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.
Similar content being viewed by others
References
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
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
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
Craig R (1983) Subfertility and the evolution of eusociality selection by kin. J Theor Biol 100:379–397
Cronin AL, Field J (2007) Social aggression in an age-dependent dominance hierarchy. Behaviour 144:753–765
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
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
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
Fletcher D, Blum MS (1981) Pheromonal control of dealation and oogenesis in virgin queen fire ants. Science 212:73–76
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
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
Gerling D, Hermann HR (1978) Biology and mating behavior of Xylocopa virginica L. (Hymenoptera, Anthophoridae). Behav Ecol Sociobiol 3:99–111
Gerling D, Velthuis HHW, Hefetz A (1989) Bionimics of the large carpenter bees of the genus Xylocopa. Annu Rev Entomol 34:163–190
Hogendoorn K (1996) Socio-economics of brood destruction during supersedure in the carpenter bee Xylocopa pubescens. J Evol Biol 9:931–952
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
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
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
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
Keller L, Nonacs P (1993) The role of Queen pheromones in social insects- queen control of queen signal. Anim Behav 45:787–794
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
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
Michener CD (1974) The Social Behavior of the Bees. Harvard University Press, Cambridge
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
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
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
Packer C, Pusey AE (2008) Adaptations of female lions to infanticide by incoming males. Am Nat 121:716–728
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
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
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
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
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
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
Rozen JG Jr (1990) Pupa of the bee Pararhophites orobinus (Hymenoptera: Apoidea : Megachilidae). J N Y Entomol Soc 98:379–382
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
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
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
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
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
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
Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58:17–25. https://doi.org/10.1641/B580106
Yanega D (1988) Social plasticity and early-diapausing females in a primitively social bee. Proc Natl Acad Sci 85:4374–4377
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
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
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00040-018-0653-4