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Background. With their charismatic nighttime flashes, fireflies are a classic organismal system for studying the evolution of visual mating signals. However, across their diversity, fireflies employ a variety of mating strategies that include both chemical and visual signals. While phylogenetic evidence points to a common ancestor that relied on longrange pheromones, behavioral evidence suggests that light-dependent flashing fireflies do not use smell for mating. We tested this hypothesis by investigating the olfactory genetics of the dusk-active, light-using common eastern firefly, Photinus pyralis. In insects, odors are primarily detected by odorant receptor (OR) proteins embedded in the dendritic membranes of olfactory receptor neurons. If pheromones are part of mate signaling in light-using fireflies, then one or more OR genes should be upregulated in the antennae of the searching sex (males). We therefore annotated the complete suite of ORs in the genome of P. pyralis and measured expression of OR genes between the sexes using RNAseq. Results. We identified 102 ORs in the P. pyralis genome, including the conserved single-copy Orco. Our phylogenetic analysis showed lineage-specific OR diversification in P. pyralis relative to other beetle species. Differential expression analysis of male and female antennae and hind legs revealed that a subset of ORs were upregulated in antennae as compared to legs, suggesting a role in adult olfaction. Notably, PpyrOR6 was one of two genes, and the only OR, that was significantly upregulated between male and female antennae, suggesting a sex-specific role such as mate location. Conclusions. These findings increase known diversity of insect ORs in an understudied beetle family and suggest that fireflies with flashing adults use multimodal signals during mating.
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Identification of a Female-Produced Sex Attractant Pheromone of the Winter Firefly, Photinus corruscus Linnaeus (Coleoptera: Lampyridae)
Abstract Firefly flashes are well-known visual signals used by these insects to find, identify, and choose mates. However, many firefly species have lost the ability to produce light as adults. These “unlighted” species generally lack developed adult light organs, are diurnal rather than nocturnal, and are believed to use volatile pheromones acting over a distance to locate mates. While cuticular hydrocarbons, which may function in mate recognition at close range, have been examined for a handful of the over 2000 extant firefly species, no volatile pheromone has ever been identified. In this study, using coupled gas chromatography - electroantennographic detection, we detected a single female-emitted compound that elicited antennal responses from wild-caught male winter fireflies,Photinus corruscus. The compound was identified as (1S)-exo-3-hydroxycamphor (hydroxycamphor). In field trials at two sites across the species’ eastern North American range, large numbers of maleP. corruscuswere attracted to synthesized hydroxycamphor, verifying its function as a volatile sex attractant pheromone. Males spent more time in contact with lures treated with synthesized hydroxycamphor than those treated with solvent only in laboratory two-choice assays. Further, using single sensillum recordings, we characterized a pheromone-sensitive odorant receptor neuron in a specific olfactory sensillum on maleP. corruscusantennae and demonstrated its sensitivity to hydroxycamphor. Thus, this study has identified the first volatile pheromone and its corresponding sensory neuron for any firefly species,and provides a tool for monitoringP. corruscuspopulations for conservation and further inquiry into the chemical and cellular bases for sexual communication among fireflies.
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- Award ID(s):
- 2035286
- PAR ID:
- 10491698
- Publisher / Repository:
- Springer
- Date Published:
- Journal Name:
- Journal of Chemical Ecology
- Volume:
- 49
- Issue:
- 3-4
- ISSN:
- 0098-0331
- Page Range / eLocation ID:
- 164 to 178
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1007/s10886-023-01417-2
