Deformed wing virus (DWV) and its vector, the mite Varroa destructor, are a major threat to the world's honeybees. Although the impact of Varroa on colony-level DWV epidemiology is evident, we have little understanding of wider DWV epidemiology and the role that Varroa has played in its global spread. A phylogeographic analysis shows that DWV is globally distributed in honeybees, having recently spread from a common source, the European honeybee Apis mellifera. DWV exhibits epidemic growth and transmission that is predominantly mediated by European and North American honeybee populations and driven by trade and movement of honeybee colonies. DWV is now an important reemerging pathogen of honeybees, which are undergoing a worldwide manmade epidemic fueled by the direct transmission route that the Varroa mite provides.

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This article reviews research on the evolutionary mechanisms leading to different transmission modes. Such modes are often under genetic control of the host or the pathogen, and often in conflict with each other via trade-offs. Transmission modes may vary among pathogen strains and among host populations. Evolutionary changes in transmission mode have been inferred through experimental and phylogenetic studies, including changes in transmission associated with host shifts and with evolution of the unusually complex life cycles of many parasites. Understanding the forces that determine the evolution of particular transmission modes presents a fascinating medley of problems for which there is a lack of good data and often a lack of conceptual understanding or appropriate methodologies. Our best information comes from studies that have been focused on the vertical versus horizontal transmission dichotomy. With other kinds of transitions, theoretical approaches combining epidemiology and population genetics are providing guidelines for determining when and how rapidly new transmission modes may evolve, but these are still in need of empirical investigation and application to particular cases. Obtaining such knowledge is a matter of urgency in relation to extant disease threats.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

The number of pathogens that are required to infect a host, termed infective dose, varies dramatically across pathogen species. It has recently been predicted that infective dose will depend upon the mode of action of the molecules that pathogens use to facilitate their infection. Specifically, pathogens which use locally acting molecules will require a lower infective dose than pathogens that use distantly acting molecules. Furthermore, it has also been predicted that pathogens with distantly acting immune modulators may be more virulent because they have a large number of cells in the inoculums, which will cause more harm to host cells. We formally test these predictions for the first time using data on 43 different human pathogens from a range of taxonomic groups with diverse life-histories. We found that pathogens using local action do have lower infective doses, but are not less virulent than those using distant action. Instead, we found that virulence was negatively correlated with infective dose, and higher in pathogens infecting wounded skin, compared with those ingested or inhaled. More generally, our results show that broad-scale comparative analyses can explain variation in parasite traits such as infective dose and virulence, whilst highlighting the importance of mechanistic details.

An influential ecological theory, the intermediate disturbance hypothesis (IDH), predicts that intermediate levels of disturbance will maximize species diversity. Empirical studies, however, have described a wide variety of diversity-disturbance relationships (DDRs). Using experimental populations of microbes, we show that the form of the DDR depends on an interaction between disturbance frequency and intensity. We find that diversity shows a monotonically increasing, unimodal or flat relationship with disturbance, depending on the values of the disturbance aspects considered. These results confirm recent theoretical predictions, and potentially reconcile the conflicting body of empirical evidence on DDRs.

One of the most striking facts about parasites and microbial pathogens that has emerged in the fields of social evolution and disease ecology in the past few decades is that these simple organisms have complex social lives, indulging in a variety of cooperative, communicative and coordinated behaviours. These organisms have provided elegant experimental tests of the importance of relatedness, kin discrimination, cooperation and competition, in driving the evolution of social strategies. Here, we briefly review the social behaviours of parasites and microbial pathogens, including their contributions to virulence, and outline how inclusive fitness theory has helped to explain their evolution. We then take a mechanistically inspired ‘bottom-up’ approach, discussing how key aspects of the ways in which parasites and pathogens exploit hosts, namely public goods, mobile elements, phenotypic plasticity, spatial structure and multi-species interactions, contribute to the emergent properties of virulence and transmission. We argue that unravelling the complexities of within-host ecology is interesting in its own right, and also needs to be better incorporated into theoretical evolution studies if social behaviours are to be understood and used to control the spread and severity of infectious diseases.

Coinfection of parasite genotypes can select for various changes in parasite life history strategies relative to single genotype infections, with consequences for disease dynamics and severity. However, even where coinfection is common, a parasite genotype is also likely to regularly experience single genotype infections over relatively short periods of evolutionary time, due to chance, changes in local disease transmission, and parasite population structuring. Such alternating conditions between single genotype and coinfections will impose conflicting pressures on parasites, potentially selecting for facultative responses to coinfection. Although such adaptive phenotypic plasticity in response to social environment has been observed in protozoan parasites and viruses, here we show it evolving in real time in response to coinfection under conditions in which both single infections and coinfections are common. We experimentally evolved an obligate-killing virus under conditions of single virus infections (single lines) or a mix of single infections and coinfections (mixed lines) and found mixed lines to evolve a plastic lysis time: they killed host cells more rapidly when coinfecting than when infecting alone. This behavior resulted in high fitness under both infection conditions. Such plasticity has important consequences for the epidemiology of infectious diseases and the evolution of cooperation.

The harm that pathogens cause to hosts during infection, termed virulence, varies across species from negligible to a high likelihood of rapid death. Classic theory for the evolution of virulence is based on a trade-off between pathogen growth, transmission and host survival, which predicts that higher within-host growth causes increased transmission and higher virulence. However, using data from 61 human pathogens, we found the opposite correlation to the expected positive correlation between pathogen growth rate and virulence. We found that (i) slower growing pathogens are significantly more virulent than faster growing pathogens, (ii) inhaled pathogens and pathogens that infect via skin wounds are significantly more virulent than pathogens that are ingested, but (iii) there is no correlation between symptoms of infection that aid transmission (such as diarrhoea and coughing) and virulence. Overall, our results emphasize how virulence can be influenced by mechanistic life-history details, especially transmission mode, that determine how parasites infect and exploit their hosts.This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.