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bioRxiv · 10.1101/324632

When parasites are selected to kill the young

Iritani, R.·Visher, E.·Boots, M.
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Abstract

The impact of infectious disease is often very different in juveniles and adults, but theory has focused on the drivers of stage-dependent defense in hosts rather than the potential for stage-dependent virulence evolution. Stage-structure has the potential to be important to the evolution of pathogens because it exposes parasites to heterogeneous environments in terms of both host characteristics and transmission routes. We develop a stage-structured (juvenile-adult) epidemiological model and examine the evolutionary outcomes of stage-specific virulence under the classic assumption of a transmission-virulence trade-off. We show that selection on virulence against adults remains consistent with the classic theory. However, the evolution of juvenile virulence is sensitive to both demography and transmission pathway with higher virulence against juveniles being favored either when the transmission pathway is assortative (juveniles preferentially interact together) and the juvenile stage is short, or in contrast when the transmission pathway is disassortative and the juvenile stage is long. These results highlight the potentially profound effects of host stage-structure on determining parasite virulence in nature. This new perspective may have broad implications for both understanding and managing disease severity. Impact summaryUnderstanding the evolution of parasite virulence remains one of the most important questions in evolutionary ecology. Virulence is often very different in young and old hosts, but previous theory has presumed that these differences are attributed to adaptation in host defense rather than parasite adaptation. However, stage-structure within host populations can expose parasites to heterogeneous environments, which may lead to differential selection on parasite virulence (stage-specific virulence). Surprisingly, no study has investigated the effects of hosts stage-structure on the evolution of stage-specific virulence. We present a theoretical analysis to examine when selection can favor higher virulence against juveniles (juvenile-virulence) versus adults (adult-virulence). Our key result is that higher juvenile-virulence is selected for either when the transmission is assortative within age classes and maturation is slow, or when the transmission is disassortative (occurring predominantly between-classes) and maturation is relatively fast. These at first sight contrasting outcomes can be understood as adaptation to the exploitation of the more available host stage. Although the data on assortativity in infectious disease systems is limited, empirical studies for the virulence of Great Island Virus in guillemots (Uria aalge) and for salmon louse in pink salmon (Oncorhynchus gorbuscha) are consistent with our predictions. Our work provides testable predictions for stage-specific virulence and presents a novel mechanism that may explain variation in virulence in nature. There are also management implications for conservation, public health, vaccination programs, and farming to understanding the drivers of stage dependent virulence.

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Iritani, R., Visher, E., Boots, M.. 2018-05-20. When parasites are selected to kill the young. https://doi.org/10.1101/324632

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