The evolution of sex-specific virulence in infectious diseases

Úbeda, Francisco; Jansen, Vincent

doi:10.1038/ncomms13849

Cited by 54 publications

(63 citation statements)

References 63 publications

(81 reference statements)

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“…; Gipson and Hall ). Together, this heterogeneity between the sexes is increasingly being linked to the performance of a single pathogen genotype within a male or female host and its subsequent transmission between susceptible hosts (e.g., Cousineau and Alizon ; Úbeda and Jansen ; Hall and Mideo ). Yet, it remains largely unexplored how each sex can influence the relationship between within‐host pathogen competition and virulence (but see Thompson et al.…”

Section: Description Of the Four Infection Types Used In This Study mentioning

confidence: 99%

Host sexual dimorphism affects the outcome of within‐host pathogen competition

2019

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Natural infections often consist of multiple pathogens of the same or different species. When coinfections occur, pathogens compete for access to host resources and fitness is determined by how well a pathogen can reproduce compared to its competitors. Yet not all hosts provide the same resource pool. Males and females, in particular, commonly vary in both their acquisition of resources and investment in immunity, but their ability to modify any competition between different pathogens remains unknown. Using the Daphnia magna–Pasteuria ramosa model system, we exposed male and female hosts to either a single genotype infection or coinfections consisting of two pathogen genotypes of varying levels of virulence. We found that coinfections within females favored the transmission of the more virulent pathogen genotype, whereas coinfections within male hosts resulted in equal transmission of competing pathogen genotypes. This contrast became less pronounced when the least virulent pathogen was able to establish an infection first, suggesting that the influence of host sex is shaped by priority effects. We suggest that sex is a form of host heterogeneity that may influence the evolution of virulence within coinfection contexts and that one sex may be a reservoir for pathogen genetic diversity in nature.

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Section: Description Of the Four Infection Types Used In This Study mentioning

confidence: 99%

Host sexual dimorphism affects the outcome of within‐host pathogen competition

2019

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“…The evolution of parasite adaptations that are specific to males or females could also shape differences in infection between the sexes, regardless of whether or not they inherently differ in immunocompetence (Duneau & Ebert ; Duneau et al . ; Ubeda & Jansen ).…”

Section: Introductionmentioning

confidence: 98%

Sexual dimorphism in immunity across animals: a meta‐analysis

Stoehr²,

et al. 2018

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In animals, sex differences in immunity are proposed to shape variation in infection prevalence and intensity among individuals in a population, with females typically expected to exhibit superior immunity due to life‐history trade‐offs. We performed a systematic meta‐analysis to investigate the magnitude and direction of sex differences in immunity and to identify factors that shape sex‐biased immunocompetence. In addition to considering taxonomic and methodological effects as moderators, we assessed age‐related effects, which are predicted to occur if sex differences in immunity are due to sex‐specific resource allocation trade‐offs with reproduction. In a meta‐analysis of 584 effects from 124 studies, we found that females exhibit a significantly stronger immune response than do males, but the effect size is relatively small, and became non‐significant after controlling for phylogeny. Female‐biased immunity was more pronounced in adult than immature animals. More recently published studies did not report significantly smaller effect sizes. Among taxonomic and methodological subsets of the data, some of the largest effect sizes were in insects, further supporting previous suggestions that testosterone is not the only potential driver of sex differences in immunity. Our findings challenge the notion of pervasive biases towards female‐biased immunity and the role of testosterone in driving these differences.

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“…Therefore, sources of heterogeneity in hosts can lead to different predictions than classic virulence evolution theory based on the marginal value theorem, as claimed in a recent conceptual review (Lion & Metz 2018). Our novel results arise because we explicitly assumed stage-structure with maturation from juveniles to adults and reproduction by adults, rather than more generic host heterogeneity, e.g., multiple host species (Regoes et al 2000;Gandon 2004;Osnas & Dobson 2011), vaccination (Gandon et al 2001;Gandon et al 2003;Yates et al 2006;Zurita-Gutiérrez & Lion 2015), or sex (Úbeda & Jansen 2016).…”

Section: Discussionmentioning

confidence: 89%

The evolution of stage-specific virulence: differential selection of parasites in juveniles

Iritani

Visher

Boots

2018

Preprint

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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...

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The evolution of sex-specific virulence in infectious diseases

Cited by 54 publications

References 63 publications

Host sexual dimorphism affects the outcome of within‐host pathogen competition

Host sexual dimorphism affects the outcome of within‐host pathogen competition

Sexual dimorphism in immunity across animals: a meta‐analysis

The evolution of stage-specific virulence: differential selection of parasites in juveniles

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