Morphological Variability and Molecular Identification ofUncinariaspp. (Nematoda: Ancylostomatidae) from Grizzly and Black Bears: New Species or Phenotypic Plasticity?

Abstract

The hookworms Uncinaria rauschi Olsen, 1968 and Uncinaria yukonensis ( Wolfgang, 1956 ) were formally described from grizzly ( Ursus arctos horribilis) and black bears ( Ursus americanus ) of North America. We analyzed the intestinal tracts of 4 grizzly and 9 black bears from Alberta and British Columbia, Canada and isolated Uncinaria specimens with anatomical traits never previously documented. We applied morphological and molecular techniques to investigate the taxonomy and phylogeny of these Uncinaria parasites. The morphological analysis supported polymorphism at the vulvar region for females of both U. rauschi and U. yukonensis. The hypothesis of morphological plasticity for U. rauschi and U. yukonensis was confirmed by genetic analysis of the internal transcribed spacers (ITS-1 and ITS-2) of the nuclear ribosomal DNA. Two distinct genotypes were identified, differing at 5 fixed sites for ITS-1 (432 base pairs [bp]) and 7 for ITS-2 (274 bp). Morphometric data for U. rauschi revealed host-related size differences: adult U. rauschi were significantly larger in black bears than in grizzly bears. Interpretation of these results, considering the historical biogeography of North American bears, suggests a relatively recent host-switching event of U. rauschi from black bears to grizzly bears which likely occurred after the end of the Wisconsin glaciation. Phylogenetic maximum parsimony (MP) and maximum likelihood (ML) analyses of the concatenated ITS-1 and ITS-2 datasets strongly supported monophyly of U. rauschi and U. yukonensis and their close relationship with Uncinaria stenocephala (Railliet, 1884), the latter a parasite primarily of canids and felids. Relationships among species within this group, although resolved by ML, were unsupported by MP and bootstrap resampling. The clade of U. rauschi, U. yukonensis, and U. stenocephala was recovered as sister to the clade represented by Uncinaria spp. from otariid pinnipeds. These results support the absence of strict host-parasite co-phylogeny for Uncinaria spp. and their carnivore hosts. Phylogenetic relationships among Uncinaria spp. provided a framework to develop the hypothesis of similar transmission patterns for the closely related U. rauschi, U. yukonensis, and U. stenocephala.

Ancylostoma ailuropodae n. sp. (Nematoda: Ancylostomatidae), a new hookworm parasite isolated from wild giant pandas in Southwest China

“…Recent epidemiological surveys revealed that some wild animal-derived species of Ancylostoma are emerging as important helminthic zoonotic agents because of rapid urbanization and increased human-wildlife interactions [11, 13–21]. The giant panda, for example, is an endangered and rare wild species in China that has been artificially protected and even partially housed for decades due to habitat loss [33].…”

“…Previously, the hookworm Uncinaria yukonensis (Wolfgang, 1956) was characterized in black bears and Uncinaria rauschi (Olsen, 1968) in grizzly and black bears [81, 82]. On the basis of comparisons of morphometric and distribution data of ursine hookworms as well as the historical biogeography of bears, Catalano et al [13] proposed that there was a relatively recent host-switching event of U. rauschi from black bears to grizzly bears.…”

“…It is noteworthy that nearly all of these species can also be found in wildlife, such as A. duodenale in Crocuta crocuta (Erxleben); A. caninum and A. braziliense in Acinonyx jubatus (Schreber) and Canis mesomelas Schreber; A. ceylanicum in Canis lupus dingo Meyer; A. paraduodenale in Leptailurus serval (Schreber); A. malayanum in Ursus thibetanus G. Cuvier; A. pluridentatum in Puma concolor coryi (Bangs); A. kusimaense in Nyctereutes procyonoides viverrinus Temminck; A. taxideae in Taxidea taxus taxus (Schreber); A. genettae in Genetta genetta (Linnaeus); A. protelesis in Proteles cristata (Sparrman); and A. somaliense in C. mesomelas [5–12]. Although a diverse assemblage of carnivorans is recognized as hosts for Ancylostoma , only one species had been documented or described previously among the Ursidae [7]; species of the distantly related Uncinaria Frölich, 1789, are considered typical in ursine hosts [13]. …”

The diversity and impact of hookworm infections in wildlife

“…The most important hookworm species in black bears is Uncinaria rauschi, which can reach up to 72% prevalence in some areas of Canada (Catalano et al., 2015a, Catalano et al., 2015b). Uncinaria yukonenesis is more common in brown bears in North America, while in Japan brown bears are infected with Ancylostoma malayanum (Catalano et al., 2015a, Catalano et al., 2015b, Asakawa et al., 2006).…”

“…The most important hookworm species in black bears is Uncinaria rauschi, which can reach up to 72% prevalence in some areas of Canada (Catalano et al., 2015a, Catalano et al., 2015b). Uncinaria yukonenesis is more common in brown bears in North America, while in Japan brown bears are infected with Ancylostoma malayanum (Catalano et al., 2015a, Catalano et al., 2015b, Asakawa et al., 2006). The canine hookworm, A. caninum, and the raccoon hookworm, A. lotoris, infect black bears in the southeastern United States; however, the mean intensities are usually low (<15 nematodes per animal) (Crum et al., 1978, Foster et al., 2011).…”