As has been recently exemplified by the global Covid19 pandemic, emerging diseases can pose important risks to their hosts, while at the same time being critical test cases for understanding the evolutionary ecology of host-pathogen interactions. The origins of disease emergence generally lie in a change in host-pathogen ecology, such as increased transmission opportunities through an increase in contact, for example through habitat destruction or range expansion. Another mechanism for increasing transmission is the acquisition of novel transmission routes. Effects on both host and pathogen can be particularly drastic when transmission changes from direct to vector-borne transmission, i.e. such as transmission of malaria or viruses via mosquitoes to humans or aphids to plants, or even transmission routes that mimic vector-borne transmission, such as blood or organ donations. Compared to direct transmission, vector-borne transmission is expected to lead to increases in pathogen prevalence and virulence, that is pathogens are expected to become more widespread and cause more harm to their hosts. Despite its importance for disease prevention and control, we lack empirical and theoretical understanding of the evolutionary ecology of vector-borne transmission, and particularly of the acquisition of this transmission route. The emergence of the ectoparasitic mite Varroa destructor in honeybees provides a unique opportunity to study how a novel vector affects pathogen ecology and evolution: this mite which feeds mainly on the fat body of honeybees is a novel vector for Deformed Wing Virus (DWV), a disease linked to severe increases in individual and hive mortality. To study the fundamental evolutionary ecology of emerging vector-borne diseases, we are exploiting a unique natural experiment, the presence of Varroa-free island refugia. We test how this novel vector affects epidemiology and viral evolution, and how we might ultimately mitigate the effects of these evolving viruses on host populations. Using this system, we have already shown that the acquisition of Varroa as a viral vector in honeybees has virus-dependent knock-on effects in wild bees. With this project, we aim to elucidate how transmission dynamics change in response to a novel vector and how this affects virus evolution in the field. We then aim to dissect the drivers of these changes in evolutionary ecology in the lab, to ask, for example, which characteristics of vector-borne transmission are key in driving changes observed in the field. With this knowledge, we then aim to improve our general understanding of pathogen evolution through modelling, as well as testing whether control and mitigation strategies can help to protect the hosts of this evolving pathogen. With this body of work, we aim to deepen our knowledge of the ecological and evolutionary risk factors driving disease emergence, specifically the role of vector-borne transmission; this knowledge is crucial for human societies in preventing and mitigating emerging diseases in wildlife, agriculture and in human health. Furthermore, the honeybees and wild bees we work with are crucial pollinators of crops and wild flowering plants, key for maintaining biodiversity and human food security. We specifically aim to test strategies for mitigating the effects of evolving viruses on these communities through conservation measures, thereby promoting wild and managed pollinators that are crucial for human and environmental health.
