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Identification of a queen primer pheromone in higher termites

. 2022 Nov 02 ; 5 (1) : 1165. [epub] 20221102

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 36323794
PubMed Central PMC9630296
DOI 10.1038/s42003-022-04163-5
PII: 10.1038/s42003-022-04163-5
Knihovny.cz E-resources

It is long established that queens of social insects, including termites, maintain their reproductive dominance with queen primer pheromones (QPPs). Yet, the QPP chemistry has only been elucidated in a single species of lower termites. By contrast, the most diversified termite family Termitidae (higher termites), comprising over 70% of termite species, has so far resisted all attempts at QPP identification. Here, we show that the queen- and egg-specific sesquiterpene (3R,6E)-nerolidol acts as the QPP in the higher termite Embiratermes neotenicus. This species has a polygynous breeding system, in which the primary queen is replaced by multiple neotenic queens of parthenogenetic origin. We demonstrate that (3R,6E)-nerolidol suppresses the development of these parthenogenetic queens and thus mimics the presence of mature queen(s). It acts as an airborne signal and may be used to optimize the number of queens, thus being the key regulatory element in the special breeding system of E. neotenicus.

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Le Conte Y, Hefetz A. Primer pheromones in social hymenoptera. Annu. Rev. Entomol. 2007;53:523–542. doi: 10.1146/annurev.ento.52.110405.091434. PubMed DOI

Holman L. Queen pheromones and reproductive division of labor: a meta-analysis. Behav. Ecol. 2018;29:1199–1209.

Kocher SD, Grozinger CM. Cooperation, conflict, and the evolution of queen pheromones. J. Chem. Ecol. 2011;37:1263–1275. doi: 10.1007/s10886-011-0036-z. PubMed DOI

Peso M, Elgar MA, Barron AB. Pheromonal control: reconciling physiological mechanism with signalling theory. Biol. Rev. 2015;90:542–559. doi: 10.1111/brv.12123. PubMed DOI

Keller L, Nonacs P. The role of queen pheromones in social insects: queen control or queen signal? Anim. Behav. 1993;45:787–794. doi: 10.1006/anbe.1993.1092. DOI

van Zweden JS. The evolution of honest queen pheromones in insect societies. Commun. Integr. Biol. 2010;3:50–52. doi: 10.4161/cib.3.1.9655. PubMed DOI PMC

Ratnieks FL, Foster KR, Wenseleers T. Conflict resolution in insect societies. Annu. Rev. Entomol. 2006;51:581–608. doi: 10.1146/annurev.ento.51.110104.151003. PubMed DOI

Butler CG, Callow RK, Johnston NC. The isolation and synthesis of queen substance, 9-oxodec-trans-2-enoic acid, a honeybee pheromone. Proc. R. Soc. B. 1962;155:417–432.

Holman L, Jørgensen CG, Nielsen J, d’Ettorre P. Identification of an ant queen pheromone regulating worker sterility. Proc. R. Soc. B. 2010;277:3793–3800. doi: 10.1098/rspb.2010.0984. PubMed DOI PMC

Holman L, Lanfear R, d’Ettorre P. The evolution of queen pheromones in the ant genus Lasius. J. Evol. Biol. 2013;26:1549–1558. doi: 10.1111/jeb.12162. PubMed DOI

Van Oystaeyen A, et al. Conserved class of queen pheromones stops social insect workers from reproducing. Science. 2014;343:287–290. doi: 10.1126/science.1244899. PubMed DOI

Oi CA, Millar JG, van Zweden JS, Wenseleers T. Conservation of queen pheromones across two species of vespine wasps. J. Chem. Ecol. 2016;42:1175–1180. doi: 10.1007/s10886-016-0777-9. PubMed DOI

Holman L, Hanley B, Millar JG. Highly specific responses to queen pheromone in three Lasius ant species. Behav. Ecol. Sociobiol. 2016;70:387–392. doi: 10.1007/s00265-016-2058-6. DOI

Oi CA, et al. The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems. BioEssays. 2015;37:808–821. doi: 10.1002/bies.201400180. PubMed DOI

Matsuura K, et al. Identification of a pheromone regulating caste differentiation in termites. Proc. Natl Acad. Sci. USA. 2010;107:12963–12968. doi: 10.1073/pnas.1004675107. PubMed DOI PMC

Myles TG. Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology. 1999;33:1–91.

Matsuura K, et al. Queen succession through asexual reproduction in termites. Science. 2009;323:1687. doi: 10.1126/science.1169702. PubMed DOI

Vargo EL, Labadie PE, Matsuura K. Asexual queen succession in the subterranean termite Reticulitermes virginicus. Proc. R. Soc. B. 2012;279:813–819. doi: 10.1098/rspb.2011.1030. PubMed DOI PMC

Luchetti A, Velona A, Mueller M, Mantovani B. Breeding systems and reproductive strategies in Italian Reticulitermes colonies (Isoptera: Rhinotermitidae) Insectes Soc. 2013;60:203–211. doi: 10.1007/s00040-013-0284-8. DOI

Fournier D, Hellemans S, Hanus R, Roisin Y. Facultative asexual reproduction and genetic diversity of populations in the humivorous termite Cavitermes tuberosus. Proc. R. Soc. B. 2016;283:20160196. doi: 10.1098/rspb.2016.0196. PubMed DOI PMC

Hellemans S, et al. Widespread occurrence of asexual reproduction in higher termites of the Termes group (Termitidae: Termitinae) BMC Evol. Biol. 2019;19:14. doi: 10.1186/s12862-019-1459-3. PubMed DOI PMC

Fougeyrollas R, et al. Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus. Mol. Ecol. 2017;26:3295–3308. doi: 10.1111/mec.14095. PubMed DOI

Fougeyrollas R, et al. Asexual queen succession in the higher termite Embiratermes neotenicus. Proc. R. Soc. B. 2015;282:20150260. doi: 10.1098/rspb.2015.0260. PubMed DOI PMC

Lüscher, M. In Insect Polymorphism (ed Kennedy, J. S.) 57–67 (Royal Entomolological Society London Symposium, 1961).

Light SF. Experimental studies on ectohormonal control of the development of supplementary reproductives in the termite genus Zootermopsis (formerly Termopsis) Univ. Calif. Publ. Zool. 1944;53:1–40.

Grassé PP, Noirot C. La production des sexués néoteniques chez le termite à cou jaune (Calotermes flavicollis F.): inhibition germinale et inhibition somatique. C. R. Acad. Sci. Paris. 1946;223:869–871.

Liebig J, Eliyahu D, Brent CS. Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav. Ecol. Sociobiol. 2009;63:1799–1807. doi: 10.1007/s00265-009-0807-5. DOI

Weil T, Hoffmann K, Kroiss J, Strohm E, Korb J. Scent of a queen-cuticular hydrocarbons specific for female reproductives in lower termites. Naturwissenschaften. 2009;96:315–319. doi: 10.1007/s00114-008-0475-8. PubMed DOI

Funaro CF, Böröczky K, Vargo EL, Schal C. Identification of a queen and king recognition pheromone in the subterranean termite Reticulitermes flavipes. Proc. Natl Acad. Sci. USA. 2018;115:3888–3893. doi: 10.1073/pnas.1721419115. PubMed DOI PMC

Eyer, P.-A., Salin, J., Helms, A. M. & Vargo, E. L. Distinct chemical blends produced by different reproductive castes in the subterranean termite Reticulitermes flavipes. Sci. Rep. 11, 4471 (2021). PubMed PMC

Hoffmann K, Gowin J, Hartfelder K, Korb J. The scent of royalty: a P450 gene signals reproductive status in a social insect. Mol. Biol. Evol. 2014;31:2689–2696. doi: 10.1093/molbev/msu214. PubMed DOI

Yamamoto Y, Matsuura K. Queen pheromone regulates egg production in a termite. Biol. Lett. 2011;7:727–729. doi: 10.1098/rsbl.2011.0353. PubMed DOI PMC

Suehiro W, Matsuura K. Queen pheromone promotes production of salivary lysozyme by workers in a termite. Insectes Soc. 2015;62:193–198. doi: 10.1007/s00040-015-0396-4. DOI

Matsuura K, Matsunaga T. Antifungal activity of a termite queen pheromone against egg-mimicking termite ball fungi. Ecol. Res. 2015;30:93–100. doi: 10.1007/s11284-014-1213-7. DOI

Matsuura K. Multifunctional queen pheromone and maintenance of reproductive harmony in termite colonies. J. Chem. Ecol. 2012;38:746–754. doi: 10.1007/s10886-012-0137-3. PubMed DOI

Krishna K, Grimaldi DA, Krishna V, Engel MS. Treatise on the Isoptera of the world. Vol. 1. Introduction. Bull. Am. Mus. Nat. Hist. 2013;377:1–200. doi: 10.1206/377.1. DOI

Himuro C, Yokoi T, Matsuura K. Queen-specific volatile in a higher termite Nasutitermes takasagoensis (Isoptera: Termitidae) J. Insect Physiol. 2011;57:962–965. doi: 10.1016/j.jinsphys.2011.04.012. PubMed DOI

Machara A, et al. Identification and enantiodivergent synthesis of (5Z,9S)-tetradec-5-en-9-olide, a queen-specific volatile of the termite Silvestritermes minutus. J. Nat. Prod. 2018;81:2266–2274. doi: 10.1021/acs.jnatprod.8b00632. PubMed DOI

Havlíčková J, et al. (3R,6E)-nerolidol, a fertility-related volatile secreted by the queens of higher termites (Termitidae: Syntermitinae) Z. Naturforsch. C. 2019;74:251–264. doi: 10.1515/znc-2018-0197. PubMed DOI

Yamamoto Y, Matsuura K. Genetic influence on caste determination underlying the asexual queen succession system in a termite. Behav. Ecol. Sociobiol. 2012;66:39–46. doi: 10.1007/s00265-011-1249-4. DOI

Matsuura, K. et al. Genomic imprinting drives eusociality. Preprint at bioRxiv10.1101/2021.04.28.441822 (2021).

Matsuura K. Genomic imprinting and evolution of insect societies. Popul. Ecol. 2020;62:38–52. doi: 10.1002/1438-390X.12026. DOI

Matsuura K, et al. A genomic imprinting model of termite caste determination: not genetic but epigenetic inheritance influences offspring caste fate. Am. Nat. 2018;191:677–690. doi: 10.1086/697238. PubMed DOI

Fougeyrollas R, et al. Dispersal and mating strategies in two neotropical soil-feeding termites, Embiratermes neotenicus and Silvestritermes minutus (Termitidae, Syntermitinae) Insectes Soc. 2018;65:251–262. doi: 10.1007/s00040-018-0606-y. DOI

Mitaka, Y. & Fujita, T. Cuticular hydrocarbon profile for queen recognition in the termite Reticulitermes speratus. Res. Sq.10.21203/rs.3.rs-490573/v1 (2021).

Korb J. Chemical fertility signaling in termites: idiosyncrasies and commonalities in comparison with ants. J. Chem. Ecol. 2018;44:818–826. doi: 10.1007/s10886-018-0952-2. PubMed DOI

Holman L. Costs and constraints conspire to produce honest signaling: insights from an ant queen pheromone. Evolution. 2012;66:2094–2105. doi: 10.1111/j.1558-5646.2012.01603.x. PubMed DOI

Gilg AB, Bearfield JC, Tittiger C, Welch WH, Blomquist GJ. Isolation and functional expression of an animal geranyl diphosphate synthase and its role in bark beetle pheromone biosynthesis. Proc. Natl Acad. Sci. USA. 2005;102:9760–9765. doi: 10.1073/pnas.0503277102. PubMed DOI PMC

Bearfield JC, Henry AG, Tittiger C, Blomquist GJ, Ginzel MD. Two regulatory mechanisms of monoterpenoid pheromone production in Ips spp. of bark beetles. J. Chem. Ecol. 2009;35:689–697. doi: 10.1007/s10886-009-9652-2. PubMed DOI

Cusson M, McNeil JN. Involvement of juvenile hormone in the regulation of pheromone release activities in a moth. Science. 1989;243:210. doi: 10.1126/science.243.4888.210. PubMed DOI

Brent CS, Penick CA, Trobaugh B, Moore D, Liebig J. Induction of a reproductive-specific cuticular hydrocarbon profile by a juvenile hormone analog in the termite Zootermopsis nevadensis. Chemoecology. 2016;26:195–203. doi: 10.1007/s00049-016-0219-8. DOI

Oi CA, Brown RL, da Silva RC, Wenseleers T. Reproduction and signals regulating worker policing under identical hormonal control in social wasps. Sci. Rep. 2020;10:18971. doi: 10.1038/s41598-020-76084-4. PubMed DOI PMC

Darragh K, et al. A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies. PLoS Biol. 2021;19:e3001022. doi: 10.1371/journal.pbio.3001022. PubMed DOI PMC

Gilg AB, Tittiger C, Blomquist GJ. Unique animal prenyltransferase with monoterpene synthase activity. Naturwissenschaften. 2009;96:731–735. doi: 10.1007/s00114-009-0521-1. PubMed DOI

Beran F, et al. Novel family of terpene synthases evolved from trans-isoprenyl diphosphate synthases in a flea beetle. Proc. Natl Acad. Sci. USA. 2016;113:2922. doi: 10.1073/pnas.1523468113. PubMed DOI PMC

Lancaster J, et al. De novo formation of an aggregation pheromone precursor by an isoprenyl diphosphate synthase-related terpene synthase in the harlequin bug. Proc. Natl Acad. Sci. USA. 2018;115:E8634. doi: 10.1073/pnas.1800008115. PubMed DOI PMC

Chan WK, Tan LT, Chan KG, Lee LH, Goh BH. Nerolidol: a sesquiterpene alcohol with multi-faceted pharmacological and biological activities. Molecules. 2016;21:529. doi: 10.3390/molecules21050529. PubMed DOI PMC

Dolejšová, K. et al. Sex-pairing pheromones in three sympatric Neotropical termite species (Termitidae: Syntermitinae). J. Chem. Ecol. 44, 534–546 (2018). PubMed

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