Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors.

The potential for infectious pathogens to spillover and emerge from managed populations to wildlife communities is poorly understood, but ecological, evolutionary and anthropogenic factors are all likely to influence the initial exposure and subsequent infection, spread and impact of disease. Fast-evolving RNA viruses, known to cause severe colony losses in managed honeybee populations, deserve particular attention for their propensity to jump between host species and thus threaten ecologically and economically important wild pollinator communities. We review the literature on pollinator viruses to identify biological and anthropogenic drivers of disease emergence, highlight gaps in the literature, and discuss potential management strategies. We provide evidence that many wild pollinator species are exposed to viruses from commercial species, resulting in multiple spillover events. However, it is not clear whether species become infected as a result of spillover or whether transmission is occurring within these wild populations. Ecological traits of pollinating insects, such as overlapping ranges, niches and behaviours, clearly promote cross-species transmission of RNA viruses. Moreover, we conclude that the social behaviour and phylogenetic relatedness of social pollinators further facilitate within- and between-host transmission, leaving these species particularly vulnerable to emerging diseases. We argue that the commercial use of pollinators is a key driver of disease emergence in these beneficial insects and that this must be addressed by management and policy. Synthesis and applications. There are important knowledge gaps, ranging from disease distribution and prevalence, to pathogen life history and virulence, to the impacts of disease emergence, which need to be addressed as research priorities. It is clear that avoiding anthropogenic pathogen spillover is crucial to preventing and managing disease emergence in pollinators, with far-reaching effects on our food security, ecosystem services and biodiversity. We argue that it is crucial to prevent the introduction of diseased pollinators into natural environments, which can be achieved through improved monitoring and management practices.

Dynamics of a morbillivirus at the domestic-wildlife interface: Canine distemper virus in domestic dogs and lions.

Morbilliviruses cause many diseases of medical and veterinary importance, and although some (e.g., measles and rinderpest) have been controlled successfully, others, such as canine distemper virus (CDV), are a growing concern. A propensity for host-switching has resulted in CDV emergence in new species, including endangered wildlife, posing challenges for controlling disease in multispecies communities. CDV is typically associated with domestic dogs, but little is known about its maintenance and transmission in species-rich areas or about the potential role of domestic dog vaccination as a means of reducing disease threats to wildlife. We address these questions by analyzing a long-term serological dataset of CDV in lions and domestic dogs from Tanzania's Serengeti ecosystem. Using a Bayesian state-space model, we show that dynamics of CDV have changed considerably over the past three decades. Initially, peaks of CDV infection in dogs preceded those in lions, suggesting that spill-over from dogs was the main driver of infection in wildlife. However, despite dog-to-lion transmission dominating cross-species transmission models, infection peaks in lions became more frequent and asynchronous from those in dogs, suggesting that other wildlife species may play a role in a potentially complex maintenance community. Widespread mass vaccination of domestic dogs reduced the probability of infection in dogs and the size of outbreaks but did not prevent transmission to or peaks of infection in lions. This study demonstrates the complexity of CDV dynamics in natural ecosystems and the value of long-term, large-scale datasets for investigating transmission patterns and evaluating disease control strategies.

Pathogen regulation of plant diversity via effective specialization.

The Janzen-Connell (JC) hypothesis, one of the most influential hypotheses explaining forest diversity, is inconsistent with evidence that tree species share the same natural enemies. Through the discussion of seedling diseases from a pathogen-centered perspective, we expand the JC hypothesis to tie in host-pathogen-environment interactions at three levels: local adaptation, host specificity of the combined effect of multiple infections, and environmental modulation of disease. We present evidence from plant pathology, disease ecology, and host-parasite evolution relevant to (but not commonly associated with) forest species diversity maintenance. This expanded view of the JC hypothesis suggests ways to direct new experiments to integrate research on pathogen local adaptation, co-infection, and environmental effects on infection by using high-throughput molecular techniques and statistical models.