Defensive variability of crops and natural systems can alter herbivore communities and reduce herbivory [1, 2]. However, it is still unknown how defense variability translates into herbivore suppression. Nonlinear averaging and constraints in physiological tracking (also more generally called time-dependent effects) are the two mechanisms by which defense variability might impact herbivores [3, 4]. We conducted a set of experiments manipulating the mean and variability of a plant defense, showing that defense variability does suppress herbivore performance and that it does so through physiological tracking effects that cannot be explained by nonlinear averaging. While nonlinear averaging predicted higher or the same herbivore performance on a variable defense than on an invariable defense, we show that variability actually decreased herbivore performance and population growth rate. Defense variability reduces herbivore performance in a way that is more than the average of its parts. This is consistent with constraints in physiological matching of detoxification systems for herbivores experiencing variable toxin levels in their diet and represents a more generalizable way of understanding the impacts of variability on herbivory [5]. Increasing defense variability in croplands at a scale encountered by individual herbivores can suppress herbivory, even if that is not anticipated by nonlinear averaging.
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Hymenopterans make up about 20% of all animal species, but most are poorly known and lack high-quality genomic resources. One group of important, yet under-studied hymenopterans, are parasitoid wasps in the family Braconidae. Among this under-studied group are braconid wasps in the genus Cotesia; a clade of ~1,000 species routinely used in studies of physiology, ecology, biological control, and genetics. However, our ability to understand these organisms has been hindered by a lack of genomic resources. We helped bridge this gap by generating a high-quality genome assembly for the parasitoid wasp, Cotesia glomerata (Braconidae; Microgastrinae). We generated this assembly using multiple sequencing technologies, including Oxford Nanopore, whole-genome shotgun sequencing, and 3-D chromatin contact information (Hi-C). Our assembly is one of the most contiguous, complete, and publicly available hymenopteran genomes, represented by 3,355 scaffolds with a scaffold N50 of ~28Mb and a BUSCO score of ~99%. Given the genome sizes found in closely related species, our genome assembly was ~50% larger than expected, which was apparently induced by runaway amplification of three types of repetitive elements: simple repeats, Long Terminal Repeats (LTRs), and Long Interspersed Nuclear Elements (LINEs). This assembly is another step forward for genomics across this hyper-diverse, yet understudied, order of insects. The assembled genomic data and metadata files are publicly available via Figshare (https://doi.org/10.6084/m9.figshare.13010549).
Herbivore populations are regulated by a combination of plant defences and natural enemies. While plant defence can suppress herbivore populations, these defences can also adversely affect natural enemies, thereby releasing herbivores from top‐down control. Over their life spans, herbivores and their natural enemies may experience substantial variation in plant defence. Recent studies have demonstrated that individual herbivores feeding on diets containing variable concentrations of plant toxins suffer substantially reduced fitness compared to herbivores feeding on a constant toxin concentration, even when both groups of herbivores experience equivalent means. However, the impacts of defence variability on natural enemies and top‐down control of herbivores are unknown. Using artificial diets, we independently manipulated the mean concentration and variation of a plant toxin experienced by individual Trichoplusia ni caterpillars and its parasitoid Copidosoma floridanum. Additionally, by combining the performance of individual caterpillars on different constant diet concentrations of toxin, we were able to estimate the effect of toxin variability between herbivores using nonlinear averaging. Increases in the mean toxin concentration in the diet of parasitized T. ni hosts decreased the fitness of C. floridanum, while variance in individual diets did not impact parasitoid fitness, even though both mean and variance decreased the fitness of T. ni caterpillars. Increased variability in encountered plant defences suppressed individual herbivore fitness with no perceptible cost to top‐down control. At the population level, however, increased variability between individual herbivore diets decreased the success of parasitoids relative to herbivores, thus reducing the strength of top‐down control. Our study highlights the importance of defence variability at different scales in regulating herbivore performance. Variability in plant defence has the potential to reduce herbivore populations through a combination of bottom‐up and top‐down effects, but only at small spatial scales experienced by individual herbivores. A free Plain Language Summary can be found within the Supporting Information of this article.
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