Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant

Hidehiro Watanabe; Shoji Ogata; Nonoka Nodomi; Kosuke Tateishi; Hiroshi Nishino; Ryosuke Matsubara; Mamiko Ozaki; Fumio Yokohari

doi:10.3389/fncel.2023.1084803

Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant

Front Cell Neurosci. 2023 Feb 6:17:1084803. doi: 10.3389/fncel.2023.1084803. eCollection 2023.

Authors

Hidehiro Watanabe¹, Shoji Ogata¹, Nonoka Nodomi¹, Kosuke Tateishi¹, Hiroshi Nishino², Ryosuke Matsubara³, Mamiko Ozaki^{4

5}, Fumio Yokohari¹

Affiliations

¹ Department of Earth System Science, Fukuoka University, Fukuoka, Japan.
² Research Institute for Electronic Science, Hokkaido University, Sapporo, Japan.
³ Department of Chemistry, Graduate School of Science, Kobe University, Kobe, Japan.
⁴ Department of Biology, Graduate School of Science, Kobe University, Kobe, Japan.
⁵ KYOUSEI Science Center for Life and Nature, Nara Women's University, Nara, Japan.

Abstract

To maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or central neural mechanism is mainly responsible for discrimination of CHC blends. In the Japanese carpenter ant, Camponotus japonicus, about 140 sensory neurons (SNs) are co-housed in a single basiconic sensillum and receive colony-specific blends of 18 CHCs. The complexity of this CHC sensory process makes the neural basis of peripheral nestmate recognition difficult to understand. Here, we electrophysiologically recorded responses of single basiconic sensilla to each of 18 synthesized CHCs, and identified CHC responses of each SN co-housed in a single sensillum. Each CHC activated different sets of SNs and each SN was broadly tuned to CHCs. Multiple SNs in a given sensillum fired in synchrony, and the synchronicity of spikes was impaired by treatment with a gap junction inhibitor. These results indicated that SNs in single basiconic sensilla were electrically coupled. Quantitative analysis indicated that the Japanese carpenter ants have the potential to discriminate chemical structures of CHCs based on the combinational patterns of activated SNs. SNs of ants from different colonies exhibited different CHC response spectra. In addition, ants collected from the same colony but bred in separate groups also exhibited different CHC response spectra. These results support the hypothesis that the peripheral sensory mechanism is important for discrimination between nestmate and non-nestmate ants.

Keywords: ant; basiconic sensilla; cuticular hydrocarbons; nestmate recognition; sensory neurons; social insect.

Grants and funding

This research was supported by JSPS KAKENHI Grant numbers JP19K06775 (to HW), JP21H05766 (to HN), and JP16K07446 (to FY), Grant-in-Aid for JSPS fellows Grant number JP21J14202 (to KT), and by the Central Research Institute of Fukuoka University, Grant number 206001 (to HW).