Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite. Predators may shift this cost–benefit balance by consuming infected hosts or changing host behaviour, but the strength of these effects remains unclear. Here we use field and lab data on Trinidadian guppies and their Gyrodactylus spp. parasites to show how differential predation pressure influences parasite virulence and transmission. We use an experimentally demonstrated virulence–transmission trade-off to parametrize a mathematical model in which host shoaling (as a means of anti-predator defence), increases contact rates and selects for higher virulence. Then we validate model predictions by collecting parasites from wild, Trinidadian populations; parasites from high-predation populations were more virulent in common gardens than those from low-predation populations. Broadly, our results indicate that reduced social contact selects against parasite virulence.
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Predation shifts coevolution toward higher host contact rate and parasite virulence
Hosts can avoid parasites (and pathogens) by reducing social contact, but such isolation may carry costs, e.g. increased vulnerability to predators. Thus, many predator–host–parasite systems confront hosts with a trade-off between predation and parasitism. Parasites, meanwhile, evolve higher virulence in response to increased host sociality and consequently, increased multiple infections. How does predation shift coevolution of host behaviour and parasite virulence? What if predators are selective, i.e. predators disproportionately capture the sickest hosts? We answer these questions with an eco-coevolutionary model parametrized for a Trinidadian guppy–
- Award ID(s):
- 2010826
- PAR ID:
- 10482603
- Publisher / Repository:
- The Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 289
- Issue:
- 1978
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Virulence, the degree to which a pathogen harms its host, is an important but poorly understood aspect of host-pathogen interactions. Virulence is not static, instead depending on ecological context and potentially evolving rapidly. For instance, at the start of an epidemic, when susceptible hosts are plentiful, pathogens may evolve increased virulence if this maximizes their intrinsic growth rate. However, if host density declines during an epidemic, theory predicts evolution of reduced virulence. Although well-studied theoretically, there is still little empirical evidence for virulence evolution in epidemics, especially in natural settings with native host and pathogen species. Here, we used a combination of field observations and lab assays in the
Daphnia -Pasteuria model system to look for evidence of virulence evolution in nature. We monitored a large, naturally occurring outbreak ofPasteuria ramosa inDaphnia dentifera , where infection prevalence peaked at ~ 40% of the population infected and host density declined precipitously during the outbreak. In controlled infections in the lab, lifespan and reproduction of infected hosts was lower than that of unexposed control hosts and of hosts that were exposed but not infected. We did not detect any significant changes in host resistance or parasite infectivity, nor did we find evidence for shifts in parasite virulence (quantified by host lifespan and number of clutches produced by hosts). However, over the epidemic, the parasite evolved to produce significantly fewer spores in infected hosts. While this finding was unexpected, it might reflect previously quantified tradeoffs: parasites in high mortality (e.g., high predation) environments shift from vegetative growth to spore production sooner in infections, reducing spore yield. Future studies that track evolution of parasite spore yield in more populations, and that link those changes with genetic changes and with predation rates, will yield better insight into the drivers of parasite evolution in the wild. -
Predators and parasites are critical, interconnected members of the community and have the potential to shape host populations. Predators, in particular, can have direct and indirect impacts on disease dynamics. By removing hosts and their parasites, predators alter both host and parasite populations and ultimately shape disease transmission. Selective predation of infected hosts has received considerable attention as it is recognized to have important ecological implications. The occurrence and consequences of preferential consumption of uninfected hosts, however, has rarely been considered. Here, we synthesize current evidence suggesting this strategy of selectively predating uninfected individuals is likely more common than previously anticipated and address how including this predation strategy can change our understanding of the ecology and evolution of disease dynamics. Selective predation strategies are expected to differentially impact ecological dynamics and therefore, consideration of both strategies is required to fully understand the impact of predation on prey and host densities. In addition, given that different strategies of prey selectivity by predators change the fitness payoffs both for hosts and their parasites, we predict amplified coevolutionary rates under selective predation of infected hosts compared to uninfected hosts. Using recent work highlighting the critical role that predators play in disease dynamics, we provide insights into the potential mechanisms by which selective predation on healthy individuals can directly affect ecological outcomes and impact long‐term host–parasite coevolution. We contrast the consequences of both scenarios of selective predation while identifying current gaps in the literature and future research directions.more » « less
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Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2021.2800
