The sensory basis of behavior underlies nearly every critical ecological and evolutionary interaction. Research in my laboratory focuses on sensory neurophysiology and ecology, primarily focusing on olfactory-mediated behaviors because chemical signals control many fundamental interactions structuring populations and even communities (from finding mates, to pollination ecology). My previous and future research foci combine physiological and ecological approaches to the sensory modulation of behavior. This research scales from sensory stimuli, to organismal interactions and populations, and can be divided into foci described below.
Each research theme employs novel chemical analytical approaches, and combines those methods with physiological, behavioral and field assays. This interdisciplinary research provides a unique perspective in the study of animal behavior and sensory neurophysiology.
The Neural Basis of Floral Scent in Mosquito-Plant Interactions
What is the role of scent from flowers and fruits in mediating plant-mosquito interactions, and how does the environment shape these interactions? Floral scent is an important “advertisement” used by pollinators for flower discrimination, but relative to other floral traits – like color and shape –, little is understood about the role of scent in reproductive isolation between floral species, and how floral scent is processed by pollinators, including mosquitoes. Moreover, the milieu of scents from other environmental sources – ranging from anthropogenic pollutants from vehicle exhaust, to more natural volatiles from nearby plants – could have a strong, indirect, impact on pollinators, but these effects are poorly understood. To address these gaps, my current research can be broken up into 2 questions: (1) how do flowers and other nectar sources (fruit, extrafloral nectar) compare in their scent profile, and how these scents processed by the mosquito? (2) How does the chemical background shape the sensory environment experienced by the pollinator?
Behavioral Response and
Processing of Complex Odors
All olfactory systems, from insects to humans, can group biologically important odors into unique percepts. Humans can identify and differentiate wines – such as Pinot Noir from different vineyards – based solely on aroma. Similarly, an insect pollinator can have the same behavioral response elicited by scents from different flower species. Furthermore, these scents are complex mixtures of volatiles. How are these scents, which can differ from one another in their composition and intensity, processed by the olfactory system to elicit the same behaviors and olfactory percepts? To address these gaps, research in my laboratory examined how the olfactory system processes complex olfactory stimuli, like the scent of a rose, which is comprised of more than 200 volatile compounds.
Olfactory Learning and Behavior in Mosquitoes
Beyond those odors that drive instinctive behaviors, insects can also learn associations between volatile stimuli and aversive or appetitive stimuli. For example, our recent work with the Aedes aegypti mosquito demonstrated that it exhibits an innate attraction to certain human blood hosts but can learn to avoid individuals that swat, and then switch their preferences for less ‘defensive’ hosts (Vinauger et al., 2014; Vinauger et al., 2018). We found that, in the acquisition phase of appetitive learning, the neural representation in the AL changes due to modulation by the amine, octopamine, which is released in the AL.
Furthermore, the learning ability of the mosquito was dependent upon the odor stimuli – many of the volatiles in human body odor were readily learned, whereas other odors, including those from plants, went from aversive to attractive after training (Z-3-hexen-1-ol) or were untrainable (b-myrcene). We also found that mosquitoes had the ability to learn the association between DEET and a blood reward, and that once learned, DEET became attractive. Last, these experiments showed that both short-term and long-term memory were involved in the mosquitoes’ responses. Together, these results showed that learning is a critical component in olfactory responses in Ae. aegypti, and provided the first evidence for the functional role of different memory traces in these responses.
Sensory Integration in Mosquitoes
Insects have robust behavioral repertoires for locating and navigating to biologically important sites and are able to do this using a combination of sensory cues. For example, blood-feeding insects, such as the yellow-fever mosquito, Aedes aegypti, use a combination of olfactory, visual, and thermal cues to locate their hosts. A mosquito can detect a suitable host from as far away as 15 m by the presence of a CO2 plume, which they track by using a reiterative program of cross-wind casting during olfactory search and upwind surges when encountering the CO2. Once a mosquito approaches the host, local cues such as the visual display of the host, heat, and humidity can help them identify a landing site. Despite the robust blood-host seeking behaviors in hematophagous insects, the relative contribution of these different cues, and how they might interact to mediate host-seeking behaviors remains unclear. Moreover, the neural bases of these behaviors are unknown.
Olfactory Responses in Single Cells
Chemical communication is not only critical in mediating macroorganismal interactions, but plays a profound importance in controlling processes that occur at the level of the single cell. In contrast to the neural approach used for insect olfaction, the relatively simple system of the single cell (bateria, sperm, HEK) permits a molecular approach towards understanding the physiological mechanisms controlling chemosensory behavior (Riffell et al., 2004). To establish the physiological mechanisms controlling sperm chemotaxis, we examined the expression of olfactory receptor proteins on non-nasal epithelial tissues, and found incredibly high levels in male testes. Our work identified the olfactory receptor (OR) protein, hOR-17-4, in mediating sperm chemotactic behaviors (Spehr et al., 2003). This OR was de-orphaned, and was found to be activated by the agonist bourgeonal. Moreover, hOR17-4 activation is coupled to a cAMP transduction pathway through particulate adenylate cyclase, which controls flagellar beating and sperm turning behavior (Spehr et al., 2004; Riffell et al., 2011a,b). Thus, sperm cells respond to olfactory stimuli in an equivalent manner to that of olfactory neurons (Spehr et al., 2006).
