Michael S. Singer

Host specificity of Lepidoptera in tropical and temperate forests

For numerous taxa, species richness is much higher in tropical than in temperate zone habitats. A major challenge in community ecology and evolutionary biogeography is to reveal the mechanisms underlying these differences. For herbivorous insects, one such mechanism leading to an increased number of species in a given locale could be increased ecological specialization, resulting in a greater proportion of insect species occupying narrow niches within a community. We tested this hypothesis by comparing host specialization in larval Lepidoptera (moths and butterflies) at eight different New World forest sites ranging in latitude from 15° S to 55° N. Here we show that larval diets of tropical Lepidoptera are more specialized than those of their temperate forest counterparts: tropical species on average feed on fewer plant species, genera and families than do temperate caterpillars. This result holds true whether calculated per lepidopteran family or for a caterpillar assemblage as a whole. As a result, there is greater turnover in caterpillar species composition (greater β diversity) between tree species in tropical faunas than in temperate faunas. We suggest that greater specialization in tropical faunas is the result of differences in trophic interactions; for example, there are more distinct plant secondary chemical profiles from one tree species to the next in tropical forests than in temperate forests as well as more diverse and chronic pressures from natural enemy communities.

Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars

Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory.

The global distribution of diet breadth in insect herbivores

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration. Understanding variation in resource specialization is important for progress on issues that include coevolution, community assembly, ecosystem processes, and the latitudinal gradient of species richness. Herbivorous insects are useful models for studying resource specialization, and the interaction between plants and herbivorous insects is one of the most common and consequential ecological associations on the planet. However, uncertainty persists regarding fundamental features of herbivore diet breadth, including its relationship to latitude and plant species richness. Here, we use a global dataset to investigate host range for over 7,500 insect herbivore species covering a wide taxonomic breadth and interacting with more than 2,000 species of plants in 165 families. We ask whether relatively specialized and generalized herbivores represent a dichotomy rather than a continuum from few to many host families and species attacked and whether diet breadth changes with increasing plant species richness toward the tropics. Across geographic regions and taxonomic subsets of the data, we find that the distribution of diet breadth is fit well by a discrete, truncated Pareto power law characterized by the predominance of specialized herbivores and a long, thin tail of more generalized species. Both the taxonomic and phylogenetic distributions of diet breadth shift globally with latitude, consistent with a higher frequency of specialized insects in tropical regions. We also find that more diverse lineages of plants support assemblages of relatively more specialized herbivores and that the global distribution of plant diversity contributes to but does not fully explain the latitudinal gradient in insect herbivore specialization.

Revisiting the evolution of ecological specialization, with emphasis on insect–plant interactions

Ecological specialization is a fundamental and well-studied concept, yet its great reach and complexity limit current understanding in important ways. More than 20 years after the publication of D. J. Futuyma and G. Morenos oft-cited, major review of the topic, we synthesize new developments in the evolution of ecological specialization. Using insect-plant interactions as a model, we focus on important developments in four critical areas: genetic architecture, behavior, interaction complexity, and macroevolution. We find that theory based on simple genetic trade-offs in host use is being replaced by more subtle and complex pictures of genetic architecture, and multitrophic interactions have risen as a necessary framework for understanding specialization. A wealth of phylogenetic data has made possible a more detailed consideration of the macroevolutionary dimension of specialization, revealing (among other things) bidirectionality in transitions between generalist and specialist lineages. Technological advances, including genomic sequencing and analytical techniques at the community level, raise the possibility that the next decade will see research on specialization spanning multiple levels of biological organization in non-model organisms, from genes to populations to networks of interactions in natural communities. Finally, we offer a set of research questions that we find to be particularly pressing and fruitful for future research on ecological specialization.

Phytophagous Insect-Microbe Mutualisms and Adaptive Evolutionary Diversification

Abstract Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.

ROLES OF FOOD QUALITY AND ENEMY‐FREE SPACE IN HOST USE BY A GENERALIST INSECT HERBIVORE

The relative importance of food quality vs. enemy-free space remains an unresolved but central issue in the evolutionary ecology of host use by phytophagous insects. In this study, we investigate their relative importance in determining host-plant use by a generalist caterpillar, Estigmene acrea (Lepidoptera: Arctiidae). In nature, E. acrea late- instar caterpillars preferred Senecio longilobus (Asteraceae), which contains pyrrolizidine alkaloids that the caterpillars sequester, over Viguiera dentata (Asteraceae), a natal host, and typically suffered a 28% mortality risk from parasitoids. We hypothesized that the natural, mixed diet of caterpillars provides high-quality food via hosts like Viguiera as well as antiparasitoid defense via sequestered toxins from Senecio. We found that a pure Viguiera diet provides superior growth performance over a pure Senecio or mixed diet in the absence of parasitism. However, when parasitism risk is at least moderate, the mixed diet provides a survival advantage over the pure diets of Viguiera or Senecio. We therefore conclude that the balance between benefits of growth (food quality) and defense (enemy-free space) maintains the use of a mixed diet in nature. Furthermore, the value of enemy-free space supercedes the value of food quality in determining the host-plant preference of late-instar caterpillars.

The interplay between nutrient balancing and toxin dilution in foraging by a generalist insect herbivore

Food mixing by herbivores is thought to balance nutrient intake and possibly dilute secondary metabolites characteristic of different host plant species. Most empirical work on insect herbivores has focused on nutrient balancing in laboratory settings. In this study, we characterize food mixing behaviour of the caterpillar Grammia geneura (Strecker) (Lepidoptera: Arctiidae) in nature and use the observed patterns to design ecologically relevant experiments that reveal the relative importance of these processes in food-switching behaviour. Our design involved both choice and no-choice experiments with chemically defined diets in which primary nutrients and secondary metabolites were manipulated in tandem. We analysed two stages in the process of food-switching behaviour: leaving food and accepting new food. In nature, an individual’s rate of leaving host plants was positively associated with its probability of rejecting plant species most recently eaten, but not related to its probability of accepting different host plant species. Furthermore, an individual’s leaving rate was negatively related to its average feeding bout duration. This relationship resulted partly from variation in the response of individuals to nutrient imbalance and partly from shortened feeding bouts prior to switching, suggesting that a decline in feeding excitation preceded searching for food that differed from that most recently eaten. Laboratory experiments with synthetic diets indicated the importance of secondary metabolites in the decline in feeding excitation prior to switching. Preference for new food depended strongly on secondary metabolites in a manner consistent with toxin dilution. This is the first experimental evidence for the process of toxin dilution in caterpillars, and for the combined influence of nutrients and secondary metabolites on their foraging patterns in nature.

Disentangling Food Quality from Resistance against Parasitoids: Diet Choice by a Generalist Caterpillar

The relative importance of food quality and enemy‐reduced space is a central but unresolved issue in the evolutionary ecology of host use by phytophagous insects. Indeed, a practical obstacle to experimentally disentangling the functional roles of these factors is the host specificity of insect herbivores, particularly toxic plant specialists. In this study, we employ a toxic plant generalist to uniquely disentangle these alternative explanations. We experimentally demonstrate that the value of enemy‐reduced space supersedes that of food quality in determining the diet and host preference of the polyphagous woolly bear caterpillar Grammia geneura (Lepidoptera: Arctiidae). Caterpillars sacrificed superior growth efficiency in choosing a mixed diet that included toxic host plants and provided resistance against parasitoids. The resistance of individual caterpillars was associated with the relative amount of defensive plants eaten as well as with the sequestration of pyrrolizidine alkaloids from one such plant (Senecio longilobus).

DETERMINANTS OF PARASITOID-HOST ASSOCIATIONS: INSIGHTS FROM A NATURAL TACHINID-LEPIDOPTERAN COMMUNITY

A major goal of insect community ecology is to understand how and why herbivorous insect species vary in the diversity of their parasitoid assemblages and the rates of parasitism that they experience. Most studies investigating these issues with Lep- idoptera as hosts have relied on literature records of parasitoid-host associations that are often of limited quality and that do not necessarily reflect local interactions between hosts and parasitoids. We sampled externally feeding Lepidoptera in mesquite-oak savanna hab- itats of southeastern Arizona (USA) to assess the ecological and evolutionary determinants of parasitoid community structure. We focused on parasitoids in the family Tachinidae (Diptera) due to their dominance as larval parasitoids of macrolepidoptera at our site. Host abundance, morphology, coloration, gregariousness, and diet breadth of the host were all significantly correlated with tachinid species richness among hosts. Tachinid species rich- ness also varied according to host taxonomy (family), but most of this variation appeared to be better explained by morphology and ecology than by phylogenetic position. Char- acteristics of host habitat and body size had no significant effect on tachinid species richness. Tachinid parasitism rates were higher for abundant, hairy, non-aposematic, and gregarious hosts. Hymenopteran parasitism rates were low and variable with only host family ex- plaining a significant amount of variation. In general, we found that a substantial amount of the variation in tachinid species richness and parasitism rates among hosts can be ex- plained by ecological attributes, and that interactions of host species with their host plants and predators may determine their suitability as hosts for parasitoids.

Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths

Abstract.  1. Seventy‐seven individual last‐instar caterpillars foraging in the field were examined for 6 h each. They represented four species of Arctiidae of similar size and habitat use. Two, Hypocrisias minima and Pygarctia roseicapitis, are specialists restricted to particular plant genera. The other two, Grammia geneura and Estigmene acrea, are extreme generalists that use many host plant species from multiple plant families.