Whence river blindness? The domestication of mammals and host-parasite co-evolution in the nematode genus Onchocerca.
The genus Onchocerca includes 34 described species and represents one of the largest genera of the filarial nematodes within the family Onchocercidae. Representative members of this genus are mainly parasites of ungulates, with some exceptions such as Onchocerca lupi and Onchocerca volvulus, infecting carnivores and/or humans. For a long time, the evolutionary relationships amongst onchocercids remained poorly studied, as the systematics of this genus was impaired by the high morphological variability of species included in the taxon. Although some molecular phylogenies were developed, these studies were mainly focused on bovine Onchocerca spp. and O. volvulus, including assessments of Wolbachia endosymbionts. In the present study, we analysed 13 Onchocerca spp. from a larger host spectrum using a panel of seven different genes. Analysis of the coxI marker supports its usefulness for the identification of species within the genus. The evolutionary history of the genus has been herein revised by multi-gene phylogenies, presenting three strongly supported clades of Onchocerca spp. Analyses of co-evolutionary scenarios between Onchocerca and their vertebrate hosts underline the effect of domestication on Onchocerca speciation. Our study indicates that a host switch event occurred between Bovidae, Canidae and humans. Cophylogenetic analyses between Onchocerca and the endosymbiotic bacterium Wolbachia indicate the strongest co-evolutionary pattern ever registered within the filarial nematodes. Finally, this dataset indicates that the clade composed by O. lupi, Onchocerca gutturosa, Onchocerca lienalis, Onchocerca ochengi and O. volvulus derived from recent speciation.
Unité Molécules de Communication et Adaptation des Microorganismes (MCAM, UMR 7245), Sorbonne Universités, Muséum National d'Histoire Naturelle, CNRS, Paris, France.
Emilie
E
Lefoulon
Department of Veterinary Medicine, Università degli Studi di Bari, Valenzano, Italy.
Alessio
A
Giannelli
Institute of Infection and Global Health, The University of Liverpool, Liverpool, United Kingdom.
Benjamin L
BL
Makepeace
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Sofia, Bulgaria.
Yasen
Y
Mutafchiev
Tropical Parasitic Diseases Unit, Northwick Park Institute for Medical Research, Harrow, Middlesex, United Kingdom.
Simon
S
Townson
Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia.
Shigehiko
S
Uni
Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA, USA.
Guilherme G
GG
Verocai
Department of Veterinary Medicine, Università degli Studi di Bari, Valenzano, Italy.
Domenico
D
Otranto
Unité Molécules de Communication et Adaptation des Microorganismes (MCAM, UMR 7245), Sorbonne Universités, Muséum National d'Histoire Naturelle, CNRS, Paris, France. Electronic address: cmartin@mnhn.fr.
Coralie
C
Martin
D000818:Animals; D000829:Animals, Domestic / Q000235:genetics / Q000469:parasitology*; D000073930:Biological Coevolution; D003576:Electron Transport Complex IV / Q000235:genetics / Q000378:metabolism; D015971:Gene Expression Regulation, Enzymologic; D006801:Humans; D008322:Mammals / Q000469:parasitology*; D009854:Onchocerca / Q000235:genetics* / Q000502:physiology*
D003576:Electron Transport Complex IV
Co-evolution; Diagnostic marker; Domestication; Filariae; Host-switching; Onchocerca; Phylogeny; Wolbachia