Rats and the city: Implications of urbanization on zoonotic disease risk in Southeast Asia.

Urbanization is rapidly transforming much of Southeast Asia, altering the structure and function of the landscape, as well as the frequency and intensity of the interactions between people, animals, and the environment. In this study, we explored the impact of urbanization on zoonotic disease risk by simultaneously characterizing changes in the ecology of animal reservoirs (rodents), ectoparasite vectors (ticks), and pathogens across a gradient of urbanization in Kuching, a city in Malaysian Borneo. We sampled 863 rodents across rural, developing, and urban locations and found that rodent species diversity decreased with increasing urbanization-from 10 species in the rural location to 4 in the rural location. Notably, two species appeared to thrive in urban areas, as follows: the invasive urban exploiter Rattus rattus (n = 375) and the native urban adapter Sundamys muelleri (n = 331). R. rattus was strongly associated with built infrastructure across the gradient and carried a high diversity of pathogens, including multihost zoonoses capable of environmental transmission (e.g., Leptospira spp.). In contrast, S. muelleri was restricted to green patches where it was found at high densities and was strongly associated with the presence of ticks, including the medically important genera Amblyomma, Haemaphysalis, and Ixodes. Our analyses reveal that zoonotic disease risk is elevated and heterogeneously distributed in urban environments and highlight the potential for targeted risk reduction through pest management and public health messaging.

Duplication and divergence of the retrovirus restriction gene Fv1 in Mus caroli allows protection from multiple retroviruses.

Viruses and their hosts are locked in an evolutionary race where resistance to infection is acquired by the hosts while viruses develop strategies to circumvent these host defenses. Forming one arm of the host defense armory are cell autonomous restriction factors like Fv1. Originally described as protecting laboratory mice from infection by murine leukemia virus (MLV), Fv1s from some wild mice have also been found to restrict non-MLV retroviruses, suggesting an important role in the protection against viruses in nature. We surveyed the Fv1 genes of wild mice trapped in Thailand and characterized their restriction activities against a panel of retroviruses. An extra copy of the Fv1 gene, named Fv7, was found on chromosome 6 of three closely related Asian species of mice: Mus caroli, M. cervicolor, and M. cookii. The presence of flanking repeats suggested it arose by LINE-mediated retroduplication within their most recent common ancestor. A high degree of natural variation was observed in both Fv1 and Fv7 and, on top of positive selection at certain residues, insertions and deletions were present that changed the length of the reading frames. These genes exhibited a range of restriction phenotypes, with activities directed against gamma-, spuma-, and lentiviruses. It seems likely, at least in the case of M. caroli, that the observed gene duplication may expand the breadth of restriction beyond the capacity of Fv1 alone and that one or more such viruses have recently driven or continue to drive the evolution of the Fv1 and Fv7 genes.

Ecological factors shaping the ectoparasite community assembly of the Azara's Grass Mouse, Akodon azarae (Rodentia: Cricetidae).

Parasites are integral members of the global biodiversity. They are useful indicators of environmental stress, food web structure and diversity. Ectoparasites have the potential to transmit vector-borne diseases of public health and veterinary importance and to play an important role in the regulation and evolution of host populations. The interlinkages between hosts, parasites and the environment are complex and challenging to study, leading to controversial results. Most previous studies have been focused on one or two parasite groups, while hosts are often co-infected by different taxa. The present study aims to assess the influence of environmental and host traits on the entire ectoparasite community composition of the rodent Akodon azarae. A total of 278 rodents were examined and mites (Mesostigmata), lice (Phthiraptera), ticks (Ixodida) and fleas (Siphonaptera) were determined. A multi-correspondence analysis was performed in order to analyze interactions within the ectoparasite community and the influence of environmental and host variables on this assembly. We found that environmental variables have a stronger influence on the composition of the ectoparasite community of A. azarae than the host variables analyzed. Minimum temperature was the most influential variable among the studied. In addition, we found evidence of agonistic and antagonistic interactions between ticks and mites, lice and fleas. The present study supports the hypothesis that minimum temperature plays a major role in the dynamics that shape the ectoparasite community of A. azarae, probably through both direct and indirect processes. This finding becomes particularly relevant in a climate change scenario.

Development and standardization of a specific real-time PCR assay for the rapid detection of Candida auris.

Candida auris is an emerging multiresistant pathogen causing nosocomial fungal infection. Specific detection and identification are necessary. Our goal is to develop a new qPCR system that enables rapid detection of C. auris, based on a GPI (glycosyl-phosphatidylinositol) protein-encoding gene. This system is reproducible and sensitive with a limit of detection of 13 C. auris CFU/qPCR reaction. The 100% specificity of this system is confirmed on 2073 clinical and environmental samples, 50 different bacterial species, and 9 Candida spp. (70 strains). This system is suitable to correctly identify C. auris infections and to trace its source.

Was the COVID-19 pandemic avoidable? A call for a "solution-oriented" approach in pathogen evolutionary ecology to prevent future outbreaks.

Concerns about the prospect of a global pandemic have been triggered many times during the last two decades. These have been realised through the current COVID-19 pandemic, due to a new coronavirus SARS-CoV2, which has impacted almost every country on Earth. Here, we show how considering the pandemic through the lenses of the evolutionary ecology of pathogens can help better understand the root causes and devise solutions to prevent the emergence of future pandemics. We call for better integration of these approaches into transdisciplinary research and invite scientists working on the evolutionary ecology of pathogens to contribute to a more "solution-oriented" agenda with practical applications, emulating similar movements in the field of economics in recent decades.

Distinct spread of DNA and RNA viruses among mammals amid prominent role of domestic species.

AIM: Emerging infectious diseases arising from pathogen spillover from mammals to humans constitute a substantial health threat. Tracing virus origin and predicting the most likely host species for future spillover events are major objectives in One Health disciplines.We assessed patterns of virus sharing among a large diversity of mammals, including humans and domestic species. LOCATION: Global. TIME PERIOD: Current. MAJOR TAXA STUDIED: Mammals and associated viruses. METHODS: We used network centrality analysis and trait-based Bayesian hierarchical models to explore patterns of virus sharing among mammals. We analysed a global database that compiled the associations between 1,785 virus species and 725 mammalian host species as sourced from automatic screening of meta-data accompanying published nucleotide sequences between 1950 and 2019. RESULTS: We show that based on current evidence, domesticated mammals hold the most central positions in networks of known mammal-virus associations. Among entire host-virus networks, Carnivora and Chiroptera hold central positions for mainly sharing RNA viruses, whereas ungulates hold central positions for sharing both RNA and DNA viruses with other host species. We revealed strong evidence that DNA viruses were phylogenetically more host specific than RNA viruses. RNA viruses exhibited low functional host specificity despite an overall tendency to infect phylogenetically related species, signifying high potential to shift across hosts with different ecological niches. The frequencies of sharing viruses among hosts and the proportion of zoonotic viruses in hosts were larger for RNA than for DNA viruses. MAIN CONCLUSIONS: Acknowledging the role of domestic species in addition to host and virus traits in patterns of virus sharing is necessary to improve our understanding of virus spread and spillover in times of global change. Understanding multi-host virus-sharing pathways adds focus to curtail disease spread.

The diversity and distribution of chigger mites associated with rodents in the South African savanna.

Chigger mites (Trombiculidae) are temporary habitat-specific ectoparasites that often occur on rodents. Little ecological data are available on chiggers associated with rodents in South Africa. The study aims were to (1) record the chigger species associated with rodents in the savanna, (2) assess if chigger species display parasitope preference on the rodent body and (3) compare the distribution of chigger species in natural, agricultural and urban habitats. Rodents (n = 314) belonging to eight genera were trapped in the savanna biome during 2014 and 2015. Twelve chigger species, of which five are recently described species, were recorded from 161 rodent hosts. The data include three new country locality records. Microtrombicula mastomyia was the most prevalent species across sampling seasons and habitat types. Significant parasitope preference was recorded for two species, with the ear, face and tail base some of the preferred attachment sites. Sampling season and habitat type had a significant effect on chigger communities with summer and agricultural habitats recording the highest species richness, while the highest species diversity was recorded in natural habitats. The study contributes to our current knowledge regarding rodent-associated chigger diversity and distribution in South Africa and further highlights the importance of environmental characteristics in shaping chigger communities.

Intestinal parasites in rural communities in Nan Province, Thailand: changes in bacterial gut microbiota associated with minute intestinal fluke infection.

Gastrointestinal helminth infection likely affects the gut microbiome, in turn affecting host health. To investigate the effect of intestinal parasite status on the gut microbiome, parasitic infection surveys were conducted in communities in Nan Province, Thailand. In total, 1047 participants submitted stool samples for intestinal parasite examination, and 391 parasite-positive cases were identified, equating to an infection prevalence of 37.3%. Intestinal protozoan species were less prevalent (4.6%) than helminth species. The most prevalent parasite was the minute intestinal fluke Haplorchis taichui (35.9%). Amplicon sequencing of 16S rRNA was conducted to investigate the gut microbiome profiles of H. taichui-infected participants compared with those of parasite-free participants. Prevotella copri was the dominant bacterial operational taxonomic unit (OTU) in the study population. The relative abundance of three bacterial taxa, Ruminococcus, Roseburia faecis and Veillonella parvula, was significantly increased in the H. taichui-infected group. Parasite-negative group had higher bacterial diversity (α diversity) than the H. taichui-positive group. In addition, a significant difference in bacterial community composition (ß diversity) was found between the two groups. The results suggest that H. taichui infection impacts the gut microbiome profile by reducing bacterial diversity and altering bacterial community structure in the gastrointestinal tract.

Emerging diseases, livestock expansion and biodiversity loss are positively related at global scale.

Infectious diseases, biodiversity loss and livestock expansion are increasing globally, and examining patterns that link them is important for both public health and conservation. This study is a first attempt to analysis globally these patterns using General additive modelling and Structural equation modelling. A positive association between the number of infectious and parasitic diseases recorded in humans and the total number of animal species between nations was observed. A similar positive association between the number of outbreaks of human infectious diseases, corrected for the number of surveys, and the number of threatened animal species, corrected for the number of animal species, suggests that outbreaks of human infectious diseases are linked with threatened biodiversity. Results of the analyses over the longest period of the dataset (2000-2019) showed a positive correlation between the increasing number of cattle and the number of threatened species, a positive correlation between the increasing number of cattle and the number of outbreaks of human diseases, and a lack of correlation between the number of outbreaks and the number of threatened animal species. As a result, the growing importance of livestock on the planet, while threatening biodiversity, increasingly puts human and animal health at risk. This study calls for further analyses on the consequences of livestock expansion, which depends on several factors that vary by country, namely the growth of human population, changes in diet linked to the westernization of habits, agricultural industrialization and the integration into the world trade, but also the cultural values of livestock.

Helminth fauna of small mammals from public parks and urban areas in Bangkok Metropolitan with emphasis on community ecology of infection in synanthropic rodents.

In 2018, extensive field studies of diversity and prevalence of helminth infection in synanthropic rodents and non-rodent small mammals from public parks and citified areas in the Bangkok Metropolitan were conducted. Rattus rattus complex was the dominant small mammal in public parks. Of the 197 animals, 147 individuals were infected with one or more species of helminths, yielding an infection prevalence of 74.6%. Twenty-five species of helminths were recovered during necropsy. Pterygodermatites tani was the most prevalent (36.2%); other encountered species included Raillietina celebensis, Hydatigera taeniaformis (metacestode in liver tissue), Gongylonema neoplasticum and Hymenolepis diminuta. Different helminth assemblages infected three different host taxa, i.e. synanthropic Rattus spp., Tupaia belangeri (Northern treeshrew) and Suncus murinus (Asian house shrew). Nine species of possible zoonotic helminths were identified. The focus on synanthropic rats influenced the findings of helminth diversity by either host intrinsic or extrinsic factors. A significant positive correlation was found between host body mass and helminth species richness. Greater helminth species richness was found in rats from public parks compared with animals from citified areas (e.g. inside buildings or offices). Also, helminth species richness was negatively correlated with the proportion of post-flooding/rain-fed land. These results provide essential information for assessing the incidence of potential zoonotic health threats in Bangkok and updating research in parasite ecology.

Out of Southern East Asia of the Brown Rat Revealed by Large-Scale Genome Sequencing.

The geographic origin and migration of the brown rat (Rattus norvegicus) remain subjects of considerable debate. In this study, we sequenced whole genomes of 110 wild brown rats with a diverse world-wide representation. We reveal that brown rats migrated out of southern East Asia, rather than northern Asia as formerly suggested, into the Middle East and then to Europe and Africa, thousands of years ago. Comparison of genomes from different geographical populations reveals that many genes involved in the immune system experienced positive selection in the wild brown rat.

Changing landscapes of Southeast Asia and rodent-borne diseases: decreased diversity but increased transmission risks.

The reduction in biodiversity from land use change due to urbanization and agricultural intensification appears to be linked to major epidemiological changes in many human diseases. Increasing disease risks and the emergence of novel pathogens result from increased contact among wildlife, domesticated animals, and humans. We investigated the relationship between human alteration of the environment and the occurrence of generalist and synanthropic rodent species in relation to the diversity and prevalence of rodent-borne pathogens in Southeast Asia, a hotspot of threatened and endangered species, and a foci of emerging infectious diseases. We used data from an extensive pathogen survey of rodents from seven sites in mainland Southeast Asia in conjunction with past and present land cover analyses. At low spatial resolutions, we found that rodent-borne pathogen richness is negatively associated with increasing urbanization, characterized by increased habitat fragmentation, agriculture cover and deforestation. However, at a finer spatial resolution, we found that some major pathogens are favored by environmental characteristics associated with human alteration including irrigation, habitat fragmentation, and increased agricultural land cover. In addition, synanthropic rodents, many of which are important pathogen reservoirs, were associated with fragmented and human-dominated landscapes, which may ultimately enhance the opportunities for zoonotic transmission and human infection by some pathogens.

Antimicrobial Resistance of Salmonella spp. Isolates and Heavy Metal Traces from Rodent Meat Purchased from Roadside Markets, Central Thailand.

Although game meat consumption is widespread across the globe, involving a great diversity of species in very different ecological and sociocultural environments, the safety of wild meat products is rarely assessed routinely. We conducted a survey to evaluate the safety of two rodents products (Rattus tanezumi and Bandicota indica) purchased from roadside markets in central Thailand. Total aerobic bacteria and Escherichia coli counts measured were above Thai poultry product standards for 83.3% and 100% of the samples, respectively (n = 108), although there was no difference between rat species (analysis of variance [ANOVA], p > 0.05). Salmonella spp. were isolated from 32% of the swabs collected (67/208), including 19 different serovars. All strains were resistant or partially resistant to at least 2 of the 16 antibiotics tested, with levels of resistance varying greatly among antibiotics (e.g., 97% of strains sensitive to ciprofloxacin and 98.5% of strains resistant to cloxacillin). Detectable traces of Cd and Pb were found in 98% and 46% of the samples analyzed, respectively (n = 61). Pb and Cd concentrations measured in the kidneys of R. tanezumi were significantly higher than in the liver and muscles and significantly higher than B. indica muscles and kidneys but not liver (ANOVA, p < 0.05). These results highlight potential health hazards that may be associated with rodent-meat consumption, including contamination by coliform bacteria, multiresistant Salmonella spp. strains, and heavy metals. The significance of these results for public health cannot be determined precisely in the absence of appropriate standards, and information gaps remain regarding the frequency of rodent-meat consumption and the origin of bacterial and heavy metal contaminations (i.e., capture environment or during carcass handling and processing). We suggest that appropriate information and training on best hygienic practices for preparing, cooking, and preserving rodent meat should be provided to the producers and to the consumers.

Global spread of helminth parasites at the human-domestic animal-wildlife interface.

Changes in species distributions open novel parasite transmission routes at the human-wildlife interface, yet the strength of biotic and biogeographical factors that prevent or facilitate parasite host shifting are not well understood. We investigated global patterns of helminth parasite (Nematoda, Cestoda, Trematoda) sharing between mammalian wildlife species and domestic mammal hosts (including humans) using >24,000 unique country-level records of host-parasite associations. We used hierarchical modelling and species trait data to determine possible drivers of the level of parasite sharing between wildlife species and either humans or domestic animal hosts. We found the diet of wildlife species to be a strong predictor of levels of helminth parasite sharing with humans and domestic animals, followed by a moderate effect of zoogeographical region and minor effects of species' habitat and climatic niches. Combining model predictions with the distribution and ecological profile data of wildlife species, we projected global risk maps that uncovered strikingly similar patterns of wildlife parasite sharing across geographical areas for the different domestic host species (including humans). These similarities are largely explained by the fact that widespread parasites are commonly recorded infecting several domestic species. If the dietary profile and position in the trophic chain of a wildlife species largely drives its level of helminth parasite sharing with humans/domestic animals, future range shifts of host species that result in novel trophic interactions may likely increase parasite host shifting and have important ramifications for human and animal health.

Advances and challenges in barcoding of microbes, parasites, and their vectors and reservoirs.

DNA barcoding is now a common tool in parasitology and epidemiology, which require good methods for identification not only of parasites and pathogens but vectors and reservoirs. This special issue presents some advances and challenges in barcoding of microbes, parasites, and their vectors and reservoirs. DNA barcoding found new applications in disease ecology, conservation parasitology, environmental parasitology and in paleoparasitology. New technologies such as next-generation sequencing and matrix-assisted laser desorption-ionization time-of-flight have made it now possible to investigate large samples of specimens. By allowing the investigation of parasites at the interface between environment, biodiversity, animal and human health, barcoding and biobanking have important policy outcomes as well as ethics and legal implications. The special issue 'Advances and challenges in the barcoding of parasites, vectors and reservoirs' illustrates some recent advances and proposes new avenues for research in barcoding in parasitology.

Genetic diversity and evolution of Pneumocystis fungi infecting wild Southeast Asian murid rodents.

Pneumocystis organisms are airborne-transmitted fungal parasites that infect the lungs of numerous mammalian species with strong host specificity. In this study, we investigated the genetic diversity and host specificity of Pneumocystis organisms infecting Southeast Asian murid rodents through PCR amplification of two mitochondrial genes and tested the co-phylogeny hypothesis among these fungi and their rodent hosts. Pneumocystis DNA was detected in 215 of 445 wild rodents belonging to 18 Southeast Asian murid species. Three of the Pneumocystis lineages retrieved in our phylogenetic trees correspond to known Pneumocystis species, but some of the remaining lineages may correspond to new undescribed species. Most of these Pneumocystis species infect several rodent species or genera and some sequence types are shared among several host species and genera. These results indicated a weaker host specificity of Pneumocystis species infecting rodents than previously thought. Our co-phylogenetic analyses revealed a complex evolutionary history among Pneumocystis and their rodent hosts. Even if a significant global signal of co-speciation has been detected, co-speciation alone is not sufficient to explain the observed co-phylogenetic pattern and several host switches are inferred. These findings conflict with the traditional view of a prolonged process of co-evolution and co-speciation of Pneumocystis and their hosts.

Detection of Neospora caninum (Toxoplasmatidae) in wild small mammals from Thailand.

The presence of Neospora caninum Dubey, Carpenter, Speer, Topper et Uggla, 1988 in small mammals (i.e. murid rodents, Erinaceomorpha, Eulipotyphla and Scadentia) was explored for first time in South-East Asia. A total of 192 individuals from six localities across Thailand were analysed. A general prevalence of N. caninum of 22% was observed, with some variation among localities (5-36%). Four main types of habitat were included and rodents trapped in dry-land habitat (17 positive among 41 individuals) were more likely to be infected with N. caninum than those from other habitats (forest, rain-fed land and settlement). Rodent species identity and individual rodent weight had no influence on individual infection. Our results provided the first data on the presence of N. caninum in rodents in South-East Asia and first report of N. caninum in the order Scadentia.

Molecular genetic diversity of Gongylonema neoplasticum (Fibiger & Ditlevsen, 1914) (Spirurida: Gongylonematidae) from rodents in Southeast Asia.

More than a dozen Gongylonema spp. (Spirurida: Spiruroidea: Gongylonematidae) have been described from a variety of rodent hosts worldwide. Gongylonema neoplasticum (Fibiger & Ditlevsen, 1914), which dwells in the gastric mucosa of rats such as Rattus norvegicus (Berkenhout) and Rattus rattus (Linnaeus), is currently regarded as a cosmopolitan nematode in accordance with global dispersion of its definitive hosts beyond Asia. To facilitate the reliable specific differentiation of local rodent Gongylonema spp. from the cosmopolitan congener, the genetic characterisation of G. neoplasticum from Asian Rattus spp. in the original endemic area should be considered since the morphological identification of Gongylonema spp. is often difficult due to variations of critical phenotypical characters, e.g. spicule lengths and numbers of caudal papillae. In the present study, morphologically identified G. neoplasticum from 114 rats of seven species from Southeast Asia were selected from archived survey materials from almost 4,500 rodents: Thailand (58 rats), Cambodia (52 rats), Laos (three rats) and Philippines (one rat). In addition, several specimens from four rats in Indonesia were used in the study. Nucleotide sequences of the ribosomal RNA gene (rDNA) (5,649 bp) and the cytochrome c oxidase subunit 1 gene (cox1) (818 bp) were characterised. The rDNA showed little nucleotide variation, including the internal transcribed spacer (ITS) regions. The cox1 showed 24 haplotypes, with up to 15 (1.83%) nucleotide substitutions regardless of parasite origin. Considering that Rattus spp. have been shown to originate from the southern region of Asia and G. neoplasticum is their endogenous parasite, it is reasonable to propose that the present study covers a wide spectrum of the genetic diversity of G. neoplasticum, useful for both the molecular genetic speculation of the species and the molecular genetic differentiation of other local rodent Gongylonema spp. from the cosmopolitan congener.