Geography is more important than host plant use for the population genetic structure of a generalist insect herbivore.

Population divergence can occur due to mechanisms associated with geographic isolation and/or due to selection associated with different ecological niches. Much of the evidence for selection-driven speciation has come from studies of specialist insect herbivores that use different host plant species; however, the influence of host plant use on population divergence of generalist herbivores remains poorly understood. We tested how diet breadth, host plant species and geographic distance influence population divergence of the fall webworm (Hyphantria cunea; FW). FW is a broadly distributed, extreme generalist herbivore consisting of two morphotypes that have been argued to represent two different species: black-headed and red-headed. We characterized the differentiation of FW populations at two geographic scales. We first analysed the influence of host plant and geographic distance on genetic divergence across a broad continental scale for both colour types. We further analysed the influence of host plant, diet breadth and geographic distance on divergence at a finer geographic scale focusing on red-headed FW in Colorado. We found clear genetic and morphological distinction between red- and black-headed FW, and Colorado FW formed a genetic cluster distinct from other locations. Although both geographic distance and host plant use were correlated with genetic distance, geographic distance accounted for up to 3× more variation in genetic distance than did host plant use. As a rare study investigating the genetic structure of a widespread generalist herbivore over a broad geographic range (up to 3,000 km), our study supports a strong role for geographic isolation in divergence in this system.

Bottom-up vs. top-down effects on terrestrial insect herbivores: a meta-analysis.

Primary consumers are under strong selection from resource ('bottom-up') and consumer ('top-down') controls, but the relative importance of these selective forces is unknown. We performed a meta-analysis to compare the strength of top-down and bottom-up forces on consumer fitness, considering multiple predictors that can modulate these effects: diet breadth, feeding guild, habitat/environment, type of bottom-up effects, type of top-down effects and how consumer fitness effects are measured. We focused our analyses on the most diverse group of primary consumers, herbivorous insects, and found that in general top-down forces were stronger than bottom-up forces. Notably, chewing, sucking and gall-making herbivores were more affected by top-down than bottom-up forces, top-down forces were stronger than bottom-up in both natural and controlled (cultivated) environments, and parasitoids and predators had equally strong top-down effects on insect herbivores. Future studies should broaden the scope of focal consumers, particularly in understudied terrestrial systems, guilds, taxonomic groups and top-down controls (e.g. pathogens), and test for more complex indirect community interactions. Our results demonstrate the surprising strength of forces exerted by natural enemies on herbivorous insects, and thus the necessity of using a tri-trophic approach when studying insect-plant interactions.

Quantitative measure of fitness in tri-trophic interactions and its influence on diet breadth of insect herbivores.

Herbivore-plant interactions should be studied using a tri-trophic approach, but we lack a quantitative measure of the combined effect of top-down and bottom-up forces on herbivore fitness. We propose the combination of the bi-trophic fitness slopes as a tri-trophic fitness measure. We use the relationship between fitness associated with top-down and bottom-up forces and the frequency of host plant use to calculate the top-down and bottom-up fitness slopes, which we then combine to obtain three possible directions of tri-trophic slopes. A positive tri-trophic slope indicates that herbivores have overall greater tri-trophic fitness on the more frequently used hosts. A null tri-trophic fitness slope indicates that herbivores have similar fitness on all host plants. A negative tri-trophic slope indicates that herbivores have generally lower fitness on the more frequently used hosts. We tested the explanation power of our method using data from the literature that tested herbivore host shifts and experimentally using a generalist herbivore with variable diet breadth across populations. We found that in host shifts, herbivores have higher tri-trophic fitness on the novel host, while in generalist populations, herbivores use most frequently the best host available. We present applications in other research areas and consider the limitations of our approach. Our approach is a first step towards a comprehensive model of multiple selective forces acting on the evolution of interactions.

Mutualism exploitation: predatory drosophilid larvae sugar-trap ants and jeopardize facultative ant-plant mutualism.

An open question in the evolutionary ecology of ant-plant facultative mutualism is how other members of the associated community can affect the interaction to a point where reciprocal benefits are disrupted. While visiting Qualea grandiflora shrubs to collect sugary rewards at extrafloral nectaries, tropical savanna ants deter herbivores and reduce leaf damage. Here we show that larvae of the fly Rhinoleucophenga myrmecophaga, which develop on extrafloral nectaries, lure potentially mutualistic, nectar-feeding ants and prey on them. Foraging ants spend less time on fly-infested foliage. Field experiments showed that predation (or the threat of predation) on ants by fly larvae produces cascading effects through three trophic levels, resulting in fewer protective ants on leaves, increased numbers of chewing herbivores, and greater leaf damage. These results reveal an undocumented mode of mutualism exploitation by an opportunistic predator at a plant-provided food source, jeopardizing ant-derived protection services to the plant. Our study documents a rather unusual case of predation of adult ants by a dipteran species and demonstrates a top-down trophic cascade within a generalized ant-plant mutualism.

Sphingid caterpillars conspicuous patches do not function as distractive marks or warning against predators.

To avoid predation by visual predators, caterpillars can be cryptic to decrease detectability or aposematic to warn predators of potential unpalatability. However, for some species, it is not clear if conspicuous patches are selected to avoid predation. For example, Pandora sphinx (Eumorpha pandorus, Lepidoptera: Sphingidae) caterpillars are assumed to be palatable and have both cryptic (green, brown) and conspicuous (orange, red) color morphs. Five lateral, off-white to yellow patches on either side may serve as a warning for predators or to draw attention away from the caterpillar's form to function as distractive marks. We conducted a field study in three temperate fragmented forests in Massachusetts to investigate the potential utility of E. pandorus coloration and conspicuous patches. Using four plasticine caterpillar prey model treatments, green and red with and without lateral conspicuous patches, we tested the effects of color, patch patterning, and seasonality on attack rates by a variety of taxa. We found that 43% of the prey models (n = 964) had bite marks by an array of predators including arthropods (67.5%), birds (18.2%), rodents (11.5%), and large mammals (2.8%). Arthropods as dominant predators align with conclusions from previous studies of prey models placed near ground level. Attack rates peaked for arthropods in late August and early September but were more constant across trials for vertebrates. Arthropods, a heterogeneous group, as indicated by the variety of bite marks, showed significantly higher attack rates on green colored prey models and a tendency of higher attack on solid (non-patch patterned) prey models. Vertebrates, more visually oriented predators, had significantly higher attack rates on red colored prey models and patch patterned prey models. Thus, our results did not suggest that conspicuous patch patterning reduced predation and therefore, we did not find support for the distractive mark hypothesis or warning hypothesis. Further, our study shows clear contrasting interpretations by different predators regarding visual defensive strategies.

Interspecific Host Variation and Biotic Interactions Drive Pathogen Community Assembly in Chinese Bumblebees.

Bumblebees have been considered one of the most important pollinators on the planet. However, recent reports of bumblebee decline have raised concern about a significant threat to ecosystem stability. Infectious diseases caused by multiple pathogen infections have been increasingly recognized as an important mechanism behind this decline worldwide. Understanding the determining factors that influence the assembly and composition of pathogen communities among bumblebees can provide important implications for predicting infectious disease dynamics and making effective conservation policies. Here, we study the relative importance of biotic interactions versus interspecific host resistance in shaping the pathogen community composition of bumblebees in China. We first conducted a comprehensive survey of 13 pathogens from 22 bumblebee species across China. We then applied joint species distribution modeling to assess the determinants of pathogen community composition and examine the presence and strength of pathogen-pathogen associations. We found that host species explained most of the variations in pathogen occurrences and composition, suggesting that host specificity was the most important variable in predicting pathogen occurrences and community composition in bumblebees. Moreover, we detected both positive and negative associations among pathogens, indicating the role of competition and facilitation among pathogens in determining pathogen community assembly. Our research demonstrates the power of a pluralistic framework integrating field survey of bumblebee pathogens with community ecology frameworks to understand the underlying mechanisms of pathogen community assembly.

Coevolved mutualists experience fluctuating costs and benefits over time.

Understanding how mutualisms persist over time requires investigations of how mutualist species coevolve and adapt to the interaction. In particular, the key factors in the evolution of mutualisms are the costs and benefits mutualists experience during the interaction. Here, we used a yeast nutritional mutualism to test how mutualists coevolve and adapt in an obligate mutualism. We allowed two yeast mutualists to evolve together for 15 weeks (about 150 generations), and then we tested if the mutualists had coevolved using time-shift assays. We also examined two mutualistic traits associated with the costs and benefits: resource use efficiency and commodity production. We found that the mutualists quickly coevolved. Furthermore, the changes in benefits and costs were nonlinear and varied with evolutionary changes occurring in the mutualist partner. One mutualist initially evolved to reduce mutualistic commodity production and increase efficiency in mutualistic resource use; however, this negatively affected its mutualist partner that evolved reduced commodity production and resource use efficiency. As a result, the former increased commodity production, resulting in an increase in benefits for its partner. The quick, nonlinear, and asynchronous evolution of yeast mutualists closely resembles antagonistic coevolutionary patterns, supporting the view that mutualisms should be considered as reciprocal exploitation.

The variable effects of global change on insect mutualisms.

Insect mutualisms are essential for reproduction of many plants, protection of plants and other insects, and provisioning of nutrients for insects. Disruption of these mutualisms by global change can have important implications for ecosystem processes. Here, we assess the general effects of global change on insect mutualisms, including the possible impacts on mutualistic networks. We find that the effects of global change on mutualisms are extremely variable, making broad patterns difficult to detect. We require studies focusing on changes in cost-benefit ratios, effects of partner dependency, and degree of specialization to further understand how global change will influence insect mutualism dynamics. We propose that rapid coevolution is one avenue by which mutualists can ameliorate the effects of global change.

Species richness and redundancy promote persistence of exploited mutualisms in yeast.

Mutualisms, or reciprocally beneficial interspecific interactions, constitute the foundation of many ecological communities and agricultural systems. Mutualisms come in different forms, from pairwise interactions to extremely diverse communities, and they are continually challenged with exploitation by nonmutualistic community members (exploiters). Thus, understanding how mutualisms persist remains an essential question in ecology. Theory suggests that high species richness and functional redundancy could promote mutualism persistence in complex mutualistic communities. Using a yeast system (Saccharomyces cerevisiae), we experimentally show that communities with the greatest mutualist richness and functional redundancy are nearly two times more likely to survive exploitation than are simple communities. Persistence increased because diverse communities were better able to mitigate the negative effects of competition with exploiters. Thus, large mutualistic networks may be inherently buffered from exploitation.

Natural History of a Sit-and-Wait Dipteran Predator That Uses Extrafloral Nectar as Prey Attractant.

Sit-and-wait predators use different strategies to encounter potential prey. Rhinoleucophenga myrmecophaga Vidal et (Vidal et Vilela; Diptera: Drosophilidae) larvae build sticky shelters on top of extrafloral nectaries (EFNs) of Qualea grandiflora Mart (Vochysiaceae), a common plant in the Brazilian cerrado savanna. Although larval shelters block the EFNs, nectar production is not obstructed and is used by the larvae to attract and trap nectar-gathering ants that are eventually eaten by the dipteran. Here we describe the natural history of R. myrmecophaga, its infestation pattern in Q. grandiflora, the ant assemblage at EFNs, and the insects used as prey. We use stable isotope composition (δ13C and δ15N) of R. myrmecophaga and potential food sources to infer its diet, and perform chemical analyses of the droplets found at shelter openings to determine whether nectar is used as a prey attractant. We found that Rhinoleucophenga larvae occur on the majority of Qualea plants and occupy active EFNs mainly in the rainy season. The two most frequent visiting species were also the most common insects found trapped at larval shelters. The stable isotope analyses confirmed that ants are the main food sources of R. myrmecophaga. Chemical analyses and field observations revealed that Rhinoleucophenga larvae use extrafloral nectar to attract prey to their shelters by pushing this liquid to the shelter opening where it forms a droplet. This is a rare case of sit-and-wait predator exploiting an ant-plant mutualism through the use of the very food reward produced by the plant to attract and capture potential ant mutualists.

Global change and the importance of fire for the ecology and evolution of insects.

Climate change is drastically altering global fire regimes, which may affect the structure and function of insect communities. Insect responses to fire are strongly tied to fire history, plant responses, and changes in species interactions. Many insects already possess adaptive traits to survive fire or benefit from post-fire resources, which may result in community composition shifting toward habitat and dietary generalists as well as species with high dispersal abilities. However, predicting community-level resilience of insects is inherently challenging due to the high degree of spatiotemporal and historical heterogeneity of fires, diversity of insect life histories, and potential interactions with other global change drivers. Future work should incorporate experimental approaches that specifically consider spatiotemporal variability and regional fire history in order to integrate eco-evolutionary processes in understanding insect responses to fire.