Effects of pathogen exposure on life‐history variation in the gypsy moth (<i>Lymantria dispar</i>)

Páez, David J.; Fleming-Davies, Arietta; Dwyer, Greg

doi:10.1111/jeb.12699

Cited by 20 publications

(36 citation statements)

References 61 publications

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“…Moreover, the insect ecology literature suggests that eco-evolutionary dynamics may play a role in population cycles of other forest defoliating insects (Anderson and May 1981; Myers 1988, 1993). First, although previous studies used only dose-response experiments, gypsy moth dose-response experiments have shown the same trends as in our field transmission experiments (Páez et al 2015). This in turn suggests that laboratory observations of heritable variation and costs of resistance in other insects (Boots and Begon 1993; Cory and Myers 2009; Watanabe 1987) may likewise indicate that natural selection plays a role in those insects in the field.…”

Section: Discussionsupporting

confidence: 57%

“…B) Variation in average infection risk across half-sibling families, again suggesting that infection risk is heritable. C) Fecundity cost of resistance, as demonstrated by a positive relationship between infection risk and female pupal mass, a surrogate measure of fecundity (Páez et al 2015).…”

Section: Resultsmentioning

confidence: 99%

“…Part of the reason why it is important to measure infection risk in the field is because infection risk depends on feeding behavior, which cannot be easily allowed for in laboratory experiments (Dwyer et al 2005). Feeding behavior affects the overall risk of infection by determining the risk of exposure, with the proviso that the overall risk of infection is also affected by the risk of infection given exposure, which is instead determined by the insect’s immune response (Páez et al 2015). Feeding behavior is thus important because gypsy moth larvae can sometimes detect and avoid virus-infected cadavers (Capinera et al 1976), a heritable behavior (Parker et al 2010), but variation in risk given exposure is also heritable (Páez et al 2015).…”

Section: Methodsmentioning

confidence: 99%

“…Feeding behavior affects the overall risk of infection by determining the risk of exposure, with the proviso that the overall risk of infection is also affected by the risk of infection given exposure, which is instead determined by the insect’s immune response (Páez et al 2015). Feeding behavior is thus important because gypsy moth larvae can sometimes detect and avoid virus-infected cadavers (Capinera et al 1976), a heritable behavior (Parker et al 2010), but variation in risk given exposure is also heritable (Páez et al 2015). By measuring overall infection risk, we thus allowed for variation in both components of infection risk.…”

Section: Methodsmentioning

confidence: 99%

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Eco-evolutionary theory and insect outbreaks

Páez

Dukić

Dushoff

et al. 2016

Preprint

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Eco-evolutionary theory argues that population cycles in consumer-resource interactions are partly driven by natural selection, such that changes in densities and changes in trait values 3 are mutually reinforcing. Evidence that this theory explains cycles in nature, however, is almost nonexistent. Experimental tests of model predictions are almost always impossible because of the long time scales over which cycles occur, but for most organisms, even tests of model assump-6 tions are logistically impractical. For insect baculoviruses in contrast, tests of model assumptions are straightforward, and baculoviruses often drive outbreaks of forest-defoliating insects, as in the gypsy moth that we study here. We therefore used field experiments with the gypsy moth 9 baculovirus to test two key assumptions of eco-evolutionary models of host-pathogen population cycles, that reduced host infection risk is heritable and costly. Our experiments confirm the two assumptions, and inserting parameters estimated from our data into the models gives cy-12 cles closely resembling gypsy moth outbreak cycles in North America, whereas standard models predict unrealistic stable equilibria. Our work shows that eco-evolutionary models are useful for explaining outbreaks of forest insect defoliators, while widespread observations of intense 15 selection imposed by natural enemies on defoliators, and frequent laboratory observations of heritable and costly resistance in defoliators, suggest that eco-evolutionary dynamics may play a general role in defoliator outbreaks. 18 only infection risk given exposure (Altizer et al. 2003). Previous work has therefore not provided 45 robust tests of model assumptions.An underlying problem is that overall infection risk is best measured in the field, but for most host-pathogen interactions, field experiments are impractical. Meanwhile, for the few host-48 pathogen interactions for which experiments have measured infection risk in the laboratory or the greenhouse (Auld et al. 2014, 2013; Henter and Via 1995; Herzog et al. 2007; Zbinden et al. 2008), there are no data demonstrating that population cycles occur in nature. For insect bac-51 uloviruses in contrast, field experiments are straightforward (Elderd 2013), and because of the economic importance of the gypsy moth as an outbreaking forest pest, there are extensive data documenting gypsy moth population cycles (Johnson et al. 2005). 54Previous efforts to explain these cycles, however, have met with limited success. Classical insect-pathogen models require variability in host infection risk to prevent pathogen extinction, but realistically high variability causes the models to produce a stable equilibrium instead of 57 cycles (Dwyer et al. 2000). Extending classical models to allow pathogen transmission to be affected by induced plant defenses leads to models that can explain gypsy moth cycles, but the resulting host-pathogen/induced-defense models require particular spatial configurations of tree 60 species (Elderd et al. 2013), and so cannot explai...

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Section: Discussionsupporting

confidence: 57%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Eco-evolutionary theory and insect outbreaks

Páez

Dukić

Dushoff

et al. 2016

Preprint

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“…Natural selection may therefore play a key role in tussock moth population cycles, as in the gypsy moth (Páez et al, 2017). More broadly, genetic variation in susceptibility to disease is omnipresent (Keeling and Rohani, 2008), and so it seems likely that 501 the lack of evidence for host-variation effects in other pathogens is due to a lack of consideration of host-variation effects, rather than to an actual lack of host variation.…”

Section: Discussionmentioning

confidence: 99%

An empirical test of the role of small-scale transmission in large-scale disease dynamics

Mihaljevic

Polivka

Mehmel³

et al. 2018

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Mathematical models have provided important insights into infectious disease spread in animal populations, but are only rarely used in environmental management. Part of the problem 3 may be that direct tests of the models have focused on long-term model predictions, whereas short-term epizootics (= epidemics in animals) can sometimes be more informative about mechanisms of disease transmission. To illustrate this point, we tested models of density-dependent 6 disease transmission and host variation in infection risk using multiple, single-host-generation epizootics of a fatal baculovirus of the Douglas-fir tussock moth (Orgyia pseudotsugata). The tussock moth baculovirus causes epizootics naturally, but because of its narrow host range, it is used 9 in biological control to mitigate defoliation, an approach known as "microbial control". Using a combination of experiments, observational data, and nonlinear-fitting algorithms, we fit a set of stochastic epidemiological models to data from tussock moth microbial control programs. We 12 then used formal model comparisons to show that there are strong effects of host and pathogen density and host variation on epizootic severity, and that transmission events at small scales help explain epizootic severity at large scales. When host density is high, even very low initial virus 15 densities can lead to high cumulative infection rates, suggesting that, in some cases, baculovirus sprays may have been applied to populations that would have collapsed from natural epizootics, even without intervention. Our study illustrates the usefulness of linking epidemiological mod-18 eling and nonlinear fitting routines in understanding animal diseases, and shows that simple models can provide important guidance for microbial control programs.

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