Morphological and molecular analyses of Taenia and Mesocestoides species from red foxes (Vulpes vulpes) in northwestern China

Background The red fox (Vulpes vulpes) is a geographically widespread predator species, occurring across the northern Hemisphere. It has high veterinary-medical significance, in part owing to its definitive host role in the life cycle of several tapeworm species, including zoonotic ones. However, there have been only few reports on cyclophyllid tapeworm (Cestoda: Cyclophyllidea) infection in red foxes from China. Methods In this study, 263 tapeworms were collected from eight road-killed red foxes in Xinjiang Uygur Autonomous Region (XUAR, northwestern China). The tapeworms were analyzed based on morphological characters and mitochondrial cytochrome c oxidase subunit 1 (cox1) gene sequences. Results 83 Taenia and 180 Mesocestoides tapeworms were identified according to the presence or absence of rostellum, and the number, the length and the shape of the large rostellar hooks. The morphological and molecular analyses revealed that i) 180 Mesocestoides tapeworms, here named as Mesocestoides sp. Vulpes vulpes, showed 99.21% (378/381 bp) identity to Mesocestoides sp. reported from red fox in Mongolia; and ii) 83 Taenia tapeworms belonged to three species. The first Taenia species (n = 16, named as Taenia sp. Vulpes vulpes), based on the length of large rostellar hooks (337–342 µm) and its cox1 sequence, was identified as a potentially novel species, which is phylogenetically close to Taenia laticollis. The second species (n = 54, named as Taenia sp. Vulpes vulpes & Rhombomys opimus), was morphologically similar to Taenia endothoracicus according to the number (n = 52), the length (319–332 µm) and the shape of the large rostellar hooks. This species, infecting three red foxes, shared 100% cox1 sequence identity with Taenia sp. Rhombomys opimus genotype C found previously in great gerbils (Rhombomys opimus) in the same region. The third species (n = 13, named as Taenia polyacantha-like), had shorter large rostellar hooks (178–180 µm) and showed 96.27% (361/375 bp) sequence identity to Taenia polyacantha reported from red fox in Italy. In addition, co-infections with two Taenia species and with Taenia and Mesocestoides species were also demonstrated. Conclusions The “great gerbil-red fox” life cycle of Taenia sp. Vulpes vulpes & Rhombomys opimus, belonging to the mitochondrial lineage of T. endothoracicus, is confirmed. The T. polyacantha-like species and Mesocestoides sp. Vulpes vulpes were found for the first time in red fox in China. Taenia sp. Vulpes vulpes is a potentially novel species, which is close to Taenia laticollis based on its phylogenetic properties. The life cycle of Taenia sp. Vulpes vulpes and Mesocestoides sp. Vulpes vulpes should be further explored.

Ecological niche modeling of genetic lineages of the great gerbil, Rhombomys opimus (Rodentia: Gerbillinae)

Great gerbil (Rhombomys opimus Lichtenstein, 1823) is distributed in Central Asia and some parts of the Middle East. It is widely found in central and northeast parts of Iran with two distinct genetic lineages: R. o. sodalis in the northern slopes of the Elburz Mountains and R. o. sargadensis in the southern slopes. This large rodent acts as the main host of natural focal diseases. No study has surveyed the ecological niche of the lineages and how their distribution might be influenced by different climatic variables. To examine the distribution patterns of this murid rodent, we aimed to determine the habitat preferences and effects of environmental variables on the ecological niche. Using a species distribution approach for modeling of regional niche specialization, suitable habitats predicted for R. o. sodalis were mainly located in Golestan province in northern Iran, along the northern slope of Elburz, while R. o. sargadensis, showed great potential distribution along the southern slope of Elburz and around the Kavir Desert and the Lut Desert. Despite the widest potential distribution of R. o. sargadensis from northeast to northwest and through Central Iran, the geographic range of R. o. sodalis was smaller and mostly confined to Golestan province. The results support the presence of the two genetic lineages of Rhombomys in Iran and confirm that there is no significant niche overlap between the two subspecies. Furthermore, it provided several perspectives for future taxonomic studies and prevention hygiene programs for public health.

Demarcation of the Boundaries of the Central Asian Desert Natural Focus of Plague of Kazakhstan and Monitoring the Areal of the Main Carrier, Rhombomys opimus

The aim of the study was to clarify the boundaries of the Central Asian natural plague focus of Kazakhstan and the modern boundaries of the areal of the great gerbil (Rhombomys opimus) in order to improve epizootiological monitoring and increase the effectiveness of preventive (anti-epidemic) measures.Materials and methods. Data from the epizootiological monitoring of the great gerbil populations in 14 autonomous foci of the Central Asian desert natural plague focus in the Republic of Kazakhstan between 2010 and 2020 were used for the analysis. An epizootiologic survey of an area of 875350 km2 was carried out. When processing the data, epidemiological, epizootiological, statistical research methods, as well as GIS technologies were used.Results and discussion. An increase in the total area of the Central Asian desert natural plague focus of the Republic of Kazakhstan by 79710 km2 (9.98 %) has been established for the period of 1990–2020. It is noted that the change in the area of plague-enzootic territory was a consequence of the ever changing areal of the main carrier of plague pathogen – the great gerbil – under the influence of climatic and anthropogenic factors. The most significant changes were found in the southeastern part of the plague-enzootic territory, including those for the Betpakdala (50 %), Balkhash (34.3 %), Taukum (13.3 %) and Mojynkum (0.32 %) autonomous foci. The area of the Aryskum-Dariyalyktakyr autonomous focus decreased by 2100 km2 (4 %). In 2000–2002, new Alakol’sky and Ili intermountain autonomous foci with a total area of 26759 km2 were discovered. It is shown that due to the regression of the Aral Sea, the areal of the great girbil expanded and the area of the North Aral and Kyzylkum natural plague foci increased by 10500 km2 (29.2 %) and 560 km2 (0.4%), respectively. The areas of the Aral-Karakum and UralEmba desert autonomous foci, on the contrary, decreased by 2000 km2 (2.6 %) and 12300 km2 (17.6 %), respectively. Passportization and landscape-epizootiologic zoning of the territory of the Central Asian desert natural plague focus of the Republic of Kazakhstan has been completed.

Polygenic plague resistance in the great gerbil uncovered by population sequencing

Pathogens may elicit a high selective pressure on hosts and can alter genetic diversity over short evolutionary timescales. Intraspecific variation in immune response can be observed as variable survivability from specific infections. The great gerbil (Rhombomys opimus) is a rodent plague host with a heterogenic but highly resistant phenotype. Here, we investigate if the most plague-resistant phenotypes are linked to genomic differences between survivors and susceptible individuals by exposure of wild-caught great gerbils from Northwest China to plague (Yersinia pestis). Whole genome sequencing of ten survivors and ten moribund individuals revealed a low genome-wide mean divergence, except for a subset of genomic regions that showed elevated differentiation. Gene ontology (GO) analysis of candidate genes within regions of increased differentiation, demonstrated enrichment of pathways involved in transcription and translation and their regulation), as well as genes directly involved in immune functions, cellular metabolism and the regulation of apoptosis. Differential RNA expression analysis revealed that the early activated great gerbil immune response to plague consisted of classical components of the innate immune system. Our approach combining challenge experiments with transcriptomics and population level sequencing, provides new insight into the genetic background of plague-resistance and confirms its complex nature, most likely involving multiple genes and pathways of both the immune system and regulation of basic cellular functions.

POPULATIONS OF THE MAJOR CARRIER RHOMBOMYS OPIMUS, VECTORS OF XENOPSYLLA FLEAS AND THE CAUSATIVE AGENT OF YERSINIA PESTIS IN THE CENTRAL ASIAN DESERT NATURAL FOCUS OF PLAGUE

In the Central Asia desert natural focus of plague, the major carrier of the Yersinia pestis agent is the great gerbil Rhombomys opimus, and its vectors include fleas of the Xenopsylla genus. Phenotypical and genotypical properties of the R. opimus populations, Xenopsylla fleas and Yersinia pestis strains have been studied in the Central Asia desert natural focus of plague. Phenotypic distinctions and population discreteness have been identified in R. opimus on the cytochrome b gene of the mitochondrial genome from three autonomous plague foci: Pre-Balkhash, Betpakdala and Pre-Ustyurt. Phenotypic distinctions have been found in Xenopsylla fleas in the Central Asia desert natural focus of plague, and the genotype of X. gerbilli minax fleas on the Cox2 gene of the mitochondrial DNA; these had been captured in the Betpakdala autonomous focus. The repertoire diversity in phenotypical properties of Y. pestis strains from different natural foci of plague has been demonstrated, and population discreteness of Y. pestis strains has been determined using the next-generation sequencing method for single nucleotide polymorphism genes. Results of the study suggest that geographical and environmental isolation and natural selection have led to heterogeneity in the three populations of the great gerbil, vector fleas and Y. pestis.