Molecular detection of Cercopithifilaria, Cruorifilaria and Dipetalonema-like filarial nematodes in ticks of French Guiana

Abstract

Filarial nematodes of the Dipetalonema lineage are widespread parasites and include some species that are transmitted by ticks. In this study, we conducted a large molecular survey of ticks in French Guiana, South America, to understand the overall diversity of tick-borne filarioids in this remote region largely covered by dense tropical forests. Out of 682 ticks belonging to 22 species and 6 genera, 21 ticks (3.1%) of the species Amblyomma cajennense, A. oblongoguttatum, A. romitii, Ixodes luciae and Rhipicephalus sanguineus sensu lato were positive for infection by filarioids. Molecular typing and phylogenetic analysis identified all these filarioids as members of the Dipetalonema lineage. While the filarioid of R. sanguineus sensu lato is a previously described species, the canine worm Cercopithifilaria bainae Almeida & Vicente, 1984, all other filarioids detected in this study are related but distinct to already known species in the genera Cercopithifilaria, Cruorifilaria and Dipetalonema. Their vertebrate host range may include a wide variety of mammals present in French Guiana, but dogs, capybaras, and opossums are the best candidate hosts for some of these filarioids. Although the detection of members of the Dipetalonema lineage in ticks of significant medical or veterinary interest is of concern, the risk of contracting a tick-borne filarial infection is still largely unknown. The pathogenicity of these filarioids, their epidemiology, developmental cycles, and mechanisms of transmission by South American tick species now require further study.

Multi-locus sequence analysis unveils a novel genus of filarial nematodes associated with ticks in French Guiana

“…Ticks are vectors of major viruses, bacteria, and protozoan parasites of medical and veterinary significance [24,33,34]. However, surveys of tick-borne pathogens often neglect filarial nematodes from the family Onchocercidae, commonly referred to as filariae or filarioids, while these parasites are regularly detected in most tick genera [1,4,6,10,11,17,29,36,39,43,45,46,50,51]. Microscopic observations and molecular typing consistently categorize most tick-associated filarioids into the genera Acanthocheilonema, Monanema, Yatesia, and Cercopithifilaria [1,4,6,10,11,17,29,35,36,39,43,45,46,50,51], although most were initially classified in the genus Dipetalonema [7,9,23].…”

“…However, surveys of tick-borne pathogens often neglect filarial nematodes from the family Onchocercidae, commonly referred to as filariae or filarioids, while these parasites are regularly detected in most tick genera [1,4,6,10,11,17,29,36,39,43,45,46,50,51]. Microscopic observations and molecular typing consistently categorize most tick-associated filarioids into the genera Acanthocheilonema, Monanema, Yatesia, and Cercopithifilaria [1,4,6,10,11,17,29,35,36,39,43,45,46,50,51], although most were initially classified in the genus Dipetalonema [7,9,23]. Phylogenetic analyses based on molecular and morphological data further showed that the genera Acanthocheilonema, Monanema, Yatesia, and Cercopithifilaria (all associated with ticks), as well as Cruorifilaria (not yet associated with a vector, but detected in ticks [17]), Litomosoides (associated with parasitic mites) and Dipetalonema (associated with biting midges), cluster in a monophyletic clade of filarioids, termed the Dipetalonema lineage or the ONC4 clade, within the family Onchocercidae [7,9,23,36].…”

“…In a recent survey of ticks in French Guiana, South America, molecular analysis and phylogenetic studies revealed the presence of novel filarioids belonging to the Dipetalonema lineage in several tick species [17]. Based on cytochrome c oxidase subunit I (cox1) mitochondrial gene sequences, all but one of these filarioids are distinct to already known species of Dipetalonema lineage.…”

“…Based on cytochrome c oxidase subunit I (cox1) mitochondrial gene sequences, all but one of these filarioids are distinct to already known species of Dipetalonema lineage. Indeed, in the Cayenne tick Amblyomma cajennense (Fabricius, 1787) and in the opossum tick Ixodes luciae Sénevet, 1940, one filarioid, provisionally named Dipetalonema-like (DLF hereafter), showed a cox1 gene sequence substantially divergent from other species and genera of the Dipetalonema lineage [17]. DLF could be of health concern since it was detected in A. cajennense [17], the predominant tick species biting humans in South America [16].…”

“…Indeed, in the Cayenne tick Amblyomma cajennense (Fabricius, 1787) and in the opossum tick Ixodes luciae Sénevet, 1940, one filarioid, provisionally named Dipetalonema-like (DLF hereafter), showed a cox1 gene sequence substantially divergent from other species and genera of the Dipetalonema lineage [17]. DLF could be of health concern since it was detected in A. cajennense [17], the predominant tick species biting humans in South America [16]. This feature may not apply to I. luciae, as it is a specialized tick species with a primary feeding preference for opossums [16].…”