Proc. Helminthol. Soc. Wash. 51(2), 1984, pp. 196-204 Evolution of the Elaphostrongylinae (Nematoda: Metastrongyloidea: Protostrongylidae) Parasites of Cervids (Mammalia) THOMAS R. PLATT Department of Biology, University of Richmond, Richmond, Virginia 23173 ABSTRACT: The phylogenetic relationships of the Elaphostrongylinae were evaluated by cladistic analysis. Ela- phostrongylus cervi is considered the most plesiomorphic member of the subfamily and is the sister-group of Parelaphostrongylus. Parelaphostrongylus, which consists of P. andersoni, P. odocoilei, and P. tenuis, is mono- phyletic based on the presence of crura on the gubernaculum and a bifurcate gubernacular corpus. P. tenuis is the most plesiomorphic member of the genus and is the sister-group of a monophyletic muscleworm lineage composed of P. andersoni and P. odocoilei. Elaphostrongylus cervi originated in the nearctic, cospeciating with Rangifer. The current holarctic distribution of E. cervi is interpreted as colonization of more primitive cervids with the retention of broad coaccommodation within the family. The meningeal worm, P. tenuis, originated prior to the formation of extant species of Odocoileus. Cospeciation of the muscleworm ancestor with the ancestor of the extant species of Odocoileus resulted in P. andersoni in O. virginianus and P. odocoilei in O. hemionus. The extensive distribution of E. cervi, a generalist, can be attributed to its broad coaccommodation within the Cervidae, broad coaccommodation with and the ubiquitous nature of suitable molluscan intermediate hosts, and the absence of competitors in Eurasia. The distribution of P. tenuis, a specialist, in North America is attributed to the success of white-tailed deer and in part to the pathogenic effects of the meningeal worm in sympatric cervids. Two hypotheses for the current distribution of the species of Parelaphostrongylus are presented. The Elaphostrongylinae (Protostrongylidae) onization as an alternative means of parasite ac- comprise a small but economically important quisition. group of nematode parasites of cervids. Although Recent studies of host-parasite evolution and commonly referred to as "lungworms," all species zoogeography have centered exclusively on the of the subfamily inhabit extrapulmonary sites in relationship between the parasite and the defin- the definitive host. Life cycles are complex, and itive host (Brooks, 1977, 1978, 1979b; Brooks terrestrial gastropods are used as obligate inter- et al., 1981; Chabaud and Bain, 1976). The role mediate hosts (see Anderson, 1968 for a review). of intermediate hosts however has not been given Coevolution of parasitic organisms with their equal attention. The following analysis of the hosts has been considered axiomatic. Cameron Elaphostrongylinae includes an evaluation of the (1964) stated, "parasites have obviously evolved role of the intermediate and definitive hosts as co-incidentally with their hosts" and that "par- they relate to the distribution and evolution of asite phylogeny and classification can only be the parasite. interpreted in terms of host phylogeny and clas- Materials and Methods sification." However, Inglis (1965) stated, "evo- lution of most groups of nematodes has tended Specimens of P. odocoilei were obtained from ex- perimentally infected mule deer (Odocoileus h. hem- to occur in hosts with similar ecological require- ionus) as reported by Platt and Samuel (197 8a, b). Spec- ments." Brooks (1979a) recently reexamined the imens of P. tenuis were obtained from naturally infected concept of coevolution and identified two dis- wapiti (Cervus elaphus canadensis) in PennsyJvania. tinct components: coaccommodation, "the mu- Type specimens of P. andersoni were obtained from tual adaptation of a given parasite species and the USNM Helm. Coll., Beltsville, Maryland. Speci- mens of E. cervi were not available, and the description its host through time" and cospeciation, "clado- by Lankester and Northcott (1979) was used as a source genesis of an ancestral parasite species as a result of morphological characters. of or, concomitant with, host cladogenesis." This The direction of change of characters within the Ela- distinction forms an important framework for phostrongylinae was determined through the use of out-group comparison (Hennig, 1966; Wiley, 1981). the study of the evolution of host-parasite sys- As some parasitologists may not be familiar with the tems, as it emphasizes the historical relationship terminology of phylogenetic systematics, the following of host and parasite but does not disregard col- definitions are provided (following Wiley, 1981). Ple- 196 Copyright © 2011, The Helminthological Society of Washington 197 P. andersoni P. odocoilei P. tenuis E. cervi Figure 1. Male reproductive structures of the species of the Elaphostrongylinae. la-d, gubernacula, le-h, spicules. li-1, copulatory bursa. (Fig. b, c, e, f, i, 1, and k, original; Fig. la, redrawn from Prestwood [1972]; Fig. Ig, redrawn from Dougherty, 1945, Parasitology 36:199-208; Fig. Id, h, and 1, redrawn from Lankester and Northcott [1979].) siomorphic and apomorphic refer to the original and state and a 1, -1, or 2 for the apomorphic state. An derived states, respectively, of a pair of homologous outline and explanation for the decision of the deter- characters. Synapomorphies are "evolutionary novel- mination of character state polarity is presented below. ties" (derived characters) shared by two or more species forming a monophyletic group. Autapomorphies are 1. Crura of the gubernaculum.—The gubernaculum of derived characters restricted to a single species. Homo- the majority of the Protostrongylidae (sensu An- plasies are structurally similar characters that are derson, 1978) is complex, consisting of a corpus, thought to be of independent origin. crura, and capitulum. The gubernaculum of the re- As the sister-group of the elaphostrongylines is un- maining metastrongylids is simple, corpus only, or known, members of the Metastrongyloidea, excluding absent. Two states: crura absent (0); crura present the Protostrongylidae, were employed as the out-group. (1) (Fig. la-d). Each character was assigned a 0 for the plesiomorphic 2. Corpus of the gubernaculum.—The corpus is a solid Copyright © 2011, The Helminthological Society of Washington 198 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY Table 1. Data matrix of the character state distribu- however in recognizing P. andersoni and P. ten- tion used in the analysis of the Elaphostrongylinae. uis, which are parasites of white-tailed deer, as a monophyletic group based on the position of Characters the branches of the dorsal ray. A single homo- Species 1 2 3 4 5 6 7 8 plasy, the presence of a compact dorsal ray, is E. cervi 0 0 0 0 0 0 0 1 shared by P. odocoilei and P. andersoni. P. tenuis 1 1 0 1 0 1 0 0 P. andersoni 1 1 1 0 1 1 1 0 Discussion P. odocoilei 1 2 0 0 1 0 -1 0 Although the two cladograms are equally par- simonius based on character distributions, the phylogeny in Figure 2a is preferred based on the piece in nonprotostrongylid members of the Meta- location of the adult worms in the definitive host. strongyloidea. Three states; solid corpus (0); distally Elaphostrongylus cervi, the most plesiomorphic notched corpus (1); distally split corpus (2) (Fig. la- species, has been reported from the meninges of d). the brain (Mitskevitch, 1964) as well as the con- 3. Spicules.—The distal end of the spicules in the ma- nective tissue of the skeletal muscles (Mitske- jority of metastrongylids is solid. Two states: solid (0); bifid (1) (Fig. le-h). vitch, 1964;LankesterandNorthcott, 1979) and 4. Spicular foramen.—A spicular foramen is only found occasionally deep muscle sites (Lankester and in P. tenuis. Two states: absent (0); present (1) (Fig. Northcott, 1979). Species of Parelaphostrongylus Ib). are more restricted in their site of maturation. 5. Shape of the dorsal ray.—The dorsal ray in the ma- jority of nonprotostrongylids (excluding highly spe- Adult P. tenuis have only been found in close cialized forms with marked bursal reduction) is not association with the central nervous system (CNS) compact. Two states: not compact (0); compact bulb (Anderson, 1968). The muscleworms are re- (1) (Fig. li-1). stricted to the skeletal muscles and associated 6. Branches of the dorsal ray.—The branches of the connective tissue (Prestwood, 1972; Platt and dorsal ray in nonprotostrongylids (not exhibiting bursal reduction) are terminally placed. Two states: Samuel, 1978b). Therefore, following the phy- terminal (0); ventral (1) (Fig. li-1). logeny in Figure 2a, habitat specialization is a 7. Location of the dorsal ray.—The dorsal ray in non- direct process requiring no reversals or parallel- protostrongylids (not exhibiting bursal reduction) is isms. In the alternate phylogeny (Fig. 2b) neu- terminal. Three states: terminal (0); ventral (1); dor- rotropic behavior would have been lost in the sal (-1) (Fig. li-1). 8. Perityls.—Nonmovable lips are found in the ma- ancestral Parelaphostrongylus and then reap- jority of metastrongylids. Two states: present (0); peared in P. tenuis, or the muscleworms lost their absent (1). neurotropic behavior independently and P. ten- A summary of the distribution of character states is uis retained the behavior as a plesiomorphic trait. given in Table 1. Both of these scenarios require reversals or par- allel evolution, hence Figure 2a is preferred. Results Strict adherence to the rules of phylogenetic Two equally parsimonius cladograms can be classification (Hennig,