Primates and Their Pinworm Parasites: The Cameron

Syst. Biol. 48(3):523– 546, 1999

Primates and Their Pinworm Parasites: The Cameron Hypothesis Revisited J. P. H UGOT Muséum National d’Histoire Naturelle, Institut de Systématique, FR 1541 du CNRS, Laboratoire de Zoologie des Mammifères et Oiseaux (Biosystématique et Coévolution chez les Né matodes Parasites), 55, rue Buffon, 75231 Paris cedex 05, France; E-mail: [email protected] Abstract.— A morphologically based cladistic analysis of the Enterobiinae, which includes most of the Oxyuridae parasitic in Primates, allows a reevaluation of the Cameron’s hypothesis of close coevolution with cospeciation between hosts and parasites. Each of the three genera separated in the Enterobiinae ts with one of the suborders dened in Primates: Lemuricola with the Strepsirhini, Trypanoxyuris with the Platyrrhini, and Enterobius with the Catarrhini. Inside each of the three main groups, the subdivisions observed in the parasite tree also t with many of the subdivisions generally accepted within the Primate order. These results conrm the subgroups previously described in the subfamily and support Cameron’s hypothesis in its aspect of association by descent. Although the classication of the Enterobiinae generally closely underlines the classication of Primates, several discordances also are observed. These are discussed case by case, with use of computed reconstruction scenarios. Given that the occurrences of the same pinworm species as a parasite for several congenerichost species is not the generalized pattern,and given that several occurrences also are observed in which the speciations of the parasites describe a more complex network, Cameron’s hypothesis of a slower rhythm of speciation in the parasites can be considered partly refuted. The presence of two genera parasitic on squirrels in a family that contains primarily primate parasites also is discussed. The cladistic analysis does not support close relationships between the squirrel parasites and suggests an early separation from the Enterobiinae for the rst (Xeroxyuris), and a tardy host-switching from the Platyrrhini to the squirrels for the second ( Rodentoxyuris ). [Cameron’s hypothesis; cospeciation; Enterobiinae; host/parasite coevolution; Nematoda; Oxyurid; pinworm; Primate]

Members of the parasite family Oxyuridae (Cobbold, 1864) can be found in most families and genera of primates. The pattern of distribution observed in the parasites, in which each species of parasitic nematode occurs in a specic host, allowed Cameron (1929) to speculate a close correspondence between phylogenetic histories of both oxyurids and primates. Later, Sandosham (1950), Inglis (1961), and Brooks and Glen (1982), using cladistic analysis, gave additional arguments for coevolutionary relationships among primates and their oxyurid parasites. Recent redescriptions have revealed that most members of the Oxyuridae parasitic in primates share derived characters that group them in a new subfamily: the Enterobiinae (Hugot et al., 1996). The present work provides a cladistic analysis of the Enterobiinae based upon morphological characters. The hypothesis of coevolution with cospeciation between the Enterobiinae and their primate hosts is then examined. The Enterobiinae includes three

species parasitic of squirrels (in two genera). Their presence in a family that contains primarily primate parasites also is discussed.

M ATERIAL AND M ETHODS Sampling The cladistic analysis of the Enterobiinae includes 46 species of the subfamily and 2 outgroup species. Appendix 1 lists the 48 species analyzed, their specic hosts, the “sources” (i.e., the documents used for description of the different parasite taxa), and the identication of the examined specimens. The outgroup includes one species belonging to a different family of the Oxyurida, the Pharyngodonidae (Ctenodactylina tunetae is a parasite of African rodents of the family Ctenodactylidae), and a second species that is an Oxyuridae not belonging to the Enterobiinae (Ingloxyuris inglisi is a parasite for Lepilemur rucaudatus in Madagascar).

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The general classication of the Primates follows Purvis (1995). Different classications proposed either for the Platyrrhini (Porter et al., 1997; Rosenberger, 1981, 1984; Schneider et al., 1993) or for the Strepsirhini (Jablonski, 1986; Barton et al., 1995; Yoder et al., 1996; Stanger-Hall, 1997) also are considered for discussion. The identication of the hosts follows Wilson and Reeder (1993). For the denition of the Callitrichidae, I refer to Hoffstetter (1982). Analyses The cladistic analysis is based on 45 morphological characters from various organ systems (see Table 1 and Appendix 2). Character states used for this analysis have been explained in our work establishing the definition of the subfamily (Hugot et al., 1996) and are gured in the documents referenced as “source” in Appendix 1. For characters of the head and lateral alae, only females were considered; the characters of the head and lateral alae are roughly identical in both sexes, and consequently, introducing characters of the males would merely duplicate the phylogenetic information given by the females. Also, all the females of the taxa considered in this paper have been described, but the males are unknown for ve of these species. Available hypotheses concerning parasitic nematode character evolution are poor and are generally based on two assumptions: (1) The morphology of larval stages can be considered “primitive” (Quentin, 1969), and (2) parasites that are specic for “primitive hosts” have “primitive” character states (Chabaud and Petter, 1961). The rst hypothesis, which deals with the ontogenic criterion, has to be tested case by case and cannot be generalized a priori. The second hypothesis is completely subjective and cannot be considered in a cladistic analysis. For these reasons, and because I agree with Sundberg and Hylbom’s (1994:362) opinion that “the most reliable criterion for transformation series. . .[is]. . . the cladogram itself and the congruence with other characters,” I have left all characters unordered. When necessary, I have used the method proposed by Madison (1993) for coding multistate

characters. Inapplicable characters (in the sense used by Madison, 1993) were coded “-”; missing characters were coded “?” For cladistic analysis, character weights were scaled so that each character received the same total weight regardless of the number of states observed. For computation of decay indices, character weights were scaled to 1, whatever the number of their character states. Parsimony analysis was conducted with the PAUP 4.0.0d63 test version (Swofford, 1998). MACCLADE 3.07 (Maddison and Maddison, 1997) was used for data and tree handling and for computation of tree statistics. A UTODECAY 2.9.5 (Eriksson, 1996) and T REEVIEW 1.3 (Page, 1996a) were used for computation and printing of decay indices on trees. Runs were performed by heuristic search with tree bisection– reconnection (TBR) branch-swapping, addition sequence random = 1,000 replicates, MULPARS option in effect, steepest descent option not in effect, branches collapsed (creating polytomies) if maximum branch length = 0, and multistate taxa interpreted as polymorphism. Comparing host and parasite cladograms was performed by using T REEM AP 1.0b (Page, 1995). Following Page (1996b), speciation events are divided into three categories: cospeciation, duplication, and host-switch. Sorting events cover any case in which a parasite species can be expected on one host species and has not been observed. RESULTS AND D ISCUSSION Results of Cladistic Analysis The analysis gave three trees from which a strict consensus tree was computed (Fig. 1): tree length = 52.91; consistency index (CI) = 0.8551; homoplasy index (HI) = 0.1496; CI excluding uninformative characters = 0.8494; HI excluding uninformative characters = 0.1506; retention index = 0.9407; rescaled consistency index = 0.8044. The consensus tree is fully resolved except for the trichotomies including Paraoxyuronema lagothricis, P. duplicidens and the adjacent clades, Colobenterobius longispiculum, and C. pitheci and the adjacent clades.

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Data matrix. Inapplicable characters coded as dashes, missing characters coded ?

All trees suggest the same basic arrangement of the ingroup. Xeroxyuris parallela is a sister group for all other species, which are distributed within 3 major monophyletic groups corresponding to the genera Lemuri-

cola, Enterobius, and Trypanoxyuris, respectively. Within the genus Lemuricola, the subgenus Lemuricola is monophyletic and the subgenus Madoxyuris is paraphyletic, with M. daubentoniae (Madoxyuris 1) separated

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F IGU RE 1. Results of cladistic analysis (48 taxa and 45 characters): strict consensus of 3 trees. Terminal clades named according to the current classication of the Enterobiinae. Clades tting with a previously described genus or subgenus are in bold. Tick marks with numbers indicate unambiguous synapomorphies (character and character state). Bold integers are decay indices. Cte. = Ctenodatctylina; Ingl. = Inglisoxyuris ; X . = Xeroxyuris; L. = Lemuricola; E. = Enterobius; T. = Trypanoxyuris .

from the other 4 species (Madoxyuris 2) by the monotypic subgenus Biguetius. Within

the genus Enterobius, the subgenus Enterobius is subdivided into 2 clades: The rst

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assembles the parasites of Homo and Pan, the second the parasites of the Cercopithecidae (Macaca, Cercopithecus , and Papio) with the parasites of Gorilla and Pongo. Subgenus Colobenterobius appears to be monophyletic and can be subdivided into 2 clades: The rst assembles the African species and the second the Asian species. In the genus Trypanoxyuris, the subgenera Hapaloxyuris, Rodentoxyuris, and Paraoxyuronema appear as monophyletic groups, and subgenus Trypanoxyuris is subdivided into different clades. Trypanoxyuris 1 is associated with Hapaloxyuris and Rodentoxyuris and groups the parasites of the Cebidae (Saimiri and Cebus); Trypanoxyuris 2 is a paraphyletic group associated with Paraoxyuronema. Synapomorphic characters and decay indices, as represented on Figure 1, show that the monophyly of the Enterobiinae and each of its major subgroups is robust. However, the basal relationship among Xeroxyuris, Lemuricola, and Enterobius/Trypanoxyuris, is weakly supported by the decay index (0). In the following, I will consider: (1) explanations for the presence of squirrel parasites in the Enterobiinae, (2) the consistency of Cameron’s hypothesis, and (3) which different scenarios can be proposed to explain the discordances of host and parasite phylogenies within each of the 3 major monophyletic groups. What Can Explain the Presence of Squirrel Parasites in the Enterobiinae? Host and parasite distributions.—Squirrel parasites are classied into two genera. Xeroxyuris (Hugot, 1995) has a single species whose host, Xerus inauris, is a ground squirrel living in the dry steppes of southern Africa. The type species of the second taxon was rst described as Enterobius sciuri (Cameron, 1932) from Sciurus carolinensis in Scotland. Later, Kreiss (1944), described as a new species a pinworm parasite collected in Sciurus vulgaris in Switzerland, which ignoring Cameron’s work, he also named Enterobius sciuri (sic). Since then “Enterobius sciuri” has been recorded from S. vulgaris, in Switzerland (H orning, ¨ 1963), Czechoslovakia (Erhardova, 1958; Tenora, 1967), France (Quentin and Tenora,

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1975; Hugot, 1984a), Britain (Keymer, 1983; Hugot, 1984a), Spain (Rocamora et al., 1978; Hugot and Feliu, 1990), and Ukraine (Sharpilo and Lugovaya, 1984). Specimens identied as “E. sciuri” also were recorded from the North American squirrels: Glaucomys volans (Rausch and Tiner, 1948; Eckerlin, 1975), Sciurus niger (Rausch and Tiner, 1948), S. carolinensis (Davidson, 1976), and Sciurus aberti (Patrick and Wilson, 1995). In 1975, Quentin and Tenora classied “E. sciuri” sensu lato in a new genus, Rodentoxyuris. In an earlier work (Hugot, 1984a), I showed that: (1) the European specimens, described from S. vulgaris in different localities, must be identied with the type species described in Britain from S. carolinensis by Cameron (1932); (2) the specimens collected in different hosts in North America are a different species, Rodentoxyuris bicristata, described from specimens collected in Glaucomys sabrinus; and (3) Rodentoxyuris could be classied as a subgenus of Trypanoxyuris (Vevers, 1923). Sciurus vulgaris is found in the palearctic region, from Spain to Kamchatka. In America the respective ranges of S. niger, S. carolinensis, and G. volans are widely overlapping, from the East Coast west to the Rocky Mountains and north to the Canadian border; southward, the three species approach the Mexican boundary. In addition, G. volans has montane populations scattered from Mexico to Honduras. Glaucomys sabrinus has a very different range extending from Alaska and Canada, to the U.S. Northwest. The range of G. sabrinus is overlapping with the respective ranges of the other three American squirrels around the Great Lakes and in the Appalachian Mountains. Sciurus aberti has a very restricted range divided into two nonconuent areas: The rst extends through a part of Utah, Colorado, Wyoming, New Mexico, and Arizona, and the second is in northern Mexico. Phylogeny of the hosts.—The phylogenetic relationships between Glaucomys spp. and the other squirrels still are debated. Glaucomys has been proposed to be classied together with all the other ying squirrels in a different subfamily within the Sciuridae; this supposition that the ying squirrels are

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a monophyletic group has been supported by Johnson-Murray (1977) and Thorington (1984). Conversely, some authors have suggested that Glaucomys could be more closely related to other holarctic squirrels, particularly to the Sciurini (Gorgas, 1967). These different hypothesis can be represented by two different topologies: (1) Xerus as the sister group of Sciurus spp. + Glaucomys spp., and (2) Glaucomys spp. as the sister group of Sciurus spp. + Xerus. Investigating evolutionary scenarios.— Figure 2 proposes different scenarios reconstructed using T REE M AP (Page, 1995). Figures 2a and b use topology 1 as host tree and suppose that the parasites switched from the Platyrrhini to the common ancestor of Glaucomys spp. and Sciurus spp. Figure 2a hypothezises a duplication (speciation of a parasite without speciation of its host) after the initial host switch from the Platyrrhini. This duplication produces two independent lineages, the rst developing with the North American squirrels and missing S. vulgaris (one sorting event), and the second having S. vulgaris as primitive host and missing the others (two sorting events). T REE M AP also gives an alternative solution (not illustrated) to scenario 2a, i.e., two independent host-switching events from the Platyrrhini, giving birth to R. sciuri and R. bicristata, respectively. Figure 2b describes a parallel evolution between Rodentoxyuris and the Glaucomys/Sciurus lineage, interrupted on the Sciurus branch, which is missing the Nearctic Sciurus spp. (sorting event). The presence of R. bicristata on the Nearctic Sciurus spp. results from a hostswitch from Glaucomys spp. Using topology 2 gave the same reconstructions of the parasite tree but with an initial host-switching on the common ancestor of Xerus, Sciurus and Glaucomys. Figure 2c, using topology 1, and Figure 2d, using topology 2, describe a different reconstruction of the parasite tree: an initial host switch from the Platyrrhini to the common ancestor of Sciurus spp., with which Rodentoxyuris spp. evolve in parallel; and later, a second host switch from the Nearctic Sciurus spp. to Glaucomys spp. All the scenarios require host-switching of R. sciuri from S. vulgaris to S. carolinensis.

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Discussion.—Two a priori hypothesis could possibly be proposed to explain the distribution of the Enterobiinae parasitic in squirrels: (1) At the beginning of their respective radiation, squirrels and primates shared common parasites that coevolved with their hosts. These parasites were successful in primates and became established in most of their descendants. They generally aborted in squirrels (in which other pinworm families were successful; see Hugot, 1982), and thus the contemporary species must be considered relictual. (2) The squirrel parasites result from several independent host-switching events. All the scenarios of Figure 2 contradict the rst proposition. If Xeroxyuris could be interpreted as relictual on an ancient squirrel lineage, the appearance of Rodentoxyuris is independent and is the result of one or several host switches, from the Platyrrhini to the squirrels. In addition, the position of Rodentoxyuris on the cladogram implies that the parasites switched onto the squirrels after the Enterobiinae had differentiated into several lineages within the Platyrrhini. Because during most of the Tertiary the Platyrrhini were isolated in South America, and squirrels are presumed not to have been present in the Neotropics during the period, this implies that the contact between the Neotropical monkeys and the squirrels occurred after a land connection was reestablished between North and South America. Therefore, the proposed reconstructions of evolutionary scenarios have to be compatible with host-switching from the Platyrrhini to the holarctic squirrels, chronologically situated in the latest part of the Tertiary. Xeroxyuris and Rodentoxyuris result from independent evolutionary events; Rodentoxyuris results from one or two initial hostswitchings from the Platyrrhini to the common ancestor of either (1) Sciurus spp., or (2) Glaucomys spp. and Sciurus spp., or (3) Xerus, Glaucomys spp., and Sciurus spp. Because Xerus is known only from Africa, the scenarios that propose host-switching from the Platyrrhini to the common ancestor of Xerus, Sciurus, and Glaucomys are unlikely; this concerns all scenarios using topology 2 except scenario 2d. To be reliable, scenarios

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(a)

Xerus inauris X. parallela R. bicristata Sciurus niger Sciurus aberti R. bicristata R. bicristata Sciurus carolinensis R. sciuri

R. bicristata Sciurus carolinensis R. sciuri

Sciurus vulgaris R. sciuri Glaucomys sabrinus R. bicristata


R. bicristata Glaucomys volans


Platyrrhini Trypanoxyuris


Enterobius Catarrhini

Enterobius Catarrhini

Strepsirhini Lemuricola Xerus inauris X. parallela R. bicristata Sciurus niger Sciurus aberti R. bicristata

(c)

(b)

Xerus inauris X. parallela R. bicristata Sciurus niger Sciurus aberti R. bicristata

cospeciation duplication sorting event host switch pinworms hosts

Strepsirhini Lemuricola Xerus inauris X. parallela R. bicristata Sciurus niger Sciurus aberti R. bicristata









Enterobius Catarrhini Strepsirhini Lemuricola

(d)

Enterobius Catarrhini Strepsirhini Lemuricola

F IGUR E 2. Different scenarios explaining the presence of squirrel parasites in the Enterobiinae. Xeroxyuris; R. = Rodentoxyuris .

2a and 2b require that the common ancestor of Glaucomys and Sciurus was still living in America during the latest part of the Tertiary. This supposes close phyletic relationships between these two genera and conicts with the hypothesis of monophyly of the ying squirrels. The reconstruction of the parasite tree proposed by scenarios 2c and 2d is independent of which phyletic relationships can be hypothesized between Sciurus and Glaucomys. To be valid, this re-

construction requires two assumptions: (1) a rst host-switching from the Platyrrhini to the ancestor of Sciurus spp., and (2) a later host-switching from Sciurus to Glaucomys. Because Sciurus probably migrated into the Neotropics during the late Tertiary, the rst assumption seems valid. Considering the present distribution of Glaucomys spp. and Sciurus spp. in the Nearctic, the second assumption also is acceptable. Consequently, the scenario represented on Figures 2c and

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2d looks most reliable. Whatever the scenario considered, the Neotropical squirrels probably were involved in the story. Unfortunately, we have absolutely no data concerning the presence of pinworms in these hosts. Sciurus carolinensis, the type host of the European species, is a native from North America and was introduced recently into the United Kingdom. The origin of the parasites collected in S. vulgaris was questioned by Sandosham (1950:199), who concluded that “because the North American Sciurus carolinensis has been introduced in the British Isles since 1889 , . . . Sciurus vulgaris has become infected in recent years by S. carolinensis which, in turn, brought the infection from the New World.“ This conclusion looks questionable because S. carolinensis has never been recorded from the European continent, whereas the European parasite has been recorded from S. vulgaris in numerous localities from western and central Europe and especially in Spain. Furthermore, Spain is known to be an area of endemism for its parasitic fauna (Hugot and Feliu, 1990). This suggests that S. vulgaris is the earliest host for R. sciuri and that S. carolinensis was infested when introduced in Britain. This last assumption is supported by all the scenarios of Figure 2. The Cameron Hypothesis Revisited Cameron (1929:180–181) rst noticed that The examination of the forms. . .[of pinworms found in Primates]. . .suggests that one species restricts itself to one genus of host rather than to one species; in other words the evolution of the parasite is slower than that of the primate. It would seem legitimate to assume, . . .that the parasite has evolved with the host. If one assumes the existence of a preenterobius form in the pre-simian host, then the modications of the parasite should accompany the generic difference of the host. One will expect to nd forms more closely related to the human parasite in apes, while those in old world monkeys would be closer to E. vermicularis than those in new world monkeys and the lorises but not so close as in apes.

Therefore, the Cameron hypothesis includes two different claims: rst, Primates and their pinworms are an example of “association by descent,” and the phylogeny of the parasites parallels the phylogeny of the hosts; second,

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because the parasites speciated more slowly that the primates, a single parasite species has to be recorded for each host genus. Figure 3 shows that the 3 genera separated in the Enterobiinae t with one of the suborders dened in Primates: Lemuricola comprises the parasites of the Strepsirhini, Trypanoxyuris the parasites of the Platyrrhini, and Enterobius the parasites of the Catarrhini. In addition, Trypanoxyuris and Enterobius appear as sister groups on the cladogram, and the distribution of the Enterobiinae t with Hoffstetter (1982) subdivisions: Strepsirhini and Haplorhini (= Platyrrhini + Catarrhini). Inside each of the three main groups, the subdivisions observed in the parasite tree also t with many of the subdivisions generally accepted within the primate order. Hapaloxyuris ts with the Callitrichidae and Paraoxyuronema with the Atelidae. Colobenterobius comprises all the parasites of the Colobidae and parallels the host tree in its subdivision into two clades, which t, respectively, with the African or the Asian species. Subgenus Lemuricola comprises the parasites of the Cheirogaleidae, and the parasites of the other lemurs are a monophyletic group (including Madoxyuris and Biguetius). The parasites of the Cercopithecidae are classied in a monophyletic group, as are the parasites of humans and chimpanzees. Thus, the results from the cladistic analysis of the Enterobiinae generally support the Cameron hypothesis in its assertion of “association by descent,” and the rst claim can be considered validated. Given that in only seven occurrences can it be inferred the same pinworm species is a parasite for several congeneric host species (Fig. 3), and that the correspondence of “one parasite species per host species” appears to be the generalized pattern (28 occurrences), Cameron’s second claim “one (parasite) species restricts itself to one genus of host,” cannot be considered validated. Furthermore, in ve occurrences two closely related parasite species parasitize a single host species, and in four occurrences each one of two congeneric host species is parasitized by its specic pinworm. These examples refute Cameron’s second claim. Because our knowledge of the distribution of the Entero-

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Gorilla gorilla Pan spp. Homo sapiens Daubentonia madagascariensis Propithecus verrauxei Hapalemur simus Eulemur macaco Eulemur fulvus Cheirogaleus major Microcebus murinus Nycticebus coucang

L.contagiosus L.microcebi

Hapaloxyuris

Trypanoxyuris Enterobius

Trachypithecus phayrei Chlorocebus aethiops Macaca spp. Papio spp. Pongo pygmaeus

Protenterobius

Lemuricola

Ateles ater Procolobus badius Colobus sp. Colobus guereza Semnopithecus entellus Trachypithecus spp.

Paraoxyuronema

Colobenterobius

Cebus spp. Saimiri spp. Aotes trivirgatus Callicebus moloch Callicebus torquatus Chiropotes spp. Pithecia spp.

Enterobius

Callithrix jacchus Saguinus oedipus Saguinus nigricollis

H.goeldii H.oedipi H.callithricis H.tamarini T.clemenentinae T.sceleratus T.microon T.callicebi T.croizati T.satanas T.trypanuris T.minutus Paraoxyuronema spp. P.brachytelesis P.atelis C.pesteri C.inglisi C.colobis C.guerezae C.paraguerezae Colobenterobius spp. C.zakiri C.entellus C.presbytis E.bipapillatus E.macaci E.brevicauda E.buckleyi E.lerouxi E.anthropopitheci E.gregorii E.vermicularis M.daubentoniae Big.trichuroides M.bauchotis M.lemuris M.baltazardi M.vauceli Prt.nycticebi

Madoxyuris

Callithrichidae Cebidae Pitheciidae

Atelidae

Alouatta seniculus Brachyteles arachnoides Lagothrix lagotricha

Cheirogaleidae Lemuridae

Catarrhini Lorisidae

Strepsirhini

Callimico goeldii

Cercopithecidae Colobidae Hominidae

Haplorhini

Platyrrhini


Lemuricola

F IGUR E 3. Tree reconciliation of parasite species versus host species; parasite tree as Figure 1 on the right, host tree modied from Purvis (1995:Fig. 4) on the left. Squirrel parasites have been removed. Parasite abbreviations as in Figure 1.

biinae among the primate order cannot be considered complete, it is not implausible that further investigations would reveal that the differentiation of the parasites mimics the zoogeography of the hosts with more detail that we currently know. Figure 3 also indicates several disagreements between host and parasite distribution. In the following section, they are considered group by group. The Lemuricola/Strepsirhini Lineages Host and parasite phylogenies.—Some authors (Jablonski, 1986; Andrews, 1988) have proposed grouping the cheirogaleids with the Afro-Asian lorises, thereby making Malagasy primates paraphyletic. Recent

works distinguish an Afro-Asian loris group and a Malagasy lemur group and agree with Malagasy primate monophyly (Barton et al., 1995; Purvis, 1995; Yoder et al., 1996; Stanger-Hall, 1997); however, they disagree on the relationships within their subgroups. Phylogenetic debate centers on the Malagasy mouse, dwarf lemur (Cheirogaleidae), and aye-aye (Daubentoniidae), but the relationships between Hapalemur, Propithecus, and Eulemur also are questioned (Fig. 4). The parasite tree comprises the parasites of the Cheirogaleidae and the other Malagasy lemurs, respectively, in two monophyletic groups separated by the parasite of the loris: Protenterobius nycticebi (Fig. 1).

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F IGU RE 4. Different hypotheses of the phylogenetic relationships within the Strepsirhini. Tree a: after Jablonski (1986:Fig. 2); tree b: after Barton et al. (1995:Fig. 2); tree c: after Purvis (1995:Fig. 4); tree d: after Yoder et al. (1996:Fig. 1a, molecular tree); tree e: after Yoder et al. (1996:Fig. 1b, morphological tree); tree f: after Stanger-Hall (1997:Fig. 5). Daub. = Daubentonia .

Investigating evolutionary scenarios.— Using successively the different hypotheses represented on Figure 4 as host trees, exact search routines were performed by using T REEMAP. The results are presented in Table 2. The reconstructions admitting the maximum number of cospeciations and the lowest number of other evolutionary events are obtained when using Yoder et al. (1996), and Stanger-Hall (1997) trees. Yoder et al. (1996) gave two different trees. The rst, based on molecular data, is shown in Figure 4d; the second, based on morpho-

logical data, is shown in Figure 4e. The best t is observed with Yoder ’s morphological tree, which gives two reconstructions with only three extra evolutionary events (one is shown in Fig. 5b), and a third one with ve extra evolutionary events (Fig. 5a). Scenario 5a hypothesizes an initial duplication (speciation of a parasite without speciation of its host) in the Lemuricola lineage, giving birth to two independent branches— the rst developing with the Cheirogaleidae and missing the other lemurs and the lorises (two sorting events), and the second

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T AB LE 2. Statistics for reconstructions of the parasite tree when using the different phylogenies of the Strepsirhini depicted in Figure 4. For each host tree the reconstruction admitting the highest number of cospeciation events and the lowest number of other evolutionary events is detailed. Host tree

a b c d e f

Jablonski (1986) Barton et al. (1995) Purvis (1995) Yoder et al. (1996) Yoder et al. (1996) Stanger-Hall (1997)

Reconstructions a

Pb

Cospeciations

Duplications

21 5 10 2 3 2

0.029 0.004 0.003 0.001 0.001 0.001

6 7 7 8 8 8

1 1 1 1 1 1

Host-switching Sorting events

3 2 2 1 1 1

Totalc

2 4 1 4 1 3

6 7 4 6 3 5

Number of reconstructions given by an exact search. Probability of independence between host and parasite phylogenies when the host tree was compared with 1,000 random parasite cladograms generated by a Markovian test. c Sum of 3 previous columns. a

b

(a)

cospeciation duplication sorting event host switch pinworms hosts

Catarrhini Enterobius

Catarrhini Enterobius Platyrrhini Trypanoxyuris

(b)


Nycticebus Prot. nycticebi Daubentonia M. daubentoniae

Nycticebus Prot. nycticebi

Propithecus B. trichuroides

Propithecus B. trichuroides

Hapalemur M. bauchotis

Hapalemur M. bauchotis

Eulemur macaco M. lemuris

Eulemur macaco M. lemuris

Eulemur fulvus M. baltazardi M. vauceli

Eulemur fulvus M. baltazardi

Microcebus L. microcebi Cheirogaleus L. contagiosus

Daubentonia M. daubentoniae

M. vauceli Microcebus L. microcebi Cheirogaleus L. contagiosus

F IGUR E 5. Two of the best reconstructions for the parasites of Strepsirhini given by an exact search, when using tree e of Figure 4 as host tree. Prot. = Protenterobius; M. = Madoxyuris; B. = Biguetius; L. = Lemuricola.

developing with all the others and missing the Cheirogaleidae (one sorting event). Scenario 5b hypothezises an initial cospeciation giving birth to a lemur and a loris parasite lineages. The rst lineage survives in the Cheirogaleidae and misses the others, whereas the parasites of the other Malagasy primates derive from host-switching from the loris lineage onto the common ancestor of the lemurs. T REE M AP also gives an alter-

native solution (not illustrated) to scenario 5b, in which the initial cospeciation occurs on the common ancestor of the lemurs and cheirogaleids, with the parasite of Nycticebus coucang resulting from host-switching from the lemur branch. Using the other host trees of Figure 4 gives the same three events; the differences appear in the upper parts of the respective reconstructions. Whatever host tree is considered, the presence of M. vauceli

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and M. baltazardi on the same host (Eulemur fulvus) is explained by a duplication. Discussion. —Concerning the topology of the Lemuricola clade, two explanations can be proposed: (1) The distribution of hosts and parasites results from close coevolution with cospeciation, and the parasite tree mirrors the phylogeny of the hosts; this supposes that Malagasy primates are paraphyletic. (2) The parasite tree does not strictly match primate phylogeny, and the classication of Protenterobius must be explained in a different way. Because the best scenarios are found when mapping the parasite tree on the host trees resulting from the most recent studies (Yoder et al., 1996; Stanger-Hall, 1997) and because these works, using either molecular or morphological data, have given very strong arguments for Malagasy primate monophyly, the rst hypothesis probably can be refuted. Those scenarios involving a host switch (Fig. 5b or its alternative) require that Nycticebus (or its ancestor) and the common ancestor of Daubentonia, Propithecus, Hapalemur, and Eulemur had to be sympatric after the phylogenetic separation of their respective lineages. Only scenario 5a allows an early and denitive separation of the lemurs and lorises. Therefore I consider that scenario the most reliable. The Trypanoxyuris/Platyrrhini Lineages Host and parasite phylogenies.—Separate independent hypotheses of the phylogenetic relationships among the Platyrrhini monkeys have been produced, based either on morphological or molecular data (Rosenberger, 1981, 1984; Schneider et al., 1993; Purvis, 1995; Porter et al., 1997), but the results are generally conicting and the phylogeny of the group is still debated. Four several phylogenetic hypotheses for the Platyrrhini are represented on Figure 6. All these trees strongly support the monophyly of three main groups: (1) the Atelidae/Alouattidae (Alouatta, Brachyteles, Lagothrix, and Ateles), (2) the Pitheciidae (Cacajao, Chiropotes, and Pithecia), (3) the Callitrichidae (Cebuella, Callithrix, Saguinus, Leontopithecus, and Callimico), and (4) the sis-

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ter grouping of Cebus and Saimiri in a family Cebidae. They conict in how the main groups relate to each other and to Aotus and Callicebus. However, only the Schneider tree (Fig. 6b) disagrees with a close relationship between the Atelidae/Alouatta and the Pitheciidale; the Purvis tree (Fig. 6c) proposes a sister grouping for these groups. All the trees of Figure 6, excluding the Porter tree (Fig. 6d), agree in the sister grouping of the Callitrichidae and the Cebidae. The cladistic analysis of the pinworms agrees with all of the main groups dened above and with the sister grouping of the Callitrichidaewith the Cebidae; the parasite tree also agrees with the Purvis tree in grouping the Atelidae/Alouatta and the Pitheciidae in sister groups. The respective positions of Aotus and Callicebus are the most variable; only the Rosenberger tree (Fig. 6a) and the Purvis tree (Fig. 6c) propose their association in a monophyletic group. All trees, excluding the Rosenberger tree and the parasite tree, agree with a close association of Aotus with the Cebidae/Callitrichidae. Investigating evolutionary scenarios.— Using successively the different hypotheses represented on Figure 6 as host trees, I performed exact search routines, using T REE M AP. The results are presented in Table 3 and Figure 7. Discussion. —The reconstruction admitting the maximum number of cospeciations (5) and the lowest number of other evolutionary events (1) is obtained by using the Purvis (1995) tree (Fig. 7c). This scenario suggests an initially close coevolution with cospeciation between the parasites and a host clade grouping the Callitrichidae/Cebidae and Aotus/Callicebus and, later, host switching from Callicebus to the common ancestor of the Atelidae/Alouatta + the Pitheciidae, followed by cospeciation within this second group. Because this scenario implies a very asymmetric timing of diversication within the Platyrrhini, this reconstruction is unlikely. The other reconstructions represented on Figure 7 admit 4 cospeciations only. The reconstructions obtained by using either the Rosenberg (1981, 1984) or the Porter (1997) trees (Figs. 7a and

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F IGUR E 6. Different hypotheses of the phylogenetic relationships within the Platyrrhini. Tree a after Rosenberger (1981:Fig. 1); tree b after Schneider et al. (1993:Fig. 3); tree c after Purvis (1995:Fig. 4); tree d after Porter et al. (1997:Fig. 4). T AB LE 3. Statistics for reconstructionsof the parasite tree when using the different phylogeniesof the Platyrrhini depicted on Figure 6. For each host tree the reconstruction admitting the highest number of cospeciation events and the lowest number of other evolutionary events is detailed in the last 5 columns. Host tree

a b c d

Rosenberger (1981, 1984) Schneider et al. (1993) Purvis (1995) Porter et al. (1997)

Reconstructions a

Pb

Cospeciations

Duplications

Hostswitching

Sorting events

Totalc

6 3 1 6

0.042 0.043 0.003 0.046

4 4 5 4

0 0 0 0

2 2 1 2

2 0 0 2

4 2 1 4

Footnotes as in Table 2.

d, respectively) have the greatest number of other evolutionary events (4). Both describe a parallel evolution of the Enterobiinae and the Platyrrhini beginning with the common ancestor of the hosts, and a delayed diversication of the Atelidae/Alouatta clade. The lowest number of other evolutionary events (2) is obtained when using the Schneider (1993) tree (Fig. 7b). This last scenario implies two successive host-switchings: from Aotus, or its ancestor, to the common ancestor of a Pitheciidae/Callicebus clade, and later from the Pitheciidae to the common ancestor of the Atelidae/Alouatta clade. Again, a delayed diversication of the different hosts clades is necessary. The reconstructions of Figures 7a, b, and d, and the parasite data support those phylogenetic hypotheses of the Neotropical mon-

keys that suppose close relationships between Callicebus and the Pitheciidae. The parasite data, which support none of the published hypotheses concerning Aotus (either a close association with the Callitrichidae/Cebidae, or with genus Callicebus, or both), do not provide any help in understanding the exact position of Aotus within the Platyrrhini. The Enterobius/Catarrhini Lineages Host and parasite phylogenies.—All the most recent hypotheses concerning the phylogeny of the Catarrhini agree with the general subdivisions of the Purvis tree: Apes and human beings opposed to a monkey group subdivided into a Colobidae and a Cercopithecidae families. In addition, a Western African group and an Eastern Asian

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(a)

Atelidae Paraoxyuronema

(b)

Alouatta seniculus Trypanoxyuris minutus


Pitheciidae Trypanoxyuris 2


Callicebus spp. Trypanoxyuris 2


Aotus trivirgatus Trypanoxyuris microon


Cebidae Trypanoxyuris 1

cospeciation sorting event host switch pinworms hosts


Cebidae Trypanoxyuris 1

Callithrichidae Hapaloxyuris

Callithrichidae Hapaloxyuris










Aotus trivirgatus

Trypanoxyuris microon

Cebidae

Trypanoxyuris 1

(c) Callithrichidae Hapaloxyuris

(d)

Callithrichidae Hapaloxyuris Cebidae Trypanoxyuris 1

F IGU RE 7. Best reconstructions for the parasites of Platyrrhini given by an exact search, when using successively tree a, b, c, or d of Figure 6 as host tree.

group also are distinguished within the Colobidae. Within the Cercopithecidae, baboons and macaca are generally associated as sister groups and opposed to the guenons. Within the apes and humans group, the family Pongidae, in which were previously classied all of the apes (Pongo, Gorilla, and

Pan), has been reduced to the single genus Pongo, because Gorilla and Pan have been demonstrated to be more closely related to Homo. Finally, several recent works have given a strong support to the sister grouping of Homo and Pan (Ruvolo, 1997). The parasite tree agrees with the distribution of

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the Colobidae and with the sister grouping of Homo and Pan but disagrees with the Purvis tree on three different points: (1) The association of the parasites of Gorilla and Pongo with the parasites of the cercopithecids implies that the parasites of apes are paraphyletic. (2) The association of the cercopithecid group with the parasites of human and apes distributes the monkey parasites in two monophyletic groups (together a polyphyletic group). (3) The sister grouping of Macaca and Chlorocebus parasites conict with the monophyly of Papio and Macaca. Investigating evolutionary scenarios.— When T REE M AP exact search routines were performed, opposing the Enterobius clade of the parasite tree and Purvis tree, 12 different reconstructions were found (Fig. 8), all of which gave ve cospeciation events. One single reconstruction was found with the highest number of 11 required extra evolutionary events (Fig. 8a). The shortest were two reconstructions with six extra evolutionary events; one of these is represented in Figure 8c. Within the 12 different reconstructions found, the rst point of discordance described above is explained in three scenarios (Fig. 8a, b, and c). Figure 8a shows a duplication (speciation of a parasite without speciation of its host) on the common ancestor of the parasites of humans and apes and requires 3 subsequent sorting events. In Figure 8b the parasites evolve in parallel with the humans and apes but miss the Gorilla branch (1 sorting event), which requires a host-switching from Pongo toward Gorilla. Figure 8c depicts an equivalent scenario in which the humans and apes branch misses the Pongo parasite (1 sorting event)—which requires a host switch from Gorilla toward Pongo. The second point of discord mentioned above is explained either by a host-switching from either Gorilla or Pongo toward the cercopithecids (Fig. 8a, b, and c), or by 2 host switchings (not illustrated): the rst from either Pongo or Gorilla toward the common ancestor of Macaca and Papio, the second one toward Chlorocebus . The third point of discordance is explained by following the three different scenarios depicted in Figures 8a, b, and c. On Figure

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8a, a duplication of the parasite occurs in the common ancestor of the cercopithecids. On Figure 8b, the evolution of the parasites parallels the host tree but misses the Macaca branch, which is explained by a host-switch from Chlorocebus toward Macaca. On Figure 8c, the parasites of Macaca and Papio have a common ancestor, and a host-switch from Macaca gives birth to the parasite of Chlorocebus. All 12 scenarios explain the presence of two different parasite species in humans by a duplication. Discussion.—Because all the different lineages recognized in the Catarrhini are supposed to be born in Africa (Hoffstetter, 1982), and because all the scenarios that explain the origin of the parasites of the cercopithecids require either that Pongo or Gorilla (or both), or their respective ancestors, were sympatric with the common ancestor of these monkeys (Figs. 8a and b) or at least with the common ancestor of the pair Macaca/Papio (Fig. 8c), the simplest hypothesis is that the evolutionary events described on Figure 8 took place in Africa. However, the association of E. lerouxi with the other four species is only weakly supported by the cladogram in Figure 1, the decay index is low, and this node is not sustained by any synapomorphy. Enterobius lerouxi is a species for which several characters are undescribed (Table 1). This means that the position of E. lerouxi on the cladogram results, in part, from the interplay between homoplasic and missing characters. Thus, the monophyly of the parasites of Gorilla, Pan, and Homo is not denitively refuted by the results of the cladistic analysis. Therefore, scenario 8c, which is congruent with the monophyly of this group and requires the lowest number of extra hypotheses, looks the most acceptable. Biogeography Figure 9 superimposes the cladogram of the Enterobiinae on a world map and, for each of the main groups, summarizes the reconstructions considered the most reliable in previous discussions. The rst dichotomy separates a short “squirrel” African branch from a widespread radiation with Primates, resulting in (1) an early withdrawal of

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(c) (a)

Chlorocebus E.bipapillatus

Western Colobidae Colobenterobius

(b)

Macaca E.macaci

Eastern Colobidae Colobenterobius

Chlorocebus E.bipapillatus

Papio E.brevicauda

E.macaci Macaca Papio E.brevicauda

Pongo E.buckleyi

Chlorocebus E.bipapillatus Macaca E.macaci Papio

Pongo E.buckleyi

E.brevicauda Pongo E.buckleyi

Gorilla E.lerouxi

Gorilla E.lerouxi

Pan E.anthropopitheci

Pan E.anthropopitheci

Homo E.gregorii

Homo E.gregorii E.vermicularis

E.vermicularis

Gorilla E.lerouxi Pan E.anthropopitheci Homo E.gregorii E.vermicularis cospeciation duplication sorting event host switch pinworms hosts

F IGU RE 8. Different reconstructions given for the parasites of Catarrhini by an exact search, when using Purvis (1995:Fig. 4) tree as host tree.

the Lemuricola/Strepsirhini lineage toward Madagascar, separating from (2) the common ancestor of the Enterobius/Catarrhini and Trypanoxyuris /Platyrrhini lineages. (3) An extensive radiation of the Trypanoxyuris/Platyrrhini lineage in South America has a terminal branch extending into the Holarctic, where once again the squirrels were parasitized. (4) Enterobius/Catarrhini differentiates into several African lineages, each migrating toward Eurasia and southeast Asia, and nally with Enterobius and humans all around the world. In the Lemuricola/Strepsirhini lineage, the scenario that requires a duplication and three sorting events for the reconciliation of the parasite and host trees looks the most acceptable (see above). In the Enterobius/Catarrhini lineage, parallel evolution between the colobes and their parasites is strongly supported; the best explanation for the distribution of the other

parasites is a double host-switch from the African apes toward the Asiatic apes and the cercopithecids, respectively. In the Trypanoxyuris/Platyrrhini lineage, parallel evolution is inferred between the parasites and a Callitrichidae/Cebidae monophyletic group. Two successive host-switchings toward the common ancestor of a Callicebus/Pitheciidae clade, and later toward the common ancestor of the Atelidae and Alouatta, explains the evolution of the other parasites. Discussion. —The evolutionary history depicted on Figure 9 strongly suggests a Gondwanan distribution for the Enterobiinae at the beginning of their radiation, and Africa appears to be the most convincing center for their origin. This agrees with the hypothesis by Yoder et al. (1996) of an African origin for the common ancestor of lemurs and lorises, the hypothesis of an African common ances-

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Paraoxyuronema Trypanoxyuri s 2 Trypanoxyuris 2 Rodentoxyuris Trypanoxyuris 2 Trypanoxyuris 1 Hapaloxyuris

Enterobius Enterobius Rodentoxyuris

Xeroxyuris

Enterobius

Enterobius Colobenterobius

Lemuricola

Colobenterobius

Madoxyuris.1&2 and Biguetius

Protenterobius F IGUR E 9. Cladogram of the Enterobiinae superimposed on a world map (actual). · = parallel phylogenies between hosts and parasites; ° = sorting event; = duplication of a parasite lineage; ® = host switching. Squirrel parasite lineages in grey dashed lines.

tor for the Catarrhini and Platyrrhini (Ciochon and Chiarelli, 1980), and the hypothesis of Africa as a center of origin for the main component lineages in the Catarrhini (Hoffstetter, 1982). All this suggests that the Enterobiinae would have accompanied the living primates since they began to disperse at the

beginning of the Tertiary. However, because squirrels are not presumed to be present in Africa before the Pleistocene (MacLaughlin, 1984), the position of Xeroxyuris as the rst branch of the cladogram must be questioned. Three explanations are possible: (1) We are misinterpreting the relationships be-

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tween Xeroxyuris and the rest of the family; (2) the squirrels were present in Africa earlier than is generally accepted, despite no fossils having been found; or (3) the beginning of the radiation of the Enterobiinae must be found elsewhere and earlier, where and when primates and squirrels, or their ancestors, were sympatric—which probably means in the Northern continents. The best explanation for the distribution of Rodentoxyuris is a host-switch from the Platyrrhini to the Sciurini at the end of the Tertiary, when terrestrial connections were reestablished between North and South America. Because the European parasite, R. sciuri, is probably a native species whose specic host is Sciurus vulgaris, the simplest explanation for this parasite is a parallel evolution and dispersal of Rodentoxyuris with Sciurus spp., in the Holarctic. In the Asiatic part of its range, S. vulgaris is parasitized not by Rodentoxyuris but by a different genus of pinworm, Syphabulea, which is closely related to another subfamily: the Syphaciinae. This last group extends from southeast Asia to North America and to Spain and parazites squirrels exclusively (Hugot and Feliu, 1990). In the Holarctic part of its range, Syphabulea, which is a parasite for Sciurus, Sciurotamias, Tamiasciurus, and Glaucomys spp. (Hugot, 1988), challenges Rodentoxyuris in the Sciuridae and separates the range of Rodentoxyuris into two disconnected areas. This could explain the appearance of a different species of Rodentoxyuris in the Western Palearctic. C ONCLUSION The classication of the Enterobiinae resulting from the cladistic analysis generally conrms the subgroups previously described in the subfamily, closely underlines the classication of the Primate order, and provides evidence supporting the Cameron (1929) hypothesis of close coevolution with cospeciation. The presence of several squirrel parasites within the Enterobiinae apparently results from two independent evolutionary events, each of which can be linked with ancient biogeographic circumstances. Thus, the existence of these parasites does

not challenge the general pattern of a parallel radiation of the living primates with their pinworm parasites. Given that the occurrence of the same pinworm species as a parasite for several congeneric host species is not the generalized pattern, Cameron’s hypothesis of a slower rhythm of speciation in the parasites is not validated. In addition, several occurrences are observed in which the speciations of the parasites parallel very closely the speciations of the hosts, such that several hypotheses of duplication are required in the different groups for reconstruction of evolutionary scenarios. This signies that in several cases the evolution of the parasites strictly underlines the history of the hosts and that several different lineages of the Enterobiinae have sometimes been in competition for the same host group. These observations refute Cameron’s second hypothesis. The Enterobiinae occur in most families and numerous genera of the order Primates. However, no pinworm parasites were discovered in the following host taxa: the family Tarsiidae; the lemuriform genera Allocebus, Avahi, Indri, Lichanotus, Lemur, Phaner, and Varecia and the lorisiform genera Arctocebus, Euoticus, Galagoides, Loris, Otolemur, and Perodicticus . In the Platyrrhini is found the most complete distribution; only Leontopithecus, Cebuella, and Cacajao lack a pinworm parasite. In the Catarrhini, pinworm parasites are lacking in the cercopithecid genera Allenopithecus, Cercocebus, Cercopithecus, Erythrocebus, Lophocebus, Mandrillus, Miopithecus , and Theropithecus and in Nasalis and Pygathrix within the Colobidae. Until now no specic parasites were described from family Hylobatidae, but human parasites were found in a Hylobates lar in the London zoo (Sandosham, 1950). The gaps in the distribution of the Enterobiinae throughout the Primate order probably result in part from undiscovered species; a careful examination of host specimens will certainly reveal new species. A CKNOWLEDGMENTS I thank Thierry Bourgoin, Pierre Deleporte, Vé ronique Barriel, and Roderick Page for their help and comments on early drafts of this manuscript and

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David Canatella and Richard Olmstead for constructive suggestions and kind assistance in editing. All of them have contributed to improve this work. This work was supported in part by NATO collaborative research grant no. CRG 920612 to S. L. Gardner, J. P. H., and S. Morand and by the Groupe de Travail Morphomé trie et Analyse de Forme du Musé m National d’Histoire Naturelle. MENRT-EA2586: “Systematique et Evolution” des T e´ trapudes, pub. no. 99-5.

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H U GO T, J. P. 1988. Les n e´ matodes Syphaciinae parasites de rongeurs et de lagomorphes. Taxonomie. Zoogé ographie. Evolution. M e´ m. Mus. Natl. Hist. Nat. Sect. A Zool. 141:1–153. H U GO T, J. P. 1993. Redescription of Enterobius anthropopitheci (Nematoda,Oxyurida), parasite of the chimpanzees. Syst. Parasitol. 26:201–207. H U GO T, J. P. 1995. Redescription of Xeroxyuris parallela (Linstow, 1908) n. gen., n. cb., parasite of Xerus inauris . Parasite 2:1–7. H U GO T, J. P., AN D C. F EL IU. 1990. Description de Syphabulea mascomai n. sp. Analyse du genre Syphabulea. Syst. Parasitol. 17:219–230. H U GO T, J. P., S. L. GA RD N ER, AN D S. MOR AN D. 1996. The Enterobiinae fam. nov. (Nematoda, Oxyurida), parasites of primates and rodents. Int. J. Parasitol. 26:147– 159. H U GO T, J. P., S. MOR AN D, A N D S. L. GAR DN E R. 1995. Morphology and morphometrics of three oxyurids parasitic in primates. Description of Lemuricola microcebi n. sp. Int. J. Parasitol. 25:1065–1075. H U GO T, J. P., S. MO RAN D, AN D R. GU ER RE RO. 1994. Trypanoxyuris croizati n. sp. and T. callicebi , two vicariant forms parasite of Callicebus spp. ( Primate, Cebidae). Syst. Parasitol. 27:35–43. H U GO T, J. P., A N D C. T OU RT E-S CH A FFER. 1985. Etude morphologique des deux oxyures parasites de l’Homme: Enterobius vermicularis et E. gregorii . Ann. Parasitol. Hum. Comp. 60:57–64. H U GO T, J. P., A N D C. VA UC H E R. 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. I N GL IS , W. G. 1961. The oxyurids parasites (Nematoda) of primates. Proc. Zool. Soc. Lond. 136:103–122. I N GL IS , W. G., AN D G. E. C O SGR OVE. 1965. The pinworms parasites (Nematoda: Oxyuridae) of the Hapalidae (Mammalia: Primates). Parasitology 55:731– 737. I N GL IS , W. G., A N D C. D IAZ -U N GRÍA . 1960. Nematodes parasitos de vertebrados venezolanis. I. Una revision del genero Trypanoxyuris (Ascaridata: Oxyuridae). Mem. Soc. Cienc. Nat. La Salle 19:176–212. I N GL IS , W. G., AN D F. L. D U N N. 1963. The occurrence of Lemuricola (Nematoda: Oxyurida) in Malaya: With the description of a new species. Z. Parasitenkd. 23:354–359. I N GL IS , W. G., AN D F. L. D UN N . 1964. Some oxyurids from Neotropical primates. Z. Parasitenkd. 24:83–87. J AB LO N SKI, 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. J OH N SO N-M U RRAY, J. L. 1977. Myology of the gliding membranes of some petauristine rodents (Genera: Glaucomys, Petaurista, Petinomys, and Pteromys). J. Mammal. 58:374–384. KE YME R, I. F. 1983. Diseases of squirrels in Britain. Mammal Rev. 13:155–158.

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TR AVASSO S, L. 1925. Fauna Brasiliense. Nematodes: Oxyuroidea-Oxyuridae. Revisao do genero Enterobius Leach, 1853. Mus. Nac. Rio J. 2:5–11. VEVE RS, C. M. 1923. Some new and little known helminths from British Guyana. J. Helminthol. 1:35– 45. ´ VUYL STEKE , C. 1964. Mission de Zoologie m e´ dicale au Maniema (Congo L e´ opoldville). (P. L. G. Benoˆõ t, 1959). 3. Vermes. Nematoda. Ann. Mus. R. Afr. Cent. Ser. Zool. 132:41–66. W AH ID, S. 1961. On two new species of the genus Enterobius Leach, 1853, from a Colobus monkey. J. Helminthol. 35:345. W IL SO N, D. E., A N D D. M. RE ED ER. 1993. Mammal species of the world. A taxonomic and geographic reference, 2nd edition. Smithsonian Institution Press, Washington, D.C. 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. YO DE R, A. D., M. C ART MILL, M. RUVO LO, K. SM IT H , AN D R. VIL GALY S. 1996. Ancient single origin for Malagasy primates. Proc. Natl. Acad. Sci. USA 93:5122–5126. Received 27 May 1998; accepted 17 September 1998 Associate Editor: R. Page

A PPENDIX 1. T AXA A NALYZED For preliminary studies and redescriptions, specimens have been borrowed from the following people and institutions: Prof. R. Guerrero, Prof. C. Feliu, Prof. R. Rausch, Prof. F. Puylaert, Prof. C. Vaucher, Prof. A. Verster, and Prof. W. Z. Yin; National Museum of Natural History, Washington D.C. (USNM); British Museum (Natural History) (BMNH); International Institute of Parasitology (CAB); Musé e Royal d’Afrique Centrale, Tervueren (MRAC); Muséum National d’Histoire naturelle, Paris (MNHN). Family Pharyngodonidae Travassos, 1919 Genus Ctenodactylina Bernard, 1969. — Ctenodactylina tunaetae Bernard, 1969. Host taxa: Ctenodactylus gundi (Rothmann) [Algeria]; Pectinator spekei Blyth [Ethiopia]. Source: Hugot (1983b). Material examined: MNHN 150KH, 161KH. Family Oxyuridae Cobbold, 1864 Subfamily Oxyurinae.—Genus Ingloxyuris (Chabaud, Petter, and Golvan, 1961. Ingloxyuris inglisi Chabaud, Petter and Golvan, 1961. Host taxon: Lepilemur rucaudatus Grandidier [Madagascar]. Source: Chabaud et al. (1961), Hugot (unpub.). Material examined: MNHN F 804, F 805, F 820, F 841. Subfamily Enterobiinae Hugot, Gardner, and Morand, 1996. —Genus Enterobius Leach, 1853, Subgenus Enterobius: E. anthropopitheci (Gedoelst, 1916). Host taxa: Pan troglodytes (Blumenbach) [Zaire, Senegal], P. paniscus Schwartz [Zaire]. Source: Gedoelst (1916), Sandosham (1950), Hugot (1993). Materialexamined: MRAC 10827–

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10915 (paratypes); MNHN 433KH, 851H, 432KH. E. bipapillatus (Gedoelst, 1916). Host taxon: Chlorocebus aethiops (L.) [Zaire, South Africa]. Source: Gedoelst (1916), Hugot (unpub.). Material examined: MNHN 109KB. E. buckleyi Sandosham, 1950. Host taxon: Pongo pygmaeus (L.) [Zoo]. Source: Sandosham (1950). E. brevicauda Sandosham, 1950. Host taxa: Papio cynocephalus (L.) [Kenya, Rhodesia, Zaire]; Papio ursinus [South Africa]. Source: Sandosham (1950), Hugot (unpub.). Material examined: MRAC 3675-3714; MNHN 373KH. E. gregorii Hugot, 1983a. Host taxon: Homo sapiens L. Source: Hugot (1983a), Hugot and Tourte-Schaeffer (1985). Material examined: MNHN 310KH (type and paratypes). E. lerouxi Sandosham, 1950. Host taxon: Gorilla gorilla (Savage & Wyman) [Zoo]. Source: Sandosham (1950). E. macaci (Yin, 1973). Host taxa: Macaca mulatta (Zimmermann) [Yunnan, India], M. cyclopis (Swinhoe)[Taiwan]. Source: Yin (1973), Hugot (unpub.). Material examined: MNHN 80KH (paratypes), 90KJ, 91KJ. E. vermicularis (L., 1758). Host taxon: Homo sapiens L. Source: Hugot and Tourte-Schaeffer (1985). Material examined: MNHN 115KH, 172KH, 310KH, 311KH, 320KH, 335KH/338KH. Subgenus Colobenterobius Quentin, Betterton, and Krishnasamy, 1979: C. colobis Vuylstéke, 1964. Host taxon: Procolobus badius (Kerr) [Zaire]. Source: Vuylstéke (1964), Hugot (1987a). Material examined: MRAC 32410, 32381 (paratypes). C. entellus Hugot, 1987b. Host taxon: Semnopithecus entellus (Dufresne) [Zoo]. Material examined: BMNH 1968: 203 (types and paratypes). Comments: no mature female was observed in this species, and characters concerning eggs were coded as missing. C. guerezae Hugot, 1987a. Host taxon: Colobus guereza Ruppel ¨ [Ethiopia, Congo]. Material examined: MNHN 499D, 768H (types and paratypes). C. inglisi Wahid, 1961. Host taxon: Colobus sp. [West Africa]. Source: Wahid (1961), Hugot (unpub.). Material examined: CAB: 504, 505 (type and paratype). C. longispiculum Quentin, Betterton, and Krishnasamy, 1979. Host taxon: Trachypithecus obscurus (Reid) [Malaysia]. Source: Quentinet al. (1979). Materialexamined: MNHN 98SF. C. paraguerezae Hugot, 1987a. Host taxon: Colobus ¨ [Ethiopia]. Material examined: MNHN guereza Ruppel 333KH, 768H (types and paratypes). C. pesteri Wahid, 1961. Host taxon: Colobus sp. [West Africa]. Source: Wahid (1961), Hugot (unpub.). Material examined: CAB 504, 505 (type and paratype). C. pitheci Cameron, 1929. Host taxon: Trachypithecus pileatus (Blyth) [Assam]. Source: Cameron (1929), Hugot (1987b). Material examined: CAB 161/A (paratypes). Comments: male unknown. C. presbytis Yin, 1973. Host taxon: Trachypithecus phayrei (Blyth) [Yunnan]. Source: Yin (1973), Quentin et al. (1979), Hugot (1987b). Material examined: MNHN 82KH (paratypes), 99SF. C. zakiri Siddiqi and Mirza, 1954. Host taxon: Semnopithecus entellus (Dufresne) [Zoo and Allahabad Wood-

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land]. Source: Siddiqi and Mirza (1954), Hugot (1987b). Material examined: BMNH 1968: 203, BMNH 1964: 91/104. Genus Lemuricola Chabaud and Petter, 1959, Subgenus Lemuricola: L. contagiosus Chabaud and Petter, 1959. Host taxon: Cheirogaleus major E. Geoffroy [Madagascar]. Source: Chabaud and Petter (1959), Hugot et al. (1995). Material examined: MNHN 395KB (lectotype and paratypes). L. microcebi Hugot, Morand, and Gardner, 1995. Host taxon: Microcebus murinus (J. F. Miller) [Madagascar]. Source: Chabaud and Petter (1959), Hugot et al. (1995). Material examined: MNHN Q10, Q298 (type and paratypes). Subgenus Biguetius Chabaud, Petter, and Golvan, 1961: B. trichuroides Chabaud, Petter, and Golvan, 1961. Host taxon: Propithecus verreauxi (Rothschild) [Madagascar]. Source: Chabaud et al. (1961). Subgenus Madoxyuris Chabaud, Brygoo, and Petter, 1965: M. baltazardi Chabaud, Brygoo, and Petter, 1965. Host taxon: Eulemur fulvus (E. Geoffroy) [Madagascar]. Source: Chabaud et al. (1965), Hugot (unpub.). Material examined: MNHN 849F (paratypes). M. bauchoti Chabaud, Brygoo, and Petter, 1965. Host taxon: Hapalemur simus Gray [Madagascar]. Source: Chabaud et al. (1965), Hugot (unpub.). Material examined: MNHN 634F (paratypes). M. daubentoniae Petter, Chabaud, Delavenay, and Brygoo, 1972. Host taxon: Daubentonia madagascariensis (Gmelin) [Madagascar]. Source: Petter et al. (1972), Hugot (unpub.). Material examined: MNHN 179BA (paratypes), 346K. M. lemuris (Baer, 1935). Host taxon: Eulemur macaco (L.) [Madagascar]. Source: Baer (1935), Hugot (unpub.). Material examined: MNHN 264E. M. vauceli Chabaud, Brygoo, and Petter, 1965. Host taxon: Eulemur fulvus (E. Geoffroy). Source: Chabaud et al. (1965), Hugot (unpub.). Material examined: MNHN 849F (paratypes), 457F, 836F. Subgenus Protenterobius Inglis, 1961: P. nycticebi (Baylis, 1928). Host taxon: Nycticebus coucang (Boddaert) [Malaysia, Borneo]. Source: Baylis (1928), Inglis and Dunn (1963), Hugot (unpub.). Material examined: MNHN 92PX, 100SF. Genus Trypanoxyuris Vevers, 1923, Subgenus Trypanoxyuris: T. callicebi Hugot and Vaucher, 1985. Host taxon: Callicebus moloch (Hoffmannsegg) [Paraguay]. Material examined: MNHN 380KH (type and paratypes). Comments: male unknown. T. clementinae Hugot, 1985. Host taxa: Cebus apella (L.), C. albifrons (Humboldt) [Brazil, Colombia]. Material examined: USM 65830 (type and paratypes), 65800. Comments: male unknown. T. croizati Hugot, Morand, and Guerrero, 1994. Host taxon: Callicebus torquatus (Hoffmannsegg) [Venezuela]. Material examined: MNHN 380KH. T. microon (Linstow, 1907). Host taxon: Aotus trivirgatus (Humboldt) [Colombia]. Source: Travassos (1925), Sandosham (1950), Inglis and Diaz-Ungr´õ a (1960), Hugot (1985). Material examined: MNHN 773CA.

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T. minutus (Schneider, 1866). Host taxon: Alouatta seniculus (L.) [French Guiana] Source: Hugot (1985). Material examined: MNHN 1098CA. T. satanas Hugot, 1985. Host taxa: Chiropotes satanas (Hoffmannsegg) [Venezuela], C. chiropotes Humboldt [Venezuela]. Material examined: BMNH 1960: 1708/1727 (type and paratypes), 1960: 1428/1487, 1960: 1838/1857. T. sceleratus (Travassos, 1925). Host taxa: Saimiri orstedii (Reinhardt) [Guyana], S. sciureus L. [French Guiana]. Source: Hugot (1985). Material examined: MNHN 345KH, 375KH, 1063CA, 650NE. T. trypanuris Vevers, 1923. Host taxa: Pithecia pithecia (L.) [French Guiana], P. monachus (E. Geoffroy) [Guyana]. Source: Hugot (1985). Material examined: MNHN 227KH, 228KH, 229KH. Subgenus Hapaloxyuris Inglis and Cosgrove, 1965: H. callitrichis (Solomon, 1933). Host taxon: Callithrix jacchus (L.) [Brazil]. Source: Hugot (1984b). Material examined: USM 69/306; MNHN 157U. H. goeldii Inglis and Cosgrove, 1965. Host taxon: Callimico goeldii (Thomas) [locality unknown]. Source: Inglis and Cosgrove (1965), Hugot (1984b). Material examined: BMNH 1965: 331/336. H. oedipi Inglis and Cosgrove, 1965. Host taxa: Saguinus oedipus (L.) [Brazil]. Source: Inglis and Cosgrove (1965), Hugot (1984b). Material examined: USM 69/316. H. tamarini (Inglis and Dunn, 1964). Host taxa: Saguinus nigricollis (Spix) [Peru]. Source: Inglis and Dunn (1964), Hugot (1984b). Material examined: BMNH 1963: 644/658, 661/664. Subgenus Paraoxyuronema Artigas, 1936: P. atelis (Cameron, 1929). Host taxon: Ateles paniscus (L.) [French Guiana]. Source: Cameron (1929), Dollfus and Chabaud (1955), Inglis and Diaz-Ungr´õ a (1960), Hugot (1985). Material examined: MNHN 87KB. P. brachytelesi Artigas, 1936. Host taxon: Brachyteles arachnoides (E. Geoffroy) [Brazil]. Source: Artigas (1936). Comments: male unknown. P. duplicidens Buckley, 1931. Host taxon: Lagothrix lagotricha (Humbolt) [Zoo]. Source: Buckley (1931). P. lagothricis Buckley, 1931. Host taxon: Lagothrix lagotricha (Humbolt) [Zoo]. Source: Buckley (1931), Hugot (1985). Material examined: CAB 162b (type). MNHN 313KH. Subgenus Rodentoxyuris (Quentin and Tenora, 1975): R. bicristata Hugot, 1984. Host taxa: Sciurus niger L. [Michigan]; Sciurus carolinensis Gmelin [USA]; Sciurus aberti Woodhouse [New Mexico]; Glaucomys volans (L.) [Michigan, Connecticut]; Glaucomys sabrinus (Shaw) [Oregon]. Material examined: MNHN 47HB (type and paratypes). R. sciuri (Cameron, 1932). Host taxa: Sciurus carolinensis Gmelin [UK], Sciurus vulgaris L. [UK, France, Spain, Switzerland, Czechoslovakia, Ukraine]. Source: Hugot (1984a). Material examined: MNHN 357KH, 508BA, 307KH, 569SB. Genus Xeroxyuris Hugot, 1995: Xeroxyuris parallela (Linstow, 1908). Host taxon: Xerus inauris (Zimmermann) [South Africa]. Source: Le Roux (1930), Inglis (1961), Hugot (1995). Material examined: MNHN 89KB, 90KB, 123KB, 21KH.

545

A PPENDIX 2. L IST OF C HARACTERS 1. Impaired uterine tube divided into 2 parts by a cellular wall forming a diaphragm .—0 = absent, 1 = present. 2. Spermatheca on oviducts.—0 = absent, 1 = present. 3. Genital tract.—0 = prodelphic, 1 = amphidelphic. 4. If character 1 = 1 .—0 = (a) diaphragm dividing impaired uterine tube into two equal parts, (b) muscular vagina directed posteriorly, (c) cuticular vagina invisible; 1 = (a, c) same as 0, (b) muscular vagina directed anteriorly and impaired uterine tube directed posteriorly, forming a handle shaped curve; 2 = (a, b) same as 1, (c) short valvular cuticular vagina visible; 3 = (a,b) same as 2, (c) long valvular cuticular vagina visible; 4 = (a) diaphragm dividing impaired uterine tube into two unequal parts, (b) muscular vagina directed posteriorly, (c) cuticular vagina invisible. 5. Area rugosa of males.—0 = generalized type, represented by a split in the ventral region of each annulus posteriorto excretory pore; 1 = Inglisoxyuris type; 2 = (a) cuticle inated into a large ventral crest between excretory pore and cloacal aperture, (b) crest V-shaped on a cross section; 3 = (a) same as 2, (b) crest U-shaped on a cross-section; 4 = (a) cuticle inated into a large ventral crest limited to the posterior third of the ventral cuticle,(b) V-shaped crest on a cross-section; 5 = ventral striation widened forming thick prominences limited to posterior third of the ventral cuticle. 6. Cloacal opening in males.—0 = I-shaped, 1 = Y-shaped, 2 = with a hood-shaped ap extremity from which spicular pouch is protruding, 3 = with a genital cone including a V-shaped cuticularized piece. 7. Disposition of male genital papillae .—0 = Pharyngodonidae type, 1 = Inglisoxyuris type, 2 = Enterobiinae type with (a) four pairs of caudal papillae, (b) 1st and 4th pairs pedunculated and supporting the bursa, (c) 2nd and 3rd pairs sessile anking the opening of the cloaca, and (d) tubes of phasmids beginning at base of peduncles of 4th pair of caudal papillae. 8. If character 7 = 2.—0 = (a) peduncles of 1st pair of caudal papillae visible, (b) no differentiation of the cuticlearound the 4th pair of genital papillae;1 = (a) same as 0, (b) cuticle inated into a ventral tumescent bubble supported by peduncles of 4th pair of genital papillae; 2 = (a) peduncles of 1st pair of caudal papillae invisible, (b) phasmid tubes oriented posteriorly; 3 = (a) same as 2, (b) phasmid tubes oriented anteriorly. 9. Ring-shaped cuticular thickening around genital papillae .—0 = absent, 1 = around 2nd pair of genital papillae, 2 = around 2nd and 3rd pairs, 3 = around 2nd and 3rd pairs, linked with a square cuticular blade posterior to cloacal aperture, 4 = around 2nd and 3rd pairs, extending laterally ornamenting lateral part of body, 5 = around 2nd and 3rd pairs, forming two lateral cones including the phasmidian tubes, 6 = around 2nd and 3rd pairs, forming buttery wing-shaped lateral cuticularthickenings. 10. If character 9 = 3 .—0 = simple square cuticularblade, 1 = square cuticular blade with leaf-shaped exten-

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11. 12. 13. 14. 15.

16. 17. 18. 19. 20.

21.

22.

23.

24. 25. 26. 27. 28.

SYSTEMATIC BIOLOGY

sion between papillae of 3rd pair, 2 = square cuticular blade with lozenge-shaped extension between papillae of 3rd pair. Spicule manubrium.—0 = thin, 1 = thick spherical and smooth, 2 = thick spherical and rough, 3 = thick oval, 4 = thick rectangular, 5 = thick elongated. Spicule corpus.—0 = feebly curved ventrally, 1 = rectilinear, 2 = double bowed, 3 = long and exible. If character 12 = 3 .—0 = spicule length < 250 m m, 1 = spicule length $ 250 m m. Spicule point.—0 = sharp, 1 = rounded, 2 = hookshaped, 3 = thin, 4 = angled ventrally. Tip of tail.—0 = absent, 1 = atrophied, 2 = present at $ 25% and < 70% of total tail length, 3 = present at < 25% of total tail length, 4 = present at # 70% of total tail length. Amphids pedunculated.—0 = absent, 1 = present. Disposition of cephalic plate.—0 = circular, 1 = hexagonal, 2 = rectangular, 3 = square. If character 17 = 1.—0 = hexagonal regular, 1 = hexagonal irregular, 2 = hexagonal surrounded by a cuticular slot. Cephalic vesicle.—0 = generalized type, 1 = thick making longitudinal folds, 2 = rst ring enlarged skullcap-shaped, 3 = striation accentuated. Buccal aperture.—0 = surrounded by 6 lips; 1 = surrounded by 3 lips, buccal opening large; 2 = surrounded by 3 lips, buccal opening narrow; 3 = surrounded by 2 lips. Lip edges.—0 = rounded, lips extended, 1 = rounded, lips reduced, 2 = horseshoe-shaped, 3 = thickened, 4 = lobulated, 5 = edge of dorsal lobe horizontal, 6 = dorsal lip stuck with dorsal teeth. If character 21 = 4.—0 = symmetrical weakly accentuated lobes, 1 = symmetrical strongly indentated lobes, 3 = asymmetrical lobes, microon type, 4 = asymmetrical lobes, minutus type. Apex of teeth.—0 = rounded simple,1 = rounded with 3 minute denticles, 2 = at, 3 = with composite superstructures, 4 = dorsal teeth reduced, 5 = dorsal teeth atrophied, 6 = with a strong and sharp denticle Madoxyuris type, 7 = with a strong and thick denticle Enterobius type. If character 23 = 2 .—0 = at pentagonal, 1 = at triangular. If character 23 = 3 .—0 = mushroom-shaped superstructures, 1 = superstructures composed of 2 parallel cuticular blades. If character 25 = 0 .—0 = simple mushroom-shaped superstructures, 1 = mushroom-shaped superstructures with a denticle. If character 25 = 1 .—0 = narrow cuticular blades, 1 = large cuticular blades. Esophageal bulb.—0 = smashing apparatus absent; 1 = smashing apparatus present, ratio total esophagus length/esophageal bulb length > 3 .15 in both

29. 30.

31. 32. 33. 34. 35. 36.

37. 38. 39. 40. 41. 42. 43.

44.

45.

VOL. 48

sexes; 2 = smashing apparatus present, ratio total esophagus length/esophageal bulb length # 3. 15 in both sexes. Lateral alae of females.—0 = absent, 1 = present beginning at level of bulb or posteriorly, 2 = present beginning anteriorly to bulb. If character 29 = 1 .—0 = 2 crests triangular on a crosssection; 1 = 2 crests partially fused, Y -shaped on a cross-section; 2 = 2 crests partially fused, U -shaped on a cross-section. If character 29 = 2 .—0 = cervical part nondifferentiated, 1 = cervical part differentiated. If character 31 = 0.—0 = lateral alae triangular on a cross-section, 1 = lateral alae rounded on a crosssection. If character 32 = 0 .—0 = 2 simple crests, 1 = 2 distant crests, 2 = 2 reduced crests. If character 33 = 2 .—0 = crests distinct, 1 = crests partially fused. If character 32 = 1 .—0 = 1 crest, 1 = 2 crests distinct, 2 = 2 crests partially fused. If character 31 = 1.—0 = one crest triangular on a cross-section, 1 = 2 crests triangular on a crosssection, 2 = 1 crest rounded on a cross-section, 3 = 1 crest rounded on a cross-section with a lesser crest on each side, 4 = 2 crests partially fused, Y -shaped on a cross-section. Egg.—0 = with embryo, 1 = without embryo. If character 37 = 1 .—0 = eggs with sharp ends, 1 = eggs with rounded ends. If character 38 = 1 .—0 = thin-shelled eggs, 1 = thickshelled eggs. If character 39 = 0.—0 = eggs symmetrical, 1 = eggs asymmetrical. If character 39 = 1.—0 = eggs symmetrical, 1 = eggs asymmetrical convex on each edge, 2 = eggs asymmetrical, 1 edge attened. If character 40 = 1.—0 = egg length $ 80 m m, 1 = egg length < 80 m m and > 60 m m, 2 = egg length # 60 m m. If character 41 = 0 .—0 = egg length $ 70 m m and ratio body length/egg length < 100, 1 = egg length < 70 m m and $ 50 m m and ratio body length/egg length < 100, 2 = egg length < 70 m m and $ 45 m m and ratio body length/egg length > 100, 3 = egg length < 45 m m and ratio body length/egg length > 100. If character 41 = 1 .—0 = body length/egg length > 100 and # 115, 1 = ratio body length/egg length > 115 and # 175, 2 = ratio body length/egg length > 175. If character 41 = 2 .—0 = egg length = 45 m m and ratio body length/egg length < 100, 1 = egg length $ 45 m m and ratio body length/egg length > 100, 2 = egg length < 45 m m and ratio body length/egg length > 100.