Plant genotype and induced defenses affect the productivity of an insect-killing obligate viral pathogen

© 2017 Elsevier Inc. Plant-mediated variations in the outcomes of host-pathogen interactions can strongly affect epizootics and the population dynamics of numerous species, including devastating agricultural pests such as the fall armyworm. Most studies of plant-mediated effects on insect pathogens focus on host mortality, but few have measured pathogen yield, which can affect whether or not an epizootic outbreak occurs. Insects challenged with baculoviruses on different plant species and parts can vary in levels of mortality and yield of infectious stages (occlusion bodies; OBs). We previously demonstrated that soybean genotypes and induced anti-herbivore defenses influence baculovirus infectivity. Here, we used a soybean genotype that strongly reduced baculovirus infectivity when virus was ingested on induced plants (Braxton) and another that did not reduce infectivity (Gasoy), to determine how soybean genotype and induced defenses influence OB yield and speed of kill. These are key fitness measures because baculoviruses are obligate-killing pathogens. We challenged fall armyworm, Spodoptera frugiperda, with the baculovirus S. frugiperda multi-nucleocapsid nucleopolyhedrovirus (SfMNPV) during short or long-term exposure to plant treatments (i.e., induced or non-induced genotypes). Caterpillars were either fed plant treatments only during virus ingestion (short-term exposure to foliage) or from the point of virus ingestion until death (long-term exposure). We found trade-offs of increasing OB yield with slower speed of kill and decreasing virus dose. OB yield increased more with longer time to death and decreased more with increasing virus dose after short-term feeding on Braxton compared with Gasoy. OB yield increased significantly more with time to death in larvae that fed until death on non-induced foliage than induced foliage. Moreover, fewer OBs per unit of host tissue were produced when larvae were fed induced foliage than non-induced foliage. These findings highlight the potential importance of plant effects, even at the individual plant level, on entomopathogen fitness, which may impact epizootic transmission events and host population dynamics

Direct and indirect effects of host plant selection on larval performance in the cabbage looper, Trichoplusia ni

Generalist insects should possess the ability to rank potential host plants for the suitability of their offspring. The decision to oviposit on a host plant that is inferior for larval development could have significant consequences for their offspring. Host plant quality can affect larval development and survival directly via nutrients and/or defensive chemicals, as well as indirectly by influencing larval condition and consequently their susceptibility to pathogens. In this thesis I examine the relationship between host preference and plant quality for larval performance in the cabbage looper, Trichoplusia ni (Hubner). I also examine the relationship between host plant quality, insect condition, immune responsiveness and resistance to pathogens. No-choice, two-choice, and multiple-choice experiments were performed to measure adult oviposition preference and neonate larval preference for six plant species. Two baseline and induced immune parameters, haemocyte numbers and haemolymph phenoloxidase (PO) activity, were estimated for larvae on two host plants, broccoli and cucumber. Haemolymph protein concentration was assessed as an indication of insect condition, and the susceptibility of larvae to T. ni single nucleopolyhedrovirus (SNPV) was used as a measure of disease resistance. Trichoplusia ni adults and larvae both preferred the same two plant species out of six that maximised larval performance. Larvae however, also correctly identified anise hyssop as a suitable host, whereas adults did not, indicating that larval diet breadth can be wider than adult host range. Larval development, survival and condition were much higher when larvae were reared on broccoli than on cucumber. Haemocyte numbers were significantly higher in broccoli-reared larvae, whereas PO activity was not. An immune challenge induced significantly elevated numbers of haemocytes for larvae reared on both hosts, but did not affect PO activity or protein concentrations. Susceptibility to T. ni SNPV was significantly greater in larvae reared on cucumber than on broccoli. These results clearly indicate that T. ni are capable of ranking the suitability of plants for larval performance. Larval development on an inferior host plant can affect both immune response and disease resistance indicating that bottom-up effects could be important in interactions between insects and entomopathogens.Land and Food Systems, Faculty ofGraduat

The impact of nutrition on within and trans-generational disease resistance in the cabbage looper, Trichoplusia ni

Parasites and pathogens are ubiquitous, and pose a threat to all living organisms. Investment in resistance mechanisms to fight parasite challenge can be costly, often resulting in trade-offs with other life-history traits. Host nutrition can alter the availability of resources to invest in resistance mechanisms and influence host-parasite interactions and their outcomes. I investigated the impact of nutrition on disease resistance in the cabbage looper, Trichoplusia ni. I assessed the role of dietary macronutrients on the expression of fitness costs exhibited by a T. ni strain that has evolved resistance to the bacterial pathogen, Bacillus thuringiensis (Bt). Reduced pupal weight and growth rate, which are fitness costs associated with Bt-resistance, resulted from reduced food intake rather than impaired macronutrient utilization. When given a choice, Bt-resistant T. ni self-composed a higher ratio of protein to carbohydrate (P:C ratio) than Bt-susceptible T. ni, allowing males to eliminate a fitness cost (reduced pupal weight), but not females. Next, I investigated the interaction between host nutrition and another key environmental factor, temperature, on the interaction between T. ni and two species of baculoviruses differing in host range (TnSNPV, narrow range; AcMNPV, broad range). Optimal performance of T. ni shifted to higher P:C ratios when challenged by either virus as survival increased with dietary protein content. This effect was strongly affected by temperature when challenged by AcMNPV but not TnSNPV. Virus performance was also differentially affected by the host’s environmental condition, such that AcMNPV had a broader peak of optimal performance (combined measure of host mortality and virus production) across environmental conditions than TnSNPV. Lastly, I examined the impact of nutritional stress on the ability of Bt-challenged T. ni to prime the immune system of their offspring. If parental T. ni experienced only nutritional stress or Bt-challenge, they transferred nutritional stress tolerance or immune priming to their offspring respectively. However, as surviving each stressor is costly, when experienced simultaneously a trade-off was observed where only immune priming was transferred. This study highlights the important influence of host nutrition on host resistance to pathogens, costs associated with resistance, and pathogen virulence and growth

Enemy-Risk Effects in Parasitoid-Exposed Diamondback Moth Larvae: Potential Mediation of the Interaction by Host Plants

Enemy-risk effects (i.e., non-consumptive effects) describe the non-lethal fitness costs incurred by animals when they perceive a risk of predation. These effects can result from fear-associated changes in behavior and physiology. Diamondback moth larvae (Plutella xylostella) are known to violently wriggle backwards and drop from their host plants, usually suspending themselves with a silk thread, when threatened by predators and parasitoids. Here, we investigated the developmental costs associated with this behavior when larvae were exposed to its specialist parasitoid wasp (Diadegma insulare). Additionally, the structural and chemical properties of plants are well-known to influence predation and parasitism rates of herbivorous insects. Yet, few studies have examined the influence of plants on enemy-risk effects. Therefore, we examined the developmental costs associated with parasitism risk on two host plants. Diamondback moth larvae were placed on either cabbage or Virginia pepperweed plants and exposed to gravid parasitoids with truncated ovipositors, which prevented piercing of the host cuticle without affecting host searching and attacking behaviors. On Virginia pepperweed, risk of parasitism resulted in reduced larval weight gain, longer development time, and smaller adult size compared to larvae that were not exposed to parasitoids. However, on cabbage, parasitoid exposure prolonged development time but had no significant effects on larval weight gain and adult size. On both plants, parasitoid-exposed larvae were found feeding on older foliage than younger foliage. Our findings demonstrate that the enemy-escape behavior of diamondback moths has developmental costs and that plants may mediate the intensity of these enemy-risk effects

Genetic Resistance to Bacillus thuringiensis Alters Feeding Behaviour in the Cabbage Looper, Trichoplusia ni

Evolved resistance to xenobiotics and parasites is often associated with fitness costs when the selection pressure is absent. Resistance to the widely used microbial insecticide Bacillus thuringiensis (Bt) has evolved in several insect species through the modification of insect midgut binding sites for Bt toxins, and reports of costs associated with Bt resistance are common. Studies on the costs of Bt-resistance restrict the insect to a single artificial diet or host-plant. However, it is well documented that insects can self-select appropriate proportions of multiple nutritionally unbalanced foods to optimize life-history traits. Therefore, we examined whether Bt-resistant and susceptible cabbage loopers Trichoplusia ni differed in their nutrient intake and fitness costs when they were allowed to compose their own protein:carbohydrate diet. We found that Bt-resistant T. ni composed a higher ratio of protein to carbohydrate than susceptible T. ni. Bt-resistant males exhibited no fitness cost, while the fitness cost (reduced pupal weight) was present in resistant females. The absence of the fitness cost in resistant males was associated with increased carbohydrate consumption compared to females. We demonstrate a sex difference in a fitness cost and a new behavioural outcome associated with Bt resistance

Għajdut Malti

L-awtur jagħti lista ta’ xi espressjonijiet Maltin li jingħadu mill-kelliema nattivi fit-taħdit tagħhom.N/

Fitness costs associated with <i>Bt</i> resistance in <i>T. ni</i>.

<p>(A) Pupal dry weight and (B) relative growth rate (RGR) for final instar Bt-S and Bt-RU larvae across the five P∶C ratio diets, presented as least squares means (±SE) adjusted for initial larval weight and sex. (C) Mean (±SE) number of days to pupation. RGR  =  [ln(dry pupal mass) – ln(dry initial larval mass)]/days to pupation <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0105864#pone.0105864-Gotthard1" target="_blank">[53]</a>. Different letters indicate significant differences (Tukey HSD comparison).</p

Comparisons of nutrient conversion efficiency between <i>Bt</i>-resistant and susceptible <i>T. ni</i>.

<p>(A) Efficiency of conversion of ingested carbohydrate to pupal lipid content and (B) ingested protein to pupal nitrogen content of pupated Bt-S (solid bars) and Bt-RU (open bars) across the five P∶C diet treatments. Efficiency of conversion of ingested macronutrients to body content are presented as least squares means of body content adjusted for the amount of ingested macronutrient (carbohydrate or protein), initial larval weight, and sex. Different letters indicate significant differences (Tukey HSD comparison).</p

Sex differences in compensatory feeding.

<p>Least squares means (±SE) of total protein and carbohydrate consumption for female and male Bt-S and Bt-RU. Different letters indicate significant differences from Tukey HSD comparison (p<0.05).</p