The Relationship Between Parasite Fitness and Host Condition in an Insect - Virus System

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The Relationship Between Parasite Fitness and Host Condition in an Insect - Virus System The Relationship between Parasite Fitness and Host Condition in an Insect - Virus System Michelle Tseng*, Judith H. Myers Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada Abstract Research in host-parasite evolutionary ecology has demonstrated that environmental variation plays a large role in mediating the outcome of parasite infection. For example, crowding or low food availability can reduce host condition and make them more vulnerable to parasite infection. This observation that poor-condition hosts often suffer more from parasite infection compared to healthy hosts has led to the assumption that parasite productivity is higher in poor- condition hosts. However, the ubiquity of this negative relationship between host condition and parasite fitness is unknown. Moreover, examining the effect of environmental variation on parasite fitness has been largely overlooked in the host-parasite literature. Here we investigate the relationship between parasite fitness and host condition by using a laboratory experiment with the cabbage looper Trichoplusia ni and its viral pathogen, AcMNPV, and by surveying published host-parasite literature. Our experiments demonstrated that virus productivity was positively correlated with host food availability and the literature survey revealed both positive and negative relationships between host condition and parasite fitness. Together these data demonstrate that contrary to previous assumptions, parasite fitness can be positively or negatively correlated with host fitness. We discuss the significance of these findings for host-parasite population biology. Citation: Tseng M, Myers JH (2014) The Relationship between Parasite Fitness and Host Condition in an Insect - Virus System. PLoS ONE 9(9): e106401. doi:10. 1371/journal.pone.0106401 Editor: Matty Knight, George Washington University School of Medicine and Health Sciences, United States of America Received March 29, 2014; Accepted July 30, 2014; Published September 10, 2014 Copyright: ß 2014 Tseng, Myers. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. Data are avilable on the DRYAD depository using the DOI doi:10.5061/dryad.v3t23. Funding: This study was funded by an Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to JHM and an NSERC Postdoctoral Fellowship to MT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * Email: [email protected] Introduction resources to allocate to immune functions or to other defenses against parasites [17,18] thus leaving parasite growth and or Parasites play a significant role in the ecology and evolution of reproduction less inhibited by attack from host defenses. their hosts. For example, parasites can regulate host population As a sidebar, we note here that in general, lifetime parasite fitness dynamics [1–3], drive the maintenance of host sexual reproduc- is typically defined as the parasite basic reproductive ratio, R0, but tion [4–6], and shape the evolution of sexually dimorphic traits because of the multiple components that make up R0 [19–22], [7]. Environmental variation can play a large role in mediating the many studies instead use parasite productivity as a measure of immediate outcome of parasite infection, as hosts that are reared parasite fitness (e.g. [16,22–24] but see [25] for measures of lifetime in crowded conditions or with limited food can suffer greater parasite fitness). Parasite productivity is a reasonable proxy for R0,if morbidity or mortality from parasitism compared to hosts in better productivity is correlated with the number of transmission health [8–14]. Far less is known about how stressful conditions for propagules produced, and if the latter is positively correlated with the host such as crowding or food limitation affect the fitness of the the likelihood of infecting a susceptible host (e.g. [26,27]). parasites. Examining this question is a subtle but significant Here we use the term ‘potential parasite fitness’ (PPF) because departure from most host-parasite studies, where the focus is we do not directly measure parasite R0. Rather, we measure primarily on host performance. Understanding how environmen- components of parasite fitness that are typically positively tal factors affect parasite fitness might result in more accurate correlated with R0. In this study we ask whether parasite predictions regarding the number of parasite propagules available productivity is positively correlated with host food availability (a for subsequent infection. This information can in turn result in proxy of host condition) in the virus Autographa californica more accurate predictions regarding both the likelihood of multiple nucleopolyhedrovirus (AcMNPV), and one of its natural infection, and the severity of infection. hosts, the cabbage looper moth (Trichoplusia ni,Hu¨bner, How might variation in the host’s environment affect parasite Lepidoptera: Noctuidae). fitness? For parasites that depend solely on their hosts for resources and shelter, a poor environment for the host may translate into a Methods poor environment for the parasite. For example, parasites inhabiting low-quality hosts may have less to eat (both quantita- Parasite biology tively and qualitatively), which may reduce parasite production AcMNPV is the type species of the genus Alphabaculovirus in [15,16]. Conversely, hosts in poor condition may have fewer the family Baculoviridae [28]. Baculoviruses are DNA viruses that PLOS ONE | www.plosone.org 1 September 2014 | Volume 9 | Issue 9 | e106401 Environmental Variation and Parasite Fitness primarily infect Lepidoptera [29,30]. Caterpillars typically become (12 hours food/day), or high (continuous access to food). Larvae infected upon ingesting virus occlusion bodies (OB), which are were reared in 25 mL cups and the food source was a wheat germ- proteinaceous structures that contain virions (virus particles) [30]. based diet modified from [38]. Larvae in experiment 1 were Virions released by OBs spread throughout the larval body, and assigned to their food treatment after infection and larvae in eventually the bulk of host tissue is converted into OBs [30–32]. At experiment 2 were assigned to their food treatment before the end of a successful infection, the larva dies and OBs are infection (Table 1). released into the environment. AcMNPV has a wide host range One day after moulting into 4th instar, 90 of the 120 larvae were and can infect species of at least 15 families of Lepidoptera [30]. each given one 0.125 cm3 piece of diet dosed with 5 mLof 1000 OB/mL virus suspension. Preliminary data have shown this Host biology infection method to be sufficient to infect $95% of larvae. After Trichoplusia ni are typically found in the subtropics worldwide 24-hour access to the virus-dosed diet, larvae were assigned to [33] and are also common pests of greenhouse vegetables and their food treatment (experiment 1), or returned to their initial agricultural cole crops at higher latitudes [34]. AcMNPV has been food treatment (experiment 2). The remaining thirty larvae were 3 considered as a possible biological control agent of T. ni [35,36] each fed a 0.125 cm piece of diet dosed with 5 mL distilled water. because it infects T. ni in the wild and has high virulence. This These uninfected larvae were randomly and evenly distributed virus-host system is thus ideal for addressing questions related to into the three food treatments (i.e. 10 uninfected larvae per food PPF because the laboratory results could be applicable in nature, treatment, experiment 1), or returned to their original food as well as to other lepidopteran hosts. treatment (experiment 2). Insect collections and colony maintenance Data collected and statistical analyses Cabbage loopers were collected from commercial greenhouses Infected larvae were maintained on low, medium or high food in the lower mainland of British Columbia, Canada and treatments until death. One day prior to death, when larvae were maintained continuously in the laboratory at the University of rendered immobile, bloated and discoloured by virus infection, British Columbia for 10 years (,50 generations). AcMNPV was larvae were weighed and transferred to 1.5 mL eppendorf tubes. originally isolated from naturally infected T. ni early 2000s. The After death, the tube containing the virus-killed larva was filled virus was used in various laboratory experiments and was purified with distilled water so that the total volume (dead larva plus water) and stored at 220uC when not in use [37]. equaled 1 mL. The entire sample was macerated and total OB To maintain T. ni colonies, neonates were reared in groups of number was quantified using a hemocytometer. Virus OBs were 25 in 200 mL Styrofoam cups filled with 25 mL wheat-germ based counted in each of ten 0.260.2 mm squares. The average number diet [38]. Pupae were transferred to in emergence cages. Adults of OBs per ten squares was then multiplied by 46106 to obtain the mated in these cages and females laid their eggs on a paper towel total OB per larva. We collected data on days to death, weight at lining of the mating cage. Larval rearing cups and adult mating death, and total OBs per larva. We use virus OB number as our cages were maintained at 2661uC 16:8 light:dark. Egg-impreg- measure of PPF. nated paper towels were stored at 5u until eggs were needed. We used ANOVA to examine whether food treatment had a Trichoplusia ni eggs readily hatch at room temperature. statistically significant effect on larval weight at death, days to death, and on virus OB number. We transformed both OB Experimental design number (log OB number +1) and larval weight (log-weight) to We conducted two experiments to examine the relationship meet assumptions of ANOVA.
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