Shoaling guppies evade predation but have deadlier parasites

Walsman, Jason Cosens; Janecka, Mary J.; Clark, David R.; Kramp, Rachael D.; Rovenolt, Faith; Patrick, Regina; Mohammed, Ryan S.; Konczal, Mateusz; Cressler, Clayton E.; Stephenson, Jessica F.

doi:10.1038/s41559-022-01772-5

Cited by 10 publications

(28 citation statements)

References 72 publications

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“…But if predation does not interact with anti-infection defence, increased selective predation should decrease prevalence and virulence as previously expected. Higher predation in guppy populations results in higher prevalence of worm ectoparasite infection and more virulent parasites [21], as our model predicts, but the selectivity of predation in this focal system has been indirectly supported by one study [32] and challenged by another [46].…”

Section: Discussionmentioning

confidence: 64%

“…Increased host mortality generally leads to declining force of infection and thus decreasing investment in the resistance that prevents infection [41]; we get equivalent results when increasing d (electronic supplementary material, figure S5), which does not interact directly with contact rate. Predictably [21], we get very different results when the mortality source (predation) selects for higher contact rates, leading to increasing contact rates and increasing prevalence with predation (figures 1 and 2). Increased host mortality is also expected to lead to increased virulence if multiple infections are unimportant or decreased virulence if they are important [27]; we find this result without contact rate evolution (see orange curve in figure 2 j ) but with contact rate evolution, increasing contact rates drive much stronger selection for virulence (compare figure 2 j , n ; see also electronic supplementary material, table S2).…”

Section: Discussionmentioning

confidence: 99%

“…We focus on outcomes at the model's single endemic equilibrium, which is stable if the parasite R 0 > 1 (for our parameters). We use a biologically relevant parameter range for the guppy– Gyrodactylus system [21] and focus on model behaviour in this range. The uncharacterized parameter in the guppy– Gyrodactylus system is the selectivity of predation (value of ϕ ); thus, we explore a broad range of ϕ from 0 to 100 so that, at the highest values of v in our focal parameter range, infected hosts are predated upon approximately 2.7 times more than susceptible hosts.…”

Section: Methodsmentioning

confidence: 99%

“…We tease apart these interactions with biologically relevant parameter values, shown in table 1, from the well-characterized predator–prey/host–parasite system of generalist piscivores, Trinidadian guppy prey/hosts ( Poecilia reticulata ) and guppies' helminth parasites ( Gyrodactylus sp.). The focal system, and many other host–parasite systems across taxa, meet multiple model assumptions: hosts trade-off predator defence against parasite transmission, parasites have a trade-off that selects for intermediate virulence [21,30], parasites compete in multiple infections which lead to selection for increased virulence [21,31] and selective predation likely raises the effective cost of virulence [15]. In our focal system, infection intensity (likely correlated with the rate of parasite reproduction on the host), is linked with transmission rate and virulence [21] and possibly also with selective predation [32].…”

Section: Introductionmentioning

confidence: 99%

“…Values and units of state variables and parameters. As discussed in Methods, all parameter values are sourced from Walsman et al[21] except for ϕ and we use a lower range of predation (but ϕ > 0 compensates somewhat by making overall predation higher and see the electronic supplementary material for results with higher predation). State variables then parameters listed, each in order of appearance in equation (2.1).…”

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confidence: 99%

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Predation shifts coevolution toward higher host contact rate and parasite virulence

Walsman

Cressler

2022

Proc. R. Soc. B.

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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– Gyrodactylus spp. system. Here, increased predation drives host coevolution of higher grouping, which selects for higher virulence. Additionally, higher predator selectivity drives the contact rate higher and virulence lower. Finally, we show how predation and selectivity can have very different impacts on host density and prevalence depending on whether hosts or parasites evolve, or both. For example, higher predator selectivity led to lower prevalence with no evolution or only parasite evolution but higher prevalence with host evolution or coevolution. These findings inform our understanding of diverse systems in which host behavioural responses to predation may lead to increased prevalence and virulence of parasites.

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Section: Discussionmentioning

confidence: 64%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Predation shifts coevolution toward higher host contact rate and parasite virulence

Walsman

Cressler

2022

Proc. R. Soc. B.

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Effects of predation risk on parasite–host interactions and wildlife diseases

Thieltges,

Johnson,

van Leeuwen

et al. 2024

Ecology

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Landscapes of fear can determine the dynamics of entire ecosystems. In response to perceived predation risk, prey can show physiological, behavioral, or morphological trait changes to avoid predation. This in turn can indirectly affect other species by modifying species interactions (e.g., altered feeding), with knock‐on effects, such as trophic cascades, on the wider ecosystem. While such indirect effects stemming from the fear of predation have received extensive attention for herbivore–plant and predator–prey interactions, much less is known about how they alter parasite–host interactions and wildlife diseases. In this synthesis, we present a conceptual framework for how predation risk—as perceived by organisms that serve as hosts—can affect parasite–host interactions, with implications for infectious disease dynamics. By basing our approach on recent conceptual advances with respect to predation risk effects, we aim to expand this general framework to include parasite–host interactions and diseases. We further identify pathways through which parasite–host interactions can be affected, for example, through altered parasite avoidance behavior or tolerance of hosts to infections, and discuss the wider relevance of predation risk for parasite and host populations, including heuristic projections to population‐level dynamics. Finally, we highlight the current unknowns, specifically the quantitative links from individual‐level processes to population dynamics and community structure, and emphasize approaches to address these knowledge gaps.

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Ornaments indicate parasite load only if they are dynamic or parasites are contagious

et al. 2023

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Choosing to mate with an infected partner has several potential fitness costs, including disease transmission and infection-induced reductions in fecundity and parental care. By instead choosing a mate with no, or few, parasites, animals avoid these costs and may also obtain resistance genes for offspring. Within a population, then, the quality of sexually selected ornaments on which mate choice is based should correlate negatively with the number of parasites with which a host is infected (“parasite load”). However, the hundreds of tests of this prediction yield positive, negative, or no correlation between parasite load and ornament quality. Here, we use phylogenetically controlled meta-analysis of 424 correlations from 142 studies on a wide range of host and parasite taxa to evaluate explanations for this ambiguity. We found that ornament quality is weakly negatively correlated with parasite load overall, but the relationship is more strongly negative among ornaments that can dynamically change in quality, such as behavioral displays and skin pigmentation, and thus can accurately reflect current parasite load. The relationship was also more strongly negative among parasites that can transmit during sex. Thus, the direct benefit of avoiding parasite transmission may be a key driver of parasite-mediated sexual selection. No other moderators, including methodological details and whether males exhibit parental care, explained the substantial heterogeneity in our data set. We hope to stimulate research that more inclusively considers the many and varied ways in which parasites, sexual selection, and epidemiology intersect.

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Shoaling guppies evade predation but have deadlier parasites

Cited by 10 publications

References 72 publications

Predation shifts coevolution toward higher host contact rate and parasite virulence

Predation shifts coevolution toward higher host contact rate and parasite virulence

Effects of predation risk on parasite–host interactions and wildlife diseases

Ornaments indicate parasite load only if they are dynamic or parasites are contagious

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