Bric à brac controls sex pheromone choice by male European corn borer moths

Authors: UNBEHEND, MELANIE - Max Planck Institute Of Chemical Ecology; KOZAK, GENEVIEVE - University Of Massachusetts; KOUTROUMPA, FOTINI - University Of Amsterdam; Coates, Brad; DEKKER, TEUN - Swedish University Of Agricultural Sciences; GROOT, ASTRID - University Of Amsterdam; HECKEL, DAVID - Max Planck Institute Of Chemical Ecology; DOPMAN, ERIK - Tufts University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/28/2021
Publication Date: 5/14/2021
Citation: Unbehend, M., Kozak, G.M., Koutroumpa, F., Coates, B.S., Dekker, T., Groot, A.T., Heckel, D.G., Dopman, E.B. 2021. Bric à brac controls sex pheromone choice by male European corn borer moths. Nature Communications. 12. Article 2818. https://doi.org/10.1038/s41467-021-23026-x.
DOI: https://doi.org/10.1038/s41467-021-23026-x

Interpretive Summary: Selection of mating partners within a species determines how or if subsets of the population will accumulate differences over time. Selection of mating partners between closely related species allows advantageous traits to be shared between species, impacting the adaptation of entire groups of species to their changing environments. Among animals, pheromones are volatile chemical compounds released by one sex to attract mates of the opposite sex. Each species must be able to distinguish its own pheromones from all others in the environment, including those from closely related species. Despite the importance of pheromones in mate selection, the genetic and genomic mechanisms involved in pheromone perception remain poorly understood. The European corn borer (ECB) is a major insect pest of corn in the United States and Eurasia, and is extensively used to study pheromone differences within a species. Specifically, females from two strains of ECB produce one of two different pheromone blends. The pheromone gland fatty acyl-reductase (pgfar) gene was previously identified as the gene responsible for these differences in female pheromones. However, the mechanism males use to detect and respond to different female pheromones remains unknown. As part of national and international collaboration, an ARS researcher used a genetic mapping approach to identify a region of the ECB genome containing several candidate genes for differences in pheromone detection and responses by corresponding males within each strain. A candidate gene called bric-a-brac (bab), was the only one of these candidate genes active in pupae, the developmental stage when neurons connecting antennae used for pheromone detection to the brain are formed. Ability to distinguish between pheromone blends were linked with sequence differences in the bab gene. In the model fruit fly species, Drosophila melanogaster, similar sequence differences result in changes in bab activity and pheromone perception. These research findings are crucial in understanding how male insects evolve behaviors tuned to attract females, and how these interactions shape differences within and between species. This research will have broad interest within the scientific community including university, government and industry scientists and regulators interested in predicting how ECB population genetic structure may impact the spread of advantageous traits, such as insecticide resistance, within and between species.

Technical Abstract: The sex pheromone system of ~160,000 species of moths acts as a powerful reproductive isolating barrier by which females attract conspecific males with a species-specific blend of volatile compounds. Understanding how female pheromone production and male preference coevolve to produce this diversity requires knowledge of the genes underlying both traits. In the European corn borer moth, variation in pheromone blend is controlled by two alleles of a fatty-acyl reductase gene expressed in the female pheromone gland (pgFAR). Here we show that male preference is controlled by allelic variation in a transcription factor expressed in the antenna, bric à brac (bab). Fine-scale recombinational mapping of laboratory populations eliminated all other candidate genes in a chromosomal region found by a previous investigation. An independent genome-wide association study on field-trapped males identified variation in the first intron of bab, not the coding sequence, as most strongly associating with preference in nature. A genome scan of signatures of assortative mating shows the bab intron 1 to be in strong linkage disequilibrium with pgFAR, even though the genes are on different chromosomes. Pheromone receptor genes, although genetically linked to bab, do not vary with male preference, contrasting with a study in a different moth genus where variation in pheromone receptors explained male preference. Here, however, variation in preference correlates with differences in connectivity between antennal neurons and the brain. Thus, genetic mechanisms altering pheromone responses in moths may affect information processing controlled by neuronal circuitry as well as direct perception of pheromones.