge zur Kenntnis parasitischer Nematoden. XI. Neue parasitische Nematoden. Rev. Suisse Zool. 51:227-262.
52. LE ROUX, P. L. 1930. The generic position of Oxyuris polyoon Linstow, 1909 in the subfamily Oxyurinae Hall, 1916. Rep. Dir. Vet. Serv. South Africa 16:205-210.
53. LINSTOW, O. F. B. 1907. Neue und beknnante Nematoden. Zentralbl. Bakteriol. 44:1-265.
54. LINSTOW, O. F. B. 1908. Zoologische und Anthropologische Ergebisse einer Forschungsreise im Westlichen und Zentralen Südafrika ausgefürhrt in den Jahren 1903-1905. II. Helminthes. Nematoden und Acanthocephalen. Denkschr. Med. Ges. Jenia 13:19-28.
55. MACLAUGHLIN, C. A. 1984. Protogomorph, sciuromorph, castorimorph, myomorph (Geomyoid, anomaluroid, pedetoid and ctenodactyloid) rodents. Pages 267-288 in Orders and families of recent mammals of the world (S. Anderson, and J. K. Jones, Jr., eds.). Wiley & Sons, New York.
56. MADDISON, W. P. 1993. Missing data versus missing characters in phylogenetic analysis. Syst. Biol. 42:576-581.
57. MADDISON, W. P., AND D. R. MADDISON. 1997. MacClade Analysis of phylogeny and character evolution, version 3. 07. Sinauer, Sunderland, Massachusetts.
58. PAGE, R. D. M. 1995. Parallel phylogenies: Reconstructing the history of host-parasite assemblages. Cladistics 10:155-173.
59. PAGE, R. D.M. 1996a. TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
60. PAGE, R. D. M. 1996b. Temporal congruence revisited: Comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Syst. Biol. 45:151-167.
61. PATRICK, M. J., AND W. D. WILSON. 1995. Parasites of the Abert's squirrel (Sciurus aberti) and red squirrel (Tamiasciurus hudsonicus) of New Mexico. J. Parasitol. 81:321-324.
62. PETTER, A. J., A. G. CHABAUD, R. DELAVENAY, AND E. R. BRYGOO. 1972. Une nouvelle espèce de nématode du genre Lemuricola, parasite de Daubentonia madagascariensis Gmelin, et considérations sur le genre Lemuricola. Ann. Parasitol. Hum. Comp. 47:391-398.
63. PORTER, C. A., S. L. PAGE, J. CZELUSNIAK, H. SCHNEIDER, M. P. C. SCHNEIDER, I. SAMPAIO, AND M. GOODMAN. 1997. Phylogeny and evolution of selected primates as determined by sequences of the ε-globin locus and 5′ flanking regions. Int. J. Primatol. 18:261-295.
64. PURVIS, A. 1995. A composite estimate of primate phylogeny. Philos. Trans. R. Soc. Lond. 348:405-421.
65. QUENTIN, J. C. 1969. Essai de classification des nématodes Rictulaires. Mém. Mus. Natl. Hist. Nat. Sect. A Zool. 54:55-115.
66. QUENTIN, J. C., C. BETTERTON, AND M. KRISHNASAMY. 1979. Oxyures nouveaux ou peu connus, parasites de primates, de rongeurs et de dermoptères en Malaisie. Création du sous-genre Colobenterobius n. subgen. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 1:1031-1050.
67. QUENTIN, J. C., AND F. TENORA. 1975. Morphologie et position systématique de Lemuricola (Rodentoxyuris) sciuri (Cameron, 1932) nov. comb. nov. subgen., et Syphacia (Syphatineria) funambuli Johnson, 1967. Oxyures (Nematoda) parasites de rongeurs sciuridés. Bull. Mus. Natl. Hist. Nat. Sect. A Zool. 178:1525-1535.
68. RAUSCH, R., AND J. D. TINER. 1948. Studies on the parasitic helminths of the North Central States. I. Helminths of Sciuridae. Am. Midl. Nat. 39:728-747.
69. ROCAMORA, J. M., C. FELIU, AND S. MAS-COMA. 1978. Sobre algunos helmintos de Sciurus vulgaris Linnaeus, 1758 (Rodentia: Sciuridae) y Meles meles Linnaeus, 1758 (Carnivora: Mustelidae) en Cataluna (Espana). Rev. Iber. Parasitol. 38:155-163.
70. ROSENBERGER, A. L. 1981. Systematics: The higher taxa. Pages 9-27 in Ecology and behaviour of neotropical primates (A. F. Coimbra-Filho, and R. A. Mittermeier, eds.). Academia Brasileira de Ciencias, Rio de Janeiro.
71. ROSENBERGER, A. L. 1984. Fossil New World monkeys dispute the molecular clock. J. Hum. Evol. 13:737-742.
72. RUVOLO, M. 1997. Molecular phylogeny of the hominoids: Inferences from multiple independent DNA sequence data sets. Mol. Biol. Evol. 14:248-265.
73. SANDOSHAM, A. A. 1950. On Enterobius vermicularis (Linnaeus, 1758) and some related species from primates and rodents. J. Helminthol. 24:171-204.
74. SCHNEIDER, A. 1866. Monographie der Nematoden. Berlin.
75. SCHNEIDER, H., M. P. C. SCHNEIDER, I. SAMPAIO, M. L. HARADA, M. STANHOPE, J. CZELUSNIAK, AND M. GOODMAN. 1993. Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol. Phylogenet. Evol. 2:225-242.
76. SHARPILO, L. D., AND L. V. LUGOVAYA. 1984. A rare species. Vestn. Zool. 5:79, (in Russian).
77. SIDDIQI, A. H., AND M. B. MIRZA. 1954. On a new oxyurid worm, Enterobius zakiri n. sp. from the rectum of Semnopithecus entellus schistaceus (Tarai langur). Indian J. Helminthol. 6:24-25.
78. SOLOMON, S. G. 1933. On a new species of Enterobius from the marmoset (Callithrix jacchus). J. Helminthol. 11:95-100.
79. STANGER-HALL, K. F. 1997. Affinities among the extant Malagasy lemurs. J. Mammal Evol. 4:163-194.
80. SUNDBERG, P., AND R. HYLBOM. 1994. Phylogeny of the Nemertean subclass Paleonemertea (Anopla, Nemertea). Cladistics 10:347-402.
81. SWOFFORD, D. 1998. PAUP Phylogenetic analysis using parsimony, test ver. 4.0d63. Laboratory of Molecular Systematics, Smithsonian Institution, Washington, D.C.
82. TENORA, F. 1967. The helminthofauna of small rodents of the Rohacska dolina valley (Liptovské Hole Mts) Slovakia. Acta Sci. Nat. Brno 1:31-68.
83. THORINGTON, R. W., JR. 1984. Flying squirrels are monophyletic. Science 225:1048-1050.
84. TRAVASSOS, L. 1919. Esboço de uma chave general dos nematodes parasitos. Rev. Vet. Zootec. (Manizales) 10:1-59.
85. TRAVASSOS, L. 1925. Fauna Brasiliense. Nematodes: Oxyuroidea-Oxyuridae. Revisao do genero Enterobius Leach, 1853. Mus. Nac. Rio J. 2:5-11.
86. VEVERS, C. M. 1923. Some new and little known helminths from British Guyana. J. Helminthol. 1:35-45.
87. VUYLSTÉKE, C. 1964. Mission de Zoologie médicale au Maniema (Congo Léopoldville). (P. L. G. Benoît, 1959). 3. Vermes. Nematoda. Ann. Mus. R. Afr. Cent. Ser. Zool. 132:41-66.
88. WAHID, S. 1961. On two new species of the genus Enterobius Leach, 1853, from a Colobus monkey. J. Helminthol. 35:345.
89. WILSON, D. E., AND D. M. REEDER. 1993. Mammal species of the world. A taxonomic and geographic reference, 2nd edition. Smithsonian Institution Press, Washington, D.C.
90. YIN, W. Z. 1973. Helminths of birds and wild animals from Lin Tsan Prefecture, Yunnan Province, China. II. Parasitic nematodes of mammals. Acta Zool. Sin. 19:354-364.
91. YODER, A. D., M. CARTMILL, M. RUVOLO, K. SMITH, AND R. VILGALYS. 1996. Ancient single origin for Malagasy primates. Proc. Natl. Acad. Sci. USA 93:5122-5126.