A Conventional Approach to a New Classification of the Strongyloidea, Nematode Parasites of Mammals

Transcription

1 AMER. ZOOL., (1979). A Conventional Approach to a New Classification of the Strongyloidea, Nematode Parasites of Mammals J. RALPH LICHTENFELS Animal Parasitology Institute, U.S. Department of Agriculture, Science and Education Administration, Agricultural Research, Beltsville, Maryland SYNOPSIS. The conventional approach to systematic parasitology uses any kind of information, with a posteriori weighting of characters demonstrated to be concordant with many others. Two types of ovejectors and dorsal rays divide the strongyloid nematodes into groups that correlate with their host groups, resulting in the first phylogenetic classification of the superfamily Strongyloidea. GENERAL INTRODUCTION Thomas Cameron (1964) began a discussion of the evolution of helminth parasites by likening our knowledge of it to Dana's description of Geology, "a particularly alluring field for premature attempts at the explanation of imperfectly understood data." Much has been learned about strongyloid nematodes since 1964, but we are still far from a perfect understanding of their evolution. I was asked to describe the traditional or conventional abproach to classification and identifications!" parasites. This will be done by describing how I arrived at a new classification for the Strongyloidea, a superfamily of nematodes parasitic in mammals (Lichtenfels, 1979). To me the conventional approach involves the use of any and all kinds of information, but with weight given to characters that are apparently concordant with many Appreciation is expressed to Robert B. Ewing, Animal Parasitology Institute (API), who prepared drawings and other artwork, and to Patricia A. Pilitt (API) who prepared drawings of dorsal rays and assisted with the literature search. This work was greatly improved because of the generous cooperation of Mrs. Patricia Mawson Thomas, University of Adelaide, South Australia and Dr. Ian Beveridge, James Cook University, North Queensland, Australia, who provided specimens and advance copies of manuscripts. Specimens were also provided by Dr. David I. Gibson, British Museum, London, Dr. Delir Correa Gomez, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, and Dr. Lofti F. Khalil, Commonwealth Institute of Helminthology, St. Albans, Herts., England others. My approach to weighting characters should be labeled classical because I began by examining characters that have been used previously in defining natural groups at higher levels (Mayr, 1969). This is the conventional approach, i.e., the use of a posteriori weighting of characters to infer evolutionary relationships and to construct classifications that we hope will have high predictive value. An introduction to the Strongyloidea will be followed by: a comparison of previous classification systems for the Strongyloidea to illustrate the classical approach to selecting characters to be given weight; a description of the new classification; a description of tests for the new classification; and a brief discussion of procedures used and results obtained. SPECIFIC INTRODUCTION A review of parasitic nematodes was undertaken at the request of the editors of the CIH Keys to Nematode Parasites of Vertebrates (Anderson etal., 1974). Thesedichotomous keys are to generic level, with illustrations of key characters. The objectives of the keys are two-fold: 1) the easy and accurate identification of genera; and 2) the recognition of evolutionary lines in order to arrive at a classification with predictive value. Keys to more than half of the 27 superfamilies have already been published, and the series will be completed in the early 1980s. The Strongyloidea are nematodes of the

2 1186 J. RALPH LICHTENFELS // DORSAL KAV FIG. 1. Diagrammatic drawing of copulatory bursa of posterior end of males of the Order Strongylida. Order Strongylida in which the males have a trilobed copulatory bursa supported by fleshy rays (Fig. 1); female Strongylida have a muscular ovejector. The Strongylida also possess an intestine of few large multinucleate cells and two large excretory gland cells. The Strongylida can be separated into 5 superfamilies (Chabaud, 1974; Table 1). Most classifications of the order Strongylida have grouped the Ancylostomatoidea with the Strongyloidea because they both have large, globular buccal capsules. Both Schulz (in Skrjabin et al., 1952) and Dougherty (1951), however, stressed the presence of an ovejector of the trichostrongyloid type in concluding that the Anclostomatoidea were more closely related to the Trichostrongyloidea than to the Strongyloidea. The Ancylostomatoidea resemble the Trichostrongyloidea in characteristics of the life cycle, copulatory bursa, and ovejectors (Table 1). Also, the Ancylostomatoidea and the Trichostrongyloidea are both parasitic in the small intestine while the Strongyloidea are mostly parasitic in the large intestine. Chabaud (1965; 1974) recognized the Ancylostomatoidea as an independent superfamily intermediate between the Trichostrongyloidea and the Strongyloidea. Members of the Strongyloidea have a large globular or cylindrical buccal capsule, and usually have single or double leaf-like corona radiata (Fig. 2) or lips around the oral opening. They are parasites of the large intestine of mammals (rarely birds and tortoises). EXAMINATION OF PREVIOUS SYSTEMS The superfamily Strongyloidea includes 87 genera and subgenera, and several families. The Syngamidae have a globular buccal capsule, no lips or corona radiata, and a hexagonal oral opening. Most previous Table 1. SUPERFAMILIES OF THE STRONGYLIDA WITH DISTINGUISHING FEATURES, HOSTS, AND LOCATION IN HOSTS. Lateral jaws Strongyloidea Large Buccal Capsule without Teeth anteriorly Ovejectors with long sphincters SUPERFAMILY Large buccal capsule with teeth anteriorly Ovejectors with short sphincters Very small buccal capsul Cuticular ridges Ovejectors with short sphincters Flat muscles Diapbanocephaloidea Ancylostomatoidea Trichostrongyloidea Metastrongyloidea Very small buccal capsule U shaped muscles Snakes and Lizards Mammals, rarely birds or tortiscs Mammals Mammals, Birds, Reptiles, Amphibians Mammals Stomach and Small Intestine Large intestine Rarely stomach, small intestine or respiratory system Small intestine Stomach and Small intestine Respiratory system. Rarely other tissues or tissue spaces

3 Oesophagostomii FIG. 2. Dendrogram of possible evolutionary relationships of Strongyloidea (Nematoda) (After Lichtenfels, 1979). workers have agreed on the composition of the 10 genera and subgenera of the Syngamidae and Deletrocephalidae (see Lichtenfels, 1979); accordingly, these two families are not discussed further. My first step in the preparation of a key to genera of the Strongyloidea was to examine previous classification systems. Table 2 shows how previous workers grouped the families and subfamilies of the Strongyloidea (excluding the Syngamidae and Deletrocephalidae) and compares the previous systems with the new system that I have proposed (Lichtenfels, 1979). Yorke and Maplestone (1926) grouped the 31 genera then known into a single family and three subfamilies. The characters used to separate the subfamilies were the globular, subglobular or funnel-shaped buccal capsule in the Strongylinae, the cylindrical or ring-shaped buccal capsule of the Trichoneminae and Oesophagostominae, and the transverse cervical groove of the Oesophagostominae (Fig. 2). Chitwood (1950) further separated the group with cylindrical or ring-shaped buccal capsules into three groups. He correctly recognized the genus Cyathostomum and used the subfamily Cyathostominae for genera with a cylindrical buccal capsule but lacking a cervical groove. He placed the genera with the cervical groove in the subfamily Oesophagostominae. He placed genera with six lips and without corona radiata in the family Cloacinidae. Dougherty (1951) differed with Chitwood (1950) in his treatment of the groups with cylindrical or ring-shaped buccal cavities, and distributed these genera in two subfamilies (Cloacininae and Oesophagostominae) rather than three. Popova (1955, 1958) divided the genera with large globular, subglobular, or funnel-shaped buccal capsules into three subfamilies: the Strongylinae, with cephalic end directed straight forward; the Chaberdinae, with cephalic end curved dorsally or ventrally and with two corona radiata; and the Ransominae, with cephalic end curved dorsally and with single corona radiata. Popova (1955, 1958) arranged the genera with cylindrical or ring-like buccal capsules in two families. She mistakenly recognized Trichonema instead of the older valid genus Cyathostomum as the type genus for the Trichonematidae. (See Lichtenfels, 1975 or Mclntosh, 1951 for a discussion of this controversy.) Popova (1958) recognized

4 1188 J. RALPH LICHTENFELS Table 2. Comparison of Classification Systems for the Strongyloidea (excluding Syngamidac and Deletrocephalidae) LICHTENFELS 1979 STRONGYLIDAE Sirongylinac Cyathostominae W.WJV Phascolostrongylinae DDDD CHABERTHDAE Chaberciinae Oesophagostominae Cloacininae oooooooo ooooooo oo o CHABAUD 1965 STRONGYLIDAE Strongylinae HE H ooooo Oesophagostominae 0 Cloacininae ooooooo YAMAGUTI 1961 STRONGYLIDAE Strongylinae CYATHOSTOMIDAE Cyathostominae DDD OOOOI Sauricolinae Oesophagostominae 0 CLOACINIDAE Cloacininae O Zoniolaiminae OO PHARYNGO- -STRONGYLIDAE OOO POPOVA 1955, 1958,1960 STRONGYLIDAE Strongylinae Chabertiinac 0 0 Ransominae 0 TRICHONEMATIDAE Trichonematinae Oesophagostominac Sauricolinae Murshidiinae v.v CLOACINIDAE Cloacininae o Zoniolaiminae YORKE& MAPLESTONE 1926 STRONGYLIDAE Strongylinae Trichonematinae Ocsophagostominae OOOOO Cbabertiinat Oaopbagostommat O Cloacininae 0 Strongylinae UCyatboslominae D Pbascolostrongy/inae four subfamilies in the Trichonematidae. The Oesophagostominae with a transverse cervical groove were separated from those without the groove. Those without the transverse cervical groove were the Sauricolinae with intestinal diverticula, the Triconematinae with two corona radiata, and the Murshidiinae with a single corona radiata. The family Cloacinidae with the oral opening surrounded by small lips was divided by Popova (1960) into two subfamilies: the Cloacininae with a corona radiata and the Zoniolaiminae without a corona radiata. Yamaguti (1961) placed the genera with a large globular, subglobular, or funnelshaped buccal capsule in a single family, the Strongylidae, and did not subdivide it into subfamilies. He distributed the genera with cylindrical or ring-shaped buccal capsules into three families. He proposed a new family, the Pharyngostrongylidae (genera previously included in the Cloacinidae), for genera with a cylinidrical buccal capsule with "ringed walls." The remainder of the Cloacinidae was accepted as treated by Popova (1960). Yamaguti (1961) following Chitwood (1950), recognized Cyathostomum (rather than Trichonema) and proposed Cyathostomidae for the genera included by Popova (1955) in the Trichonematidae. Yamaguti separated the Cyathostomidae into only three subfamilies including the Murshidiinae of Popova (1955) in the Cyathostominae. Chabaud (1965) followed the system proposed by Dougherty (1951), recognizing only three subfamilies: Strongylinae, Oesophagostominae, and Cloacininae. He was the first to restrict the Cloacininae to Australian genera parasitic in marsupials. All previous workers have separated strongyloids into one group with large globular, subglobular, or funnel-shaped buccal capsules and one or more groups with smaller cylindrical or ring-shaped buccal capsules. Table 2 illustrates how the new classification I have proposed (Lichtenfels, 1979) differs from previous systems; circles represent genera of the Strongylidae and squares represent genera of the Chabertiidae. The principal differences is that my system does not use the form of the buccal

5 capsule as a basis for the two families, but to help separate subfamilies in each of the two families. Separation of the genera with cylindrical or ring-shaped buccal capsules into subfamilies was practically impossible using the previous systems and keys. Additional characters were needed to recognize natural groups and to construct a classification reflecting evolutionary patterns. Additional characters THE NEW SYSTEM As indicated above, the outstanding features of the Strongylida are the copulatory bursa of the male and the muscular ovejector of the female. These characters have been used previously to classify the Strongylida at the superfamily level, but have not been used to separate families and subfamilies. Instead, characteristics of the buccal capsule and lips have been used for this purpose. Characteristics of the dorsal ray of the copulatory bursa and of the ovejector can be used to classify the 77 genera and subgenera of Strongyloidea at the level of family and subfamily (Table 2). Furthermore, this new combination of characters greatly facilitates the separation of families and subfamilies (Figs. 2,4) that appear to be natural groups closely correlated with host groups. Ovejectors Two types of ovejectors were found within the Strongyloidea (Fig. 3). Type I ovejectors are usually Y-shaped, but may be opened to a straight line arrangement in the few genera with an anteriorly placed vulva. Type II ovejectors are usually J- shaped with the posterior branch turned anteriorly. Both types of ovejectors consist of three parts: 1) a thick-walled vestibule communicating with the vagina; 2) paired, thick-walled sphincters; and, 3) thinnerwalled infundibula which connect with the uteri. All three parts of the ovejector have a cuticular lining, a middle cellular layer, and CONVENTIONAL APPROACH TO STRONGYLOIDEA 1189 an outer muscular layer. All muscular parts of the ovejector are covered by a fluffy coat about as thick as the muscular layer which may consist of the cell bodies of the muscles. The fluffy coat aids in determining the junctions between the thin-walled infundibula and the uteri. Type I and Type II ovejectors also differ as follows: 1) the vestibule is small and round or slightly Y-shaped in the (Type I) ovejectors, but is larger and often kidneyshaped in the J-shaped (Type II) ovejectors; 2) the sphincters are relatively larger than the vestibule in the Type I ovejectors, but smaller than die vestibule in die Type II ovejectors; and 3) the infundibula are usually similar in size with only slightly thinner walls than the sphincters in the Type I ovejectors, but are usually significantly smaller with much thinner walls than the sphincters in die Type II ovejectors. There is a definite trend among the genera with Type II ovejectors toward increasing relative size and thickness of the kidney-shaped vestibule and reduction of the size and thickness of the sphincters and especially the infundibula. This trend can be illustrated (Fig. 4) in the genera parasitic in rodents: Ransomus of pocket gophers (Thomomys) of North America; Trachypharynx of thryonomyid rats of Africa; and Kuntzistrongylus parasitic in an Asian murid, Rattus coxinga. Dorsal rays Two types of dorsal rays were observed. Type I has three rami on each side of the median fissure, and Type II has two rami on each side of the median fissure. With only eight exceptions among 77 genera and subgenera those with a Type I ovejector (Y-shaped or rarely straight) also have a Type I dorsal ray (three rami on each side); and genera with a Type II ovejector (Jshaped) also have a Type II dorsal ray (two rami on each side) (Fig. 4). Six of the eight exceptions to the correlation between type of ovejector and dorsal ray were the six genera with Y-shaped (Type I) ovejectors in Australian marsupials. Instead of a dorsal ray with three rami on each side as found in almost all other genera with Type I ovejectors, those from Australia have only two

6 1190 J. RALPH LICHTENFELS Uterus Infundibulum Sphincter Vestibule TYPE 1 Y-shape TYPE 2 J-shape OVEJECTORS FIG. 3. Ovejectors: (Type I) Cyathostomum labiatum (Looss, 1902); (Type II) Oesophagostomum (O.) dentatum (After Lichtenfels, 1979). (Scale bars 100 Jim). rami on each side, as illustrated for Phascolostrongylus (Fig. 4). Males of the six genera with Type I ovejectors do differ in a bursal character from the Australian genera with a Type II ovejector, however. The six genera with Type I ovejectors have males with externodorsal rays originating from the dorsal ray, but 17 of 18 genera with Type II ovejectors have males with externodorsal rays originating separately from the dorsal ray (excepting Coroilostrongyiw). Because of the extremely high correlation between ovejector type and dorsal ray type, the possibility of the existence of two distinct groups within the superfamily separated by these characters was considered further. Host groups Excluding the Syngamidae, the Strongyloidea are almost all parasites of mammals. Most of the genera have very few species. They are very host specific and

7 CONVENTIONAL APPROACH TO STRONGYLOIDEA 1191 \/ oooo oooo oooo oooo o BHDD 0 e 0 -PLACENTALS D Pbascolostrongylinae Oesopbagostominae M Cyatbostominae Cbabertiinae B Strongylinae FIG. 4. Dendrogram of evolution of mammalian hosts of some Strongyloidea showing examples of ovejector and dorsal ray types and strongyloid genera by subfamilies (circles and squares) associated with host groups. probably have been associated with their hosts for more than 75 million years (Dougherty, 1951; Schulz, 1952). The evolution of the Strongyloidea is, therefore, closely related to the evolution of mammals. When the 77 genera and subgenera of the Strongyloidea considered herein are superimposed on a dendrogram of mammalian evolution, one finds a striking correlation between nematode morphologic type and host groups (Fig. 4). Nematodes with Type I ovejectors and dorsal rays (shown as squares) are mostly parasitic in Perissodactyla, elephants, and hyraxes (24 genera), and in vombatid and macropodid marsupials (six genera) with a few species of only two Type I genera parasitic in Artiodactyla. One genus has six species scattered in rodents, peccaries, deer and bovids; another genus usually parasitic in elephants, rhinoceroces and tapirs has two species in warthogs. Strongyloidea with Type II ovejectors and dorsal rays (shown as circles) are parasitic in Artiodactyla (ten genera in deer, cattle, sheep, and pigs), macropodid marsupials (19 genera), rodents (six genera), and primates (four genera). Proposed classification A dendrogram of the possible evolution of the Strongyloidea was constructed from the above morphologic comparison of the nematodes and the host relationships described (Fig. 2). Groups of nematodes were presumed to have separated, when their host groups separated. My new system proposed one new genus, Kuntzistrongylus Lichtenfels, 1979; one new family, Chabertiidae (Popova, 1952 subfam.) Lichtenfels, 1979; and one new subfamily, the Phascolostrongylinae Lichtenfels, 1979, for four genera previously included with the Cloacininae. The 87 genera and subgenera (including the Syngamidae and the Deletrocephalidae) are organized into four families. Excluding the ten genera and subgenera of the Syngamidae and the Deletrocephalidae, the remaining 77 genera and subgenera are grouped in two fami-

8 1192 J. RALPH LICHTENFELS lies, each subdivided into three subfamilies characterized as follows. The Strongylinae have large globular, subglobular or funnel-shaped buccal capsules and are parasites of horses, elephants, ostriches or Australian marsupials. The Phascolostrongylinae and the Cyathostominae have small cylindrical buccal capsules. The Phascolostrongylinae have a dorsal ray with 2 rami on each side, and are parasites of the intestine of vombatid and macropodid marsupials. The four genera of this subfamily were previously combined with the Cloacininae which differ in being parasites of the stomach of macropodids and also differ in type of ovejector, and have different origins of the externodorsal rays. The Cyathostominae have a dorsal ray with three rami on each side and are chiefly parasites of Perissodactyla, Proboscidea, and Hyracoidea, rarely tortoises, and with one genus in Artiodactyla and Rodentia. The Chabertiinae have large, thickwalled globular or subglobular buccal capsules, and are parasites of the large intestine of ruminants, primates, rodents, or macropodid marsupials. The Cloacininae and Oesophagostominae have relatively small, thin-walled, cylindrical, funnel-shaped or ring-shaped buccal capsules. The Cloacininae have externodorsal rays with an origin separate from the dorsal ray, an esophagus more than 0.10 of the body length, and are all parasites of the stomach of macropodid marsupials. The Oesophagostominae usually have a transverse cervical groove, externodorsal rays originating from the stem of the dorsal ray, an esophagus usually only about 0.05 of body length, and are parasites of primates, lemurs, rodents, pigs, or ruminants. TESTS OF THE NEW SYSTEM One test of whether a classification system reflects evolutionary relationships is how well it can accommodate new species and genera (Mayr, 1969). During the course of preparing the keys to this system, but after the system was conceived, several opportunities for testing the system became available: 1) Two new genera (Macropicola Mawson, 1978a, and Macroponema Mawson, 1978*) were described; 2) When I ex-- amined the Ancylostomatoidea, subsequent to studying the Strongyloidea, it became obvious that three genera (Agriostomum Railliet, 1902; Hypodontus Monnig, 1929; and Cyclodontostomum Adams, 1933) belonged in the Strongyloidea instead of the Ancylostomatoidea; and 3) During a visit to Moscow, I was able to study two genera (Schulzinema Krastin, 1927 and Bidentostomum Tshoijo, 1957) not previously seen by me and with published descriptions that were inadequate for my needs. In all seven cases the genera new to the system were perfectly accommodated, with each showing complete correlation of ovejector and dorsal ray type. The distribution of some other groups of parasites in mammals is similar to that found in the present study, thereby adding credibility to the conclusion that the proposed families are natural groups. The Anoplocephalata, considered to be an ancient group of cestodes, are parasitic in reptiles, mammals, and birds. According to Cameron (1964) the genus Anoplocephala with a primitive tubular uterus is found only in the Perissodactyla, Proboscidea, and Hyracoidea. Other genera with a more advanced, reticulate uterus are found in Artiodactyla and in Holarctic rodents. The distribution of the Trichostrongyloidea presents a similar separation of parasites of Perissodactyla, Proboscidea, and Hyracoidea from those of Artiodactyla, rodents, primates, and Australian marsupials. The Trichostrongyloidea are not found in Perissodactyla, Proboscidea, and Hyracoidea, but are well represented in the Artiodactyla, rodents and primates with a few in Australian marsupials (Cameron, 1964; Durette-Desset andchabaud, 1977). Additional tests of the new classification are planned. Because the separation of the subfamilies is based almost exclusively on the shape of the buccal capsule, considerable, work is needed to determine whether diey represent separate evolutionary lines within the two families. The cladistic methods of Hennig (1966) may provide some insight into this question. A comparison of proteins within and

9 among genera may provide an interesting test of subfamily groupings made primarily on the basis of morphology. Dvoinos (1978) has proposed in an abstract that some Strongylinae of horses may be more closely related to some Cyathostominae of horses than to other Strongylinae. The comparison of proteins that we plan may provide useful data bearing on this possibility. Avise (1975) has cautioned that overall similarities determined by electrophoresis may be of little value much beyond the generic level. However, Snyder (1977) obtained useful information with sodium dodecyl sulfate electrophoresis in a study of a superfamily of bees. He recommends this approach only for well-studied groups. The strongyloid nematodes of horses are such a group (Lichtenfels, 1975). DISCUSSION AND CONCLUSIONS CONVENTIONAL APPROACH TO STRONGYLOIDEA 1193 This approach to classifying this Strongyloidea must be considered traditional, conventional, and/or classical because it began with a study of previous classifications to find characters previously determined to be useful in delimiting natural groups (Mayr, 1969). The characters selected (ovejector type and dorsal ray type) to be used in helping to separate the 77 genera and subgenera into two groups had previously been useful for characterizing the Order Strongylida and for separating superfamilies (Schulz, 1952; Dougherty, 1951). These characters meet several tests or standards proposed by Mayr (1969) for characters to be assigned high weight. They are complex and are thus probably well integrated into the genome and are probably controlled by a large number of genes. They show constancy throughout many species and, because the ovejectors and dorsal rays are probably not concerned with special habits they are likely to be the product of an integrated genome. Conversely, shape and size of the buccal capsule are characters that are concerned with special habits. Several examples of convergence in the form of the buccal capsule are known in this group of nematodes. Perhaps the most interesting is that of the buccal capsule of Hypodontus macropi Monnig, 1929 which closely resembles those ofancyclostomatoids, except that the buccal capsule of Hypodontus is a mirror image of those of the ancylostomatoids. Inglis (1968) and Beveridge (1979) agreed that Hypodontus resembled the ancylostomatoids because of convergence rather than because of phyletic relationship. It was only after the development of the new classification for the Strongyloidea, however, that Hypodontus was correctly placed in the Strongylinae because of its possession of a Y-shaped strongyloid ovejector, a preanal vulva, a dorsal ray typical of other Australian strongyloids, three similar teeth in the esophageal funnel, and its occurrence in the large intestine of its host. Cameron (1964) also divided the Strongyloidea into two evolutionary lines: 1) the Sclerostomes in Perissodactyla, elephants, and kangaroos, with a few in ostriches, rhea, and tortoises, and with the entire group having elaborate mouth capsules and numerous branches of the dorsal ray; and 2) the Oesophagostomes in Artiodactyla and some in primates, with a more simple buccal capsule and dorsal ray. I believe he was wrong in relating the bulk of the genera in Australian marsupials to those in Perissodactyla and elephants, and he gave no details of his study, but his recognition of two major groups, one in Perissodactyla and elephants and a second in Artiodactyla and primates, is quite similar to the results of my own study (Fig. 2). Coincidentally the family level rankings assigned to the two groups defined by ovejector type, dorsal ray type and host group agree with the rankings recommended by Hennig (1966) for groups separated in the early Cretaceous. Rankings were assigned very conservatively for two reasons: 1) Separations of subfamilies are based only on morphological differences and additional characteristics are needed to test the validity of the subfamily groups; 2) the preservation of as many familiar groups as possible should help win acceptance of the new classification. In conclusion, I believe the new system provides the first classification of the Strongyloidea that delimits morphologically at the family level natural groups that are correlated closely with host groups. The new

10 1194 J. RALPH LICHTENFELS classification should have significantly improved predictive value for this group of important parasites of livestock. Like Mayr (1969), I look forward to the incorporation of the best of various methods into a synthetic approach. Symposia like this one may move us toward that goal. REFERENCES Anderson, R. C, A. G. Chabaud, and S. Willmott. (eds.) CIH keys to the nematode parasites of vertebrates. No. 1. Commonwealth Agricultural Bureaux, England. Avise, J. C Systematic value of electrophoretic data. Syst. Zool. 23: Beveridge, I Hypodontus macropi Monnig, 1929, a hookworm-like parasite of macropodid marsupials. (In press). Cameron, T. W. M Host specificity and the evolution of helminthic parasites. Adv. Parasitol. 2:1-34. Chabaud, A. G Odre des Strongylida. In P. P. Grasse (ed.), Traite de Zoologie, Vol. 4 (fasc. 3), pp Masson et Cie, Paris. Chabaud, A. G Keys to subclasses, orders and superfamilies. In R. C. Anderson, A. G.Chabaud, and S. Willmott (eds.), CIH keys to the nematode parasites of vertebrates, No. 1, pp Commonwealth Agricultural Bureaux, England. Chitwood, B. G An outline classification of the Nematoda. In B. G. Chitwood and M. B. Chitwood (eds.), An introduction to nematology, pp Monumental Printing Co., Baltimore. (Reprinted 1974, University Park Press, Baltimore.) Dougherty, E. C Evolution of zooparasitic groups in the Phylum Nematoda, with special reference to host-distribution. J. Parasitol. 37: Durette-Desset, M. C. and A. G. Chabaud Essai de classification des Nematodes Trichostrongyloidea. Ann. Parasitol. 52: Dvoinos, G. M [Suggested foundation system for strongyloids of horses.] In Russian. Short Communications. Fourth International Congress of Parasitology, Warsaw, August Section A, p. 47 (Abstr.) Hennig, W Phylogenetic systematics. University of Illinois Press, Urbana, 111. Inglis, W. G The geographical and evolutionary relationships of Australian trichostrongylid parasites and their hosts. J. Linnean Soc. (Zool.), 47: Lichtenfels, J. R Helminths of domestic equids. Illustrated keys to genera and species with emphasis on North American forms. Proc. Helminthol. Soc. Wash. 42 (Special issue): Lichtenfels, J. R Keys to genera of the Superfamily Strongyloidea. In R. C. Anderson, A. G. Chabaud and S. Willmott (eds.), CIH keys to the nematode parasites of vertebrates, No. 7. Commonwealth Agricultural Bureaux, England. Mayr, E Principles of systematic zoology. Mc- Graw-Hill, St. Louis. Mclntosh, A The generic and trivial names of the species of nematodes parasitic in the large intestine of equines. commonly known from 1831 to 1900 as Strongylus tetracanthus Mehlis, Proc. Helminthol. Soc. Wash. 18: Popova, T. I Strongyloids of animals and man. (In Russian.) Osnovy Nematodologii, Vol. 5. Akad. Nauk SSSR, Moscow. (English translation, 1964, N.T.I.S., U.S. Dept. Commerce, Springfield, Va., USA.) Popova, T. I Strongyloids of animals and man. Trichonematidae. (In Russian.) Osnovy Nematodologii, Vol. 7. Akad. Nauk SSSR, Moscow. (English translation, 1965, N.T.I.S., U.S. Dept. Commerce, Springfield, Va., USA.) Popova, T. I [Strongyloids of animals and man. Cloacinidae, Stephanuridae, Diaphanocephalidae.] (In Russian.) Osnovy Nematodologii, Vol. 9. Akad. Nauk SSSR, Moscow. Schulz, R. S Phytogeny of strongylates. In K. I. Skrjabin (ed.), Key to parasitic nematodes, Vol. 3, Strongylata, pp Akad. Nauk SSSR, Moscow. (English translation, 1961, N.T.I.S., U.S Dept. Commerce, Springfield, Va., USA.) Snyder, T. P A new electrophoretic approach to biochemical systematics of bees. Biochem. Syst. Ecol. 5: Yorke, W. and P. A. Maplestone The nematode parasites of vertebrates. J. & A. Churchill, London. Yamaguti, S The nematode parasites of vertebrates. In Systema Helminthum, Vol. 3. Interscience Publishers, Inc., New York.