Linear dominance hierarchies and conditional reproductive strategies in a facultatively social carpenter bee

Abstract

In social groups, dominance rank may have important fitness consequences, as higher ranking individuals tend to have higher overall fitness. In social nests of the eastern carpenter bee, Xylocopa virginica, females in social nests demonstrate a complete division of labour where one female is the dominant egg layer and forager while other females in the nest are non-reproductive. We investigated the nature of reproductive queues in this species by performing removal experiments across 3 years to observe how females respond to new reproductive opportunities in the nest. When a primary female was removed, a secondary female always assumed her position as replacement primary and reproductive queues formed in a linear fashion. A third type of female in the nest, the tertiary female, did not become reproductive, even if she was the only female remaining. In delaying reproduction, tertiary females were able to overwinter a second time and were often successful at becoming reproductive in their second summer. Tertiary females were smaller than primary or secondary females, had higher fat stores and lower ovarian development. When all other females in the nest were removed, tertiary females were observed ejecting the offspring of previous dominant females in the nest. Tertiary females appear to represent a novel reproductive strategy among the Hymenoptera who can drastically alter their physiology and behaviour, essentially doubling their life span to maximize reproductive potential.

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

Fig. 1
Fig. 2

References

  1. Bang A, Gadagkar R (2012) Reproductive queue without overt conflict in the primitively eusocial wasp Ropalidia marginata. Proc Natl Acad Sci U S A 109:14494–14499. https://doi.org/10.1073/pnas.1212698109

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bridge C, Field J (2007) Queuing for dominance: gerontocracy and queue-jumping in the hover wasp Liostenogaster flavolineata. Behav Ecol Sociobiol 61:1253–1259. https://doi.org/10.1007/s00265-007-0355-9

    Article  Google Scholar 

  3. Cant MA, Llop JB, Field J (2006) Individual variation in social aggression and the probability of inheritance: theory and a field test. Am Nat 167:837–852. https://doi.org/10.1086/503445

    Article  PubMed  Google Scholar 

  4. Craig R (1983) Subfertility and the evolution of eusociality selection by kin. J Theor Biol 100:379–397

    Article  Google Scholar 

  5. Cronin AL, Field J (2007) Social aggression in an age-dependent dominance hierarchy. Behaviour 144:753–765

    Article  Google Scholar 

  6. Danforth BN (1999) Emergence dynamics and bet hedging in a desert bee, Perdita portalis. Proc R Soc B Biol Sci 266:1985–1994. https://doi.org/10.1098/rspb.1999.0876

    Article  Google Scholar 

  7. Field J, Foster W (1999) Helping behaviour in facultatively eusocial hover wasps: an experimental test of the subfertility hypothesis. Anim Behav 57:633–636. https://doi.org/10.1006/anbe.1999.0995

    CAS  Article  PubMed  Google Scholar 

  8. Field J, Foster W, Shreeves G, Sumner S (1998) Ecological constraints on independent nesting in facultatively eusocial hover wasps. Proc R Soc B Biol Sci 265:973–977

    Article  Google Scholar 

  9. Fletcher D, Blum MS (1981) Pheromonal control of dealation and oogenesis in virgin queen fire ants. Science 212:73–76

    CAS  Article  Google Scholar 

  10. Gadagkar R (1990) Evolution of eusociality: the advantage of assured fitness returns. Philos Trans R Soc B Biol Sci 329:17–25. https://doi.org/10.1098/rsta.1892.0001

    Article  Google Scholar 

  11. Gadagkar R (2016) Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection? Philos Trans R Soc B Biol Sci 371:20150094

    Article  Google Scholar 

  12. Gerling D, Hermann HR (1978) Biology and mating behavior of Xylocopa virginica L. (Hymenoptera, Anthophoridae). Behav Ecol Sociobiol 3:99–111

    Article  Google Scholar 

  13. Gerling D, Velthuis HHW, Hefetz A (1989) Bionimics of the large carpenter bees of the genus Xylocopa. Annu Rev Entomol 34:163–190

    Article  Google Scholar 

  14. Hogendoorn K (1996) Socio-economics of brood destruction during supersedure in the carpenter bee Xylocopa pubescens. J Evol Biol 9:931–952

    Article  Google Scholar 

  15. Hogendoorn K, Leys R (1993) The superseded female’s dilemma: ultimate and proximate factors that influence guarding behaviour of the carpenter bee Xylocopa pubescens. Behav Ecol Sociobiol 33:371–381

    Article  Google Scholar 

  16. Hogendoorn K, Velthuis HHW (1999) Task allocation and reproductive skew in social mass provisioning carpenter bees in relation to age and size. Insectes Soc 46:198–207

    Article  Google Scholar 

  17. Houston TF (1991) Ecology and behaviour of the bee Amegilla dawsoni (Rayment) with notes on a related species (Hymenoptera: Anthophoridae). Rec West Aust Museum 15:535–553

    Google Scholar 

  18. Ishikawa Y, Yamada YY, Matsuura M et al (2010) Dominance hierarchy among workers changes with colony development in Polistes japonicus (Hymenoptera, Vespidae) paper wasp colonies with a small number of workers. Insectes Soc 57:465–475. https://doi.org/10.1007/s00040-010-0106-1

    Article  Google Scholar 

  19. Keller L, Nonacs P (1993) The role of Queen pheromones in social insects- queen control of queen signal. Anim Behav 45:787–794

    Article  Google Scholar 

  20. Leadbeater E, Carruthers JM, Green JP et al (2011) Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science 333:874–876. https://doi.org/10.1126/science.1205140

    CAS  Article  PubMed  Google Scholar 

  21. Lucas ER, Martins RP, Field J (2011) Reproductive skew is highly variable and correlated with genetic relatedness in a social apoid wasp. Behav Ecol 22:337–344. https://doi.org/10.1093/beheco/arq214

    Article  Google Scholar 

  22. Michener CD (1974) The Social Behavior of the Bees. Harvard University Press, Cambridge

    Google Scholar 

  23. Michener CD, Brothers DJ (1974) Were workers of eusocial hymenoptera initially altruistic or oppressed? Proc Natl Acad Sci 71:671–674. https://doi.org/10.1073/pnas.71.3.671

    CAS  Article  PubMed  Google Scholar 

  24. Mueller UG (2018) Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae). J Kansas Entomol Soc 69(4):116–138

    Google Scholar 

  25. 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 

  26. Packer C, Pusey AE (2008) Adaptations of female lions to infanticide by incoming males. Am Nat 121:716–728

    Article  Google Scholar 

  27. Peso M, Richards MH (2011) Not all who wander are lost: nest fidelity in Xylocopa virginica examined by mark recapture. Insectes Soc 58:127–133. https://doi.org/10.1007/s00040-010-0125-y

    Article  Google Scholar 

  28. Quinn JS, Samuelsen A, Barclay M et al (2010) Circumstantial evidence for infanticide of chicks of the communal smooth-billed Ani (Crotophaga ani). Wilson J Ornithol 122:369–374. https://doi.org/10.1676/09-119.1

    Article  Google Scholar 

  29. Reeve HK, Peters JM, Nonacs P, Starks PT (1998) Dispersal of first “workers” in social wasps: causes and implications of an alternative reproductive strategy. Proc Natl Acad Sci 95:13737–13742

    CAS  Article  Google Scholar 

  30. Richards MH (2003) Variable worker behaviour in the weakly eusocial sweat bee, Halictus sexcinctus Fabricius. Insectes Soc 50:361–364. https://doi.org/10.1007/s00040-003-0691-3

    Article  Google Scholar 

  31. Richards MH (2011) Colony social organisation and alternative social strategies in the eastern carpenter bee, Xylocopa virginica. J Insect Behav 24:399–411. https://doi.org/10.1007/s10905-011-9265-9

    Article  Google Scholar 

  32. Richards MH, Course C (2015) Ergonomic skew and reproductive queuing based on social and seasonal variation in foraging activity of eastern carpenter bees (Xylocopa virginica). Can J Zool 625:615–625

    Article  Google Scholar 

  33. Rozen JG Jr (1990) Pupa of the bee Pararhophites orobinus (Hymenoptera: Apoidea : Megachilidae). J N Y Entomol Soc 98:379–382

    Google Scholar 

  34. Schmaltz G, Quinn JS, Lentz C (2008) Competition and waste in the communally breeding smooth-billed ani: effects of group size on egg-laying behaviour. Anim Behav 76:153–162. https://doi.org/10.1016/j.anbehav.2007.12.018

    Article  Google Scholar 

  35. 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. https://doi.org/10.1016/j.anbehav.2009.06.032

    Article  Google Scholar 

  36. Smith AR, Wcislo WT, O’Donnell S (2003) Assured fitness returns favor sociality in a mass-provisioning sweat bee, Megalopta genalis (Hymenoptera: Halictidae). Behav Ecol Sociobiol 54:14–21. https://doi.org/10.1007/s00265-003-0589-0

    Article  Google Scholar 

  37. Stark RE (1992) Cooperative nesting in the multivoltine large carpenter bee Xylocopa sulcatipes Maa (Apoidea: Anthophoridae): Do helpers gain or lose to solitary females? Ethology 91:301–310

    Article  Google Scholar 

  38. van der Blom J, Velthuis HHW (1988) Social behaviour of the carpenter bee Xylocopa pubescens. Ethology 79:281–294. https://doi.org/10.1017/CBO9780511781360

    Article  Google Scholar 

  39. Vickruck JL, Richards MH (2017) Nestmate discrimination based on familiarity but not relatedness in eastern carpenter bees. Behav Processes 145:73–80. https://doi.org/10.1016/j.beproc.2017.10.005

    CAS  Article  PubMed  Google Scholar 

  40. Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58:17–25. https://doi.org/10.1641/B580106

    Article  Google Scholar 

  41. Yanega D (1988) Social plasticity and early-diapausing females in a primitively social bee. Proc Natl Acad Sci 85:4374–4377

    CAS  Article  Google Scholar 

  42. Zanette L, Field J (2009) Cues, concessions, and inheritance: dominance hierarchies in the paper wasp Polistes dominulus. Behav Ecol 20:773–780. https://doi.org/10.1093/beheco/arp060

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Jessi deHaan, Andrew Giroux and Konrad Karolak for fieldwork assistance as well as the Niagara Region Waste Management Division for supporting research at the Glenridge Quarry Naturalization Site. This research was supported by a National Science and Engineering Research Council (NSERC) postgraduate scholarship and an Ontario Graduate Scholarship to JLV and an NSERC Discovery grant to MHR.

Author information

Affiliations

Authors

Corresponding author

Correspondence to J. L. Vickruck.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 213 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vickruck, J.L., Richards, M.H. Linear dominance hierarchies and conditional reproductive strategies in a facultatively social carpenter bee. Insect. Soc. 65, 619–629 (2018). https://doi.org/10.1007/s00040-018-0653-4

Download citation

Keywords

  • Behavioural plasticity
  • Delayed reproduction
  • Reproductive queue
  • Xylocopa virginica