Abstract
In social insects, juvenile hormone (JH) affects the degree of ovarian development, reproductive status, and temporal polyethism in workers. JH also contributes to determining the epicuticular chemical composition, which differentiates the castes of queens and workers. However, a few studies have evaluated the action of JH on behavioral ontogeny, cuticular chemical profile, and oocyte length and width, especially in social wasps of independent foundation. Therefore, the following hypotheses were tested: (i) topical application of JH changes the behavioral ontogeny of newly emerged workers; and (ii) changes might be detected in the cuticular chemical composition and oocyte length and width of newly emerged females receiving topical application of JH. The treatment consisted of application of JH, at a concentration of 25 µg.µL−1 in acetone, to 1-day-old Mischocyttarus consimilis workers. The application of JH to newly emerged M. consimilis females significantly altered oocyte length and width, with effects on behavioral ontogeny and the cuticular chemical compounds signaling these parameters in the colony. No effects of the solvent on female physiology were observed, reinforcing that the observed changes were due to the specific effects of JH.
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Abdalla FC, Jones GR, Morgan ED, da Cruz-Landim C (2003) Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Genet Mol Res 2:191–199
Agrahari M, Gadagkar R (2003) Juvenile hormone accelerates ovarian development and does not affect age polyethism in the primitively eusocial wasp, Ropalidia marginata. J Insect Physiol 49:217–222. https://doi.org/10.1016/S0022-1910(02)00268-8
Billen J (2006) Signal variety and communication in social insects. Proc of the Sect Exp and Applied Ent 17:9–25
Blomquist G (2010) Structure and analysis of insect hydrocarbons. In: Bonquist GJ, Bagnéres AG (eds) insect hydrocarbons. Cambridge University Press, Cambridge, Pp, pp 19–34
Bonavita-Cougourdan A, Theraulaz G, Bagnères AG, Roux M, Pratte M, Clément PE, JL, (1991) Cuticular hydrocarbons, social organization and ovarian development in a Polistes wasp: Polistes dominulus Christ. Comp Biochem Physiol Part B 100:667–680. https://doi.org/10.1016/0305-0491(91)90272-F
Bonckaert W, Drijfhout FP, D’Ettorre P, Billen J, Wenseleers T (2012) Hydrocarbon signatures of egg maternity, caste membership and reproductive status in the common wasp. J Chem Ecol 38:42–51. https://doi.org/10.1007/s10886-011-0055-9
Bruyndonckx N, Kardile SP, Gadagkar R (2006) Dominance behaviour and regulation of foraging in the primitively eusocial wasp Ropalidia marginata (Lep.) (Hymenoptera: Vespidae). Behav Process 72:100–103. https://doi.org/10.1016/j.beproc.2005.11.013
Bussab WO, Morrettin PA (2002) Estatística Básica. 5, a. Saraiva, São Paulo
Costanzi E, Bagnères A-G, Lorenzi MC (2013) Changes in the hydrocarbon proportions of colony odor and their consequences on nestmate recognition in social wasps. PLoS ONE 8(5):e65107. https://doi.org/10.1371/journal.pone.0065107
Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. An Beh 62:165–171
Del-Claro K (2010) Introdução à Ecologia Comportamental : um manual para o estudo do comportamento animal / Kleber Del-Claro, 1st edn. Technical Books, Rio de Janeiro, p 128
Gadagkar R (1991) Belonogaster, Mischocyttarus, Parapolybia, and independent founding Ropalidia. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, pp 149–190
Gadagkar R, Bhagavan S, Chandrashekara K, Vinutha C (1991) The role of larval nutrition in pre-imaginal biasing of caste in the primitively eusocial wasp Ropalidia marginata (Hymenoptera, Vespidae). Ecol Entomol 16:435–440. https://doi.org/10.1111/j.1365-2311.1991.tb00236.x
Giannotti E, Machado VLL (1999) Behavioral castes in the primitively eusocial wasp Polistes lanio Fabricius (Hymenoptera:Vespidae). Rev Bras Entomol 43(3–4):185–190
Giray T, Giovanetti M, West-Eberhard MJ (2005) Juvenile hormone, reproduction, and worker behavior in the neotropical social wasp Polistes canadensis. Proceed Nat Acad Sci USA 102:3330–3335. https://doi.org/10.1073/pnas.0409560102
Hair JF, Black WC, Babin BJ, Anderson RE, Tatham RL (2009) Análise multivariada de dados. Trad. Adonai Schlup Sant’Anna. Rev. Maria Aparecida Gouvêa. 6. ed. Porto Alegre, Bookman. 688
Hölldobler B, Wilson E (1990) The Ants. Valenzuela Gonzalez J, Lopez-Mendez A, Garcia-Ballinas A (1994) Activity pattern and foraging habits of Pachycondyla villosa (Hymenoptera, Formicidae) in cacao agroecosystems from Soconusco. Folia Entomol Mex. Chiapas, Mexico, pp 9–21
Howard RW (2001) Cuticular hydrocarbons of adult Pteromalus cerealellae (Hymenoptera: Pteromalidae) and two larval hosts, angoumois grain mothn (Lepidoptera: Gelechiidae) and cowpea weevil (Coleptera: Bruchidae). Ann Entomol Soc Am 94:152–158. https://doi.org/10.1603/0013-8746(2001)094[0152:CHOAPC]2.0.CO;2
Howard RW, Perez-Lachaud G, Lachaud J-P (2001) Cuticular hydrocarbons of Kapala sulcifacies (Hym: Eucharitidae) and its host, the Ponerine ant Ectatomma ruidum (Hym: Formicidae). Ann Entomol Soc Am 94:707–716
Huang Z-Y, Robinson GE, Tobe SS, Yagi KJ, Strambi C, Strambi A, Stay B (1991) Hormonal regulation of behavioural development in the honey bee is based on changes in the rate of juvenile hormone biosynthesis. J Insect Physiol 37(10):733–741. https://doi.org/10.1016/0022-1910(91)90107-b
Jatsch AS, Ruther J (2021) Acetone application for administration of bioactive substances has no negative effects on longevity, fitness, and sexual communication in a parasitic wasp. PLoS ONE 16(1):e0245698. https://doi.org/10.1371/journal.pone.0245698
Jeanne RL (1991) The swarm-founding Polistinae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 191–231
Judd TM, Magnus RM, Fasnacht MP (2010) A nutritional profile of the social wasp Polistes metricus: differences in nutrient levels between castes and changes within castes during the annual life cycle. J Insect Physiol 56:42–56. https://doi.org/10.1016/j.jinsphys.2009.09.002
Keeping MG (2002) Reproductive and worker castes in the primitively eusocial wasp Belonogaster petiolata (DeGeer) (Hymenoptera: Vespidae): evidence for pre-imaginal differentiation. J Insect Physiol 48:867–879. https://doi.org/10.1016/s0022-1910(02)00156-7
Kelstrup HC, Hartfelder K, Esterhuizen N, Wossler TC (2017) Juvenile hormone titers, ovarian status and epicuticular hydrocarbons in gynes and workers of the paper wasp Belonogaster longitarsus. J Insect Physiol 98:83–92. https://doi.org/10.1016/j.jinsphys.2016.11.014
Lengyel F, Westerlund SA, Kaib M (2007) Juvenile hormone III influences task-specific cuticular hydrocarbon profile changes in the ant Myrmicaria eumenoides. J Chem Ecol 33:167–181. https://doi.org/10.1007/s10886-006-9185-x
Michelutti KB, Cardoso CAL, Antonialli-Junior WF (2017) Evaluation of chemical signatures in the developmental stages of Mischocyttarus consimilis Zikán (Hymenoptera, Vespidae) employing gas chromatography coupled to mass spectrometry. Rev Virtual Quim 9:535–547. https://doi.org/10.21577/1984-6835.20170031
Monnin T, Malosse C, Peeters C (1998) Solid Phase Microextraction and cuticular hydrocarbon differences related to reproductive activity in the queenless ant Dinoponera quadriceps. J Chem Ecol 24:473–490
Montagna TS, Raizer J, Antonialli-Junior WF (2015) Effect of larval topical application of juvenile hormone on caste determination in the independent-founding eusocial wasp Mischocyttarus consimilis (Hymenoptera: Vespidae). Open J Anim Sci 5:174–184. https://doi.org/10.13102/sociobiology.v67i3.4366
Murakami ASN, Nunes TM, Desuó IC, Shima SN, Mateus S (2015) The Cuticular Hydrocarbons Profiles in the Colonial Recognition of the Neotropical Eusocial Wasp Mischocyttarus cassununga (Hymenoptera Vespidae). Sociobiol. https://doi.org/10.13102/sociobiology.v62i1.109-115
Neves EF, Andrade LHC, Súarez YR, Lima SM, Antonialli-Junior WF (2012) Age-related changes in the surface pheromones of the wasp Mischocyttarus consimilis (Hymenoptera: Vespidae). Genet Mol 11(3):1891–1898. https://doi.org/10.4238/2012.July.19.8
Norman VC, Hughes WOH (2016) Behavioural effects of juvenile hormone and their influence on division of labour in leaf-cutting ant societies. J Exp Biol 219(1):8–11. https://doi.org/10.1242/jeb.132803
Norman VC, Pamminger T, Nascimento F, Hughes WOH (2019) The role of juvenile hormone in regulating reproductive physiology and dominance in Dinoponera quadriceps ants. PeerJ 7:e6512. https://doi.org/10.7717/peerj.6512
O’Donnell S (1998) Reproductive caste determination in eussocial wasps (Hymenoptera: Vespidae). Annu Rev Entomol 43:323–346
O’Donnell S, Jeanne RL (1993) Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis). Physiol Entomol 18:189–194. https://doi.org/10.1111/j.1365-3032.1993.tb00467.x
Oi CA, Oliveira RC, van Zweden JS, Mateus S, Millar JG, Nascimento FS, Wenseleers T (2019) Do primitively eusocial wasps use queen pheromones to regulate reproduction? A case study of the paper wasp Polistes satan. Front Ecol Evol 7:199. https://doi.org/10.3389/fevo.2019.00199
Oliveira RC, Vollet-Neto A, Oi CA, van Zweden JS, Nascimento F, Brent CS, Wenseleers T (2017) Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp. Sci Rep. https://doi.org/10.1038/s41598-017-01794-1
Paes de Oliveira VT, Cruz-Landim C (2001) Experimental control of the extra doses of juvenile hormone on bee development: the case of the wax glands of Apis mellifera (Hymenoptera: Apidae). Soc 38:513–521
Pamminger T, Treanor D, Hughes WOH (2016) Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction–immunocompetence trade-off. Proc R Soc B 283:20152409. https://doi.org/10.1098/rspb.2015.2409
Pinto LZ, Hartfelder K, Bitondi MM, Simões ZLP (2002) Ecdysteroid titers in pupae of highly social bees relate to distinct modes of caste development. J Insect Physiol 48:783–790. https://doi.org/10.1016/s0022-1910(02)00103-8
Queller DC, Strassmann JE (1989) Measuring inclusive fitness in social wasps. In: Breed MD, Page RE (eds) The genetics of social evolution. Westview Press, Boulder, Genetics Selection Evolution, pp 103–122
Quinn GP, Keough MJ (2005) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Rembold H, Czoppelt C, Grune M, Lacner B, Pfeffer J, Woker E (1992) Juvenile hormone titers during honey bee embryogenesis and metamorfhosis. In: Research IJH, fundamental and Applied Approaches, (eds) Mauchamp B. Couillaud F, Baehr JC) Institut Nacional de la Recherche Agronomique, Paris, pp 37–43
Reich GC (1793) Kurze Beschreibung neuen, oder noch wenig bekkanten Thiere, welche Herr Le Blond der naturforschenden Gesellschaft zu Paris aus Cayenne als Geschenk überschikt hat. Magazin des Thierreichs 1:128–134
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665. https://doi.org/10.1146/annurev.en.37.010192.003225
Robinson GE, Ratnieks FLW (1987) Induction of premature honey bee (Hymenoptera; Apidae) flight by juvenile hormone analogs administered orally or topically. J Econ Entomol 80:784–787. https://doi.org/10.1093/jee/80.4.784
Robinson GE, Vargo EL (1997) Juvenile hormone in adult eussocial Hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35:559–583
Röseler PF (1991) Reproductive competition during colony establishment. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University, Ithaca, pp 309–335
Röseler PF, Roseler I, Strambi A, Augier R (1984) Influence of insect hormones on the establishment of dominance hierarchies among foundresses of the paper wasp, Polistes gallicus. Behav Ecol Sociobiol 15:133–142
Ross KG, Matthews RW eds. (1991) The Social Biology of Wasps. Cornell University Press; Ithaca, New York; xvii + 678 pp.
Siegel S, Castellan JR (2006) Estatística não-paramétrica para ciências do comportamento; [Tradução: Carmona SIC], 2ª. Artmed, Porto Alegre
Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38:394–405. https://doi.org/10.1093/icb/38.2.394
Singer TL, Espelie KE, Gamboa GJ (1998) Nest and nestmate discrimination in independent-founding wasps. In: Vander Meer RK, Breed MD, Winston ML, Espelie EK editors. Pheromone communication in social insects 104–125. Boulder, Westview Press
Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409. https://doi.org/10.1007/s002650000311
Sledge MF, Trinca I, Massolo A, Boscaro F, Turillazzi S (2004) Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp. J Insect Physiol 50:73–83. https://doi.org/10.1016/j.jinsphys.2003.10.001
Soares ER, Torres VO, Antonialli-Junior WF (2014) Reproductive status of females in the eusocial wasp Polistes ferreri saussure (Hymenoptera: Vespidae). Neotrop Entomol 43(6):500–508. https://doi.org/10.1007/s13744-014-0242-9
Soares ERP, Batista NR, Souza RDS, Torres VDO, Cardoso CAL, Nascimento FS, Antonialli-Junior WF (2017) Variation of cuticular chemical compounds in three species of Mischocyttarus (Hymenoptera: Vespidae) eusocial wasps. Rev Bras Entomol 61(3):224–231. https://doi.org/10.1016/j.rbe.2017.05.001
Sullivan JP, Jassim O, Fahrbach SE, Robinson GE (2000) Juvenile hormone paces behavioral development in the adult worker honey bee. Horm Behav 37:1–14. https://doi.org/10.1006/hbeh.1999.1552
Tibbetts EA, Fearon ML, Wong E, Huang ZY, Tinghitella RM (2018) Rapid juvenile hormone downregulation in subordinate wasp queens facilitates stable cooperation. Proc Royal Soc B. https://doi.org/10.1098/rspb.2017.2645
Torres VO, Montagna TS, Fernandes WD, Antonialli-Junior WF (2011) Colony cycle of the social wasp Mischocyttarus consimilis Zikán (Hymenoptera: Vespidae). Rev Bras Entomol 55(2):247–252. https://doi.org/10.1590/S0085-56262011000200016
Torres VO, Montagna TS, Raizer J, Antonialli-Junior WF (2012) Division of labor in colonies of the eusocial wasp Mischocyttarus consimilis. J Insect Sci 12:21. https://doi.org/10.1673/031.012.2101
Torres VO, Sguarizi-Antonio D, Lima SM, Andrade LHC, Antonialli-Junior WF (2014) Reproductive Status of the social wasp Polistes versicolor (Hymenoptera Vespidae). Sociobiol 61(2): 218–224, https://doi.org/10.13102/sociobiology.v61i2.218-224
Van den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr 11, 463–471. https://doi.org/10.1016/S0021-9673(01)80947-X
Van Zweden JS, Bonckaert W, Wenseleers T, d’Ettorre P (2013) Queen signaling in social wasps. Evol 68:976–986. https://doi.org/10.1111/evo.12314
Walton A, Tumulty JP, Toth AL, Sheehan MJ (2020) Hormonal modulation of reproduction in Polistes fuscatus social wasps: Dual functions in both ovary development and sexual receptivity. J Insect Physiol 120:103972. https://doi.org/10.1016/j.jinsphys.2019.103972
Weiss I, Hofferberth J, Ruther J, Stokl J (2015) Varying importance of cuticular hydrocarbons and iridoids in the species-specific mate recognition pheromones of three closely related Leptopilina species. Front Ecol Evol 3:1–12. https://doi.org/10.3389/fevo.2015.00019
Wilson EO (1971) The insect societies. Belknap Press, Cambridge, p 548
Wilson EO (1985) The principles of caste evolution. Fortschr Zool 31:307–324
Zara FJ, Balestieri JBP (2000) Behavioural catalogue of Polistes versicolor Oliver (Vespidae: Polistinae) post–emergence colonies. Naturalia 25:301–319
Zhu G, Ye G, Hu C, Xu X, Li K (2006) Development changes of cuticular hydrocarbons in Chrysomya rufifacies larvae: potential for determining larval age. Med Vet Entomol 20:438–444. https://doi.org/10.1111/j.1365-2915.2006.00651.x
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The authors would like to thank Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for providing doctorate fellowships to the first, second, and third authors. CALC (Grant No. 312671/2021‑0) and WFAJ (Grant No. 308182/2019-7) acknowledge research grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
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Neves, E.F., dos Santos Montagna, T., Michelutti, K.B. et al. Role of juvenile hormone in oogenesis, chemical profile, and behavior of the wasp Mischocyttarus consimilis (Vespidae: Polistinae). Chemoecology 32, 197–207 (2022). https://doi.org/10.1007/s00049-022-00378-4
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DOI: https://doi.org/10.1007/s00049-022-00378-4