A sampling of research projects, past & present
Chemical ecology of cycad-feeding Lepidoptera
My ongoing research at ETH Zurich investigates the chemical ecology of cycads and their lepidopteran herbivores. Cycads are ancient tropical plants that produce potent defensive chemicals that are toxic to most animals – including humans – yet a handful of Lepidoptera are able to feed on them with apparent immunity. Cycad-herbivore interactions provide a promising but understudied study system for investigating plant-insect coevolution, convergent and divergent adaptations, and the multi-trophic significance of defensive traits. I work primarily with two North American lepidopterans - Eumaeus atala and Seirarctia echo - as well as the model organism, Spodoptera littoralis, to address the following questions:
What behavioral, physiological, and molecular adaptations are required for cycad-feeding?
What are the salient leaf volatiles that cycad specialists use to identify and select host plants?
What is the full suite of defensive chemicals found in cycad leaves, , and how are these compounds evolving?
What role do cycads' symbiotic cyanobacteria play in their interactions with herbivores?
How do cycad-feeding insects cope with cycad toxins, particularly the neurotoxin, BMAA?
Do cycad-feeding insects use cycad-derived metabolites for their own purposes, e.g., for defense or pheromone production?
How can conservation efforts prioritize the co-existence of cycads and their herbivores?
This work involves multiple collaborators, including master's students at ETH Zurich; researchers at Cornell, Harvard, and the Smithsonian; and the amazing team at the Montgomery Botanical Center.
The butterfly family Lycaenidae is one of the most trophically diverse insect groups. Whereas the vast majority of moths and butterflies are strict herbivores, the Lycaenidae includes both herbivores and carnivores, with diets ranging from lichens to ant brood, gymnosperms to aphids. To test whether these diverse diets might require different assemblages of symbiotic gut bacteria, I collected more than 20 species of lycaenid larvae from Africa, North America, Europe, and Southeast Asia and characterized their gut microbiomes using 16S amplicon sequencing. Part of this work was conducted at the Max Planck Institute for Chemical Ecology in Jena, Germany. Based on this work, my collaborators and I were some of the first to propose that symbiotic gut bacteria may not be as important for Lepidoptera as they are for many other insect groups, which has since been corroborated by further studies in other lepidopteran study systems.
Whitaker, Salzman, Sanders, Kaltenpoth, Pierce. 2016. Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet. Frontiers in Microbiology, 7, 1920.
Investigating the diets of ecologically mysterious insects
An animal's diet is one of the most basic features of its biology. But for many animals - even relatively well-studied ones like butterflies - their diets remain mysterious to scientists. Anthene usamba is a lycaenid butterfly whose larvae live inside the ant-occupied domatia of Vachellia drepanolobium trees in East Africa, and their larvae have never been observed feeding. Given their close relationship with ants, and the tendency for some ant-tended lycaenids to parasitize their ant hosts, it was unclear whether this species is an herbivore or carnivore. Working with colleagues at Harvard's Museum of Comparative Zoology and the Mpala Research Centre in Kenya, I applied stable isotope analysis and metabarcoding to discover that the larvae are feeding on the V. drepanolobium leaflets, demonstrating the utility of combining these powerful and complementary methods for trophic ecology. This work is featured in the textbook, Ecology: Concepts & Applications (9th edition), and was recently selected for PLOS ONE's curated collection on stable isotopes.
Whitaker, Baker, Salzman, Martins, Pierce. 2019. Combining stable isotope analysis with DNA metabarcoding improves inferences of trophic ecology. PLoS ONE 14(7): e0219070.
Photo: An A. usamba larva inside a V. drepanolobium domatium, surrounded by ant brood and workers. Photo credit: Dino J. Martins
Microbiome convergence among cycad-feeding insects
In 2018, colleagues and I made an unexpected discovery that some cycad-feeding insects share a small set of core bacteria in their gut microbiomes. We then decided to investigate the microbiomes of a larger sampling of cycad-feeding insects from three insect orders and four continents, and were amazed to find that this convergence is widespread among cycad-feeders, regardless of life stage, insect order, geographic distribution, or feeding guild. With collaborators at LANGEBIO in Irapuato, Mexico, we applied functional phylogenomics to the gut bacterial communities of three Zamia-feeding insects to identify biosynthetic gene clusters in the genomes of key shared bacteria. The surprising results of this work are currently being written up for submission to PNAS in fall of 2021.
Salzman, Whitaker, Pierce. 2018. Cycad-feeding insects share a core gut microbiome. Biological Journal of the Linnean Society 123:4, 728-738.
Through an EAPSI fellowship funded by the National Science Foundation and Japan Society for the Promotion of Science, I worked with researchers at the University of Kyoto to test the effects of belowground plant-rhizobia interactions on above-ground ant-aphid interactions. Using a common garden experiment with soybean (Glycine max), we found that plant-Rhizobia mutualisms significantly affect the composition and quality of aphid honeydew, with implications for nutrient cycling and aboveground community dynamics.
Whitaker, Katayama, Ohgushi. 2014. Plant-rhizobia interactions alter the quality of aphid honeydew. Arthropod-Plant Interactions 8(3): 213-220.
Measuring chemical defense in insects
Many insects are chemically defended, meaning that they are unpalatable or poisonous to natural enemies. But have you ever wondered: how do scientists know that an insect tastes bad to predators? While circumstantial evidence can be helpful (Does the insect feed on chemically defended plants? Is it warningly colored? Is it longlived?), most insects are assumed to be palatable, even without supporting data, because existing methods for quantifying palatability tend to be expensive and inaccessible. I worked with colleagues at Kibale National Forest in southeastern Uganda to develop a novel method of measuring insect palatability using behavioral trials with ants. By testing this technique on 12 butterflies species with different life histories and defensive strategies, we discovered several butterfly species that were previously assumed to be palatable appeared to be chemically defended. This method contributes to the study of animal behavior and signalling, and to understanding trade-offs among defences and life history traits.
Molleman, Kaasik, Whitaker, Carey. 2012. Partitioning variation in duration of ant feeding bouts can offer insights into the palatability of insects: experiments on African fruit-feeding butterflies. Journal of Research on the Lepidoptera 45:65-75.
Molleman, Whitaker, & Carey. 2010. Rating palatability of butterflies by measuring ant feeding behavior. Entomologische Berichten 70(2): 52-62.
Butterflies of the Sutter Buttes, California
The Sutter Buttes are a small, isolated cluster of mountains in the middle of California's Central Valley, approximately equidistant from the Coast and Sierra Nevada mountain ranges. Due to a history of private ownership, the butterfly fauna of these unique mountains had never been systematically documented. With funding from the National Geographic Society, mfellow grad student Elizabeth Long and I conducted regular surveys of the Sutter Buttes for two years, and found that the butterfly fauna was depauperate relative to nearby mountain ranges, but that it might provide important butterfly habitat for lowland species responding to regional warming.
Whitaker & Long. 2014. Survey of the Butterflies of the Sutter Buttes, California. The Journal of Research on the Lepidoptera 47:1-10.
Evolution of cycadivory
Studies of butterfly-hostplant relationships have provided the historical bedrock of chemical ecology and co-evolutionary theory. Yet the vast majority of this research has been conducted on angiosperm-feeding clades, with comparatively little investigation into the evolution of non-angiospermous diets. Cycads - and ancient group of pantropical gymnosperms - were previously believed to have very few insect herbivores due to their unique chemical defenses, but previous studies on cycad-feeding insects concentrated on just a few focal species without examining broader ecological or evolutionary patterns. In collaboration with Shayla Salzman at Cornell University, I conducted the first evolutionary synthesis of cycad-feeding among Lepidoptera and found that cycad-feeding has repeatedly and independently evolved in at least seven lepidopteran families. The butterfly family Lycaenidae appears to be particularly predisposed to cycad-feeding, yet only a few lepidopteran clades have radiated following their transitions from angiosperm hosts to cycads. We postulate that defensive traits are likely important for diversification, as many cycad specialists sequester cycad toxins and are warningly colored. Due to their diverse trophic and defensive ecologies, we propose that cycad-feeding Lepidoptera provide ideal study systems for investigating chemically mediated eco-evolutionary dynamics.
Whitaker &Salzman. 2020. Ecology and evolution of cycad-feeding Lepidoptera. Ecology Letters 23: 1862-1877.
Tradeoffs in insect defenses
Because direct observations of predator–prey interactions in nature are rare, it is often unclear how insects' defensive traits influence realized predation in the wild. However, insight can be gained by quantifying bodily damage caused by failed predator attacks, which in some organisms - such as butterflies - can be quite evident. Working in an afrotropical butterfly community that includes some of the world's longest-lived butterflies, colleagues and I quantified the effects of various prey species traits, such as crypsis, flight speed, and aposematism, on their predation risk by determining how butterflies' defensive traits correlate with wing damage caused by failed predation attempts. This work is the first robust multi-species comparative analysis of predator-induced bodily damage in wild animals.
Molleman, Javoiš, Davis, Whitaker, Tammaru, Prinzing, Õunap, Wahlberg, Kodandaramaia, Aduse-Pok, Kaasik, Carey. 2020. Quantifying the effects of species traits on predation risk in nature: A comparative study of butterfly wing damage. Journal of Animal Ecology 89(3):716-729.