The Ortholog Receptor Or67d in Drosophila Bipectinata is able to Detect Two Different Pheromones.
Drosophila bipectinata
cis-Vaccenyl acetate
(Z)-11-eicosen-1-yl-acetate
Courtship behavior
Or67d receptor
Pheromones
Journal
Journal of chemical ecology
ISSN: 1573-1561
Titre abrégé: J Chem Ecol
Pays: United States
ID NLM: 7505563
Informations de publication
Date de publication:
18 Sep 2024
18 Sep 2024
Historique:
received:
23
07
2024
accepted:
04
09
2024
revised:
02
09
2024
medline:
19
9
2024
pubmed:
19
9
2024
entrez:
18
9
2024
Statut:
aheadofprint
Résumé
Sex pheromones play a crucial role in species recognition and reproductive isolation. Despite being largely species-specific in drosophilids, the mechanisms underlying pheromone detection, production, and their influence on mating behavior remain poorly understood. Here, we compare the chemical profiles of Drosophila bipectinata and D. melanogaster, the mating behaviors in both species, as well as the tuning properties of Or67d receptors, which are expressed by neurons in antennal trichoid sensilla at1. Through single sensillum recordings, we demonstrate that the D. bipectinata Or67d-ortholog exhibits similar sensitivity to cis-vaccenyl acetate (cVA) as compared to D. melanogaster but in addition also responds uniquely to (Z)-11-eicosen-1-yl-acetate (Z11-20:Ac), a compound exclusively produced by D. bipectinata males. Through courtship behavior assays we found that, surprisingly, perfuming the flies with Z11-20:Ac did not reveal any aphrodisiacal or anti-aphrodisiacal effects in mating assays. The behavioral relevance of at1 neuron channels in D. bipectinata compared to D. melanogaster seems to be restricted to its formerly shown function as an aggregation pheromone. Moreover, the non-specific compound cVA affected copulation negatively in D. bipectinata and could potentially act as a premating isolation barrier. As both ligands of Or67d seem to govern different behaviors in D. bipectinata, additional neurons detecting at least one of those compounds might be involved. These results underscore the complexity of chemical signaling in species recognition and raise intriguing questions about the evolutionary implications of pheromone detection pathways in Drosophila species.
Identifiants
pubmed: 39294426
doi: 10.1007/s10886-024-01545-3
pii: 10.1007/s10886-024-01545-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Bartelt RJ, Schaner AM, Jackson LL (1985) cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster. J Chem Ecol 11(12):1747–1756. https://doi.org/10.1007/BF01012124
doi: 10.1007/BF01012124
pubmed: 24311338
Billeter J-C, Atallah J, Krupp JJ, Millar JG, Levine JD (2009) Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461(7266):987–991. https://doi.org/10.1038/nature08495
doi: 10.1038/nature08495
pubmed: 19829381
Billeter JC, Levine JD (2015) The role of cVA and the odorant binding protein Lush in social and sexual behavior in Drosophila melanogaster. Front Ecol Evol 3. https://doi.org/10.3389/fevo.2015.00075
Bock IR (1971) Taxonomy of the Drosophila bipectinata species complex. Univ Texas Publ 7103:273–280. https://doi.org/10.5281/zenodo.10736624
doi: 10.5281/zenodo.10736624
Bock IR (1978) The bipectinata complex: a study in interspecific hybridization in the genus Drosophila (Insecta: Diptera). Aust J Biol Sci 31(2):197. https://doi.org/10.1071/BI9780197
doi: 10.1071/BI9780197
Brieger G, Butterworth FM (1970) Drosophila melanogaster : Identity of male lipid in reproductive system. Science 167(3922):1262–1262. https://doi.org/10.1126/science.167.3922.1262
doi: 10.1126/science.167.3922.1262
pubmed: 5411913
Butterworth FM (1969) Lipids of Drosophila : a newly detected lipid in the male. Science 163(3873):1356–1357. https://doi.org/10.1126/science.163.3873.1356
doi: 10.1126/science.163.3873.1356
pubmed: 5765118
Campanacci V, Krieger J, Bette S, Sturgis JN, Lartigue A, Cambillau C, Breer H, Tegoni M (2001) Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. J Biol Chem 276(23):20078–20084. https://doi.org/10.1074/jbc.M100713200
doi: 10.1074/jbc.M100713200
pubmed: 11274212
Clyne P, Grant A, O’Connell R, Carlson JR (1997) Odorant response of individual sensilla on the Drosophila antenna. Invertebr Neurosci 3(2–3):127–135. https://doi.org/10.1007/BF02480367
doi: 10.1007/BF02480367
Das S, Trona F, Khallaf MA, Schuh E, Knaden M, Hansson BS, Sachse S (2017) Electrical synapses mediate synergism between pheromone and food odors in Drosophila melanogaster. Proc Natl Acad Sci 114(46). https://doi.org/10.1073/pnas.1712706114
Ejima A, Smith BP, Lucas C, van de Goes van Naters W, Miller CJ, Carlson JR, Levine JD, Griffith LC (2007) Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 17(7):599–605. https://doi.org/10.1016/j.cub.2007.01.053
doi: 10.1016/j.cub.2007.01.053
pubmed: 17363250
pmcid: 1913718
Fishilevich E, Vosshall LB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15(17):1548–1553. https://doi.org/10.1016/j.cub.2005.07.066
doi: 10.1016/j.cub.2005.07.066
pubmed: 16139209
Friard O, Gamba M (2016) BORIS<: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7(11):1325–1330. https://doi.org/10.1111/2041-210X.12584
doi: 10.1111/2041-210X.12584
Gonzalez F, Witzgall P, Walker III WB (2016) Protocol for heterologous expression of insect odourant receptors in Drosophila. Front Ecol Evol 4:24. https://doi.org/10.3389/fevo.2016.00024
Ha TS, Smith DP (2006) A pheromone receptor mediates 11- cis -vaccenyl acetate-induced responses in Drosophila. J Neurosci 26(34):8727–8733. https://doi.org/10.1523/JNEUROSCI.0876-06.2006
doi: 10.1523/JNEUROSCI.0876-06.2006
pubmed: 16928861
pmcid: 6674374
Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82(2):265–289. https://doi.org/10.1111/j.1469-185X.2007.00009.x
doi: 10.1111/j.1469-185X.2007.00009.x
pubmed: 17437561
Khallaf MA et al (2020) Mate discrimination among subspecies through a conserved olfactory pathway. Sci Adv 6:eaba5279
doi: 10.1126/sciadv.aba5279
pubmed: 32704542
pmcid: 7360436
Khallaf MA, Cui R, Weißflog J et al (2021) Large-scale characterization of sex pheromone communication systems in Drosophila. Nat Commun 12:4165. https://doi.org/10.1038/s41467-021-24395-z
doi: 10.1038/s41467-021-24395-z
pubmed: 34230464
pmcid: 8260797
Kopp A, Barmina O (2005) Evolutionary history of the Drosophila bipectinata species complex. Genet Res 85(1):23–46. https://doi.org/10.1017/S0016672305007317
doi: 10.1017/S0016672305007317
pubmed: 16089034
Kopp A, Frank AK (2005) Speciation in progress? A continuum of reproductive isolation in Drosophila bipectinata. Genetica 125(1):55–68. https://doi.org/10.1007/s10709-005-4787-8
doi: 10.1007/s10709-005-4787-8
pubmed: 16175455
Kurtovic A, Widmer A, Dickson BJ (2007) A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446(7135):542–546. https://doi.org/10.1038/nature05672
doi: 10.1038/nature05672
pubmed: 17392786
Lebreton S, Grabe V, Omondi AB, Ignell R, Becher PG, Hansson BS, Sachse S, Witzgall P (2014) Love makes smell blind: mating suppresses pheromone attraction in Drosophila females via Or65a olfactory neurons. Sci Rep 4(1):7119. https://doi.org/10.1038/srep07119
doi: 10.1038/srep07119
pubmed: 25406576
pmcid: 4236738
Lemeunier F, David JR, Tsacas L, Ashburner M (1986) The melanogaster species group. In: Ashburner M, Carson HL, Thompson JN (eds) The Genetics and Biology of Drosophila, vol 3e. pp 147–256
Lin C-C, Potter CJ (2015) Re-classification of Drosophila melanogaster trichoid and intermediate sensilla using fluorescence-guided single sensillum recording. PLoS ONE 10:e0139675
doi: 10.1371/journal.pone.0139675
pubmed: 26431203
pmcid: 4592000
Liu W, Liang X, Gong J, Yang Z, Zhang Y-H, Zhang J-X, Rao Y (2011) Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 14(7):896–902. https://doi.org/10.1038/nn.2836
doi: 10.1038/nn.2836
pubmed: 21685916
Mane SD, Tompkins L, Richmond RC (1983) Male esterase 6 catalyzes the synthesis of a sex pheromone in Drosophila melanogaster females. Science 222(4622):419–421. https://doi.org/10.1126/science.222.4622.419
doi: 10.1126/science.222.4622.419
pubmed: 17789533
Miller CJ, Carlson JR (2010) Regulation of odor receptor genes in trichoid sensilla of the Drosophila antenna. Genetics 186:79-U166
doi: 10.1534/genetics.110.117622
pubmed: 20551440
pmcid: 2940313
Ng R, Lin HH, Wang JW, Su CY (2017) Electrophysiological recording from Drosophila trichoid sensilla in response to odorants of low volatility. J vis Exp. https://doi.org/10.3791/56147
doi: 10.3791/56147
pubmed: 28784950
pmcid: 5613777
Olsson SB, Hansson BS (2013) Electroantennogram and single sensillum recording in insect antennae. Methods Mol Biol 1068:157–177
doi: 10.1007/978-1-62703-619-1_11
pubmed: 24014360
Prieto-Godino LL, Silbering AF, Khallaf MA, Cruchet S, Bojkowska K, Pradervand S, Hansson BS, Knaden M, Benton R (2020) Functional integration of “undead” neurons in the olfactory system. Sci Adv 6(11). https://doi.org/10.1126/sciadv.aaz7238
R Core Team (2024) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ . Accessed 16 June 2024
Rihani K, Ferveur J-F, Briand L (2021) The 40-year mystery of insect odorant-binding proteins. Biomol 11(4):509. https://doi.org/10.3390/biom11040509
doi: 10.3390/biom11040509
Ronderos DS, Smith DP (2010) Activation of the T1 neuronal circuit is necessary and sufficient to induce sexually dimorphic mating behavior in Drosophila melanogaster. J Neurosci 30(7):2595–2599. https://doi.org/10.1523/JNEUROSCI.4819-09.2010
doi: 10.1523/JNEUROSCI.4819-09.2010
pubmed: 20164344
pmcid: 3426441
Schaner AM, Graham KJ, Jackson LL (1989) Aggregation pheromone characterization and comparison in Drosophila ananassae and Drosophila bipectinata. J Chem Ecol 15(3):1045–1055. https://doi.org/10.1007/BF01015198
doi: 10.1007/BF01015198
pubmed: 24271905
Singh S, Singh BN (2001) Drosophila bipectinata species complex. Indian J Exp Biol 39(9):835–844
pubmed: 11831362
Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102(1):77–97. https://doi.org/10.1038/hdy.2008.55
doi: 10.1038/hdy.2008.55
pubmed: 18685572
van der Goes van Naters WV, Carlson JR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17(7):606–612. https://doi.org/10.1016/j.cub.2007.02.043
doi: 10.1016/j.cub.2007.02.043
pubmed: 17363256
pmcid: 1876700
Wang L, Anderson DJ (2010) Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463(7278):227–231. https://doi.org/10.1038/nature08678
doi: 10.1038/nature08678
pubmed: 19966787
Wertheim B, Dicke M, Vet LEM (2002) Behavioural plasticity in support of a benefit for aggregation pheromone use in Drosophila melanogaster. Entomol Exp Appl 103(1):61–71. https://doi.org/10.1046/j.1570-7458.2002.00954.x
doi: 10.1046/j.1570-7458.2002.00954.x
Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A 196:685–700
doi: 10.1007/s00359-010-0564-y
Wyatt TD (2017) Pheromones. Curr Biol 27:R739–R743
doi: 10.1016/j.cub.2017.06.039
pubmed: 28787598
Xu P, Atkinson R, Jones DNM, Smith DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45(2):193–200. https://doi.org/10.1016/j.neuron.2004.12.031
doi: 10.1016/j.neuron.2004.12.031
pubmed: 15664171