The Taxonomy of Leishmania-Like Parasites of Reptiles
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Leishmania. Taxonomie et phylogenèse. Applications éco-épidémiologiques. (Coll. int. CNRS/INSERM, 1984). IMEEE, Montpellier, 1986, 143-148. The taxonomy of Leishmania-like parasites of reptiles R. Killick-Kendrick*, R. Lainson**, J.-A. Rioux***, and V.M. Sarjanova**** SUMMARY — The taxonomic position of the Leishmania-hke parasites occurring as amastigotes or promasti- gotes in the gut or blood of reptiles is reviewed and it is concluded that they should be grouped in the genus Sauroleishmania Ranque, 1973, with Sauroleishmania tarentolae (Wenyon, 1920) as the type species. The principal differences between Leishmania Ross, 1903 and Sauroleishmania Ranque, 1973 include the verte- brate and invertebrate hosts, the host cells inhabited by the amastigote, the sites of development in the sandfly, the kDNA and the distance between the subpelUcular microtubules of the promastigotes. KEY-WORDS — Sauroleishmania — Lizards — Taxonomy. Ali current, modern methods of distinguishing trypanosomatids by examining nucleic acids, isoenzymes or antigens have failed to reveal a close relationship between the leishmaniae of mammals and of reptiles [7] and there now appears to be general agreement that the Leishmania-like parasites of reptiles should be classified separately from the mammalian species of Leishmania. The taxonomic position of the reptilian parasites is, however, confused. In this note, we review the relevant publications and propose that they should be transfered to the genus Sauroleishmania Ranque, 1973. : n Parasites which occur as amastigotes, promastigotes, or both in the blood or cloaca of lizards, or which can be cultured purely as promastigotes from the blood or viscera of lizards, were at first assigned to either the genus Leptomonas Kent, 1880 [21] or the genus Herpetomonas Kent, 1880 [21] (see [15] ). In 1920, Wenyon [52] named two new species of lizard parasites and put them into the genus Leishmania Ross, 1903 [41]. From that time, most other species of similar parasites of lizards have been assigned to this genus. In 1982, Saf janova [42] used the subgeneric name Sauroleishmania to accommodate the so-called leishmaniae of reptiles with Leishmania (Sauroleishmania) gymnodactyli Khodukin and Sofiev, 1947 (cited from Adler [1] ) as the type species. Saf janova's name had, however, already been used in 1973 in a thesis by Ranque [38], although as a genus with a different type species. We have looked into the question of whether or not Ranque's thesis constitutes a publication within the meaning of the International Code of Zoological Nomenclature of 1985 [19] and conclude that it is fully acceptable. It satisfies the three criteria in Article 8(a) and was produced by offset printing [Article 8(c) ], not by electrostatic or xerographic methods [see Article 9(3) ]. The next mention of the name was by Nicoli and Nourrit in 1974 [33] who wrote « Sauro• leishmania R.M. Nicoli et Ph. Ranque, 1973, pour les Trypanosomidés (sic) de Nématocères (Phlebotomidae). Développement postérieur prenant chez les Sauropsidés la forme promastigote (infestation par piqúre ou ingestion). Espèce type : Sauroleishmania tarentolae (CM. Wenyon, 1921) de Tarentola mauritanica. » There was, however, no publication by Nicoli and Ranque in 1973 and the citation was modified from that given in Ranque's thesis (R.M. Nicoli, pers. comm.). The differences between Leishmania Ross, 1903 [41], emend. Vickerman, 1976 [50], and Sauroleishmania Ranque, 1973 [38] (Table I) are sufficiently marked to warrant taxonomic * Medicai Research Council Externai Scientific Staff, Department of Pure and Applied Biologj', Imperial CoUege at Silwood Park, Ascot, United Kingdom. ** Wellcome Parasitology Unit, Instituto Evandro Chagas, Belém, Pará, Brazil. *** Laboratoire d'Ecologie médicale et de Pathologie parasitaire (Pr. J.-A. Rioux), Faculte de Médecine, Montpellier, France. **** Gamaleya Institute of Epidemiology and Microbiology, Academy of Medicai Sciences of the U.S.S.R., Moscow, U.S.S.R. 144 TABLE I Principal differences between Leishmania and Sauroleishmania. Leishmania Ross, 1903, Sauroleishmania Character emend. Vickerman, 1976 Ranque, 1973 Vertebrate host mammals snakes *" and lizards Form in vertebrate host amastigote amastigote or promastigote Host cell of amastigote* macrophage and its precursors monocyte, thrombocyte or erythrocyte Invertebrate host Phlebotomus spp. (Old World) Lutzomyia spp. (New World) Sergentomyia spp. Psychodopygus spp. (New World) (Old World) Site of development suprapylarian or peripylarian hypopylarian or peripylarian in invertebrate host Mode of transmission bite of vector ingestion or bite of vector** Maxi-circles of kDNA 26-27 kb 32-38 kb Distance between sub- pellicular microtubules 25-40 nm 60-70 nm 1. Belova and Bogdanov (1969). 2. Chatton and Blanc (1914), Léger (1918), Francini (1921). Shortt and Swaminath (1928), David (1929), Frenkel (1941), Rioux et al. (1969, 1979), Edeson and Himo (1973), Nadim (1974), Telford (1979), Ovezmukhammedov and Safjanova (1983). 3. Léger (1918). Wenyon (1920), Zmeyev (1936), Fopov (1941), Andrusko and Markov (1955), Killick-Kendrick and Wallbanks (1981). 4. Telford (1979). 5. Telford (pers. comm.). 6. Lainson and Shaw (1979) 7. Kolesnikov et al. (1984). 8. Safjanova (1982). * Amastigotes of Leishmania divide in the macrophage whereas amastigotes of Sauroleishmania, whether in monocytes, thrombocytes or erythrocytes, appear never to be in division. ** No species of Sauroleishmania has yet been transmitted experimentally from a sandfly to a reptile. recognition of two distinct groups. By Article 43(a) of the International Code of Zoológica] Nomenclature (1985), a taxon at genus or subgenus rank is simultaneously established for the other rank with the same author and date. The question of whether Sauroleishmania should be accepted as a genus, as treated in the present paper, or as a subgenus of Leishmania, as viewed by Safjanova [42, 43] is, therefore, a matter of opinion. Ranque [38] clearly indicated S. tarentolae (Wenyon, 1921) as the type species of Sauroleish• mania. However, as Gardener [15] pointed out, the date of the naming of the species tarentolae is 1920, not 1921 as usually cited. The confusion arose because of a delay in the publication of the Journal Parasiíology after World War I resulting in two volumes, 11 and 12, being published in the same year (1920) (F.E.G. Cox, Editor of Parasitology, pers. comm.). When first published, the name was spelt tarantolae, not tarentolae. This is construed as an « inadvertent error » on the assumption that Wenyon intended the name to be spelt in the same way as that of the host, Tarentola. Evidence for this is in Wenyon's monograph published in 1926 [53] where he corrected the name to tarentolae without comment. The later name now stands as a correction of an « incorrect original spelling » [Articles 32(c)(ii) and (d) of the Code (1985)]. The identity of Sauroleishmania Ranque, 1973 rests on the type species, S. tarentolae (We• nyon, 1920), of which there is no type material available. A culture of promastigotes purporting to be L. tarentolae Wenyon, 1920 (code RTAR/DZ/39/TAR VI) isolated by Parrot [35] in 1939 was recently shown by Wallbanks et al. [51] to be Trypanosoma platydactyli Catouillard, 1909. A comparison of isoenzymes revealed no differences between Parrot's parasite and a double cloned culture of the trypanosome. This work, however, did not show that the amastigotes seen in the blood of Tarentola by Chatton and Blanc [8] and Rioux et al. [39, 40] are developmental forms of a trypanosome and, without evidence to the contrary, these stages are presumably Sauroleish• mania tarentolae (Wenyon, 1920) (see [37] ). 145 In Table II a list is given of named species of Leishmania of lizards which are here transferred to Sauroleishmania Ranque, 1973. We give no opinion of the vaUdity of these names some of which may fali into synonymy [15]. Some or ali of those parasitizing the intestinal tract of lizards may be parasites of ingested insects [10, 18, 49, 50]. In addition of the named species, there are a number of reports of Sauroleishmania published without names. Particularly interesting records include : amastigotes of Chalcides ocellatus in Sicily [13] ; promastigotes cultured from the blood of five species of snakes in the Turkmenian S.S.R. [6] ; promastigotes (some of which were later identified by Saf janova (unpubl. observations) as S. gymnodactyli) cultured from the blood of 4 species of Phrynocephalus, 1 of Agama, 5 of Eremias, 1 of Gymnodactylus and 1 of Teratoscincus of the Turkmenian S.S.R. [5] ; a parasite of Alsophylax pipiens on mainland China [16] ; amastigotes seen in smears of bone marrow and liver of lizards in Iran [31] ; promastigotes cultured from the heart blood of Agama sp. near Mashad, Iran [32] ; amastigotes in the thrombocytes of Agama agilis and Teratoscincus scincus in Pakis- tan [47] ; two different promastigotes of Chamaeleo dipidis in Zâmbia, one in the cloaca and one an ephemeral infection of the peripheral blood [23] ; unusually small amastigotes in the erythro- cytes of two species of geckoes, Hemidactylus platycephalus and Chemaspis africana, in Tanzânia (Sam Telford Jr, pers. comm.); and amastigotes and promastigotes in the intestine of Anolis lucius in Cuba [20]. There are numerous other records of flagellates in the guts of lizards, often assigned to the genera Herpetomonas and Leptomonas which, like some of the named species of Sauroleishmania in the intestine and cloaca of reptiles, may have been