Skip to main content
SpringerLink
Log in

Investigating queen influence on worker behaviour using comparisons of queenless and queenright workers

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

Abstract

Female eusocial sweat bees are capable of behaving as queens or workers. Relatively few females become queens, and those that do can directly manipulate the reproductive behaviour of other females in the nest. We collected Lasioglossum (Dialictus) laevissimum workers from nests with and without queens (queenright and queenless nests, respectively) to investigate the influence queens exert on worker behaviour via direct manipulation. Overall, very few L. laevissimum workers (17%) had developed ovaries in Ontario, but queenright and queenless workers were equally likely to have developed ovaries and worn mandibles. However, queenless workers were more likely to be mated than queenright workers. These results suggest first, that queens inhibit egg-laying in most, but not all workers, and second, that queen behaviour during the first few days of workers’ adult lives exerts a lasting influence on worker behaviour. We also compared social traits of L. laevissimum and other Dialictus species using principal components analysis. A strong correlation between worker reproduction and male availability suggests that queen manipulation of the worker brood sex ratio has evolved as an indirect mechanism for queens to discourage worker reproduction.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albert JR, Packer L (2013) Nesting biology and phenology of a population of Halictus farinosus Smith (Hymenoptera, Halictidae) in northern Utah. J Hymenopt Res 32:55–73

    Article  Google Scholar 

  • Batra SWT (1966) Life cycle and behavior of the primitively social bee, Lasioglossum zephyrum. Univ Kansas Sci Bull 46:359–2423

    Google Scholar 

  • Batra SWT (1987) Ethology of the vernal eusocial bee, Dialictus laevissimus (Hymenoptera: Halictidae). J Kansas Entomol Soc 60:100–108

    Google Scholar 

  • Boomsma JJ, Eickwort GC (1993) Colony structure, provisioning and sex allocation in the sweat bee Halictus ligatus (Hymenoptera: Halictidae). Biol J Linn Soc 48:355–377

    Article  Google Scholar 

  • Bourke AFG (2011) The validity and value of inclusive fitness theory. Proc R Soc B Biol Sci 278:3313–3320

    Article  Google Scholar 

  • Breed MD (1975) Life cycle and behavior of a primitively social bee, Lasioglossum rohweri (Hymenoptera: Halictidae). J Kansas Entomol Soc 48:64–80

    Google Scholar 

  • Breed MD (1976) The evolution of social behavior in primitively social bees: A multivariate analysis. Evolution 30:234–240

    Article  PubMed  Google Scholar 

  • Crespi BJ, Ragsdale JE (2000) A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved. Proc R Soc Lond B 267:821–828

    Article  CAS  Google Scholar 

  • Eickwort GC (1986) First steps into eusociality: the sweat bee Dialictus lineatulus. Fla Entomol 69:742–754

    Article  Google Scholar 

  • Eickwort GC, Eickwort KR (1971) Aspects of the biology of Costa Rican halictine bees, II, Dialictus umbripennis and adaptations of its caste structure to different climates. J Kansas Entomol Soc 44:343–373

    Google Scholar 

  • Gibbs J (2010) Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa 2591:1–382

    Google Scholar 

  • Gibbs J (2011) Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 3073:1–216

    Google Scholar 

  • Greenberg L, Buckle GR (1981) Inhibition of worker mating by queens in a sweat bee, Lasioglossum zephyrum. Insectes Soc 28:347–352

    Article  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior: I and II. J Theor Biol 7:1–52

    Article  PubMed  CAS  Google Scholar 

  • Kapheim KM, Bernal SP, Smith AR et al (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae. Behav Ecol Sociobiol 65:1179–1190

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapheim KM, Chan T-Y, Smith AR et al (2016) Ontogeny of division of labor in a facultatively eusocial sweat bee Megalopta genalis. Insectes Soc 63:185–191

    Article  Google Scholar 

  • Kapheim KM, Nonacs P, Smith AR et al (2015) Kinship, parental manipulation and evolutionary origins of eusociality. Proc R Soc B Biol Sci 282:20142886

    Article  Google Scholar 

  • Kukuk PF, May B (1991) Colony dynamics in a primitively eusocial halictine bee Lasioglossum (Dialictus) zephyrum (Hymenoptera: Halictidae). Insectes Soc 38:171–188

    Article  Google Scholar 

  • Michener CD (1966) The bionomics of a primitively social bee, Lasioglossum versatum (Hymenoptera: Halictidae). J Kansas Entomol Soc 39:193–217

    Google Scholar 

  • Michener CD, Brothers DJ (1974) Were workers of eusocial hymenoptera initially altruistic or oppressed? Proc Natl Acad Sci USA 71:671–674

    Article  PubMed  CAS  Google Scholar 

  • Michener CD, Lange RB (1958) Observations on the behavior of Brasilian halictid bees. V, Choralictus. Insectes Soc 5:473–505

    Article  Google Scholar 

  • Michener CD, Wille A (1961) The bionomics of a primitively social bee, Lasioglossum inconspicuum. Univ Kansas Sci Bull 42:1123–1202

    Google Scholar 

  • Mueller UG (1991) Haplodiploidy and the evolution of facultative sex ratios in a primitively eusocial bee. Science 254:442–444

    Article  PubMed  CAS  Google Scholar 

  • Mueller UG (1996) Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J Kansas Entomol Soc 69:116–138

    Google Scholar 

  • Mueller UG, Eickwort GC, Aquadrot CF (1994) DNA figerprinting analysis of parent-offspring conflict in a bee. Proc Natl Acad Sci USA 91:5143–5147

    Article  PubMed  CAS  Google Scholar 

  • Pabalan N, Davey KG, Packer L (2000) Escalation of aggressive interactions during staged encounters in Halictus ligatus Say (Hymenoptera: Halictidae), with a comparison of circle tube behaviors with other halictine species’. J Insect Behav 13:627–650

    Article  Google Scholar 

  • Packer L (1992) The social organisation of Lasioglossum (Dialictus) laevissimum (Smith) in southern Alberta. Can J Zool 70:1767–1774

    Article  Google Scholar 

  • Packer L, Gravel AD, Lebuhn G (2007) Phenology and social organization of Halictus (Seladonia) tripartitus (Hymenoptera: Halictidae). J Hymenopt Res 16:281–292

    Google Scholar 

  • Packer L, Jessome V, Lockerbie C, Sampson B (1989) The phenology and social biology of four sweat bees in a marginal environment: Cape Breton Island. Can J Zool 67:2871–2877

    Article  Google Scholar 

  • Packer L, Knerer G (1985) Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera; Halictidae). Behav Ecol Sociobiol 17:143–149

    Google Scholar 

  • Packer L, Owen RE (1994) Relatedness and sex ratio in a primitively eusocial halictine bee. Behav Ecol Sociobiol 34:1–10

    Article  Google Scholar 

  • Paxton RJ, Ayasse M, Field J, Soro A (2002) Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites. Mol Ecol 11:2405–2416

    Article  PubMed  CAS  Google Scholar 

  • Ratnieks FLW, Helantera H (2009) The evolution of extreme altruism and inequality in insect societies. Philos Trans R Soc B 364:3169–3179

    Article  Google Scholar 

  • Rehan SM, Rotella A, Onuferko TM, Richards MH (2013) Colony disturbance and solitary nest initiation by workers in the obligately eusocial sweat bee, Halictus ligatus. Insectes Soc 60:389–392

    Article  Google Scholar 

  • Richards MH (2000) Evidence for geographic variation in colony social organization in an obligately social sweat bee, Lasioglossum malachurum Kirby (Hymenoptera; Halictidae). Can J Zool 78:1259–1266

    Article  Google Scholar 

  • Richards MH (2001) Nesting biology and social organization of Halictus sexcinctus (Fabricius) in southern Greece. Can J Zool 79:2210–2220

    Article  Google Scholar 

  • Richards MH (2003) Variable worker behaviour in the weakly eusocial sweat bee. Halictus sexcinctus Fabricius Insectes Soc 50:361–364

    Article  Google Scholar 

  • Richards MH (2004) Annual and social variation in foraging effort of the obligately eusocial sweat bee, Halictus ligatus (Hymenoptera: Halictidae). J Kansas Entomol Soc 77:484–502. https://doi.org/10.2317/E37.1

    Article  Google Scholar 

  • Richards MH, French D, Paxton RJ (2005) It’s good to be queen: classically eusocial colony structure and low worker fitness in an obligately social sweat bee. Mol Ecol 14:4123–4133

    Article  PubMed  Google Scholar 

  • Richards MH, Onuferko TM, Rehan SM (2015) Phenological, but not social, variation associated with climate differences in a eusocial sweat bee, Halictus ligatus, nesting in southern Ontario. J Hymenopt Res 43:19–44

    Article  Google Scholar 

  • Richards MH, Packer L (1994) Trophic aspects of caste determination in Halictus ligatus, a primitively eusocial sweat bee. Behav Ecol Sociobiol 34:385–391

    Article  Google Scholar 

  • Richards MH, Packer L (1995) Annual variation in survival and reproduction of the primitively eusocial sweat bee Halictus ligatus (Hymenoptera: Halictidae. Can J Zool 73:933–941

    Article  Google Scholar 

  • Richards MH, Packer L (1996) The socioecology of body size variation in the primitively eusocial sweat bee, Halictus ligatus (Hymenoptera: Halictidae). Oikos 77:68–76

    Article  Google Scholar 

  • Richards MH, Packer L, Seger J (1995) Unexpected patterns of parentage and relatedness in a primitively eusocial bee. Nature 373:239–241

    Article  CAS  Google Scholar 

  • Richards MH, Vickruck JL, Rehan SM (2010) Colony social organisation of Halictus confusus in southern Ontario, with comments on sociality in the subgenus H. (Seladonia). J Hymenopt Res 19:144–158

    Google Scholar 

  • Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu Rev Entomol 52:127–150

    Article  PubMed  CAS  Google Scholar 

  • Smith AR, Kapheim KM, O’Donnell S, Wcislo WT (2009) Social competition but not subfertility leads to a division of labour in the facultatively social sweat bee Megalopta genalis (Hymenoptera: Halictidae). Anim Behav 78:1043–1050

    Article  Google Scholar 

  • Soro A, Ayasse M, Zobel MU, Paxton RJ (2009) Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum. Insectes Soc 56:55–63

    Article  Google Scholar 

  • Strohm E, Bordon-Hauser A (2003) Advantages and disadvantages of large colony size in a halictid bee: the queen’s perspective. Behav Ecol 14:546–553

    Article  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263

    Article  PubMed  CAS  Google Scholar 

  • Wade MJ (2001) Maternal effect genes and the evolution of sociality in haplo-diploid organisms. Evolution 55:453–458

    Article  PubMed  CAS  Google Scholar 

  • Wcislo WT, Wille A, Orozco E (1993) Nesting biology of tropical solitary and social sweat bees, Lasioglossum (Dialictus) figueresi Wcislo and L. (D.) aeneiventre (Friese) (Hymenoptera: Halictidae). Ins Soc 40(1):21–40

    Article  Google Scholar 

  • Wenseleers T, Hart AG, Ratnieks FLW (2004) When resistance is useless: policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:6

    Article  Google Scholar 

  • Wille A, Orozoco E (1970) The life cycle and behavior of the social bee Lasioglossum (Dialictus) umbripenne. Rev Biol Trop (San Jose, Costa Rica) 17: 199–245

    Google Scholar 

  • Wyman LM, Richards MH (2003) Colony social organization of Lasioglossum malachurum Kirby (Hymenoptera, Halictidae) in southern Greece. Insectes Soc 50:201–211

    Article  Google Scholar 

  • Yanega D (1989) Caste determination and differential diapause within the first brood of Halictus rubicundus in New York (Hymenoptera: Halictidae). Behav Ecol Sociobiol 24:97–107

    Article  Google Scholar 

  • Yanega D (1990) Philopatry and nest founding in a primitively social bee, Halictus rubicundus. Behav Ecol Sociobiol 27:37–42

    Article  Google Scholar 

Download references

Acknowledgements

We thank David Clark, the Brock University gardener who originally found the nesting aggregation and whose gardening expertise keeps it thriving. We also thank Jess Vickruck, Lyndon Duff, and two anonymous reviewers for helpful comments on the manuscript. This project was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to MHR and a NSERC Postgraduate scholarship to DNA.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Brock University, 1812 Sir Isaac Brock Way, St. Catharines, ON, L2S 3A1, Canada

    D. N. Awde & M. H. Richards

Authors
  1. D. N. Awde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. H. Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. N. Awde.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 54 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Awde, D.N., Richards, M.H. Investigating queen influence on worker behaviour using comparisons of queenless and queenright workers. Insect. Soc. 65, 367–379 (2018). https://doi.org/10.1007/s00040-018-0619-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-018-0619-6

Keywords

Search

Navigation