Insectes Sociaux

, Volume 65, Issue 2, pp 289–295 | Cite as

Different reproductive strategies and their possible relation to inbreeding risk in the bumble bee Bombus terrestris

  • Gherardo Bogo
  • Natasha de Manincor
  • Alessandro Fisogni
  • Marta Galloni
  • Laura Zavatta
  • Laura Bortolotti
Research Article


In many species, inbreeding avoidance mechanisms prevent mating between close relatives, but these mechanisms are poorly studied in bumble bees. The probability of inbred matings within a colony in eusocial insects may depend on the timing of gyne and male emergence and on their sex ratio. In this study, we compared the development of 35 colonies of the bumble bee Bombus terrestris from founding to the emergence of the last gyne, and we investigated the probability of inbred mating in colonies with fertile newborn gynes and males. We calculated a novel colony inbreeding risk index (IRI), which considers the overlap period between fertile gynes and males, their numbers, and the colony sex ratio. We found that the IRI values were strictly correlated with the time elapsed between the gyne point and the switch point (i.e., from the moment of deposition of the first diploid egg that produces a gyne to the first haploid egg). We separated the colonies into two groups based on the mean value of the IRI: colonies with low IRI produced more gynes (93.8 ± 9.4), for a longer period (32.1 ± 1.8 days) and with a lower percentage of overlapped gynes (69 ± 5%) than colonies with high IRI (57.1 ± 21 gynes, 23.3 ± 2.9 days, and 100% overlapped gynes, respectively). A low IRI is connected to a reduced risk of inbred mating, while colonies with a high IRI may be advantaged in conditions of isolation, in case of the absence of non-related reproducers. Inbreeding risk index proved to be a good indicator of the colony reproductive strategy.


Bombus terrestris Fertility overlap Gyne point Inbreeding risk Colony development Switch point. 



This work was performed within the Life + Project PP-ICON (Plant-Pollinator CONservation approach: a demonstrative proposal—LIFE09/NAT/IT000212), funded by the European Union.


  1. Alaux C, Jaisson P, Hefetz A (2004a) Queen influence on worker reproduction in bumblebees (Bombus terrestris) colonies. Insect Soc 51:287–293CrossRefGoogle Scholar
  2. Alaux C, Savarit F, Jaisson P, Hefetz A (2004b) Does the queen win it all ? Queen-worker conflict over male production in the bumblebee, Bombus terrestris. Naturwissenschaften 91:400–403CrossRefPubMedGoogle Scholar
  3. Alford DV (1975) Bumblebees. Davis-Poynter, LondonGoogle Scholar
  4. Ayabe T, Hoshiba H, Ono M (2004) Cytological evidence for triploid males and females in the bumblebee, Bombus terrestris. Chromosome Res 12(3):215–223CrossRefPubMedGoogle Scholar
  5. Baer B (2003) Bumblebees as model organisms to study male sexual selection in social insects. Behav Ecol Sociobiol 54(6):521–533. CrossRefGoogle Scholar
  6. Beekman M, van Stratum P (1998) Bumblebee sex ratios: why do bumblebees produce so many males? Proc R Soc Lond B Biol Sci 265(1405):1535–1543. CrossRefGoogle Scholar
  7. Beekman M, Van Stratum P, Veerman A (1999) Selection for non-diapause in the bumblebee Bombus terrestris, with notes on the effect of inbreeding. Entomol Exp Appl 93:69–75. CrossRefGoogle Scholar
  8. Bogo G, de Manincor N, Fisogni A, Galloni M, Bortolotti L (2017) Effects of queen mating status, pre-diapause weight and pupae’s sex on colony initiation in small-scale rearing of Bombus terrestris. Apidologie 48:845–854. CrossRefGoogle Scholar
  9. Bourke AFG (1997) Sex ratios in bumblebees. Phil Trans R Soc Lond B 352:1921–1933CrossRefGoogle Scholar
  10. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Gen 10(11):783–796. CrossRefGoogle Scholar
  11. Cnaani J, Robinson GE, Hefetz A (2000) The critical period for caste determination in Bombus terrestris and its juvenile hormone correlates. J Comp Physiol A 186(11):1089–1094. CrossRefPubMedGoogle Scholar
  12. Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behav 107(3–4):186–207. CrossRefGoogle Scholar
  13. Duchateau MJ, Velthuis HHW (1989) Ovarian development and egg laying in workers of Bombus terrestris. Entomol Exp Appl 51(3):199–213. CrossRefGoogle Scholar
  14. Duchateau MJ, Hoshiba H, Velthuis HH (1994) Diploid males in the bumble bee Bombus terrestris. Entomol Exp Appl 71(3):263–269. CrossRefGoogle Scholar
  15. Duchateau MJ, Velthuis HHW, Boomsma JJ (2004) Sex ratio variation in the bumblebee Bombus terrestris. Behav Ecol 15(1):71–82. CrossRefGoogle Scholar
  16. Foster RL (1992) Nestmate recognition as an inbreeding avoidance mechanism in bumble bees (Hymenoptera: Apidae). J Kans Entomol Soc 65:238–243Google Scholar
  17. Gerloff CU, Ottmer BK, Schmid-Hempel P (2003) Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Funct Ecol 17:582–589. CrossRefGoogle Scholar
  18. Gerloff CU, Schmid-Hempel P (2005) Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111(1):67–80. CrossRefGoogle Scholar
  19. Gosterit A (2011) Effect of different reproductive strategies on colony development characteristics in Bombus terrestris. J Apic Sci 55(2):45–51Google Scholar
  20. Gosterit A (2016) Adverse effect of inbreeding on colony foundation success in bumblebee, Bombus terrestris (Hymenoptera: Apidae). Appl Entomol Zool 51:521–526CrossRefGoogle Scholar
  21. Goulson D (2010) Bumblebees: behaviour, ecology and conservation, 2nd edn. Oxford University Press, New York, p. 336Google Scholar
  22. Imhoof B, Schmid-Hempel P (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Soc 46(3):233–238. CrossRefGoogle Scholar
  23. Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467–475. CrossRefPubMedGoogle Scholar
  24. Rasmont P, Coppée A, Michez D, De Meulemeester T (2008) An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Ann Soc Entomol Fr 44(2):243–250. CrossRefGoogle Scholar
  25. Schmid-Hempel R, Schmid-Hempel P (2000) Female mating frequencies in Bombus spp. from Central Europe Insectes Soc 47(1):36–41. Google Scholar
  26. Tabadkani SM, Nozari J, Lihoreau M (2012) Inbreeding and the evolution of sociality in arthropods. Naturwissenschaften 99(10):779–788. CrossRefPubMedGoogle Scholar
  27. Tasei JN, Moinard C, Moreau L, Himpens B, Guyonnaud S (1998) Relationship between aging, mating and sperm production in captive Bombus terrestris. J Apic Res 37(2):107–113. CrossRefGoogle Scholar
  28. Van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design. Front Zool. PubMedPubMedCentralGoogle Scholar
  29. Whitehorn PR, Tinsley MC, Goulson D (2009) Kin recognition and inbreeding reluctance in bumblebees. Apidologie 40(6):627–633. CrossRefGoogle Scholar
  30. Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336(6079):351–352. CrossRefPubMedGoogle Scholar
  31. Wolf S, Toev T, Moritz RLV, Moritz RFA (2012) Spatial and temporal dynamics of the male effective population size in bumblebees (Hymenoptera: Apidae). Popul Ecol 54(1):115–124. CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Consiglio per la ricerca in agricoltura e l’analisi dell’economia agrariaCentro di ricerca agricoltura e ambienteBolognaItaly
  2. 2.Dipartimento di Scienze Biologiche, Geologiche e AmbientaliUniversità di BolognaBolognaItaly
  3. 3.UMR 8198-Evo-Eco-PaléoUniversité de Lille, CNRSLilleFrance

Personalised recommendations