Genetic and spatial characterization of the red fox (Vulpes vulpes) population in the area stretching between the Eastern and Dinaric Alps and its relationship with rabies and canine distemper dynamics

Zecchin, Bianca; Nardi, Marco De; Nouvellet, Pierre; Vernesi, Cristiano; Babbucci, Massimiliano; Crestanello, Barbara; Bagó, Zoltán; Bedeković, Tomislav; Hostnik, Peter; Milani, Adelaide; Donnelly, Christl A.; Bargelloni, Luca; Lorenzetto, Monica; Citterio, Carlo Vittorio; Obber, Federica; Benedictis, Paola De; Cattoli, Giovanni

doi:10.1371/journal.pone.0213515

Cited by 16 publications

(16 citation statements)

References 79 publications

(109 reference statements)

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“…The exact role of foxes in the epidemiology of certain RVA genotypes is currently unknown; however, a rising presence of foxes in urban and semi-urban settings may pose as a risk for disease spillover among humans and animals [12]. Our results indicate a possible role of foxes as RVA reservoirs of a broad range of genotypes usually considered typical of domestic animals and humans.…”

Section: Discussionmentioning

confidence: 71%

“…Among wild animals, red foxes (Vulpes vulpes) are especially interesting since they colonize urban and semi-urban areas and, therefore, may represent a disease spillover risk to human and animal health [12]. So far, the research on RVAs in red foxes comes down to one result obtained by negative-contrast electron microscopy [13] and the recent description of RVA as a causative agent of encephalitis [14].…”

Section: Introductionmentioning

confidence: 99%

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A Remarkable Genetic Diversity of Rotavirus A Circulating in Red Fox Population in Croatia

et al. 2021

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Rotaviruses (RV), especially Rotavirus A (RVA), are globally recognized as pathogens causing neonatal diarrhea, but they also affect intensive animal farming. However, the knowledge on their significance in wildlife is rather limited. The aim of the study was to unveil the prevalence, molecular epidemiology, and genetic diversity of RVA strains circulating in the red fox (Vulpes vulpes) population in Croatia. From 2018 to 2019, 370 fecal samples from fox carcasses hunted for rabies monitoring were collected. All samples were first tested using a VP2 real-time RT-PCR; in the subsequent course, positives were subjected to VP7 and VP4 genotyping. The results revealed an RVA prevalence of 14.9%, while the circulating RVA strains showed a remarkable genetic diversity in terms of 11 G and nine P genotypes, among which one G and three P were tentatively identified as novel. In total, eight genotype combinations were detected: G8P[14], G9P[3], G9P[23], G10P[11], G10P[3], G11P[13], G15P[21], and G?P[?]. The results suggest a complex background of previous interspecies transmission events, shedding new light on the potential influence of foxes in RVA epidemiology. Their role as potential reservoirs of broad range of RVA genotypes, usually considered typical solely of domestic animals and humans, cannot be dismissed.

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Section: Discussionmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

A Remarkable Genetic Diversity of Rotavirus A Circulating in Red Fox Population in Croatia

et al. 2021

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“…[69]). Influencing factors may include variations in host population density, host population dynamics, social, behavioural and spatial ecology (including dispersal, migration and changes in home range sizes), as well as by various other factors including landscape structure, environmental and climatic factors, host(s) life history, and host and pathogen genetic diversity [11, 70–74]. It can be hypothesised that the described epidemiological transitions may have been eased by three successive processes.…”

Section: Discussionmentioning

confidence: 99%

“…Infectious diseases such as sarcoptic mange [7, 63, 92], canine distemper [93–95] and rabies [76] can drive wild canid population dynamics by altering population size, growth rate, animal distribution, migration patterns and genetic diversity [96–98]. Studies on interactions between diseases [99, 100] in wildlife are rare, but comparable interactions between distemper and sarcoptic mange were hypothesized in wolves ( Canis lupus ) in the USA [95] and in Spain [101], while an association between genetic structure of fox population and infection with distemper and rabies was observed in Northern Italy [70]. This study suggests that rabies-related changes in the fox population dynamics affected the dynamics of sarcoptic mange, a phenomenon that has also recently been observed in Estonia [102–104].…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal spread of sarcoptic mange in the red fox (Vulpes vulpes) in Switzerland over more than 60 years: lessons learnt from comparative analysis of multiple surveillance tools

et al. 2019

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Background Sarcoptic mange is a contagious skin disease of wild and domestic mammals caused by the mite Sarcoptes scabiei. Reports of sarcoptic mange in wildlife increased worldwide in the second half of the 20th century, especially since the 1990s. The aim of this study was to provide new insights into the epidemiology of mange by (i) documenting the emergence of sarcoptic mange in the red fox (Vulpes vulpes) in the last decades in Switzerland; and (ii) describing its spatiotemporal spread combining data obtained through different surveillance methods. Methods Retrospective analysis of archived material together with prospective data collection delivered a large dataset from the 19th century to 2018. Methods included: (i) a review of historical literature; (ii) screening of necropsy reports from general health surveillance (1958–2018); (iii) screening of data on mange (1968–1992) collected during the sylvatic rabies eradication campaign; (iv) a questionnaire survey (<1980–2017) and (v) evaluation of camera-trap bycatch data (2005–2018). Results Sarcoptic mange in red foxes was reported as early as 1835 in Switzerland. The first case diagnosed in the framework of the general health surveillance was in 1959. Prior to 1980, sarcoptic mange occurred in non-adjacent surveillance districts scattered all over the country. During the period of the rabies epidemic (1970s-early 1990s), the percentage of foxes tested for rabies with sarcoptic mange significantly decreased in subregions with rabies, whereas it remained high in the few rabies-free subregions. Sarcoptic mange re-emerged in the mid-1990s and continuously spread during the 2000–2010s, to finally extend to the whole country in 2017. The yearly prevalence of mange in foxes estimated by camera-trapping ranged from 0.1–12%. Conclusions Sarcoptic mange has likely been endemic in Switzerland as well as in other European countries at least since the mid-19th century. The rabies epidemics seem to have influenced the pattern of spread of mange in several locations, revealing an interesting example of disease interaction in free-ranging wildlife populations. The combination of multiple surveillance tools to study the long-term dynamics of sarcoptic mange in red foxes in Switzerland proved to be a successful strategy, which underlined the usefulness of questionnaire surveys.

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“…Goldsmith et al [37] also found evidence of fine-scale geographically isolated genetic clusters, but the levels of admixture among these clusters undermined correlations of the host genetic structure of red fox with AR strains. These findings were not surprising given red fox are widely dispersed carnivores, native to much of the northern hemisphere as a matter of their high dispersal capabilities, their generalist nature, the capacity of the species to exhibit a phenotypic plasticity in response to changes in selective pressures, and historical red fox translocations [42][43][44][45][46][47]. The lack of correlation of AR strains with low levels of red fox population genetic structure, may also be related to observations that red fox have expanded their distribution northward, coinciding with Arctic warming, a factor postulated to continue to influence and alter AR dynamics [37,[48][49][50].…”

Section: Introductionmentioning

confidence: 99%

The role of a mechanistic host in maintaining arctic rabies variant distributions: Assessment of functional genetic diversity in Alaskan red fox (Vulpes vulpes)

et al. 2021

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Populations are exposed to different types and strains of pathogens across heterogeneous landscapes, where local interactions between host and pathogen may present reciprocal selective forces leading to correlated patterns of spatial genetic structure. Understanding these coevolutionary patterns provides insight into mechanisms of disease spread and maintenance. Arctic rabies (AR) is a lethal disease with viral variants that occupy distinct geographic distributions across North America and Europe. Red fox (Vulpes vulpes) are a highly susceptible AR host, whose range overlaps both geographically distinct AR strains and regions where AR is absent. It is unclear if genetic structure exists among red fox populations relative to the presence/absence of AR or the spatial distribution of AR variants. Acquiring these data may enhance our understanding of the role of red fox in AR maintenance/spread and inform disease control strategies. Using a genotyping-by-sequencing assay targeting 116 genomic regions of immunogenetic relevance, we screened for sequence variation among red fox populations from Alaska and an outgroup from Ontario, including areas with different AR variants, and regions where the disease was absent. Presumed neutral SNP data from the assay found negligible levels of neutral genetic structure among Alaskan populations. The immunogenetically-associated data identified 30 outlier SNPs supporting weak to moderate genetic structure between regions with and without AR in Alaska. The outliers included SNPs with the potential to cause missense mutations within several toll-like receptor genes that have been associated with AR outcome. In contrast, there was a lack of genetic structure between regions with different AR variants. Combined, we interpret these data to suggest red fox populations respond differently to the presence of AR, but not AR variants. This research increases our understanding of AR dynamics in the Arctic, where host/disease patterns are undergoing flux in a rapidly changing Arctic landscape, including the continued northward expansion of red fox into regions previously predominated by the arctic fox (Vulpes lagopus).

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Genetic and spatial characterization of the red fox (Vulpes vulpes) population in the area stretching between the Eastern and Dinaric Alps and its relationship with rabies and canine distemper dynamics

Cited by 16 publications

References 79 publications

A Remarkable Genetic Diversity of Rotavirus A Circulating in Red Fox Population in Croatia

A Remarkable Genetic Diversity of Rotavirus A Circulating in Red Fox Population in Croatia

Spatiotemporal spread of sarcoptic mange in the red fox (Vulpes vulpes) in Switzerland over more than 60 years: lessons learnt from comparative analysis of multiple surveillance tools

The role of a mechanistic host in maintaining arctic rabies variant distributions: Assessment of functional genetic diversity in Alaskan red fox (Vulpes vulpes)

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