PHYLOGENY FOR SPECIES OF THE GENUS HAEMONCHUS (NEMATODA: TRICHOSTRONGYLOIDEA): CONSIDERATIONS OF THEIR EVOLUTIONARY HISTORY AND GLOBAL BIOGEOGRAPHY AMONG CAMELIDAE AND PECORA (ARTIODACTYLA)

Authors: Hoberg, Eric; Lichtenfels, James; GIBBONS, LYNDA - ROYAL VET COLLEGE,LONDON

Submitted to: Journal of Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2003
Publication Date: 12/30/2004
Citation: Hoberg, E.P., Lichtenfels, J.R., Gibbons, L. 2004. Phylogeny for species of the genus Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora (Artiodactyla). Journal of Parasitology. 90:1085-1102.

Interpretive Summary: Gastrointestinal parasites, including those that infect domestic sheep and cattle continue to cause in excess of $2 billion dollars in losses annually in the United States, with considerably greater financial impact on a global basis. Large stomach worms, represented by species of the genus Haemonchus are often significant pathogens that occur among a diverse assemblage of artiodactyl hosts including species among 46 genera of Camelidae and ruminants encompassing the Antilocapridae, Giraffidae, Cervidae, and Bovidae. Haemonchus represents the most economically important helminth parasites in cattle, sheep and goats throughout the world. Although the fauna of large stomach worms and species diversity is relatively well documented, we continue to have major gaps in knowledge about host and geographic distribution and global patterns of disease; development of such information is linked elucidation of the coevolutionary and biogeographic associations for species of Haemonchus and their camelid and pecoran ruminant hosts. We conducted the first comprehensive studies of the phylogeny among all known species of Haemonchus. Comparative morphology remains a cornerstone for phylogenetic studies among genera and species of nematodes, particularly where synoptic collections are problematic and incomplete taxon sampling hinders the development of comprehensive databases sufficient for multi-locus molecular analyses across taxa often characterized by high diversity. Comparative morphological studies promote the assessment of a large base of knowledge, and provide the opportunity to continually refine our understanding of structure and homology; ideally the power of morphological and molecular data should be combined synergistically. The first phylogenetic hypothesis for species of Haemonchus has provided the foundation for development of a clear understanding of the history of these economically important nematodes. Some general conclusions for Haemonchus are outlined as follows: (1) origins in Africa with basal diversification in antelopes; (2) colonization and development of core host associations within Antilopinae, Bovinae, Caprinae, Giraffidae, and Camelidae; (3) independent events of colonization for those species in domesticated Camelidae, Bovini, and Caprini (H. placei, H. contortus, H. similis, H. longistipes); and (4) geographically widespread species are represented only by those that have been translocated with domestic stock. Lastly, the North American fauna is characterized by 3 introduced, exotic and highly pathogenic species, H. placei, H. contortus, H. similis, which emphasizes the importance of continued documentation of faunal diversity in the context of predictive foundations derived from phylogenetic studies. Core associations in domesticated hosts are generally geographically widespread, with H. contortus, H. placei and H. similis having essentially cosmopolitan distributions linked to global translocation and introduction of sheep and cattle since the 1500's. Satellite associations for these species, particularly among Cervidae and Camelidae in the Neotropics and Cervidae, Antilocapridae, and possibly wild Caprinae in the Nearctic have been a consequence of introductions and exchange of parasites at historical interfaces for managed and natural ecosystems. Such distributions are emblematic of the overriding significance of anthropogenic factors as determinants of the global distributions of pathogenic parasites in domestic and wild ruminants. Among Haemonchus spp., a predictive classification, improved diagnostics, and an understanding of the relationships among parasites, hosts and geographic regions contribute proactively in defining the potential for dissemination, expansion of populations, and emergence of these pathogenic nematodes globally across tropical and temperate latitudes and at the interface of

Technical Abstract: Phylogenetic analysis of 25 morphological characters among the 12 species of Haemonchus resulted in one most parsimonious tree (59 steps; CI= 0.66, HI= 0.34, RI= 0.78, RC= 0.51). Monophyly for Haemonchus was diagnosed by 3 unequivocal synapomorphies, including, the asymmetric origin of the dorsal ray, relative size of the ventral rays, and the presence of a barb on each spicule tip. Species of Haemonchus have complex histories with respect to host and geographic associations: (1) origins in Africa with basal diversification in antelopes (H. krugeri, H. lawrencei, H. dinniki, H. horaki); (2) independent events of colonization for those species in Caprini and Bovinae (H. contortus, H. placei, H. bedfordi, H. similis); (3) colonization and development of core host associations within Camelidae (H. longistipes), and among Antilopinae, Tragelaphini, and Giraffidae (H. mitchelli, H. okapiae, H. vegliai); and (4) geographically widespread species that are represented only by those that have been translocated with domestic stock. The North American fauna is characterized by 3 introduced and exotic species, H. placei, H. contortus, H. similis, which emphasizes the importance of continued documentation of faunal diversity in the context of predictive foundations derived from phylogenetic studies. Satellite associations for species of Haemonchus, particularly among Cervidae and Camelidae in the Neotropics and Cervidae, Antilocapridae, and possibly wild Caprinae in the Nearctic have been a consequence of introductions and exchange of parasites at historical interfaces for managed and natural ecosystems. Such distributions are emblematic of the overriding significance of anthropogenic factors as determinants of the global distributions for pathogenic parasites in domestic and wild ruminants.