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Phylogenetic Systematic Analysis of the Trichostrongylidae (Nematoda), with an Initial Assessment of Coevolution and Biogeography

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Phylogenetic Systematic Analysis of the Trichostrongylidae (Nematoda), with an Initial Assessment of Coevolution and Biogeography University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 12-1994 Phylogenetic Systematic Analysis of the Trichostrongylidae (Nematoda), with an Initial Assessment of Coevolution and Biogeography Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected] J. Ralph Lichtenfels United States Department of Agriculture, Agricultural Research Service Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Biodiversity Commons, Evolution Commons, and the Parasitology Commons Hoberg, Eric P. and Lichtenfels, J. Ralph, "Phylogenetic Systematic Analysis of the Trichostrongylidae (Nematoda), with an Initial Assessment of Coevolution and Biogeography" (1994). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 723. https://digitalcommons.unl.edu/parasitologyfacpubs/723 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 80(6), 1994, p. 976-996 ? AmericanSociety of Parasitologists1994 PHYLOGENETICSYSTEMATIC ANALYSIS OF THE TRICHOSTRONGYLIDAE(NEMATODA), WITH AN INITIALASSESSMENT OF COEVOLUTIONAND BIOGEOGRAPHY E. P. Hoberg and J. R. Lichtenfels UnitedStates Departmentof Agriculture,Agricultural Research Service, Biosystematic Parasitology Laboratory, BARCEast, Building1180, 10300Baltimore Avenue, Beltsville, Maryland 20705-2350 ABSTRACT:Phylogenetic analysis of the subfamiliesof the Trichostrongylidaebased on 22 morphologicaltrans- formationseries produceda single cladogramwith a consistencyindex (CI) = 74.2%.Monophyly for the family was supportedby the structureof the female tail and copulatorybursa. Two major clades are recognized:the Cooperiinaeclade with the basal Cooperiinaeand Libyostrongylinae+ Trichostrongylinae,and the Graphidiinae clade with the basal Graphidiinaeand Ostertagiinae+ Haemonchinae.Dendrograms presented by Durette- Desset (1985) (CI = 56.1%)and Lichtenfels(1987), based on the key to the Trichostrongylidaeby Gibbons and Khalil (1982) (CI = 59.0%),were found to be relatively inefficientin describingcharacter evolution and in supportingputative relationshipsamong the subfamilies.Based on the currentanalysis, the intestine appearsto have constitutedthe ancestralhabitat for the trichostrongylidswith the stomach/abomasumhaving been in- dependentlycolonized in each clade. Assessment of host associationssuggests extensive colonization but also a high degreeof coevolution with Bovidae and Cervidaefor Ostertagiinae+ Haemonchinae.Biogeography for this assemblageis complex, but this analysisis compatiblewith a Palearcticor Eurasianorigin for Cooperiinae, Haemonchinae,and Ostertagiinae. Trichostrongyle nematodes are significant par- Cram, 1927) and more recently by the configu- asites among sylvatic and domesticated rumi- ration of the synlophe and characteristic genital nants. An understanding of phylogenetic rela- structures (Durette-Desset and Chabaud, 1977, tionships of these nematodes has a bearing on 1981; Durette-Desset, 1983; Gibbons and Kha- elucidating aspects of host associations, parasite lil, 1982, 1983). behavior (including pathogenesis), epidemiolo- The family has received extensive attention gy, evolution, and biogeographic history. These since it was established, e.g., Yorke and Maple- nematodes may also prove to be exceptionally stone (1926), Baylis and Daubney (1926), and useful in defining the distributional history for has been reviewed in detail by Travassos (1937), ruminants in the Holarctic, e.g., Dr6zdz (1967) Skrjabin et al. (1952, 1954), Durette-Desset and and Hoberg et al. (1993a). Chabaud (1977, 1981), Gibbons and Khalil The superfamily Trichostrongyloidea Cram, (1982) and Durette-Desset (1983, 1985). The first 1927 constitutes one of the most diverse and synoptic treatment of the family was presented complex taxa within the Strongylida or bursate by Travassos (1937) whose classification of the nematodes (Durette-Desset, 1983, 1985). Al- Trichostrongylidae contained 13 subfamilies. though not adopted in the present study, recently This represented a rather broad concept for the it has been proposed that this taxon be elevated trichostrongylids and included many taxa later to subordinal rank as the Trichostrongylina (see referred to other families and subfamilies of the Durette-Desset and Chabaud, 1993). Among the Trichostrongyloidea (see Durette-Desset, 1983). trichostrongyloids, the family Trichostrongyli- More restrictive concepts for the trichostrongyl- dae Leiper, 1912 represents groups of consider- oids were developed by Skrjabin et al. (1952, able veterinary importance as parasites of ru- 1954) who recognized 15 subfamilies and 18 minants, other mammals, and avian hosts. These tribes within the Trichostrongylidae. The cur- nematodes are typically monoxenous and occur rently accepted taxonomy for the family followed in the intestine or stomach of their terrestrial from the first exhaustive studies of the genital vertebrate hosts. Morphologically these taxa were cone and copulatory bursa (Andreeva, 1958; originally defined by a reduced buccal capsule Chabaud, 1959; Chabaud et al., 1970; Gibbons and distinctive copulatory bursa (Leiper, 1912; and Khalil, 1983) and synlophe (Durette-Desset and Chabaud, 1977). Trichostrongylidae accord- ing to Durette-Desset and Chabaud (1977, 1981), Received 14 March 1994; revised 25 May 1994; ac- Gibbons and Khalil (1982), and Durette-Desset cepted 25 May 1994. (1983) is now considered to contain 6 subfami- 976 HOBERGAND LICHTENFELS-TRICHOSTRONGYLIDAEPHYLOGENY 977 lies including 4 economically significant groups: tenfels (1987) from the keys presented by Gib- Trichostrongylinae Leiper, 1908, Ostertagiinae bons and Khalil (1982) considered a broader ar- Lopez-Neyra, 1947, Haemonchinae Skrjabin and ray of characters and 2 rather than 3 major Shul'ts, 1952, Cooperiinae Skrjabin and Shik- lineages were recognized. An evaluation of these hobalova, 1952, and the relatively minor Libyo- hypotheses revealed concepts of relationships strongylinae Durette-Desset and Chabaud, 1977, among taxa that were developed from assess- and Graphidiinae Travassos, 1937. ments of single characters, overall morphological Although Gibbons and Khalil (1982) and Dur- similarity, or unique combinations of shared ette-Desset (1983) both recognized 6 subfami- primitive characters. Although each of the lies, there was discordance between these clas- subfamilies was recognized, the reliability of con- sifications with respect to the numbers of genera clusions about phylogeny of the trichostrongylids recognized, particularly within the Ostertagiinae and relationships among the subfamilies were (see Lichtenfels and Hoberg, 1993) and to their equivocal (Jansen, 1989; Hoberg and Lichten- placement at the level of subfamily. The appar- fels, 1992; Hoberg et al., 1993b). ent disparity resulted largely from conclusions In the present study, phylogenetic analyses derived from the evaluation of 2 different sets of (Hennig, 1966; Wiley, 1981) of the Trichostron- morphological characters that were applied to gylidae were initiated to: (1) test monophyly of the construction of taxonomic keys at the generic the family; (2) assess relationships among the level. Concepts of Durette-Desset (1983) were subfamilies; (3) define the relationship of the Os- based primarily on the structure of the copula- tertagiinae and Graphidiinae (see Hoberg et al., tory bursa, whereas those of Gibbons and Khalil 1993b); (4) consider the implications of subfam- (1982) were based on a broader array of struc- ily phylogeny for trends in character evolution; tural attributes (Lichtenfels, 1987). and (5) begin preliminary assessments of host, Although all previous treatments of the tricho- habitat, and biogeographic associations of par- strongylids implied degrees of morphological asites. Results of this study provide the first phy- similarity for inclusive groups of species, genera, logenetic systematic analysis of the Trichostron- tribes, and subfamilies, specific evolutionary hy- gylidae, as an extension of the seminal research potheses for the family were seldom considered. of Chabaud (1959), Durette-Desset and Chabaud The first explicit evolutionary hypothesis for the (1977, 1981), Gibbons and Khalil (1982), and 14 families of the Trichostrongyloidea, including Durette-Desset (1983, 1985, 1992). In as much the Trichostrongylidae, was presented as a den- as systematics forms the foundation for predic- drogram derived from the pioneering studies of tive hypotheses, assessment of the phylogenetic Chabaud (1959), Durette-Desset and Chabaud relationships of the trichostrongylids at the (1977, 1981), and Durette-Desset (1983, 1985). subfamilial level can form the infrastructure for Although Gibbons and Khalil (1982) had not a more refined understanding of nematode be- intended to present a classification, their con- havior, parasite-host coevolution, and biogeog- cepts were summarized by Lichtenfels (1987) in raphy. an attempt to define relationships among the subfamilies. MATERIALSAND METHODS The competing hypotheses outlined by Lich- Phylogeneticanalysis (Hennig,
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