Multidisciplinary approach to determining the behavioral and genetic basis of chemosensation in Plodia interpunctella (Lepidoptera: Pyralidae) for improved management

Abstract

The management of stored-product pests (SPPs) poses a critical challenge to global food security, as these pests thrive in human-modified environments associated with harvested or processed food supplies. In post-harvest landscapes, chemosensation acts as the primary physiological interface governing survival-critical behaviors in these pests, including resource acquisition and reproductive success. In the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae), semiochemical based monitoring or behavioral management tactics serve to either the presence and abundance of adults in an environment or reduce the population through tactics such as mating disruption and attract and kill; however, the efficacy of these strategies remains limited by an incomplete understanding of the mechanisms used by P. interpunctella perceive and respond to stimuli and how different stimuli, such as pheromones and kairomones, influence behaviors. This dissertation synthesizes current knowledge of SPP chemosensory biology and investigates the multiple physiological mechanisms underlying P. interpunctella behavior, using a multidisciplinary approach that spans the biological hierarchy to identify how different volatiles influence dispersal and flight behavior, to identify key behaviors in courtship that could be disrupted to prevent mating, and to identify candidate genes that influence behavioral responses to food volatiles and pheromones. At the organismal level, flight and dispersal are characterized as dynamic decision-making processes shaped by internal physiological states and external semiochemical cues. Using tethered flight mills, we studied flight capacity and determined that flight distance was highest in unmated males, while the major pheromone component, (Z, E)-9,12-tetradecadienyl acetate (ZETA), acted as a behavioral catalyst by increasing flight bout frequency. While combinatorial cues of ZETA and flour together resulted in arrestment, which could be exploited to manipulate behavior in field settings such as encourage longer exposure to toxicants at attract and kill stations. Moreover, exploring the close-range reproductive interactions, Markov chain frameworks revealed that courtship operates as a probabilistic communication system. Within this architecture, head-to-head contact emerged as a critical behavioral bottleneck and a mandatory gateway for mating success, suggesting that mate choice is governed by the probabilistic control of behavioral sequences rather than discrete actions. This behavior represents a keystone in determining the outcome of reproductive behavior in P. interpunctella that could be disrupted to reduce successful mating and copulation to augment traditional mating disruption programs. To identify the life history parameters, the influence of physiological responses to volatiles and molecular drivers that influence behavioral outputs, we also characterized antennal olfactory responses of males and females at varying ages, reproductive statuses, and prior behaviors to ZETA. Electroantennography revealed that pheromone perception is highly plastic, influenced mainly by sex and mating status. Furthermore, we determined that the antennal response exhibited lateralization, with the right antenna exhibiting a 17% stronger response that varies according to P. interpunctella reproductive state and age within males and females. At the transcriptomic level, multi-factorial analysis showed that mating strongly influences gene expression: mated males exhibited a tenfold increase in ZETA-responsive differentially expressed genes, characterized by the downregulation of mate-seeking machinery in favor of broader environmental sensors. Finally, these functional shifts were anchored in the genomic architecture by manually curating 132 chemosensory genes from a chromosome-scale assembly, which revealed species-specific expansions of ionotropic receptors on chromosome 8. Collectively, this research underscores that the ecological success of P. interpunctella as a pest is driven by its behavioral plasticity and genomic architecture, which work simultaneously with underlying physiological processes associated with sex, mating status, and age to regulate the integration of chemosensory information, which provides frameworks for improving semiochemical-mediated behavioral pest management strategies.