Abstract
Disease outbreaks are a consequence of interactions among the three components of a host–parasite system: the infectious agent, the host and the environment. While virulence and transmission are widely investigated, most studies of parasite life-history trade-offs are conducted with theoretical models or tractable experimental systems where transmission is standardized and the environment controlled. Yet, biotic and abiotic environmental factors can strongly affect disease dynamics, and ultimately, host–parasite coevolution. Here, we review research on how environmental context alters virulence–transmission relationships, focusing on the off-host portion of the parasite life cycle, and how variation in parasite survival affects the evolution of virulence and transmission. We review three inter-related ‘approaches’ that have dominated the study of the evolution of virulence and transmission for different host–parasite systems: (i) evolutionary trade-off theory, (ii) parasite local adaptation and (iii) parasite phylodynamics. These approaches consider the role of the environment in virulence and transmission evolution from different angles, which entail different advantages and potential biases. We suggest improvements to how to investigate virulence–transmission relationships, through conceptual and methodological developments and taking environmental context into consideration. By combining developments in life-history evolution, phylogenetics, adaptive dynamics and comparative genomics, we can improve our understanding of virulence–transmission relationships across a diversity of host–parasite systems that have eluded experimental study of parasite life history.
Highlights
Disease outbreaks are a consequence of interactions among the three components of a host–parasite system: the infectious agent, the host and the environment
We review research on how environmental context alters virulence–transmission relationships, focusing on the off-host portion of the parasite life cycle, and how variation in parasite survival affects the evolution of virulence and transmission
We review three inter-related ‘approaches’ that have dominated the study of the evolution of virulence and transmission for different host–parasite systems: (i) evolutionary trade-off theory, (ii) parasite local adaptation and (iii) parasite phylodynamics
Summary
We reviewed three research approaches used to study the evolution of virulence and transmission, highlighting how the environment can have important effects on virulence–transmission relationships. Within this environmental context, we focused on parasite survival during the off-host life stage. An off-host perspective allows us to conceptually merge direct and environmental transmission These two transmission types are not separate processes but occur along a time continuum in the off-host environment [102], and should ideally be described by the same unified theory. We use anthrax in wildlife systems as a case study employing several aspects of this framework (box 5), since B. anthracis is an ETP commonly invoked for the evolution of high virulence and high environmental survival
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