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Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania.

ABSTRACT: Dirofilaria immitis and Dirofilaria repens are mosquito-transmitted zoonotic nematodes, causing heartworm disease and skin lesions, respectively, in carnivores. In Europe, the domestic dog is apparently the main definitive host, but patent infections occur also in other species of carnivores. The rapid spread of the golden jackals (Canis aureus) throughout Europe opens a question of involvement of this species in the sylvatic cycle of pathogens in the colonised territories, including Dirofilaria spp.Between January 2014 and May 2015, 54 golden jackals from 18 localities in Romania were examined by full necropsy for the presence of adult filarioid nematodes and blood samples from all animals were screened for the presence of microfilariae of D. immitis, D. repens and Acanthocheilonema reconditum by multiplex PCR DNA amplification.Nematodes morphologically identified as D. immitis were found in 18.52% of the animals, originating from the southern part of Romania. No D. repens or A. reconditum were found at necropsy. The molecular prevalence in blood samples from the same animals was 9.26% for D. immitis and 1.85% for D. repens. All samples were negative by PCR for A. reconditum.The relatively high prevalence of Dirofilaria spp. infections in golden jackals from Romania together with the increasing density of the jackal populations highlight their potential role in the transmission of these zoonotic parasites and in the maintenance of natural disease foci.

SUBMITTER: Ionica AM

PROVIDER: S-EPMC4848770 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania.

Ionică Angela Monica AM Matei Ioana Adriana IA D'Amico Gianluca G Daskalaki Aikaterini Alexandra AA Juránková Jana J Ionescu Dan Traian DT Mihalca Andrei Daniel AD Modrý David D Gherman Călin Mircea CM

Parasites & vectors 20160428

<h4>Background</h4>Dirofilaria immitis and Dirofilaria repens are mosquito-transmitted zoonotic nematodes, causing heartworm disease and skin lesions, respectively, in carnivores. In Europe, the domestic dog is apparently the main definitive host, but patent infections occur also in other species of carnivores. The rapid spread of the golden jackals (Canis aureus) throughout Europe opens a question of involvement of this species in the sylvatic cycle of pathogens in the colonised territories, in ...[more]

PMID: 27121617

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Project description:Golden jackal (Canis aureus) expansion in the last decades has triggered research interest in Europe. However, jackal phylogeny and taxonomy are still controversial. Morphometric studies in Europe found differences between Dalmatian and the other European jackals. Recent genetic studies revealed that African and Eurasian golden jackals are distinct species. Moreover, large Canis aureus lupaster may be a cryptic subspecies of the African golden jackal. Although genetic studies suggest changes in Canis aureus taxonomy, morphological and morphometric studies are still needed. The present study proposes the first comprehensive analysis on a wide scale of golden jackal skull morphometry. Extensive morphometric data of jackal skulls from Europe (including a very large Bulgarian sample), Asia Minor, and North Africa were analysed, by applying recently developed statistical tools, to address the following questions: (i) is there geographic variation in skull size and shape among populations from Europe, Anatolia and the Caucasus?, (ii) is the jackal population from the Dalmatian coast different?, and (iii) is there a clear distinction between the Eurasian golden jackal (Canis aureus) and the African wolf (Canis lupaster sensu lato), and among populations of African wolves as well? Principal component analysis and linear discriminant analysis were applied on the standardized and log-transformed ratios of the original measurements to clearly separate specimens by shape and size. The results suggest that jackals from Europe, Anatolia and the Caucasus belong to one subspecies: Canis aureus moreotica (I. Geoffroy Saint-Hilaire, 1835), despite the differences in shape of Dalmatian specimens. The present study confirmed morphometrically that all jackals included so far in the taxon Canis aureus sensu lato may represent three taxa and supports the hypothesis that at least two different taxa (species?) of Canis occur in North Africa, indicating the need for further genetic, morphological, behavioural and ecological research to resolve the taxonomic uncertainty. The results are consistent with recent genetic and morphological studies and give further insights on golden jackal taxonomy. Understanding the species phylogeny and taxonomy is crucial for the conservation and management of the expanding golden jackal population in Europe.

Project description:In the first continent-wide study of the golden jackal (Canis aureus), we characterised its population genetic structure and attempted to identify the origin of European populations. This provided a unique insight into genetic characteristics of a native carnivore population with rapid large-scale expansion. We analysed 15 microsatellite markers and a 406 base-pair fragment of the mitochondrial control region. Bayesian-based and principal components methods were applied to evaluate whether the geographical grouping of samples corresponded with genetic groups. Our analysis revealed low levels of genetic diversity, reflecting the unique history of the golden jackal among Europe's native carnivores. The results suggest ongoing gene flow between south-eastern Europe and the Caucasus, with both contributing to the Baltic population, which appeared only recently. The population from the Peloponnese Peninsula in southern Greece forms a common genetic cluster with samples from south-eastern Europe (ΔK approach in STRUCTURE, Principal Components Analysis [PCA]), although the results based on BAPS and the estimated likelihood in STRUCTURE indicate that Peloponnesian jackals may represent a distinct population. Moreover, analyses of population structure also suggest either genetic distinctiveness of the island population from Samos near the coast of Asia Minor (BAPS, most STRUCTURE, PCA), or possibly its connection with the Caucasus population (one analysis in STRUCTURE). We speculate from our results that ancient Mediterranean jackal populations have persisted to the present day, and have merged with jackals colonising from Asia. These data also suggest that new populations of the golden jackal may be founded by long-distance dispersal, and thus should not be treated as an invasive alien species, i.e. an organism that is "non-native to an ecosystem, and which may cause economic or environmental harm or adversely affect human health". These insights into the genetic structure and ancestry of Baltic jackals have important implications for management and conservation of jackals in Europe. The golden jackal is listed as an Annex V species in the EU Habitats Directive and as such, considering also the results presented here, should be legally protected in all EU member states.

Project description:The golden jackal (Canis aureus) is one of the most common and widely distributed carnivores in India but phylogeographic studies on the species have been limited across its range. Recent studies have observed absence of mitochondrial (mt) DNA diversity in European populations while some North African populations of golden jackal were found to carry gray wolf (Canis lupus lupaster) mtDNA lineages. In the present study, we sequenced 440 basepairs (bp) of control region (CR) and 412 bp of cytochrome b (cyt b) gene of mtDNA from 62 golden jackals sampled from India (n = 55), Israel (n = 2) and Bulgaria (n = 5), to obtain a total of eighteen haplotypes, comprising sixteen from India and one each from Israel and Bulgaria. Except for three previously described haplotypes represented by one cyt b and one CR haplotype both from India, and one CR haplotype from Bulgaria, all haplotypes identified in this study are new. Genetic diversity was high in golden jackals compared to that reported for other canids in India. Unlike the paraphyletic status of African conspecifics with the gray wolf, the Indian (and other Eurasian) golden jackal clustered in a distinct but shallow monophyletic clade, displaying no evidence of admixture with sympatric and related gray wolf and domestic dog clades in the region. Phylogeographic analyses indicated no clear pattern of genetic structuring of the golden jackal haplotypes and the median joining network revealed a star-shaped polytomy indicative of recent expansion of the species from India. Indian haplotypes were observed to be interior and thus ancestral compared to haplotypes from Europe and Israel, which were peripheral and hence more derived. Molecular tests for demographic expansion confirmed a recent event of expansion of golden jackals in the Indian subcontinent, which can be traced back ~ 37,000 years ago during the late Pleistocene. Our results suggest that golden jackals have had a potentially longer evolutionary history in India than in other parts of the world, although further sampling from Africa, the Middle East and south-east Asia is needed to test this hypothesis.

Project description:BACKGROUND:Domestic dogs are not native to sub-Saharan Africa, which may account for their susceptibility to Babesia rossi, of which endemic black-backed jackals (Canis mesomelas) are natural reservoirs. There is virtually no information on the occurrence of potentially pathogenic haemogregarines (e.g. Hepatozoon canis) or even rickettsial bacteria (e.g. Ehrlichia spp. and Anaplasma spp.) in indigenous canids in sub-Saharan Africa. Such organisms could pose a risk to domestic dogs, as well as to populations of endangered indigenous canid species. RESULTS:Genomic DNA extracted from blood samples taken from 126 free-ranging and 16 captive black-backed jackals was subjected to reverse line blot (RLB) hybridization assay; 82 (57.8%) specimens reacted only with the Ehrlichia/Anaplasma genera-specific probe. Full-length bacterial 16S rRNA gene of five of these specimens was cloned and the recombinants sequenced. The ten 16S rDNA sequences obtained were most closely related, with approximately 99% identity, to Anaplasma sp. South African Dog, various uncultured Anaplasma spp., as well as various Anaplasma phagocytophilum genotypes. Ninety-one specimens were screened for haemogregarines through PCR amplification using the 18S rRNA gene; 20 (21.9%) specimens reacted positively, of which 14 (15.4%) were confirmed positive for Hepatozoon genotypes from within H. canis. Two (2.2%) specimens were found positive for two different Hepatozoon genotypes. CONCLUSIONS:Sequence analyses confirmed the presence of 16S rDNA sequences closely related to A. phagocytophilum and Anaplasma sp. South African Dog as well as two H. canis genotypes in both free-ranging and captive black-backed jackals. Distinguishing between closely related lineages may provide insight into differences in pathogenicity and virulence of various Anaplasma and H. canis genotypes. By building up a more comprehensive understanding of the range and diversity of the bacteria and eukaryotic organisms (piroplasms and haemogregarines) in the blood of indigenous canids, we may gain insight to such infections in these often-endangered species and the potential for horizontal transmission to and from domestic dogs via ticks where favourable conditions exist.

Project description:BackgroundIn Europe, golden jackals (Canis aureus) have been expanding their range out of the southern and southeastern Balkans towards central Europe continually since the 1960s. Here, we investigated the level of functional diversity at the MHC class II DLA-DQA1 exon 2 in golden jackal populations from Bulgaria, Serbia, and Hungary. Specifically, we tested for positive selection on and geographic variation at that locus due to adaptation to supposedly regionally varying pathogenic landscapes. To test for potential fitness effects of different protein variants on individual body condition, we used linear modeling of individual body mass indexes (bmi) and accounted for possible age, sex, geographical, and climatic effects. The latter approach was performed, however, only on Serbian individuals with appropriate data.ResultsOnly three different DLA-DQA1 alleles were detected, all coding for different amino-acid sequences. The neutrality tests revealed no significant but positive values; there was no signal of spatial structuring and no deviation from the Hardy-Weinberg equilibrium across the studied range of expansion. However, we found a signal of trans-species polymorphism and significant test results for positive selection on three codons. Our information-theory based linear modeling results indicated an effect of ambient temperature on the occurrence of individual DLA-DQA1 genotypes in individuals from across the studied expansion range, independent from geographical position. Our linear modeling results of individual bmi values indicated that yearlings homozygous for DLA-DQA1*03001 reached values typical for adults contrary to yearlings carrying other genotypes (protein combinations). This suggested better growth rates and thus a possible fitness advantage of yearlings homozygous for DLA-DQA1*03001.ConclusionsOur results indicate a demographic (stochastic) signal of reduced DLA-DQA1 exon 2 variation, in line with the documented historical demographic bottleneck. At the same time, however, allelic variation was also affected by positive selection and adaptation to varying ambient temperature, supposedly reflecting geographic variation in the pathogenic landscape. Moreover, an allele effect on body mass index values of yearlings suggested differential fitness associated with growth rates. Overall, a combination of a stochastic effect and positive selection has shaped and is still shaping the variation at the studied MHC locus.

Dataset Information

Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania.

Publications

Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. in Romania.

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