Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries

Background  

Rodents are recognized as hosts for at least 60 zoonotic diseases and may represent a serious threat for human health. In the context of global environmental changes and increasing mobility of humans and animals, contacts between pathogens and potential animal hosts and vectors are modified, amplifying the risk of disease emergence. An accurate identification of each rodent at a specific level is needed in order to understand their implications in the transmission of diseases. Among the Muridae, the Rattini tribe encompasses 167 species inhabiting South East Asia, a hotspot of both biodiversity and emerging and re-emerging diseases. The region faces growing economical development that affects habitats, biodiversity and health. Rat species have been demonstrated as significant hosts of pathogens but are still difficult to recognize at a specific level using morphological criteria. DNA-barcoding methods appear as accurate tools for rat species identification but their use is hampered by the need of reliable identification of reference specimens. In this study, we explore and highlight the limits of the current taxonomy of the Rattini tribe.     

Pathogeography: leveraging the biogeography of human infectious diseases for global health management

Biogeography is an implicit and fundamental component of almost every dimension of modern biology, from natural selection and speciation to invasive species and biodiversity management. However, biogeography has rarely been integrated into human or veterinary medicine nor routinely leveraged for global health management. Here we review the theory and application of biogeography to the research and management of human infectious diseases, an integration we refer to as ‘pathogeography’. Pathogeography represents a promising framework for understanding and decomposing the spatial distributions, diversity patterns and emergence risks of human infectious diseases into interpretable components of dynamic socio‐ecological systems. Analytical tools from biogeography are already helping to improve our understanding of individual infectious disease distributions and the processes that shape them in space and time. At higher levels of organization, biogeographical studies of diseases are rarer but increasing, improving our ability to describe and explain patterns that emerge at the level of disease communities (e.g. co‐occurrence, diversity patterns, biogeographic regionalisation). Even in a highly globalized world most human infectious diseases remain constrained in their geographic distributions by ecological barriers to the dispersal or establishment of their causal pathogens, reservoir hosts and/or vectors. These same processes underpin the spatial arrangement of other taxa, such as mammalian biodiversity, providing a strong empirical ‘prior’ with which to assess the potential distributions of infectious diseases when data on their occurrence is unavailable or limited. In the absence of quality data, generalized biogeographic patterns could provide the earliest (and in some cases the only) insights into the potential distributions of many poorly known or emerging, or as‐yet‐unknown, infectious disease risks. Encouraging more community ecologists and biogeographers to collaborate with health professionals (and vice versa) has the potential to improve our understanding of infectious disease systems and identify novel management strategies to improve local, global and planetary health.     

Latitudinal gradients of parasite species richness in primates

Infectious disease risk is thought to increase in the tropics, but little is known about latitudinal gradients of parasite diversity. We used a comparative data set encompassing 330 parasite species reported from 119 primate hosts to examine latitudinal gradients in the diversity of micro and macroparasites per primate host species. Analyses conducted with and without controlling for host phylogeny showed that parasite species richness increased closer to the equator for protozoan parasites, but not for viruses or helminths. Relative to other major parasite groups, protozoa reported from wild primates were transmitted disproportionately by arthropod vectors. Within the protozoa, our results revealed that vector‐borne parasites showed a highly significant latitudinal gradient in species richness. This higher diversity of vector‐borne protozoa near the tropics could be influenced by a greater abundance or diversity of biting arthropods in the tropics, or by climatic effects on vector behaviour and parasite development. Many vector‐borne diseases, such as leishmaniasis, trypanosomiasis, and malaria pose risks to both humans and wildlife, and nearly one‐third of the protozoan parasites from free‐living primates in our data set have been reported to infect humans. Because the geographical distribution and prevalence of many vector‐borne parasites are expected to increase because of global warming, these results are important for predicting future parasite‐mediated threats to biodiversity and human health.     

Partitioning the influence of ecology across scales on parasite evolution

Vector‐borne parasites must succeed at three scales to persist: they must proliferate within a host, establish in vectors, and transmit back to hosts. Ecology outside the host undergoes dramatic seasonal and human‐induced changes, but predicting parasite evolutionary responses requires integrating their success across scales. We develop a novel, data‐driven model to titrate the evolutionary impact of ecology at multiple scales on human malaria parasites. We investigate how parasites invest in transmission versus proliferation, a life‐history trait that influences disease severity and spread. We find that transmission investment controls the pattern of host infectiousness over the course of infection: a trade‐off emerges between early and late infectiousness, and the optimal resolution of that trade‐off depends on ecology outside the host. An expanding epidemic favors rapid proliferation, and can overwhelm the evolutionary influence of host recovery rates and mosquito population dynamics. If transmission investment and recovery rate are positively correlated, then ecology outside the host imposes potent selection for aggressive parasite proliferation at the expense of transmission. Any association between transmission investment and recovery represents a key unknown, one that is likely to influence whether the evolutionary consequences of interventions are beneficial or costly for human health.     

Forest species diversity reduces disease risk in a generalist plant pathogen invasion

Empirical evidence suggests that biodiversity loss can increase disease transmission, yet our understanding of the 'diversity-disease hypothesis' for generalist pathogens in natural ecosystems is limited. We used a landscape epidemiological approach to examine two scenarios regarding diversity effects on the emerging plant pathogen Phytophthora ramorum across a broad, heterogeneous ecoregion: (1) an amplification effect exists where disease risk is greater in areas with higher plant diversity due to the pathogen's wide host range, or (2) a dilution effect where risk is reduced with increasing diversity due to lower competency of alternative hosts. We found evidence for pathogen dilution, whereby disease risk was lower in sites with higher species diversity, after accounting for potentially confounding effects of host density and landscape heterogeneity. Our results suggest that although nearly all plants in the ecosystem are hosts, alternative hosts may dilute disease transmission by competent hosts, thereby buffering forest health from infectious disease.     

推进生物多样性保护与人类健康的共同发展——One Health

随着新冠肺炎(COVID-19)的暴发, 野生动物、生物多样性和人类健康的关系再次引起广泛讨论。近20年来, 国际社会对于生物多样性与健康的研究日益增多, 并将它作为生物多样性保护与研究的重要方向之一。One Health作为一个新的理念框架, 通过交叉学科的研究和行动来推动包括人、所有其他动物及环境的健康。这个理念被不同国家、国际组织及协定所接纳及推广, 包括《生物多样性公约》等。本文通过总结近些年生物多样性对健康的影响方式、One Health的定义与发展历史、进入生物多样性议程的过程, 提出中国应用One Health改进相关野生动物管理以降低公共卫生危机的可能性的建议, 以及One Health框架内增强生物多样性保护所需的研究方向。One Health在中国的应用与发展应重视生物多样性研究和保护在其中的作用, 利用在景观生态学、群落内物种关系动态变化、气候变化影响、土地利用变化模式与趋势的研究, 与人类健康相结合, 提高One Health在应对公共健康和环境健康风险方面的准确性与及时性。同时, 需要加强我国在野生动物管理方面的投入和力度, 增强生物多样性保护与公共健康的联系, 将预警与干预措施前移, 减少疾病暴发带来的社会经济成本。     

Towards a resource‐based habitat approach for spatial modelling of vector‐borne disease risks

Given the veterinary and public health impact of vector‐borne diseases, there is a clear need to assess the suitability of landscapes for the emergence and spread of these diseases. Current approaches for predicting disease risks neglect key features of the landscape as components of the functional habitat of vectors or hosts, and hence of the pathogen. Empirical–statistical methods do not explicitly incorporate biological mechanisms, whereas current mechanistic models are rarely spatially explicit; both methods ignore the way animals use the landscape (i.e. movement ecology). We argue that applying a functional concept for habitat, i.e. the resource‐based habitat concept (RBHC), can solve these issues. The RBHC offers a framework to identify systematically the different ecological resources that are necessary for the completion of the transmission cycle and to relate these resources to (combinations of) landscape features and other environmental factors. The potential of the RBHC as a framework for identifying suitable habitats for vector‐borne pathogens is explored and illustrated with the case of bluetongue virus, a midge‐transmitted virus affecting ruminants. The concept facilitates the study of functional habitats of the interacting species (vectors as well as hosts) and provides new insight into spatial and temporal variation in transmission opportunities and exposure that ultimately determine disease risks. It may help to identify knowledge gaps and control options arising from changes in the spatial configuration of key resources across the landscape. The RBHC framework may act as a bridge between existing mechanistic and statistical modelling approaches.     

Amazonian Triatomine Biodiversity and the Transmission of Chagas Disease in French Guiana: In Medio Stat Sanitas

The effects of biodiversity on the transmission of infectious diseases now stand as a cornerstone of many public health policies. The upper Amazonia and Guyana shield are hot-spots of biodiversity that offer genuine opportunities to explore the relationship between the risk of transmission of Chagas disease and the diversity of its triatomine vectors. Over 730 triatomines were light-trapped in four geomorphological landscapes shaping French-Guiana, and we determined their taxonomic status and infection by Trypanosoma cruzi. We used a model selection approach to unravel the spatial and temporal variations in species abundance, diversity and infection. The vector community in French-Guiana is typically made of one key species (Panstrongylus geniculatus) that is more abundant than three secondary species combined (Rhodnius pictipes, Panstrongylus lignarius and Eratyrus mucronatus), and four other species that complete the assemblage. Although the overall abundance of adult triatomines does not vary across French-Guiana, their diversity increases along a coastal-inland gradient. These variations unravelled a non-monotonic relationship between vector biodiversity and the risk of transmission of Chagas disease, so that intermediate biodiversity levels are associated with the lowest risks. We also observed biannual variations in triatomine abundance, representing the first report of a biannual pattern in the risk of Chagas disease transmission. Those variations were highly and negatively correlated with the average monthly rainfall. We discuss the implications of these patterns for the transmission of T. cruzi by assemblages of triatomine species, and for the dual challenge of controlling Amazonian vector communities that are made of both highly diverse and mostly intrusive species.     

Projected climate and land use change alter western blacklegged tick phenology,seasonal host‐seeking suitability and human encounter risk in California

Global environmental change is having profound effects on the ecology of infectious disease systems, which are widely anticipated to become more pronounced under future climate and land use change. Arthropod vectors of disease are particularly sensitive to changes in abiotic conditions such as temperature and moisture availability. Recent research has focused on shifting environmental suitability for, and geographic distribution of, vector species under projected climate change scenarios. However, shifts in seasonal activity patterns, or phenology, may also have dramatic consequences for human exposure risk, local vector abundance and pathogen transmission dynamics. Moreover, changes in land use are likely to alter human–vector contact rates in ways that models of changing climate suitability are unlikely to capture. Here we used climate and land use projections for California coupled with seasonal species distribution models to explore the response of the western blacklegged tick (Ixodes pacificus), the primary Lyme disease vector in western North America, to projected climate and land use change. Specifically, we investigated how environmental suitability for tick host‐seeking changes seasonally, how the magnitude and direction of changing seasonal suitability differs regionally across California, and how land use change shifts human tick‐encounter risk across the state. We found vector responses to changing climate and land use vary regionally within California under different future scenarios. Under a hotter, drier scenario and more extreme land use change, the duration and extent of seasonal host‐seeking activity increases in northern California, but declines in the south. In contrast, under a hotter, wetter scenario seasonal host‐seeking declines in northern California, but increases in the south. Notably, regardless of future scenario, projected increases in developed land adjacent to current human population centers substantially increase potential human–vector encounter risk across the state. These results highlight regional variability and potential nonlinearity in the response of disease vectors to environmental change.     

Can domestic cats be considered reservoir hosts of zoonotic leishmaniasis?

Canine and human zoonotic leishmaniasis caused by Leishmania infantum, which is transmitted by the bite of infected phlebotomine sand flies, is a serious public health problem in the Mediterranean basin and Latin America. Among reports on newly identified mammalian hosts recurrently found infected with L. infantum, those regarding domestic cats deserve attention for the potential implications to public health. It has been shown that these animals cohabiting with humans can be infected (although only a few cases develop disease) and harbor parasites in an available way for transmission to competent vectors. Nonetheless, their role as reservoir hosts is still controversial.     

Identifying potentially invasive non‐native marine and brackish water species for the Arabian Gulf and Sea of Oman

Invasive non‐native species (NNS) are internationally recognized as posing a serious threat to global biodiversity, economies and human health. The identification of invasive NNS is already established, those that may arrive in the future, their vectors and pathways of introduction and spread, and hotspots of invasion are important for a targeted approach to managing introductions and impacts at local, regional and global scales. The aim of this study was to identify which marine and brackish NNS are already present in marine systems of the northeastern Arabia area (Arabian Gulf and Sea of Oman) and of these which ones are potentially invasive, and which species have a high likelihood of being introduced in the future and negatively affect biodiversity. Overall, 136 NNS were identified, of which 56 are already present in the region and a further 80 were identified as likely to arrive in the future, including fish, tunicates, invertebrates, plants and protists. The Aquatic Species Invasiveness Screening Kit (AS‐ISK) was used to identify the risk of NNS being (or becoming) invasive within the region. Based on the AS‐ISK basic risk assessment (BRA) thresholds, 36 extant and 37 horizon species (53.7% of all species) were identified as high risk. When the impact of climate change on the overall assessment was considered, the combined risk score (BRA+CCA) increased for 38.2% of all species, suggesting higher risk under warmer conditions, including the highest‐risk horizon NNS the green crab Carcinus maenas, and the extant macro‐alga Hypnea musciformis. This is the first horizon‐scanning exercise for NNS in the region, thus providing a vital baseline for future management. The outcome of this study is the prioritization of NNS to inform decision‐making for the targeted monitoring and management in the region to prevent new bio‐invasions and to control existing species, including their potential for spread.     

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

Vector‐borne diseases are a major health burden, yet factors affecting their spread are only partially understood. For example, microbial symbionts can impact mosquito reproduction, survival, and vectorial capacity, and hence affect disease transmission. Nonetheless, current knowledge of mosquito‐associated microbial communities is limited. To characterize the bacterial and eukaryotic microbial communities of multiple vector species collected from different habitat types in disease endemic areas, we employed next‐generation 454 pyrosequencing of 16S and 18S rRNA amplicon libraries, also known as metabarcoding. We investigated pooled whole adult mosquitoes of three medically important vectors, Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus, collected from different habitats across central Thailand where we previously characterized mosquito diversity. Our results indicate that diversity within the mosquito microbiota is low, with the majority of microbes assigned to one or a few taxa. Two of the most common eukaryotic and bacterial genera recovered (Ascogregarina and Wolbachia, respectively) are known mosquito endosymbionts with potentially parasitic and long evolutionary relationships with their hosts. Patterns of microbial composition and diversity appeared to differ by both vector species and habitat for a given species, although high variability between samples suggests a strong stochastic element to microbiota assembly. In general, our findings suggest that multiple factors, such as habitat condition and mosquito species identity, may influence overall microbial community composition, and thus provide a basis for further investigations into the interactions between vectors, their microbial communities, and human‐impacted landscapes that may ultimately affect vector‐borne disease risk.     

Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm

The twin concepts of zooprophylaxis and the dilution effect originated with vector-borne diseases (malaria), were driven forward by studies on Lyme borreliosis and have now developed into the mantra "biodiversity protects against disease". The basic idea is that by diluting the assemblage of transmission-competent hosts with non-competent hosts, the probability of vectors feeding on transmission-competent hosts is reduced and so the abundance of infected vectors is lowered. The same principle has recently been applied to other infectious disease systems--tick-borne, insect-borne, indirectly transmitted via intermediate hosts, directly transmitted. It is claimed that the presence of extra species of various sorts, acting through a variety of distinct mechanisms, causes the prevalence of infectious agents to decrease. Examination of the theoretical and empirical evidence for this hypothesis reveals that it applies only in certain circumstances even amongst tick-borne diseases, and even less often if considering the correct metric--abundance rather than prevalence of infected vectors. Whether dilution or amplification occurs depends more on specific community composition than on biodiversity per se. We warn against raising a straw man, an untenable argument easily dismantled and dismissed. The intrinsic value of protecting biodiversity and ecosystem function outweighs this questionable utilitarian justification.     

Local diversity reduces infection risk across multiple freshwater host‐parasite associations

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Colorado animal‐based plague surveillance systems: relationships between targeted animal species and prediction efficacy of areas at risk for humans

Human plague risks (Yersinia pestis infection) are greatest when epizootics cause high mortality among this bacterium's natural rodent hosts. Therefore, health departments in plague‐endemic areas commonly establish animal‐based surveillance programs to monitor Y. pestis infection among plague hosts and vectors. The primary objectives of our study were to determine whether passive animal‐based plague surveillance samples collected in Colorado from 1991 to 2005 were sampled from high human plague risk areas and whether these samples provided information useful for predicting human plague case locations. By comparing locations of plague‐positive animal samples with a previously constructed GIS‐based plague risk model, we determined that the majority of plague‐positive Gunnison's prairie dogs (100%) and non‐prairie dog sciurids (85.82%), and moderately high percentages of sigmodontine rodents (71.4%), domestic cats (69.3%), coyotes (62.9%), and domestic dogs (62.5%) were recovered within 1 km of the nearest area posing high peridomestic risk to humans. In contrast, the majority of white‐tailed prairie dog (66.7%), leporid (cottontailed and jack rabbits) (71.4%), and black‐tailed prairie dog (93.0%) samples originated more than 1 km from the nearest human risk habitat. Plague‐positive animals or their fleas were rarely (one of 19 cases) collected within 2 km of a case exposure site during the 24 months preceding the dates of illness onset for these cases. Low spatial accuracy for identifying epizootic activity prior to human plague cases suggested that other mammalian species or their fleas are likely more important sources of human infection in high plague risk areas. To address this issue, epidemiological observations and multi‐locus variable number tandem repeat analyses (MLVA) were used to preliminarily identify chipmunks as an under‐sampled, but potentially important, species for human plague risk in Colorado.     

Climate variation influences host specificity in avian malaria parasites

Parasites with low host specificity (e.g. infecting a large diversity of host species) are of special interest in disease ecology, as they are likely more capable of circumventing ecological or evolutionary barriers to infect new hosts than are specialist parasites. Yet for many parasites, host specificity is not fixed and can vary in response to environmental conditions. Using data on host associations for avian malaria parasites (Apicomplexa: Haemosporida), we develop a hierarchical model that quantifies this environmental dependency by partitioning host specificity variation into region‐ and parasite‐level effects. Parasites were generally phylogenetic host specialists, infecting phylogenetically clustered subsets of available avian hosts. However, the magnitude of this specialisation varied biogeographically, with parasites exhibiting higher host specificity in regions with more pronounced rainfall seasonality and wetter dry seasons. Recognising the environmental dependency of parasite specialisation can provide useful leverage for improving predictions of infection risk in response to global climate change.     

Experimental Evidence for Reduced Rodent Diversity Causing Increased Hantavirus Prevalence

Emerging and re-emerging infectious diseases have become a major global environmental problem with important public health, economic, and political consequences. The etiologic agents of most emerging infectious diseases are zoonotic, and anthropogenic environmental changes that affect wildlife communities are increasingly implicated in disease emergence and spread. Although increased disease incidence has been correlated with biodiversity loss for several zoonoses, experimental tests in these systems are lacking. We manipulated small-mammal biodiversity by removing non-reservoir species in replicated field plots in Panama, where zoonotic hantaviruses are endemic. Both infection prevalence of hantaviruses in wild reservoir (rodent) populations and reservoir population density increased where small-mammal species diversity was reduced. Regardless of other variables that affect the prevalence of directly transmitted infections in natural communities, high biodiversity is important in reducing transmission of zoonotic pathogens among wildlife hosts. Our results have wide applications in both conservation biology and infectious disease management.     

Species loss on spatial patterns and composition of zoonotic parasites

Species loss can result in the subsequent loss of affiliate species. Though largely ignored to date, these coextinctions can pose threats to human health by altering the composition, quantity and distribution of zoonotic parasites. We simulated host extinctions from more than 1300 host–parasite associations for 29 North American carnivores to investigate changes in parasite composition and species richness. We also explored the geography of zoonotic parasite richness under three carnivore composition scenarios and examined corresponding levels of human exposure. We found that changes in parasite assemblages differed among parasite groups. Because viruses tend to be generalists, the proportion of parasites that are viruses increased as more carnivores went extinct. Coextinction of carnivore parasites is unlikely to be common, given that few specialist parasites exploit hosts of conservation concern. However, local extirpations of widespread carnivore hosts can reduce overall zoonotic richness and shift distributions of parasite-rich areas. How biodiversity influences disease risks remains the subject of debate. Our results make clear that hosts vary in their contribution to human health risks. As a consequence, so too does the loss (or gain) of particular hosts. Anticipating changes in host composition in future environments may help inform parasite conservation and disease mitigation efforts.     

Impact of biodiversity and seasonality on Lyme-pathogen transmission

Lyme disease imposes increasing global public health challenges. To better understand the joint effects of seasonal temperature variation and host community composition on the pathogen transmission, a stage-structured periodic model is proposed by integrating seasonal tick development and activity, multiple host species and complex pathogen transmission routes between ticks and reservoirs. Two thresholds, one for tick population dynamics and the other for Lyme-pathogen transmission dynamics, are identified and shown to fully classify the long-term outcomes of the tick invasion and disease persistence. Seeding with the realistic parameters, the tick reproduction threshold and Lyme disease spread threshold are estimated to illustrate the joint effects of the climate change and host community diversity on the pattern of Lyme disease risk. It is shown that climate warming can amplify the disease risk and slightly change the seasonality of disease risk. Both the “dilution effect” and “amplification effect” are observed by feeding the model with different possible alternative hosts. Therefore, the relationship between the host community biodiversity and disease risk varies, calling for more accurate measurements on the local environment, both biotic and abiotic such as the temperature and the host community composition.     

Mosquito-borne disease and climate change in Australia: time for a reality check

Will warming climate increase the risk or prevalence of mosquito-borne disease in Australia, as has been projected in a number of scientific publications and governmental reports? Unfortunately, most of these 'predictions' do not adequately consider the current and historical distribution of the vectors and diseases, their local ecology and epidemiology and the impact of societal features and the capacity for public health interventions in Australia. Overall, a strong case can be made that we are unlikely to see significant changes in the distribution of transmission of the exotic pathogens causing malaria and dengue, and while activity of endemic arboviruses such as Murray Valley encephalitis and Ross River viruses may possibly increase in some areas, it is likely to decrease in others. The ecologies of mosquito-borne diseases can be complex and difficult to predict, and any evaluation of potential effects of changes in climate will need a detailed examination of site-specific vector, host and other factors likely to influence the outcomes on human health. Of itself, climate change as currently projected, is not likely to provide great cause for public health concern with mosquito-borne disease in Australia.