Skip to main content
Log in

Colony structure and reproductive sharing among queens in a tropical paper wasp, Polistes olivaceus

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

Abstract

Reproductive partitioning among group members is a key feature in social Hymenoptera. We investigated the genetic colony structure of a tropical paper wasp Polistes olivaceus, with an emphasis on variation in the number of queens and reproductive sharing among queens. Among 22 P. olivaceus colonies, 6 were monogynous, 9 polygynous, and 7 were queenless. Adults and brood (eggs and larvae) were genotyped based on six polymorphic microsatellite loci. In each of the polygynous colonies, progenies were assigned to their mothers using maximum-likelihood methods. Nestmate queens were full sisters. The vast majority of reproduction appeared to be monopolized by the dominant queen (α), and the overall reproductive skews were 0.63 ± 0.04 (B index) and 0.97 ± 0.02 (S c index). Although all nestmate queens had equal reproductive potential, the high magnitude of reproductive skew was enigmatic in this species. Although 9.55 ± 2.07 workers contained developed ovaries in 11 of 15 queen-right colonies, they were unrelated to the nestmate queens but related to each other as full sisters, suggesting that they were the remaining offspring of superseded queens. In 2 of the 11 colonies, we detected male eggs produced by reproductive workers. On average, 7.27 % of the total genotyped male eggs were derived from reproductive workers among the colonies. These results suggest three possibilities regarding the presence of reproductive workers in the P. olivaceus colonies: drifting between colonies, putative remaining offspring from superseded queens, and the offspring of unrelated females who joined the colonies and reproduced there. We found no worker-derived larvae or adult males, suggesting that male eggs were removed by nestmates at some point between oviposition and hatching.

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

Similar content being viewed by others

References

  • Abràmoff M.D., Magalhães P.J. and Ram S.J. 2004. Image processing with ImageJ. Biophotonics Int. 11: 36-42

    Google Scholar 

  • Alam S.M. 1958. Some interesting relations about the nest of Polistes hebraeus Fabr. (Vespidae: Hymenoptera) - the common yellow wasp of India. Proc. Zool. Soc. Calcutta 11: 113-122

    Google Scholar 

  • Arévalo E., Strassmann J.E. and Queller D.C. 1998. Conflicts of interest in social insects: male production in two species of Polistes. Evolution 52: 797-805

    Google Scholar 

  • Bassam B.J., Caetano-Anolles G. and Gresshoff P.M. 1991. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal. Biochem. 196: 80-83

    Google Scholar 

  • Bolton A., Sumner S., Shreeves G., Casiraghi M. and Field J. 2006. Colony genetic structure in a facultatively eusocial hover wasp. Behav. Ecol. 17: 873-880

    Google Scholar 

  • Bonckaert W., Tofilski A., Nascimento F.S., Billen J., Ratnieks F.L.W. and Wenseleers T. 2011. Co-occurrence of three types of egg policing in the Norwegian wasp Dolichovespula norwegica. Behav. Ecol. Sociobiol. 65: 633-640

    Google Scholar 

  • Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B. 351: 947-975

    Google Scholar 

  • Cnaani J., Schmid-Hempel R. and Schmidt J.O. 2002. Colony development, larval development and worker reproduction in Bombus impatiens Cresson. Insect. Soc. 49: 164-170

    Google Scholar 

  • Dieringer D. and Schötterer C. 2003. Microsatellite analyzer (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 3: 167-169

    Google Scholar 

  • Dugdale H.L., Macdonald D.W., Pope L.C., Johnson P.J. and Burke T. 2008. Reproductive skew and relatedness in social groups of European badgers, Meles meles. Mol. Ecol. 17: 1815-1827

    Google Scholar 

  • Field J. and Cant M.A. 2009. Reproductive skew in primitively eusocial wasps: how useful are current models? In: Reproductive Skew in Vertebrates: Proximate and Ultimate Causes (R. Hager and C.B. Jones, Eds). Cambridge University Press, Cambridge, pp 305-333

  • Field J., Solís C.R., Queller D.C. and Strassmann J.E. 1998. Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models. Am. Nat. 151: 545-563

    Google Scholar 

  • Field J., Cronin A. and Bridge C. 2006. Future fitness and helping in social queues. Nature 441: 214-217

    Google Scholar 

  • Foster K.R. and Ratnieks F.L.W. 2001. The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies. Am. Nat. 158: 615-623

    Google Scholar 

  • Foster K.R., Seppä P., Ratnieks F.L.W. and Thorén P.A. 1999. Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps. Behav. Ecol. Sociobiol. 46: 252-257

    Google Scholar 

  • Gamboa G.J. 1978. Intraspecific defense: advantage of social cooperation among paper wasp foundresses. Science 199: 1463-1465

    Google Scholar 

  • Gamboa G.J. 1980. Comparative timing of brood development between multiple- and single-foundress colonies of the paper wasp, Polistes metricus. Ecol. Entomol. 5: 221-225

    Google Scholar 

  • Goodnight K.F. and Queller D.C. 1994. Relatedness 4.2. Goodnight Software, Houston, TX. http://gsoft.smu.edu/GSoft.html

  • Hughes W.O.H., Oldroyd B.P., Beekman M. and Ratnieks F.L.W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213-1216

    Google Scholar 

  • Izzo A., Wells M., Huang Z. and Tibbetts E. 2010. Cuticular hydrocarbons correlate with fertility, not dominance, in a paper wasp, Polistes dominulus. Behav. Ecol. Sociobiol. 64: 857-864

    Google Scholar 

  • Keller L. and Krieger M.J.B. 1996. Mating success of male birds. Nature 380: 208-209

    Google Scholar 

  • Kikuta N. and Tsuji K. 1999. Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav. Ecol. Sociobiol. 46: 180-189

    Google Scholar 

  • Klahn J.E. 1988. Intraspecific comb usurpation in the social wasp Polistes fuscatus. Behav. Ecol. Sociobiol. 23: 1-8

    Google Scholar 

  • Kokko H., Mackenzie J.D., Reynolds J., Lindstrom J. and Sutherland W.J. 1999. Measures of inequality are not equal. Am. Nat. 72: 358-382

    Google Scholar 

  • Krieger M.J.B. and Keller L. 1997. Skew 1.1. http://www.unil.ch/izea/softwares/skew.html

  • Kümmerli R. and Keller L. 2007. Extreme reproductive specialization within ant colonies: some queens produce males whereas others produce workers. Anim. Behav. 74: 1535-1543

    Google Scholar 

  • Langer P., Hogendoorn K., Schwarz M.P. and Keller L. 2006. Reproductive skew in the Australian allodapine bee Exoneura robusta. Anim. Behav. 71: 193-201

    Google Scholar 

  • Leadbeater E., Carruthers J.M., Green J.P., Rosser N.S. and Field J. 2011. Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science 333: 874-876

    Google Scholar 

  • Liebert A.E. and Starks P.T. 2006. Taming of the skew: transactional models fail to predict reproductive portioning in the paper wasp Polistes dominulus. Anim. Behav. 71: 913-923

    Google Scholar 

  • Liebert A.E., Nonacs P. and Wayne R.K. 2005. Solitary nesting and reproductive success in the paper wasp Polistes aurifer. Behav. Ecol. Sociobiol. 57: 445-456

    Google Scholar 

  • Liebig J., Monnin T. and Turillazzi S. 2005. Direct assessment of queen quality and lack of worker suppression in a paper wasp. Proc. R. Soc. Lond. B. Biol. Sci. 272: 1339-1344

    Google Scholar 

  • Lopez-Vaamonde C., Koning J.W., Brown R.M., Jordan W.C. and Bourke A.F.G. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430: 557-560

    Google Scholar 

  • Metcalf R.A. and Whitt G.S. 1977a. Intra-nest relatedness in the social wasp Polistes metricus. Behav. Ecol. Sociobiol. 2: 339-351

  • Metcalf R.A. and Whitt G.S. 1977b. Relative inclusive fitness of the social wasp Polistes metricus. Behav. Ecol. Sociobiol. 2: 353-360

  • Moilanen A., Sundström L. and Pedersen J.S. 2004. MATESOFT: a program for deducing parental genotypes and estimating mating system statistics in haplodiploid species. Mol. Ecol. Notes 4: 795-797

    Google Scholar 

  • Nei M. and Roychoudhury A.K. 1974. Sampling variance of heterozygosity and genetic distance. Genetics 76: 379-390

    Google Scholar 

  • Nonacs P. 2000. Measuring and using skew in the study of social behaviour and evolution. Am. Nat. 156: 577-589

    Google Scholar 

  • Nonacs P. 2003 Measuring the reliability of skew indices: is there one best index? Anim. Behav. 65: 615-627

    Google Scholar 

  • Nonacs P. and Hager R. 2011. The past, present and future of reproductive skew theory and experiments. Biol. Rev. 86: 271-298

    Google Scholar 

  • Nonacs P. and Reeve H.K. 1995. The ecology of cooperation in wasps: causes and consequences of alternative reproductive decisions. Ecology 76: 953-967

    Google Scholar 

  • Noonan K.M. 1981. Individual strategies of inclusive-fitness-maximizing in Polistes fuscatus foundresses. In: Natural Selection and Social Behaviour: Recent Research and New Theory (R.D. Alexander and D.W. Tinkle, Eds). Chiron Press, New York, pp 18-44

  • Ohtsuki H. and Tsuji K. 2009. Adaptive reproduction schedule as a cause of worker policing in social Hymenoptera: a dynamic game analysis. Am. Nat. 173: 747-758

    Google Scholar 

  • Pardi L. 1994. Dominance order in Polistes wasps. Physiol. Zool. 21: 1-13

    Google Scholar 

  • Peters J.M., Queller D.C., Strassmann J.E. and Solís C.R. 1995. Maternity assignment and queen replacement in a social wasp. Proc. R. Soc. Lond. B. 260: 7-12

    Google Scholar 

  • Queller D.C. and Goodnight K.F. 1989. Estimating relatedness using genetic markers. Evolution 43: 258-275

    Google Scholar 

  • Queller D.C. and Strassmann J.E. 1988. Reproductive success and group nesting in the paper wasp Polistes annularis. In: Reproductive Success: Studies of Individual Variation in Contrasting Breeding System (T.H. Clutton-Brock, Ed). University of Chicago Press, Chicago, pp 76-96

  • Queller D.C., Zacchi F., Cervo R., Turillazzi S., Henshaw M.T., Santorelli L.A. and Strassmann J.E. 2000. Unrelated helpers in social insect. Nature 405: 784-787

    Google Scholar 

  • Ratnieks F.L.W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132: 217-236

    Google Scholar 

  • Reeve H.K. 1991. Polistes. In: The Social Biology of Wasps (K.G. Ross and R. Matthews, Eds). Cornell University Press, New York, pp 99-148

  • Reeve H.K. and Keller L. 2001. Tests of reproductive-skew models in social insects. Annu. Rev. Entomol. 46: 347-385

    Google Scholar 

  • Reeve H.K., Starks P.T., Peter J.M. and Nonacs P. 2000. Genetic support for the evolutionary theory of reproductive transactions in social wasps. Proc. R. Soc. Lond. B. 267: 75-79

    Google Scholar 

  • Rice W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225

    Google Scholar 

  • Rousset F. 2008. GENEPOP’007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resources 8: 103-106. http://kimura.univ-montp2.fr/~rousset/Genepop.html

  • Saigo T. and Tsuchida K. 2004. Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc. R. Soc. Lond. B. 271: S509-S512

    Google Scholar 

  • Saigo T. and Tsuchida K. 2010. Nine newly designed polymorphic microsatellite loci for the Japanese paper wasp, Polistes chinensis antennalis (Hymenoptera: Vespidae). Appl. Entomol. Zool. 45: 575-577

  • Seppä P., Queller D.C. and Strassmann J.E. 2002. Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew. Behav. Ecol. 13: 531-542

    Google Scholar 

  • Seppä P., Fogelqvist J., Gyllenstrand N. and Lorenzi M.C. 2011. Colony kin structure and breeding patterns in the social wasp, Polistes biglumis. Insect. Soc. 58: 345-355

    Google Scholar 

  • Shreeves G., Cant M.A., Bolton A. and Field J. 2003. Insurance-based advantages for subordinate co-foundresses in a temperate paper wasp. Proc. R. Soc. Lond. B. 270: 1617-1622

    Google Scholar 

  • Strassmann J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1-13

    Google Scholar 

  • Strassmann J.E., Hughes C.R., Queller D.C., Turillazzi S., Cervo R., Davis S.K. and Goodnight K. 1989. Genetic relatedness in primitively eusocial wasps. Nature 342: 268-270

    Google Scholar 

  • Strassmann J.E., Barefield K., Solís C.R., Hughes C.R. and Queller D.C. 1997. Trinucleotide microsatellite loci for a social wasp, Polistes. Mol. Ecol. 6: 97-100

    Google Scholar 

  • Sumner S., Casiraghi M., Foster W. and Field J. 2002. High reproductive skew in tropical hover wasps. Proc. R. Soc. London. B. 269: 179-186

    Google Scholar 

  • Sumner S., Lucas E., Barker J. and Isaac N. 2007. Radio-tagging technology reveals extreme nest-drifting behaviour in a eusocial insect. Curr. Biol. 17: 140-145

    Google Scholar 

  • Sumner S., Kelstrup H. and Fanelli D. 2010. Reproductive constraints, direct fitness and indirect fitness benefits explain helping behaviour in the primitively eusocial wasp, Polistes canadensis. Proc. R. Soc. Lond. B. 277: 1721-1728

    Google Scholar 

  • Takahashi J., Martin S.J., Ono M. and Shimizu I. 2010. Male production by non-natal workers in the bumblebee, Bombus deuteronymus (Hymenoptera: Apidae). J. Ethol. 28: 61-66

    Google Scholar 

  • Tibbetts E.A. and Reeve H.K. 2003. Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns. Behav. Ecol. 14: 510-514

    Google Scholar 

  • Tsuchida K., Saigo T., Tsujita S., Takeuchi K., Ito N. and Sugiyama M. 2003. Polymorphic microsatellite loci for the Japanese paper wasp, Polistes chinensis antennalis (Hymenoptera: Vespidae). Mol. Ecol. Notes 3: 384-386

  • Uddin M.M. and Tsuchida K. 2012. Genetic population structure of the paper wasp Polistes olivaceus (Hymenoptera: Vespidae) in Bangladesh. Popul. Ecol. 54: 103-114

    Google Scholar 

  • Wang J. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963-1979

    Google Scholar 

  • Wenseleers T., Tofilski A. and Ratnieks F.L.W. 2005. Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav. Ecol. Sociobiol. 58: 80-86

    Google Scholar 

  • West-Eberhard M.J. 1969. The social biology of Polistine wasps. Misc. Publ. Mus. Zool. Univ. Mich. 140: 1-101

    Google Scholar 

  • Zanette L.R.S. and Field J. 2008. Genetic relatedness in early associations of Polistes dominulus: from related to unrelated helpers. Mol. Ecol. 17: 2590-2597

    Google Scholar 

Download references

Acknowledgments

We thank everyone who helped to collect P. olivaceus colonies in Bangladesh. We sincerely thank all members of the Laboratory of Insect Ecology, Gifu University, for their cooperation in conducting this study, especially Dr. Y. KonDo who provided valuable assistance in data analysis. We give special thanks to two anonymous reviewers for valuable comments that significantly improved our manuscript. Finally, we greatly appreciate the financial support of the Ministry of Education, Culture, Sports, Science and Technology (MONBUKAGAKUSHO), Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. M. Uddin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uddin, M.M., Tsuchida, K. Colony structure and reproductive sharing among queens in a tropical paper wasp, Polistes olivaceus . Insect. Soc. 59, 401–410 (2012). https://doi.org/10.1007/s00040-012-0233-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-012-0233-y

Keywords

Navigation