Skip to main content
Log in

Cuticular hydrocarbons as cues of sex and health condition in Polistes dominula wasps

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

In the paper wasp Polistes dominula, cuticular hydrocarbons play a critical role to acquire information regarding conspecific individuals. However, the relationship between cuticular hydrocarbons, health status, and male sexually selected traits is poorly investigated. In this study, we characterized the cuticular hydrocarbon profile of adult male and female wasps, infected or not by the strepsipteran endoparasite Xenos vesparum, to assess whether the chemical signature provides information about sex and health status (parasite infection). Moreover, we tested whether the chemical profile reflects male quality as measured via morphological and behavioural (sexually selected) traits at leks. Our results showed that males and females had similar total amount of CHCs, quantitatively different profiles and, to a lesser extent, sex-specific chemical compounds. Cuticular profiles were influenced by the strepsipteran infection, and the effect was stronger in females (the primary host) than in males, according to the physiological castration of female but not of male hosts. Regarding territorial and non-territorial males, no significant difference emerged in their chemical profiles. Furthermore, sex-dimorphic visual signals (size, shape, and asymmetry of abdominal yellow spots) were related to the behavioural displays of territorial males. We hypothesize that cuticular hydrocarbons are potential multi-role cues to assess sex and health status in male and female wasps, in synergy with visual signals and territorial performance in signaling male quality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aitchison J (1982) The statistical analysis of compositional data. Royal Stat Soc 44:139–160

    Google Scholar 

  • Ayasse M, Paxton RJ, Tengö J (2001) Mating behaviour and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78

    CAS  PubMed  Google Scholar 

  • Bagnères AG, Lorenzi C (2010) Chapter 14. Chemical deception/mimicry using cuticular hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 282–324

    Google Scholar 

  • Bates D, Kliegl R, Vasishth S, Baayen H (2015) Parsimonious mixed models. http://arxiv.org/abs/1506.04967

  • Beani L (1996) Lek-like courtship in paper wasps: “a prolonged, delicate, and troublesome affair”. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford Univ Press, Oxford, pp 113–125

    Google Scholar 

  • Beani L, Calloni C (1991a) Male rubbing behaviour and the hypothesis of pheromonal release in polistine wasps (Hymenoptera vespidae). Ethol Ecol Evol 1:51–54

    Google Scholar 

  • Beani L, Calloni C (1991b) Leg tegumental glands and male rubbing behaviour at leks in Polistes dominulus (Hymenoptera: Vespidae). J Ins Behav 4:449–461

    Google Scholar 

  • Beani L, Landi M (2000) Aerial leks and marking behaviour in Parischnogaster mellyi males (Hymenoptera Stenogastrinae). Ins Soc Life 3:13–17

    Google Scholar 

  • Beani L, Sledge MF, Maiani S, Boscaro F, Landi M, Fortunato A, Turillazzi S (2002) Behavioral and chemical analyses of scent-marking in hover wasps (Vespidae, Stenogastrinae). Ins Soc 49:275–281

    Google Scholar 

  • Beani L, Turillazzi S (1988) Alternative mating tactics in males of Polistes dominulus (Hymenoptera: Vespidae). Behav Ecol Sociobiol 22:257–264

    Google Scholar 

  • Beani L, Zaccaroni M (2015) Experimental male size manipulation in Polistes dominula paper wasps: to be of the right size. Ethol Ecol Evol 27:185–189. https://doi.org/10.1080/03949370.2014.915431

    Article  Google Scholar 

  • Beani L, Dallai R, Mercati D, Giusti F, Cappa F, Manfredini F (2011) When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Anim Behav 82:1305–1312

    Google Scholar 

  • Beani L, Dessì-Fulgheri F, Cappa F, Toth A (2014) The trap of sex in social insects: from the female to the male perspective. Neurosci Biobehav Rev 46:519–533. https://doi.org/10.1016/j.neubiorev.2014.09.014

    Article  PubMed  Google Scholar 

  • Beani L, Cappa F, Petrocelli I, Gottardo M, Manfredini F, Giusti F, Dallai R (2017) Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: parasite or parasitoid? J Insect Physiol 101:22–30

    CAS  PubMed  Google Scholar 

  • Beani L, Cappa F, Manfredini F, Zaccaroni M (2018) Preference of Polistes dominula wasps for trumpet creepers when infected by Xenos vesparum: a novel example of co-evolved traits between host and parasite. PLoS One 13:e0205201

    PubMed  PubMed Central  Google Scholar 

  • Blomquist GJ, Bagnères AG (2010) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge Univ Press, Cambridge

    Google Scholar 

  • Bonavita-Cougourdan A, Theraulaz G, Bagnères AG, Roux M, Pratte M, Provost E, Clément JL (1991) Cuticular hydrocarbons, social organization and ovarian development in a polistine wasp: Polistes dominulus christ. Comp Biochem Physiol B 100:667–680

    Google Scholar 

  • Boomsma JJ, Baer B, Heinze J (2005) The evolution of male traits in social insects. Annu Rev Entomol 50:395–420

    CAS  PubMed  Google Scholar 

  • Brandstaetter AS, Endler A, Kleinidan CJ (2008) Nestmate recognition in ants is possible without tactile interaction. Naturwissenschaften 95:601–608

    CAS  PubMed  Google Scholar 

  • Brandstaetter AS, Rössler W, Kleinidan CJ (2010) Dummies versus air puffs: efficient stimulus delivery for low-volatile odors. Chem Senses 35:323–333. https://doi.org/10.1093/chemse/bjq022

    Article  CAS  PubMed  Google Scholar 

  • Bruschini C, Cervo R, Turillazzi S (2010) Pheromones in social wasps. Vitam Horm 83:447–492

    Google Scholar 

  • Cappa F, Bruschini C, Cervo R, Turillazzi S, Beani L (2013) Males do not like the working class: male sexual preference and recognition of functional castes in a primitively eusocial wasp. Anim Behav 86:801–810

    Google Scholar 

  • Cappa F, Manfredini F, Dallai R, Gottardo M, Beani L (2014) Parasitic castration by Xenos vesparum depends on host gender. Parasitology 141:1080–1087

    PubMed  Google Scholar 

  • Cappa F, Beani L, Cervo R (2016a) The importance of being yellow: visual over chemical cues in gender recognition in a social wasp. Behav Ecol 27:1182–1189

    Google Scholar 

  • Cappa F, Bruschini C, Protti I, Turillazzi S, Cervo R (2016b) Bee guards detect foreign foragers with cuticular chemical profiles altered by phoretic varroa mites. J Apic Res 55:268–277

    Google Scholar 

  • Cappa F, Cini A, Pepiciello I, Petrocelli I, Cervo R (2019) Female body size, weight and fat storage rather than nestmateship determine male attraction in the invasive yellow-legged hornet Vespa velutina nigrithorax. Ethol Ecol Evol 31:73–85

    Google Scholar 

  • Cervo R, Bertocci F, Turillazzi S (1996) Olfactory cues in host nest detection by the social parasite Polistes sulcifer (Hymenoptera, Vespidae). Behav Process 36:213–218

    CAS  Google Scholar 

  • Chung H, Carroll SB (2015) Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. Bioassays 37(7):822–830

    CAS  Google Scholar 

  • Costanzi E, Bagnères AG, Lorenzi MC (2013) Changes in the Hydrocarbon Proportions of Colony Odor and Their Consequences on Nestmate Recognition in Social Wasps. PloS one 8:e65107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dapporto L, Cini A, Palagi E, Morelli M (2007) Behaviour and chemical signature of pre-hibernating females of Polistes dominulus infected by the strepsipteran Xenos vesparum. Parasitology 134:545–552

    CAS  PubMed  Google Scholar 

  • Eickwort K (1969) Separation of the castes of Polistes exclamans and notes on its biology (Hym. Vespidae). Ins Soc 16:67–72

    Google Scholar 

  • de Souza AR, Lino-Neto J, Tibbetts EA, Turillazzi S, Beani L (2017) The leks of Polistes dominula paper wasps: tiny abdominal spots play a critical role in male attacks toward potential rivals. Ethol Ecol Evol 29:410–419

    Google Scholar 

  • de Souza AR, Guimarães Simões T, Rantala MJ, Fernando Santos E, Lino-Neto J, do Nascimento FS (2018) Sexual ornaments reveal the strength of melanization immune response and longevity of male paper wasps. J Insect Physiol 109:163–168. https://doi.org/10.1016/j.jinsphys.2018.06.002

    Article  CAS  PubMed  Google Scholar 

  • Derstine NT, Ohler B, Jimenez SI, Landolt P, Gries G (2017) Evidence for sex pheromones and inbreeding avoidance in select North American yellowjacket species. Entomol Exp Appl 164:35–44

    CAS  Google Scholar 

  • Elia M, Blancato G, Picchi L, Lucas C, Bagnères AG, Lorenzi MC (2017) Nest signature changes throughout colony cycle and after social parasite invasion in social wasps. PLoS One 12:e0190018. https://doi.org/10.1371/journal.pone.0190018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elias TH, Gelband H (1975) Nectar: its production and function in trumpet creepers. Science 189:289–291

    CAS  PubMed  Google Scholar 

  • Elmquist DC, Landolt PJ, Ream LM, Cha DH (2018) Laboratory demonstrations of pheromone-mediated scent-marking, orientation, and mounting behavior in Polistes exclamans (Hymenoptera: Vespidae). Ann Entomol Soc America 111:21–30

    CAS  Google Scholar 

  • Espelie KE, Hermann HR (1990) Surface lipid of the social wasp Polistes annularis (L.) and its nest and nest pedicel. J Chem Ecol 16:1841–1852

    CAS  PubMed  Google Scholar 

  • Foley B, Chenoweth SF, Nuzhdin SV, Blows MV (2007) Natural genetic variation in cuticular hydrocarbon expression in male and female, Drosophila melanogaster. Genetics 175:1465–1477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giusti F, Dallai R, Beani L, Manfredini F, Dallai R (2007) The midgut ultrastructure of the endoparasite Xenos vesparum (Rossi) (Insecta, Strepsiptera) during post-embryonic development and stable carbon isotopic analyses of the nutrient uptake. Arthropod Struct Dev 36:183–197

    CAS  PubMed  Google Scholar 

  • Heinze J (2016) The male has done his work—the male may go. Curr Opin Insect Sci 16:22–27

    PubMed  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioral and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:372–393

    Google Scholar 

  • Hughes DP, Beani L, Turillazzi S, Kathirithamby J (2004a) Social wasps desert the colony and aggregate outside if parasitized: an example of adaptive parasite manipulation of host behaviour? Behav Ecol 15:1037–43

    Google Scholar 

  • Hughes DP, Kathirithamby J, Beani L (2004b) Prevalence of the parasite Strepsiptera in adult Polisteswasps: field collections and literature overview. Ethol Ecol Evol 16:363–375

    Google Scholar 

  • Ingleby F (2015) Insect cuticular hydrocarbons as dynamic traits in sexual communication. Insects 6:732–742

    PubMed  PubMed Central  Google Scholar 

  • Izzo AS, Tibbetts EA (2012) Spotting the top male: sexually selected signals in male Polistes dominulus wasps. Anim Behav 83:839–845

    Google Scholar 

  • Izzo A, Tibbetts EA (2015) Heightened condition dependence of a sexually selected signal in male Polistes dominulus paper wasps. Ethology 121:586–592

    Google Scholar 

  • Jeanne RL (1996) The evolution of exocrine gland function in wasps. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford University Press, Oxford, pp 144–159

    Google Scholar 

  • Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289

    PubMed  Google Scholar 

  • Karubian J, Lindsay WR, Schwabl H, Webster MS (2011) Bill coloration, a flexible signal in a tropical passerine bird, is regulated by social environment and androgens. Anim Behav 8:795–800

    Google Scholar 

  • Keeling CI, Plettner E, Slessor KN (2004) Hymenopteran semiochemicals. Top Curr Chem 239:133–177

    CAS  PubMed  Google Scholar 

  • Keeping MG, Lipschitz D, Crewe RM (1986) Chemical mate recognition and release of male sexual behavior in polybiine wasp, Belonogaster petiolata (Degeer) (Hymenoptera: Vespidae). J Chem Ecol 12:773–779

    CAS  PubMed  Google Scholar 

  • Landolt PJ, Jeanne RL, Reed HC (1998) Chemical communication in social wasps. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects. Ants, wasps, bees and termites. Westview Press, Boulder, pp 216–235

    Google Scholar 

  • Layton JM, Camann MA, Espelie KE (1994) Cuticular lipid profiles of queens, workers, and males of social wasp Polistes metricus Say are colony-specific. J Chem Ecol 20:2307–2321

    CAS  PubMed  Google Scholar 

  • Lorenzi MC, Bertolino F, Beani L (1994) Nuptial system of a social parasite wasp, Polistes semenowi (Hymenoptera, Vespidae). Ethol Ecol Evol 3:57–60

    Google Scholar 

  • Lorenzi MC, Bagnères AG, Clément JL (1996) The role of epicuticular hydrocarbons in social insects: is the same in paper wasps? In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford Univ Press, Oxford, pp 178–189

    Google Scholar 

  • Lorenzi MC, Bagnères AG, Clément JL, Turillazzi S (1997) Polistes biglumis bimaculatus epicuticular hydrocarbons and nestmate recognition (Hymenoptera: Vespidae). Insect Soc 44:123–138

    Google Scholar 

  • Lorenzi MC, Sledge MF, Laiolo P, Sturlini E, Turillazzi S (2004) Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems. J Insect Physiol 50:935–941

    CAS  PubMed  Google Scholar 

  • Lorenzi MC, Cervo R, Bagnères AG (2011) Facultative social parasites mark host nests with branched hydrocarbons. Anim Behav 82:1149–1157

    Google Scholar 

  • Lorenzi MC, Azzani L, Bagnères AG (2014) Evolutionary consequences of deception: complexity and informational content of colony signature are favored by social parasitism. Curr Zool 60:137–148

    Google Scholar 

  • MacKenzie JK, Landolt PJ, Zack RS (2008) Sex attraction in Polistes dominulus (Christ) demonstrated using olfactometers and morphological sourceextracts. J Entomol Soc BC 105:35–43

    Google Scholar 

  • Nonacs P, Carlin NF (1990) When can ants discriminate the sex of brood? A new aspect of queen-worker conflict. Proc Natl Acad Sci 87:9670–9673

    CAS  PubMed  Google Scholar 

  • Pardi L (1948) Dominance order in Polistes wasps. Physiol. Zool. 21:1–13

    CAS  PubMed  Google Scholar 

  • Passera L, Aron S (1996) Early sex discrimination and male brood elimination by workers of the Argentine ant. Proc R Soc Lond B 263:1041–1046

    Google Scholar 

  • Polak M (1993) Competition for landmark territories among male Polistes canadensis (L.) (Hymenoptera: Vespidae): large-size advantage and alternative mate-acquisition tactics. Behav Ecol 4:325–331

    Google Scholar 

  • Post DC, Jeanne RL (1983) Male reproductive behaviour of the social wasp Polistes fuscatus (Hymenoptera: Vespidae). Z Tierpsychol 62:157–171

    Google Scholar 

  • Post DC, Jeanne RL (1984) Venom Source of a sex pheromone in the social wasp Polistes fuscatus (Hymenoptera: Vespidae). J Chem Ecol 9:259–266

    Google Scholar 

  • Reed HC, Landolt PJ (1990) Sex attraction in paper wasp, Polistes exclamans Viereck (Hymenoptera: Vespidae), in a wind tunnel. J Chem Ecol 16:1277–1287

    CAS  PubMed  Google Scholar 

  • Romani R, Isidoro N, Riolo P, Bin F, Fortunato A, Turillazzi S, Beani L (2005) A new role for antennation in paper wasps (Hymenoptera, Vespidae): antennal courtship and sex dimorphic glands in antennomeres. Ins Soc 52:96–102

    Google Scholar 

  • Ryan RE, Gamboa GJ (1986) Nestmate recognition between males and gynes of the social wasp Polistes fuscatus (Hymenoptera: Vespidae). Ann Entomol Soc 79:572–575

    Google Scholar 

  • Singer TL, Espelie KE, Gamboa GJ (1998) Nest and nestmate discrimination in independent-founding paper wasps. In: Vander Meer RK, Breed MD, Wiston MD, Espelie KE (eds) Pheromone communication in social insects. Westview Press, Boulder, pp 104–125

    Google Scholar 

  • Steiger S, Stökl J (2014) The role of sexual selection in the evolution of chemical signals in insects. Insects 5:423–438

    PubMed  PubMed Central  Google Scholar 

  • Tibbetts EA, Mettler A, Levy A (2009) Mutual assessment via visual status signals in wasps. Biol Lett 6:10–13

    PubMed  PubMed Central  Google Scholar 

  • Torres VO, Soares ERP, Lima LD, Lima SM, Andrade LHC, Antonialli-Junior WF (2016) Morphophysiological and cuticular chemical alterations caused by Xenos entomophagus endoparasites in the social wasp Polistes ferreri (Hymenoptera, Vespidae). Parasitology 143:1939–1944

    PubMed  Google Scholar 

  • Trabalon M, Plateaux L, Peru L, Bagnères AG, Hartmann N (2000) Modification of morphological characters and cuticular compounds in worker ants Leptothorax nylanderi induced by endoparasites Anomotaenia brevis. J Insect Physiol 46:169–178

    CAS  PubMed  Google Scholar 

  • Turillazzi S, Cervo R (1982) Territorial behaviour in males of Polistes nimpha (Christ) (Hymenoptera, Vespidae). Z Tier Psychol 38:174–80

    Google Scholar 

  • Wen P, Cheng YN, Dong SH, Wang ZW, Tan K, Nieh JC (2017) The sex pheromone of a globally invasive honey bee predator, the Asian eusocial hornet, Vespa velutina. Sci Rep 7:12956

    PubMed  PubMed Central  Google Scholar 

  • Wheeler WM (1892) Concerning the “Blood-Tissue” of the Insecta.—III. Psyche 6(193):253–258

    Google Scholar 

Download references

Acknowledgements

The authors are thankful to Eva Peroni, André Rodrigues de Souza, and the members of the Florence Group for the Study of Social Wasps for their support during the experiment, both in the field and in the laboratory.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Beani.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beani, L., Bagnères, AG., Elia, M. et al. Cuticular hydrocarbons as cues of sex and health condition in Polistes dominula wasps. Insect. Soc. 66, 543–553 (2019). https://doi.org/10.1007/s00040-019-00721-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-019-00721-z

Keywords

Navigation