1
Shape patterns of genital papillae in Enterobiinae
Hugot & Baylac
SHAPE PATTERNS OF GENITAL PAPILLAE IN OXYURIDS PARASITE OF PRIMATES: A LANDMARK ANALYSIS. by Jean-Pierre HUGOT1,2 & Michel BAYLAC 2 1 UR 178, Institut de Recherche pour le Développement, RCEVD-CVD , Mahidol University, 25/25 Phuttamonthon 4, Nakhon Pathom 73170, Thailand.
[email protected] 2 Muséum National d’Histoire Naturelle, Département Systématique et Évolution, UMR 5202 CNRS-MNHN, Origine, Structure et Évolution de la Biodiversité, Plateforme Morphométrie, F-75 231, Paris cedex 05, France.
ABSTRACT The Enterobiinae includes 47 species of pinworms parasite of primates. A previous cladistic analysis of this subfamily supported its monophyly and its subdivision into three genera. Based on morphological characters, this cladistic analysis excluded characters describing the shape of the genital papillae of male pinworms, because the corresponding patterns could not be described using discrete characters. In this study, the shape of the genital papillae of the males of 35 within the 47 species is analyzed using geometric morphometric approaches. The aims of this study are to investigate: (i) the relationships between the phylogeny and the shape patterns of the caudal bursa, (ii) the shape differences between and within monophyletic groups, and, (iii) the functional implications of the shape patterns observed within the subfamily. Results demonstrate that different patterns of evolution of the caudal bursa, each one characterized by a particular spatial distribution of the phasmids and genital papillae may be recognized, which are consistent with the classification of the Enterobiinae into three groups. On the whole, these patterns may be related to particular mating behavior of the pinworms. When lacks of congruence are observed between shape patterns distribution and species distribution into monophyletic groups, they are found to correspond to homoplasic events; this suggesting that convergent selective pressures are involved in the evolution of the shape of the genital papillae. This analysis also confirms that morphometric shape patterns cannot be interpreted unequivocally without the support of a preexisting phylogenetic framework. Jean-Pierre Hugot, UR 034, Institut de Recherche pour le Développement, RCEVD-CVD, Mahidol University, 25/25 Phuttamonthon 4, Nakhon Pathom 73170, Thailand. E-mail:
[email protected] INTRODUCTION Members of the parasite family Oxyuridae (Cobbold) can be found in most families and genera of Primates. Recent redescriptions revealed that most of the forty-seven pinworm species described from primate hosts share derived characters. This allowed to group them in a new subfamily, the Enterobiinae Hugot et al., 1996, which also includes 3 species parasitic on squirrels. A subsequent cladistic analysis (Hugot, 1999) confirmed the monophily of the subfamily. It confirmed also the monophily of the three main genera previously defined within the primate parasites and showed that each genus was associated with one of the suborders defined within the hosts: Lemuricola with the Strepsirhini, Trypanoxyuris with the Platyrrhini, and Enterobius with the Catarrhini. Between and within these groups, the classification of the Enterobiinae also closely under-
lines the classification of Primates. The squirrel parasites are classified into 2 distantly related genera: Xeroxyuris and Rodentoxyuris. This parasitism was interpreted as the result of independent horizontal transmissions from different groups of Primates to squirrels living in sympatry (Hugot, 1999). The Enterobiinae share a particular pattern of caudal bursa. The genital tract and the gut of the males open outside at the cloaca level, close to the caudal extremity of the body. This aperture is surrounded by four pairs of nervous papillae and by the openings of the two secretory phasmids, symmetrically arranged. The cloacal aperture, nervous endings and phasmid openings may be surrounded by a cuticular ornamentation. A more or less developed tip of tail may be present or absent. Altogether these organs and appendices make the caudal bursa. Fig. 1 gives an
2
Shape patterns of genital papillae in Enterobiinae
example of the general arrangement found in the Enterobiinae. Different examples of caudal bursa
3
1
2
15
Hugot & Baylac
found within the subfamily are represented on Fig. 2.
A 4
2
4
14
14 3 5
13
15
1
13
5 6
12
7
11 8
9
10
6
B
12
10 89 7
11
Fig. 1. A, position of the fifteen landmarks on the caudal bursa of Colobenterobius colobis Vuylstéke, 1964. B, same as depicted by links drawn between landmarks. The caudal bursa is represented in a ventral view and the top and bottom of the figures are corresponding to the anterior (=cephalic) or posterior (=caudal) ends, respectively. The cloacal aperture is a vertical and medial slit with posterior and anterior corners (landmarks 1 and 2). The four pairs of papillae may be distinguished as follows: one anterior pair (landmarks 4 and 14); the first one juxta-cloacal pair (landmarks 3 and 15); the second juxta-cloacal pair (landmarks 5 and 13; a posterior pair (landmarks 7 and 11). The anterior and posterior pairs are supported by well-developed peduncles heading laterally. The first pair of juxta-cloacal papillae never has peduncles; the second pair of juxtacloaclal papillae may have short peduncles, or no peduncle. The juxta-cloacal papillae are more or less close together and are surrounding the posterior corner of the cloacal slit. In the caudal region also are found two glandular apparatus: the phasmids; each phasmid has an excretory duct opening laterally to the caudal bursa (landmarks 6 and 12). The general pattern can be modified by the presence or absence of a caudal appendix, the tip of tail, which extremity corresponds to landmark 9; the presence of more or less developed cuticular thickenings. This ornamentation is present in all the species of the subfamily and different patterns may be distinguished (see Fig. 2).
The cladistic analysis of the Enterobiinae was based on discrete morphological characters, including most of the organs and cuticular particularities of these nematodes, but excluding the shape of the genital papillae of the male pinworms. This exclusion was motivated by the fact that an objective description of their disposition relative to each other and to the cloacal slit was impossible using simple discrete characters. Geometric morphometrics (Bookstein, 1991; Rohlf and Marcus, 1993; Adams et al., 2004) allows a rigorous and powerful statistical treatment of the morphological variation within and among samples of organisms. In the following, we analyze the patterns of the caudal bursa of males Enterobiinae using the thin plate spline approaches of Bookstein (1991). Applications of morphometrics whether geometric or multivariate in phylogeny has long been and still remain controversial (Felsenstein, 1988; Zelditch et al., 1995; Bookstein, 1994, 2002; Naylor, 1996; Monteiro, 2000, Rohlf, 2001, 2002; MacLeod, 2002). In this paper we do not use morphometric data to infer phylogenetic
relationships within a clade, a procedure that is at the root of most controversies (see McLeod, 2002 for a recent synthesis). Instead, we map shape changes of the caudal bursa onto a phylogeny obtained using different morphological characters, and tentatively try to relate these changes to functions. Such a direct procedure has been used for a long time to interpret morphological shape changes within a phylogenetic framework (see by instance among others Rohlf et al., 1996; Klingenberg and Ekau, 1996; Pretorius and Scholtz, 2001). The aims of this study are therefore to investigate: - (i) the relationships between the phylogeny and the shape patterns of the caudal bursa, - (ii) the shape differences between and within monophyletic groups, and, - (iii) the functional implications of the shape patterns observed within the subfamily.
3
Shape patterns of genital papillae in Enterobiinae
Hugot & Baylac
TRYSCEL
XERPARA HAPOEDI
TRYSATA
COLGUER RODBICR
ENTANTH
COLCOLO
LEMMIC ENTEVERM
PRONYCT
ENTEGREG
MADLEM
Fig. 2. Illustrations of the caudal bursa in ventral view, depicting landmark locations and links. Different patterns of ornamentation: cuticular rings around the first pair of juxtacloacal papillae (TRYSATA, TRYSCEL, HAPOEDI and RODBICR); cuticular rings surrounding the four juxtacloacal papillae (COLGUER, XERPARA); cuticular rings surrounding the four juxtacloacal papillae and linked together by the thickening of the posterior corner of the cloacal slit (all the other species represented). For the analysis landmarks 10 to 15 of the left half of the body have been symetrized onto homologous landmarks of the right half and landmark 9 was removed from the data set (see explanation in the text). Correspondence of the abbreviations with the scientific names of the species is given in Appendix 1.
4
Shape patterns of genital papillae in Enterobiinae
MATERIALS AND METHODS Sampling Male pinworms are generally far less numerous than their females in the collections and many species within the Oxyurida have been described from one or two male specimens. Furthermore, preparations of the genital papillae imply to cut the posterior ends, an operation that cannot be applied to types or to already mounted specimens. Thus, most available specimens are not suitable for digitization. As a consequence, we first analyzed qualitatively as many specimens as possible to get an estimation of the within-species variability, and selected representative specimens that were suitable for digitization. A single specimen represented most species. In few species, Lemuricola daubentoniae, L. contagiosus, Colobenterobius presbytis and Rodentoxyuris sciuri, a couple of individuals could be included into the data set. Forty-seven species are known in the Enterobiinae: only thirty-five species could be selected for this study. The twelve remaining species were rejected either because the male was unknown, because the description of the caudal bursa was insufficient, or because no suitable specimens were available. Thirty-two of the species studied are Primate parasites, each one being specific for one host species. The three remaining species are squirrel parasites. Most of the species were redescribed recently (see Hugot 1983, 1984a, b, 1985, 1987a, b, 1993 a, 1995; Hugot et al. 1985a, b, 1994, 1995). Ingloxyuris inglisi, a pinworm parasite for Lepilemur ruficaudatus, but not belonging to the Enterobiinae, was included as outgroup in the cladistic analysis of the subfamily (Hugot 1999). We also added this species to the present data set. Appendix 1 lists the taxa included in this study and for each one gives the abbreviation used on the Figs: each species is represented using the first three letters of the name of the genera and the first four letters of the species name.
Data collection The two-dimensional Cartesian coordinates of fifteen landmarks were recorded with a digitizing tablet using the DS-DIGIT program developed by Slice (1991). Fig. 1 shows the position of the landmarks (taken at the center of the papillae otherwise stated): (1) is the posterior corner of the cloacal slit; (2) is the anterior corner of the cloacal slit; (3) and (15) are the first juxta-cloacal papillae; (4) and (14) are the pre-cloacal papillae; (5) and (13) are the second juxta-cloacal papillae; (6) and (12) are the opening of the phasmids; (7) and (11) are the postcloacal papillae; (8) and (10) are the connections of the caudal appendix with the peduncles of the post-
Hugot & Baylac
cloacal papillae; (9) is the tip of the caudal appendix. The distance between Landmarks 8 and 9, or 10 and 9, corresponds to the length of the tip of the tail. However, this length is very different following the species: it can be absent, reduced or five times longer than the other part of the tail (Fig. 2). A preliminary study using the 15 landmarks revealed that landmark 9 attracted an excessive part of the variance that contributed to hide the between-species variation at other locations. Therefore, landmark 9 was removed from the data set. Landmarks 11, 12, 13, 14 and 15 were symetrized, since patterns of asymmetry appeared to result mostly from sampling. In the final data set, only landmarks 1, 2, 3, 4, 5, 6, 7 and 8 were used where 3, 4, 5, 6, 7 and 8 are respectively the means of the couples 3-15, 414, 5-13, 6-12, 7-11 and 8-10, first digitized.
Morphometric analyses Raw coordinates were superimposed using a Procrustes generalized least-squares (GLS) superimposition algorithm (Rohlf & Slice 1990; Goodall 1991; Goodall 1995). The superimposed coordinates were subjected to a thin-plate spline-based relative warps analysis (Bookstein 1991; Rohlf 1992). Thin plate spline parameters allow the reconstruction of shapes, leading to a direct visualization of the shape changes. The thin plate spline parameters are applied to a squared grid providing a direct and quantitative implementation of the D'Arcy-Thompson transformation grids (Bookstein, 1991). Since this study was mainly exploratory, we followed Rohlf's suggestion (Rohlf, 1992) to give the same weight to all partial warps, and set the alpha parameter to 0. In that case, the relative warp analysis corresponds to a PCA of the Procrustes residuals (Rohlf, 1992), and the thin plate spline may be seen as a simple visual tool. Procrustes superimposition, thin plate splines parameters, centroid sizes and graphical outputs were calculated and produced using the TpsRelw (Rohlf, 2004a) and TpsRegr (Rohlf, 2004b) softwares. Extra runs limited to one of the generic groups (Enterobius, Trypanoxyuris or Lemuricola) and not presented here, were performed in order to verify the robustness of our interpretation of the shape patterns. Since the corresponding results agreed perfectly with the overall analysis, they won't be further discussed. The within-species variability could be estimated only for the 4 species represented by two specimens. In all cases the within-species variability appeared very low; Additional relative warps analyses using only one specimen per species (not shown) provided axes that were almost identical to that of the main analysis. Since our analyses do not take into account the within-species variability (that otherwise appeared qualitatively and
5
Shape patterns of genital papillae in Enterobiinae
quantitatively very low, when comparison were possible) , the relative warp analysis that will be discussed roughly corresponds to an analysis of the between-species variability. The reference cladogram used in the interpretations of the shape transformations corresponds to the strict consensus of the 3 most parsimonious trees resulting from a morphologically based cladistic analysis of the Enterobiinae (Hugot, 1999).
RESULTS OF RELATIVE WARPS ANALYSIS Congruence between taxonomic groupings and shape transformations The first relative warp takes into account 38,86% of the observed variance among the 8 landmarks and the second relative warp 19,11%: together they represent 57,97% of the total variance. The third and fourth relative warps represent 14,01% and 11,74% of the total variance, respectively. Since the third or the fourth relative warps did not provide additional insights into the group differences, we will only discuss the projections of the 35 specimens on the first two relative warps. Monophyletic groups of species at the genus and subgenus levels deduced from the cladistic analysis were highlighted onto the projections using convex hulls (Fig. 3). This allowed to estimate the relative shape similitude congruence of the phylogenetic groupings as well as the patterns and levels of shape differences between groups. From the top to the bottom of the graph, the parasites classified into genus Lemuricola are arranged into: a group including the species classified in subgenus Madoxyuris; a group including the members of subgenus Lemuricola and Madoxyuris daubentoniae; approximately halfway between these two groups is the single species of subgenus Protenterobius. The members of genus Enterobius are arranged following two groups: the first one includes all the species classified in the subgenus Colobenterobius, (minus Colobenterobius guerezae), the second one all the species classified in subgenus Enterobius, plus C. guerezae. The members of genus Trypanoxyuris also are distributed into two subgroups: one is corresponding with subgenus Hapaloxyuris, the other one with subgenus Trypanoxyuris. The parasites of squirrels (Rodentoxyuris and Xeroxyuris) are grouped together. Finally Ingloxyuris inglisi is isolated at the bottom right part of the figure. When two samples of the same species are represented into the data set (colpres1 & 2, lemcont1 & 2, maddaub1 &2, rodsciu1 & 2) the corresponding projections on the graphic are sufficiently close together to be considered to belong to the same group. Within each of the
Hugot & Baylac
three genera, the most distinct subgroups are those included in the genus Lemuricola. Within the genus Enterobius the two subgroups are separated but are very close together on the graphic plan. The three subgroups of Trypanoxyuris are close together and incompletely separated; in addition, they also merge with Xeroxyuris and partly with the subgenus Enterobius. When considering the distribution of the groups and subgroups on the graphic it appears that: (i) following the diagonal extending from the bottom left to the top right, roughly separates the three main genera classically distinguished in the subfamily; (ii) within each of these groups the corresponding subgroups are separated when following directions which roughly parallel the opposite diagonal. Fig. 4 illustrates the projections onto the first two relative warps together with the transformation grids at each axis and main diagonals extremities. Following the first diagonal the differences mostly involve the landmarks 3 and 5, i.e. the juxta-cloacal nervous papillae. From the bottom to the top of the diagonal they get closer. These two points following two orthogonal directions, landmark 3 moving backward while landmark 5 moves toward the sagittal axis. On the whole, it looks like if the juxta-cloacal papillae progressively were gliding under the posterior lip of the cloaca. The consequence is also a sharpening of the angles 1,2,3 and 3,4,5. Along the other diagonal the apparent motion of the landmarks mainly deals with the landmark 6, the orifice of the phasmid, but also with the landmark 5 and to a lesser extent with landmark 3. From the bottom to the top of the diagonal landmark 6 appears shifted anteriorly and parallely to the sagittal plan, while landmarks 5 and 3 appear to move the opposite way. As a whole, it looks like if the orifice of the phasmid was progressively moving from a posterior to an anterior position relatively to the posterior lip of the cloaca. This relative motion of landmarks 6, 5 and 3 also results in the lowering of the 5-6-7 angle and in the relative shortening of the posterior part of the region represented by landmarks 5, 6, 7 and 8.
Mapping the shape changes onto the cladogram of the Enterobiinae On Fig. 5 the shapes of each of the 35 different species analyzed are depicted on the tips of the consensus cladogram of this group (Hugot, 1999), together with the shape of Ingloxyuris inglisi, which was included as an outgroup in the cladistic analysis, and with the mean consensus. Fig. 5 allows to corroborate most of the interpretations that were drawn from the relative warp analysis (Figs. 3-4):
6
Shape patterns of genital papillae in Enterobiinae
- (i) each of the main three genera is principally characterized by the position of the juxta-cloacal pa-
Hugot & Baylac
pillae (landmarks 3 and 5) and the opening of the angles formed by landmarks 1,2,3 and 3,4,5;
0.050 MADVAUC
MADBALT MADBAUC
0.033
MADLEM
COLLONG
MADNANA
FACTOR 1
0.016
PROTNYCT COLPRES1 COLENT
COLPRES2
COLPARA COLZAKI
COLCOLO
LEMCONT1 LEMCONT2
MADDAUB2 MADDAUB1
HAPOEDI
ENTBIPA -0.001
ENTANTH
LEMMIC
HAPGOEL
ENTEMACA
TRYSATA
ENTEGREG ENTBREV
HAPTAMA
COLGUER
ENTEVERM TRYCROI
TRYATEL -0.018 TRYMICR
TRYTRYP RODBICR
RODSCIU2
XERPARA RODSCIU1
TRYMINU
INGINGL
TRYSCEL -0.035 -0.045
-0.028
-0.011
FACTOR 2
0.006
0.023
0.040
Fig. 3. Projections of the 35 studied species on the first two relative warps . Taxa classified in a same subgenus are boxed using different hatching designs.
- (ii) the most contrasted genera for this character are Lemuricola and Trypanoxyuris: in Lemuricola the juxta-cloacal papillae are very close together and the posterior one is situated beneath the posterior lip of the cloaca , while in Trypanoxyuris the juxtacloacal papillae are always distant and the posterior one more laterally located than the anterior one; Enterobius appears intermediate between the other two genera for this character, some of its species being closer to Trypanoxyuris, and the other closer to Lemuricola. Within each of the three main groups two subgroups may generally be distinguished: one of them having landmark 6 (the opening of the
phasmid) more lateral and (or) more anterior and a relatively shorter posterior part defined by landmarks 5, 6, 7 and 8: - (iii) the most contrasted subgroups are observed within the genus Lemuricola where specimens of the subgenus Madoxyuris have a relatively shorter posterior part and a phasmid anterior to the juxtacloacal papillae, while specimens of the subgenus Lemuricola together with the single Madoxyuris daubentoniae species are characterized by a relatively longer posterior part and a phasmid posterior to the juxta-cloacal papillae; the subgenus Protentero-
7
Shape patterns of genital papillae in Enterobiinae
bius is intermediate between these two groups with a relatively shorter posterior part (similar to that of Madoxyuris), but a phasmid posterior to the juxta-
Hugot & Baylac
cloacal papillae, similar to that of Lemuricola and Madoxyuris daubentoniae specimens;
0.050
0.033
0.016
FACTOR 1
-0.001
FACTOR 2
-0.018
-0.035 -0.045
-0.028
-0.011
0.006
0.023
0.040
Fig. 4. Projection on the first two relative warps. At the extremity of each axe and each diagonal of the diagram are represented the shape transformations, as a grid.
- (iv) within the genus Trypanoxyuris the different subgenera cannot be easily distinguished using these characters, with the exception of Hapaloxyuris oedipi whose phasmid location is similar to that observed in the subgenus Madoxyuris; Fig. 5 also confirms that the two species included in subgenus Rodentoxyuris are very similar to the other species of the genus Trypanoxyuris; - (v) the two subgenera of Enterobius, are separated by the relative size of the posterior part which is
longer in the subgenus Enterobius; the position of the phasmid appears rather variable within that genus, where most species have a phasmid more lateral than the posterior juxta-cloacal papilla, with the exceptions of: in subgenus Colobenterobius, C. guerezae, in subgenus Enterobius, E. macaci, E. brevicauda and E. bipapillatus. Finally, the comparison of the overall shapes within the Enterobiinae to that of Ingloxyuris inglisi, that
8
Shape patterns of genital papillae in Enterobiinae
COLZAKI
Hugot & Baylac
COLPRES PROTNYCT
COLLENT
MADDAUB LEMCONT
LEMMIC
CONSENSUS COLLONG XERPARA MADLEM
COLPARA COLGUER
MADBAUC
MADNANA
COLCOLO
MADVAUC MADBALT ENTEMACA
INGINGL
ENTEBIPA RODSCIU ENTEVERM RODBICR
ENTEBREV
HAPTAMA ENTEGREG TRYSCEL TRYSATA
ENTANTH
TRYTRYP
HAPGOEL
TRYMICR
TRYATEL TRYMINU
TRYCROI
HAPOEDI
Fig. 5. Shapes of the 35 species included in the analysis, illustrated at the tip of the terminal branches of the cladogram of the Enterobiinae resulting from a morphological cladistic analysis of the subfamily (after Hugot, 1999). Different hatching designs are attributed to species classified in the same subgenus.
was used as an outgroup in the cladistic analysis, allows to recognize a common pattern for the family: - (vi) in the Enterobiinae the precloacal pair of papillae is always situated much more laterally than any of the other nervous ends of the caudal bursa during, conversely in I. inglisi this papilla is vertically lined with the others and with the orifice of the phasmid; furthermore, in the Enterobiinae the ratio of the highest vertical dimension onto the widest horizontal dimension, is always inferior or equal to 2, while this ratio in I. inglisi is greater than 5.
DISCUSSION Congruence between shape patterns and the classification of Enterobiinae The results of the landmark analysis allow to recognize different patterns of distribution of the genital papillae that are congruent with the main genera and subgenera previously described in the subfamily Enterobiinae. Within the genus Lemuricola, each of the three subgenera: Lemuricola, Madoxyuris and Protenterobius can be characterized. Within the genus Enterobius, the two subgenera Enterobius and Colobenterobius are also recognized. Wi-
9
Shape patterns of genital papillae in Enterobiinae
thin the genus Trypanoxyuris the subgenera Hapaloxyuris and Rodentoxyuris cannot be completely distinguished from Trypanoxyuris. However, some discordances appear and several species are not found in the subgroup corresponding with the subgenus in which they were respectively classified. Madoxyuris daubentoniae is clearly closer to the species of the subgenus Lemuricola than to the species of the subgenus Madoxyuris into which Chabaud et al. (1965) put M. daubentoniae. The cladistic analysis (Hugot, 1999) indicated that M. daubentoniae was the most divergent branch of the Madoxyuris clade (Fig. 5), and the present results clearly question its belonging to this group. Colobenterobius guerezae does not cluster within the other species of subgenus Colobenterobius; an additional relative warp analysis (not presented here), limited to the Enterobius/Colobenterobius group showed that the two subgroups can easily be separated and additionally showed that: in C. guerezae the position of landmark 6 is similar to that of three species of the subgenus Enterobius (E. macaci, E. bipapillatus and E. brevicauda); this contrasts with other members of the subgenus Colobenterobius and probably explains the position of C. guerezae on the plane (Fig. 3); however, Fig. 5 shows that the posterior part of the caudal bursa is relatively shorter in C. guerezae. This pattern is common to all the Colobenterobius spp. Thus, C. guerezae exhibits the general pattern of this subgenus and its presence within the Enterobius group on Fig. 3 can be interpreted resulting of an homoplasic character present only in these four species: the orifice of the phasmid being situated closer to the sagittal plan than the three posterior pairs of genital papillae. Xeroxyuris shares with the members of Trypanoxyuris the position of the juxta-cloacal papillae, and this explains its position on Fig. 3. Nevertheless, Fig. 2 and Fig. 5 show that this similitude does not apply to the rest of the caudal bursa, particularly when compared with the other parasites of squirrels (Rodentoxyuris spp.). This rather unexpected position of Xeroxyuris on the analysis may be interpreted as a result of homoplasic character states.
Phylogenetic versus functional patterns ? Within the order Oxyurida, the caudal bursa generally has a conservative shape that is used as a diagnostic character: at the family or genera level, related taxa have similar caudal bursae; at the species level, all individuals of a single species share specific characters that concern the details of the disposition of the papillae and/or the patterns of the cuticular ornamentation. Petter and Quentin (1973) already used these characters in their key to the
Hugot & Baylac
different genera and family within the order. This overall conservation of the caudal bursa pattern may be partly explained by its potential implication during the mating behavior of male pinworms. During the prelude to mating, male are slowly moving, their tail gently winded around the body of the female (Hugot, unpublished). This suggests that the cloacal papillae are used by the male pinworms to localize the opening of the vulva and are implied in the specific recognition mechanisms. The fact that several congeneric pinworm species may live in the same gut, further reinforces this hypothesis. Species have probably developed specific mating signals involving tactile mechanisms using the genital papillae (Hugot, 1982a & b, 1984c, 1986, 1993). Our results indicate that shape differences are far more important between- than within genera. Given that the phylogeny of the pinworms parallels the phylogeny of their hosts (Hugot, 1999) the separation of the genera probably go back to the origin of the main primates lineages (at the beginning of the Tertiary) and may be considered relatively old. By contrast, most speciation events are associated with the living primate, may be dated from the post Miocene, and are therefore much more recent. Nevertheless, the large similitude within genera suggests a possible additional mechanism that could be related to stabilizing selective pressures. The present landmark analysis allows to allocate a different pattern of phasmid and genital papillae distribution to each of the taxonomic groups revealed by the phylogenetic analysis of the Enterobiinae. The differences between the three main genera principally deal with more or less close each other juxta-cloacal papillae and with the position of these papillae relatively to the posterior lip of the cloaca. Fig. 2 shows that in the Enterobiinae the juxta-cloacal papillae always are surrounded by a more or less developed cuticular ornamentation. In the genus Trypanoxyuris this ornamentation is limited to a simple cuticular ring around the first pair of papillae. In the genera Enterobius and Lemuricola it is very much more developed and encloses both pairs of juxtacloacal-papillae. Finally, Lemuricola, which exhibits the most complicated patterns, is also characterized by juxta-cloacal papillae very close together and situated close to, and often adjoining, the posterior lip of the cloaca. In addition, in the species of subgenus Madoxyuris the opening of the phasmid, which also is included into the huge block of the cuticular ornamentation, is closer to the posterior lip of the cloaca than observed in the other taxa of the subfamily. No other taxa in the Oxyurida have developed such a particular ornamentation which can probably be interpreted a derived pattern.
10
Shape patterns of genital papillae in Enterobiinae
Hugot & Baylac
All occurs as if the inclusion of the papillae into a progressively stronger cuticular thickening was accompanied by the motion of the papillae toward the posterior lip of the cloaca. This suggests that the evolution of the juxta-cloacal papillae and the development of the cuticular ornamentation could be linked. The more or less developed peri-cloacal ornamentation can be interpreted as acting like a rugged surface, which avoids the male and female to loose the contact of their cuticle during insemination. Furthermore, during mating the males have a secretion of the glands associated with the cloaca. This secretion coagulates at surface of the cuticle also including the cuticular ornamentation and its protuberances, which enforces the juxtaposition of the vulva and cloacal position in the correct position.
ther hand, our results also show that within each of the main groups similar modifications of shape are observed. This suggests that convergent selective pressures may have shaped parallel anatomical features. This analysis also shows that the shape modifications involve complex patterns of landmark displacements: this explains why direct observation does not allow to distinguish non-ambiguous binary character states. Our analysis confirms (Bookstein, 1994, Monteiro, 2000, Claude et al., 2004) that morphometric shape patterns cannot be interpreted unequivocally without the support of a preexisting phylogenetic framework, due to the multiple homoplasic events that may be distinguished at the different taxonomic levels of this subfamily.
In Lemuricola the apparent displacement of the phasmid could also be interested by this evolution. In the other genera the relative motion of the phasmid opening apparently has nothing to deal with a more or less developed ornamentation, which suggests that other evolutionary mechanisms could interplay. This is also supported by the fact that the two main groups observed within genus Lemuricola, separate pinworms with a caudal appendix from the others even though the Landmark describing this appendix was finally eliminated from the data set. This indicates that the presence or absence of an appendix is linked with a different morphology of the caudal bursa.
This work owes much to the friendly and informal discussions that we had with Leslie Marcus, particularly during the Euro-American Congress of Zoology, in July 1998. Leslie strongly encouraged us to publish our results and we dedicate this paper to him.
CONCLUSIONS The present work allows to hypothesize different patterns of evolution of the caudal bursa, each one specific for a particular taxon. Generally, the differences observed between the three main genera may be interpreted linked with the evolution of the peri-cloacal ornamentation which itself plays a role in the success of the particular mating behavior of these nematodes. In addition, when an apparent lack of resolution seems to confuse the interpretation of the results (taxa observed in a unexpected position on the projection diagrams), close examination reveals that homoplasic events may explain this confusion. These results are consistent with the classification of the Enterobiinae into three groups, each one characterized by a particular spatial distribution of the phasmids and genital papillae: (i) Lemuricola, Protenterobius, Madoxyuris, (ii) Colobenterobius, Enterobius, (iii) Hapaloxyuris, Trypanoxyuris, Rodentoxyuris. As no evaluation of the intra specific variation could be performed, because our data set generally includes only one specimen (rarely two) of a same species, it could be expected that the taxonomic signal included into the patterns of the caudal bursa is particularly strong. On ano-
Acknowledgements
REFERENCES Adams, D. C. and Rohlf, F. J. and Slice, Dennis E. (2004). Geometric morphometrics: ten years of progress following the "revolution". Italian Journal of Zoology, 71:5-16 Artigas, P. de Toledo. (1936). Estudios helminthologicos. I. Paraoxyuronema brachytelesi g. n., sp. n., parasita de Brachyteles arachnoides (Geoffr., 1806); Oxyuronemidae, fam. n. Memorias du Instituto Butantan, 10, 77-85. Baylis, H. A. (1928). Some further parasitic worms from Sarawak. Annals of the Magazine of natural History, 1, 606-608. Bookstein, F. L. (1991). Morphometric Tools for Landmark Data, Geometry and Biology. Cambridge University Press. Bookstein, F.L. (1994). Can biometrical shape be a homologous character? In Homology, B.K. Hall, Ed, Academic Press. Bookstein, F.L. (2002). Creases as morphometric characters. Pages 139-174 in Morphology, shape and phylogeny (N. Macleod and P.L. Forey, eds). Taylor & Francis, London. Cameron, T. W. (1929). The species of Enterobius Leach, in Primates. Journal of Helminthology, 7, 161-182. Cameron, T. W. !1932). On a new species of Oxyuris from the grey squirrel in Scotland. Journal of Helminthology, 10, 29-32.
11
Shape patterns of genital papillae in Enterobiinae
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. Annales de Parasitologie Humaine et Comparée, 40, 181-214. Chabaud, A. G., and A. J. Petter. (1959). Les nématodes parasites de lémuriens malgaches. II. Un nouvel Oxyure: Lemuricola contagiosus Mémoire de l’Institut scientifique de Madagascar, 13, 127-132. 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. Annales de Parasitologie Humaine et Comparée, 36, 113-126. Claude, J., P. Pritchard, H. Tong, E. Paradis, and J.C. Auffray (2004). Ecological correlates and evolutionary divergence in the skull of turtles: a geometric morphometric assessment. Systematic Biology, 53: 933-948. 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. 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. Archives du Muséum natlonal d’Histoire Naturelle de Paris, 3, 27-40. Felsenstein, J. 1988. Phylogenies and quantitative characters. Annual Review of Ecology and Systematics, 19: 455-471. Felsenstein, J. (2002). Quantitative characters, phylogenies and morphometrics. Pages 27-44 in Morphology, shape and phylogeny (N. MacLeod and P.L. Forey, eds). Taylor & Francis, London. Felsenstein J., 2004. Inferring phylogenies. Sinauer Associates, Sunderland, MA. Gedoelst, L. 1916. Notes sur la faune parasitaire du Congo Belge. Revue de Zoologie africaine, 5, 2427. Goodall, C. R. (1991). Procrustes Methods in the Statistical Analysis of Shape. Journal of the Royal Statistical Society. Series B, 53, 285-339. Goodall, C. R. (1995). Procrustes methods in the statistical analysis of shape revisited. Pages 18-33. In: Mardia, K. V. & Gill, C. A. (eds.) Current Issues in Statistical Shape Analysis, University of Leeds Press. Hugot, J. P. (1983). Enterobius gregorii (Oxyuridae, Nematoda), un nouveau parasite humain (Note pré-
Hugot & Baylac
liminaire). Annales de Parasitologie Humaine et Comparée, 58, 403-404. Hugot, J. P. (1984a). Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). I. Parasites de Sciuridae: sous-genre Rodentoxyuris. Bulletin du Muséum national d'Histoire naturelle, Paris, 4e sér., 6, 711720. Hugot, J. P. (1984b. Sur le genre Trypanoxyuris (Oxyuridae, Nematoda)). II. Sous-genre Hapaloxyuris parasite de Primates Callitrichidae. Bulletin du Muséum National d'Histoire Naturelle, Série A, Zoologie, 6, 1007-1019. Hugot, J. P. (1985). Sur le genre Trypanoxyuris (Oxyuridae, Nematoda). III. Sous-genre Trypanoxyuris parasite de Primates Cebidae et Atelidae. Bulletin du Muséum National d'Histoire Naturelle, Série A, Zoologie, 7, 131-155. Hugot, J. P. (1986). Sur le genre Auchenacantha (Oxyuridae, Nematoda), parasite de Dermoptères. Étude de la morphologie et de la distribution des formes. Systematic Parasitology, 8, 243-266. Hugot, J. P. (1987a). Sur le genre Enterobius (Oxyuridae, Nematoda): s.g. Colobenterobius.I. Oxyures parasites de Primates Colobinae en région éthiopienne. Bulletin du Muséum national d'Histoire naturelle, Paris, 4e sér., 9, 341-352. Hugot, J. P. (1987b). Sur le genre Enterobius: s.g. Colobenterobius.II. Oxyures parasites de Singes Colobinae en région orientale. Bulletin du Muséum national d'Histoire naturelle, Paris, 4e sér., 9, 799813. Hugot, J. P. (1993). Redescription of Enterobius anthropopitheci (Nematoda, Oxyurida), parasite of the chimpanzees. Systematic Parasitology, 26, 201207. Hugot, J. P. (1995). Redescription of Xeroxyuris parallela (Linstow,1907) n.gen., n.cb., parasite of Xerus inauris. Parasite, 2, 1-7. Hugot, J. P. (1999). Primates and their pinworm parasites: Cameron hypothesis revisited. Systematic Biology, 48, 523-546. Hugot, J. P. & 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. Bulletin du Muséum National d'Histoire Naturelle, Série A, Zoologie, 7, 633-636. Hugot, J. P. & C. Tourte-Schaefer. (1985). Etude morphologique des deux oxyures parasites de l'Homme: Enterobius vermicularis et E. gregorii.
12
Shape patterns of genital papillae in Enterobiinae
Annales de Parasitologie Humaine et Comparée, 60, 57-64. Hugot, J. P., S. Morand & S. L. Gardner. (1995). Morphology and morphometrics of three oxyurids parasitic in Primates. Description of Lemuricola microcebi n. sp. International Journal for Parasitology, 25, 1065-1075.
Hugot & Baylac
den Jahren 1903-1905. II. Helminthes. Nematoden und Acanthocephalen. Denkschr. Medicine Naturwiss Geschichte. Jenia, 13, 19-28. MacLeod, N. (2002). Phylogenetic signals in morphometric data. Pages 100-138 in Morphology, shape and phylogeny (N. MacLeod and P.L. Forey, eds). Taylor & Francis, London.
Hugot, J. P., S. Morand & R. Guerrero. (1994). Trypanoxyuris croizati n.sp. and T. callicebi, two vicariant forms parasite of Callicebus spp (Primate, Cebidae). Systematic Parasitology, 27, 35-4365.
Monteiro, L.R. (2000). Why morphometrics is special: the problem with using partial warps as characters for phylogenetic inference. Systematic Biology, 49: 796-800.
Hugot, J.P., S. L. Gardner, & S. Morand. (1996). The Enterobiinae fam. nov. (Nematoda, Oxyurida), parasites of Primates and Rodents. International Journal for Parasitology, 26, 147-159. Inglis, W. G. (1961). The oxyurids parasites (Nematoda) of primates. Proceedings of the Zoological Society, London, 136, 103-122.
Naylor, G.J.P. (1996). Can partial warp scores be used as cladistic characters ? Page 519-530 in Advances in morphometrics (L.F. Marcus, M. Corti, A. Loy, G.J.P. Naylor and D.E. Slice, eds). Plenum Press. New York.
Inglis, W. G. & G. E. Cosgrove. (1965). The pinworms parasites (Nematoda: Oxyuridae) of the Hapalidae (Mammalia: Primates). Parasitology, 55, 731-737. Inglis, W. G. & C. Diaz-Ungría. (1960). Nematodes parasitos de vertebrados venezolanis. I. Una revision del genero Trypanoxyuris (Ascaridata: Oxyuridae). Memórios de la Sociedad de Ciencias naturales "La Salle", 19, 176-212. Inglis, W. G., and F. L. Dunn. (1963). The occurrence of Lemuricola (Nematoda: Oxyurida) in Malaya: with the description of a new species. Zoologische ParasitenKunde, 23, 354-359. Klingenberg, C.P. and Ekau, W. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biological Journal of the Linnean Society, 59: 143-177. Krzanowski, W. J. (1988). Principles of multivariate analysis. A user's perspective. Clarendon Press Oxford. Leach (ms. in W. Baird, 1853). Catalogue of the species of Entozoa, or intestinal worms, contained in the collection of the British Museum. Pages 1132. Le Roux, P. L. (1930). The generic position of Oxyuris polyoon Linstow, 1909 in the subfamily Oxyurinae Hall, 1916. Report of the Direction of the veterinary Services of South Africa, 16, 205-210. Linstow, O. F. B. (1907). Neue und beknnante Nematoden. Zentralbl. Bakteriologia, 44, 1-265. Linstow, O. F. B. (1908). Zoologische und Anthropologische Ergebisse einer Forschungsreise im Westlichen und Zentralen Südafrika ausgefürhrt in
Osche, G. (1958). Die bursa und Schwanzstrukturen und ihre Aberrationen bei den Strongylina (Nematoda). Morphologische studien zum Problem der pluri und Paripotenzerscheinungen. Zeitschnft fur Morphologie und Okologie der Tier, 46, 571-635. Petter, A. J. & J. C. Quentin. (1976). CIH keys to the nematode parasites of vertebrates. No. 4. Keys to genera of the Oxyuroidea, 30pp. 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. Annales de Parasitologie Humaine et Comparée, 47, 391-398. Pretorius, E. and Scholtz, C.H. (2001). Geometric morphometrics and the analysis of higher taxa: a case study based on the metendosternite of the Scarabaeoidea (Coleoptera) Biological Journal of the Linnean Society, 74: 35-50 Quentin, J. C., C. Betterton & 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. Bulletin du Muséum National d'Histoire Naturelle, Série A, Zoologie, 1, 1031-1050. Quentin, J. C., and F. Tenora. (1975). Morphologie et position sytématique de Lemuricola (Rodentoxyuris) sciuri (Cameron, 1932) nov. comb. nov. subgen., et Syphacia (Syphatineria) funambuli Johnson, 1967. Oxyures (Nematoda) parasites de rongeurs sciuridés. Bulletin du Muséum National d'Histoire Naturelle, Série A, Zoologie, 178, 1525-1535. Rohlf, F. J. & D. S. Slice. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40-59.
13
Shape patterns of genital papillae in Enterobiinae
Rohlf, F. J. (1992). Relative warp analysis and an example of its application to mosquito wings. Pages 131-159. In Leslie F. Marcus & Bello, E. & GarrciaValdecasas, A. (eds.), Contributions to Morphometrics. Museo Nacional de Ciencias Naturales, Madrid. Rohlf, F.J., A. Loy and M. Corti (1996). Morphometric analysis of Old World Talpidae (Mammalia, Insectivora) using partial-warp scores. Systematic Biology, 45: 344-362 Rohlf, F.J. (2001). Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution, 55: 2143-2160. Rohlf, F.J. (2002). Geometric morphometrics and phylogeny. Pages 175-193 in Morphology, shape and phylogeny (N. MacLeod and P.L. Forey, eds). Taylor & Francis, London. Rohlf, F. J. (2004a). TpsRelw software version 1.35. Stony Brook State University, Department of Ecology and Evolution. http://life.bio.sunysb.edu/morph/soft-tps.html. Rohlf, F. J. (2004b). TpsRegr software version 1.28. Stony Brook State University, Department of Ecology and Evolution. http://life.bio.sunysb.edu/morph/soft-tps.html. Rohlf, F. J. & L. F. Bookstein. (2003). Computing the uniform component of shape variation. Systematic Biology, 52, 66-69. Rohlf, F. J. & L. F. Marcus. (1993). A revolution in morphometrics. Trends in Ecology and Evolution, 8, 129–132. Sandosham, A. A. 1950. On Enterobius vermicularis (Linnaeus, 1758) and some related species from primates and rodents. Journal of Helminthology, 24, 171-204. Schneider, A. (1866). Monographie der Nematoden. Berlin. 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 Journal of Helminthology, 6, 24 - 25. Slice, D. E. (1991). DS-DIGIT 1.1:Basic Digitizing Software. Department of Ecology and Evolution. State Univ. New York. Stony Brook NY 11794. Travassos, L. (1925). Fauna Brasiliense. Nematodes, Oxyuroidea-Oxyuridae. Revisao do genero Enterobius Leach, 1853. Museo Nacional Rio Janeiro, 2, 5-11.
Hugot & Baylac
Vevers, C. M. (1923). Some new and little known helminths from British Guiana. Journal of Helminthology, 1, 35-45. Vuylstéke, C. (1964). Mission de Zoologie médicale au Maniema (Congo Léopoldville). (P. L. G. Benoît, 1959). 3. Vermes. Nematoda. Annales du Musée royal d’Afrique centrale Serie Quarto Zoologie, 132, 41-66. Wahid, S. (1961). On two new species of the genus Enterobius Leach, 1853, from a Colobus monkey. Journal of Helminthology, 35, 345. Yin, W. Z. (1973). Helminths of birds and wild animals from Lin tsan Prefecture, Yunnan Province, China. II. Parasitic nematodes of mammals. Acta zoologica sinnica, 19, 354 - 364. Zelditch, M.L., W.L. Fink, and D.L. Swiderski (1995). Morphometrics, homology and phylogenetics: quantified characters as synapomorphies. Systematic Biology, 44: 179-189.
APPENDIX 1. TAXA ANALYZED Family Oxyuridae Cobbold, 1864 Subfamily Oxyurinae Genus Ingloxyuris Chabaud, Petter and Golvan, 1961 INGINGL: Ingloxyuris inglisi Chabaud, Petter and Golvan, 1961.— Source: Chabaud et al. (1961), Hugot (unpub.).—Host taxon: Lepilemur ruficaudatus Grandidier [Madagascar]. Subfamily Enterobiinae Hugot, Gardner and Morand, 1996 Genus Enterobius Leach, 1853, Subgenus Enterobius ENTANTH: E. anthropopitheci (Gedoelst, 1916).— Source: Gedoelst (1916), Sandosham (1950), Hugot (1993). ).—Host taxa: Pan troglodytes (Blumenbach) [Zaire, Senegal], P. paniscus Schwartz [Zaire]. ENTBIPA: E. bipapillatus (Gedoelst, 1916).— Source: Gedoelst (1916), Hugot (unpub.).—Host taxon: Chlorocebus aethiops (L.) [Zaire, South Africa]. ENTEBREV: E. brevicauda Sandosham, 1950.— Source: Sandosham (1950), Hugot (unpub.). —Papio cynocephalus (L.) [Kenya, Rhodesia, Zaire]; Papio ursinus [South Africa]. ENTEGREG: E. gregorii Hugot, 1983a.— Source: Hugot (1983a), Hugot and Tourte-Schaeffer (1985). —Host taxon: Homo sapiens (L.) [cosmopolitan].
14
Shape patterns of genital papillae in Enterobiinae
ENTEMACA: E. macaci (Yin, 1973).— Source: Yin (1973), Hugot (unpub.).—Host taxa: Macaca mulatta (Zimmermann) [Yunnan, India], M. cyclopis (Swinhoe)[Taiwan]. ENTEVERM: E. vermicularis (L., 1758).— Source: Hugot and Tourte-Schaeffer (1985). Subgenus Colobenterobius Quentin, Betterton and Krishnasamy, 1979 COLCOLO: C. colobis Vuylstéke, 1964.— Source: Vuylstéke (1964), Hugot (1987a). — Host taxa: Procolobus badius (Kerr) [Zaire].
Hugot & Baylac
pub.)..— Host taxa: Hapalemur simus Gray [Madagascar]. MADDAUB: M. daubentoniae Petter, Chabaud, Delavenay and Brygoo, 1972.— Source: Petter et al. (1972), Hugot (unpub.).— Host taxa: Daubentonia madagascariensis (Gmelin) [Madagascar]. MADLEM: M. lemuris (Baer, 1935).— Source: Baer (1935), Hugot (unpub.).— Host taxa: Eulemur macaco (L.) [Madagascar]. MADNANA: M. nana Hugot (unpublished).— Host taxa: Eulemur macaco (L.) [Madagascar].
COLENT: C. entellus Hugot, 1987b.— Source: Hugot (1987a). — Host taxa: Semnopithecus entellus (Dufresne) [Zoo].
MABVAUC: M. vauceli Chabaud, Brygoo and Petter, 1965.— Source: Chabaud et al. (1965), Hugot (unpub.).— Host taxa: Eulemur fulvus (E. Geoffroy).
COLGUER: C. guerezae Hugot, 1987a. — Source: Hugot (1987a). — Host taxa:Colobus guereza Rüppel [Ethiopia, Congo].
Subgenus Protenterobius Inglis, 1961
COLLONG: C. longispiculum Quentin, Betterton and Krishnasamy, 1979.— Source: Quentin et al. (1979).— Host taxa: Trachypithecus obscurus (Reid) [Malaysia]. COLPARA: C. paraguerezae Hugot, 1987a.— Source: Hugot (1987a).— Host taxa: Colobus guereza Rüppel [Ethiopia]. COLPRES: C. presbytis Yin, 1973.— Source: Yin (1973), Quentin et al. (1979), Hugot (1987b)..— Host taxa: Semnopithecus entellus (Dufresne) [Zoo and Allahabad Woodland]. COLZAK: C. zakiri Siddiqi and Mirza, 1954.— Source: Siddiqi and Mirza (1954), Hugot (1987b)..— Host taxa: Semnopithecus entellus (Dufresne) [Zoo and Allahabad Woodland]. Genus Lemuricola Chabaud and Petter, 1959, Subgenus Lemuricola
PROTNYCT: P. nycticebi (Baylis, 1928).— Source: Baylis (1928), Inglis and Dunn (1963), Hugot, (unpub.).—Host taxa: Nycticebus coucang (Boddaert) [Malaysia, Borneo]. Genus Trypanoxyuris Vevers, 1923, Subgenus Trypanoxyuris TRYCROI: T. croizati Hugot, Morand and Guerrero, 1994.— Source: Hugot, Morand and Guerrero, 1994.—Host taxa: Callicebus torquatus (Hoffmannsegg) [Venezuela]. TRYMICR: T. microon (Linstow, 1907).— Source: Travassos (1925), Sandosham (1950), Inglis and Diaz-Ungría (1960). —Hugot (1985).Host taxa: Aotus trivirgatus (Humboldt) [Colombia]. TRYSAT: T. satanas Hugot, 1985.—Source: Hugot, 1985.—Host taxa: Chiropotes satanas (Hoffmannsegg) [Venezuela], C. chiropotes Humboldt [Venezuela].
LEMCONT: L. contagiosus Chabaud and Petter, 1959.— Source: Chabaud and Petter (1959), Hugot et al. (1995).
TRYSCEL: T. sceleratus (Travassos, 1925).— Source: Hugot (1985).—Host taxa: Saimiri orstedii (Reinhardt) [Guyana], S. sciureus L. [French Guiana].
LEMMIC: L. microcebi Hugot, Morand and Gardner, 1995.— Source: Chabaud and Petter (1959), Hugot et al. (1995)..— Host taxa: Microcebus murinus (J. F. Miller) [Madagascar].
TRYTRYP: T. trypanuris Vevers, 1923.— Source: Hugot (1985).—Host taxa: Pithecia pithecia (L.) [French Guiana], P. monachus (E. Geoffroy) [Guyana].
Subgenus Madoxyuris Chabaud, Brygoo and Petter, 1965 MADBALT: M. baltazardi Chabaud, Brygoo and Petter, 1965.— Source: Chabaud et al. (1965), Hugot (unpub.)..— Host taxa: Eulemur fulvus (E. Geoffroy) [Madagascar]. MABAUC: M. bauchoti Chabaud, Brygoo and Petter, 1965.— Source: Chabaud et al. (1965), Hugot (un-
TRYATELI: T. atelis (Cameron, 1929).— Source: Cameron (1929), Dollfus and Chabaud (1955), Inglis and Diaz-Ungría (1960), Hugot (1985a).—Host taxa: Ateles paniscus (L.) [French Guiana]. TRYMINU: T. minutus (Schneider, 1866).— Source: Hugot (1985).—Host taxa: Alouatta seniculus (L.) [French Guiana].
15
Shape patterns of genital papillae in Enterobiinae
Subgenus Hapaloxyuris Inglis and Cosgrove, 1965 HAPGOEL: H. goeldii Inglis and Cosgrove, 1965.— Source: Inglis and Cosgrove (1965), Hugot (1984b).—Host taxa: Callimico goeldii (Thomas) [locality unknown]. HAPOEDI: H. oedipi Inglis and Cosgrove, 1965.— Source: Inglis and Cosgrove (1965), Hugot (1984b).— Host taxa: Saguinus oedipus (L.) [Brazil]. HAPTAMA: H. tamarini (Inglis and Dunn, 1964).— Source: Inglis and Dunn (1964), Hugot (1984b).— Host taxa: Saguinus nigricollis (Spix) [Peru]. Subgenus Rodentoxyuris Quentin and Tenora, 1975 RODBICR: R. bicristata Hugot, 1984a.— Source: Hugot (1984a).—Host taxa: Sciurus niger L. [Michigan]; Sciurus carolinensis Gmelin [USA]; Sciurus aberti Woodhouse [New Mexico]; Glaucomys volans (L.) [Michigan, Connecticut]; Glaucomys sabrinus (Shaw) [Oregon]. RODSCIU: R. sciuri (Cameron, 1932).— Source: Hugot (1984a).—Host taxa: Sciurus carolinensis Gmelin [United Kingdom], Sciurus vulgaris L. [United Kingdom, France, Spain, Switzerland, Czechoslovakia, Ukraine]. Genus Xeroxyuris Hugot, 1995 XERPARA: Xeroxyuris parallela (Linstow, 1908).— Source: Le Roux (1930), Inglis (1961), Hugot (1995).—Host taxa: Xerus inauris (Zimmermann) [South Africa].
Hugot & Baylac
