Reproductive conflict in bumblebees and the evolution of worker policing

Evolution

Volumn 66, Issue 12, 2012, Pages 3765-3777

  Zanette, Lorenzo R S ^a,b   Miller, Sophie D L ^a   Faria, Christiana M A ^a   Almond, Edd J ^a   Huggins, Tim J ^a   Jordan, William C ^c   Bourke, Andrew F G ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c INSTITUTE OF ZOOLOGY   (United Kingdom)

Author keywords

Bombus terrestris; Inclusive fitness theory; Kin selection; Social insect; Worker reproduction

Indexed keywords

MICROSATELLITE DNA;

BEE; EGG PRODUCTION; EVOLUTION; GENOTYPE; RELATEDNESS; REPRODUCTIVE BEHAVIOR; SPECIES DIVERSITY; WORKER POLICING;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ASSOCIATION; BEE; CHEMISTRY; FEMALE; GENETICS; LARVA; MALE; OOCYTE; OVIPARITY; PHYSIOLOGY; REPRODUCTION; SEX RATIO;

ANIMALS; BEES; BEHAVIOR, ANIMAL; CUES; FEMALE; LARVA; MALE; MICROSATELLITE REPEATS; OVIPARITY; OVUM; REPRODUCTION; SEX RATIO;

APIS MELLIFERA; BOMBUS TERRESTRIS; HEXAPODA; HYMENOPTERA;

EID: 84870496263     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01709.x     Document Type: Article

References (72)

1. Alaux, C., F. Savarit, P. Jaisson, and A. Hefetz. 2004. Does the queen win it all? Queen-worker conflict over male production in the bumblebee, Bombus terrestris. Naturwissenschaften 91:400-403.
2. Alaux, C., P. Jaisson, and A. Hefetz. 2006. Regulation of worker reproduction in bumblebees (Bombus terrestris): workers eavesdrop on a queen signal. Behav. Ecol. Sociobiol. 60:439-446.
3. Alford, D. V. 1975. Bumblebees. Davis-Poynter, London.
4. Amsalem, E., and A. Hefetz. 2011. The effect of group size on the interplay between dominance and reproduction in Bombus terrestris. PLoS One 6:e18238.
5. Amsalem, E., R. Twele, W. Francke, and A. Hefetz. 2009. Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc. R. Soc. B 276:1295-1304.
6. Ayasse, M., J. Birnbaum, J. Tengö, A. Van Doorn, T. Taghizadeh, and W. Francke. 1999. Caste- and colony-specific chemical signals on eggs of the bumble bee, Bombus terrestris L. (Hymenoptera: Apidae). Chemoecology 9:119-126.
7. Baer, B., and P. Schmid-Hempel. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151-154.
8. Beekman, M., and B. P. Oldroyd. 2005. Honeybee workers use cues other than egg viability for policing. Biol. Lett. 1:129-132.
9. Beekman, M., and B. P. Oldroyd. 2008. When workers disunite: intraspecific parasitism by eusocial bees. Annu. Rev. Entomol. 53:19-37.
10. Bloch, G., and A. Hefetz. 1999a. Reevaluation of the role of mandibular glands in regulation of reproduction in bumblebee colonies. J. Chem. Ecol. 25:881-896.
11. Bloch, G., and A. Hefetz. 1999b. Regulation of reproduction by dominant workers in bumblebee (Bombus terrestris) queenright colonies. Behav. Ecol. Sociobiol. 45:125-135.
12. Bonckaert, W., K. Vuerinckx, J. Billen, R. L. Hammond, L. Keller, and T. Wenseleers. 2008. Worker policing in the German wasp Vespula germanica. Behav. Ecol. 19:272-278.
13. Bonckaert, W., A. Tofilski, F. S. Nascimento, J. Billen, F. L. W. Ratnieks, and T. Wenseleers. 2011. Co-occurrence of three types of egg policing in the Norwegian wasp Dolichovespula norwegica. Behav. Ecol. Sociobiol. 65:633-640.
14. Bourke, A. F. G. 1994. Worker matricide in social bees and wasps. J. Theor. Biol. 167:283-292.
15. Bourke, A. F. G. 2011. Principles of social evolution. Oxford Univ. Press, Oxford, U.K.
16. Bourke, A. F. G., and N. R. Franks. 1995. Social evolution in ants. Princeton Univ. Press, Princeton, NJ.
17. Bourke, A. F. G., and F. L. W. Ratnieks. 2001. Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae). Proc. R. Soc. Lond. B 268:347-355.
18. Brown, M. J. F., R. Schmid-Hempel, and P. Schmid-Hempel. 2003. Queen-controlled sex ratios and worker reproduction in the bumble bee Bombus hypnorum, as revealed by microsatellites. Mol. Ecol. 12:1599-1605.
19. Brunner, E., and J. Heinze. 2009. Worker dominance and policing in the ant Temnothorax unifasciatus. Insectes Soc. 56:397-404.
20. Cameron, S. A., H. M. Hines, and P. H. Williams. 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linn. Soc. 91:161-188.
21. Cardinal, S., and B. N. Danforth. 2011. The antiquity and evolutionary history of social behavior in bees. PLoS One 6:e21086.
22. Crozier, R. H., and P. Pamilo. 1996. Evolution of social insect colonies: sex allocation and kin selection. Oxford Univ. Press, Oxford, U.K.
23. Duchateau, M. J. 1989. Agonistic behaviors in colonies of the bumblebee Bombus terrestris. J. Ethol. 7:141-151.
24. Duchateau, M. J., and H. H. W. Velthuis. 1988. Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107:186-207.
25. Duchateau, M. J., and H. H. W. Velthuis. 1989. Ovarian development and egg laying in workers of Bombus terrestris. Entomol. Exp. Appl. 51:199-213.
26. Duchateau, M. J., H. H. W. Velthuis, and J. J. Boomsma. 2004. Sex ratio variation in the bumblebee Bombus terrestris. Behav. Ecol. 15:71-82.
27. Endler, A., J. Liebig, T. Schmitt, J. E. Parker, G. R. Jones, P. Schreier, and B. Hölldobler. 2004. Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc. Natl. Acad. Sci. USA 101:2945-2950.
28. Endler, A., J. Liebig, and B. Holldobler. 2006. Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav. Ecol. Sociobiol. 59:490-499.
29. Estoup, A., M. Solignac, M. Harry, and J.-M. Cornuet. 1993. Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nucl. Acids Res. 21:1427-1431.
30. Foster, K. R., F. L. W. Ratnieks, N. Gyllenstrand, and P. A. Thorén. 2001. Colony kin structure and male production in Dolichovespula wasps. Mol. Ecol. 10:1003-1010.
31. Frank, S. A. 2003. Repression of competition and the evolution of cooperation. Evolution 57:693-705.
32. Hartmann, A., J. Wantia, J. A. Torres, and J. Heinze. 2003. Worker policing without genetic conflicts in a clonal ant. Proc. Natl. Acad. Sci. USA 100:12836-12840.
33. Hughes, W. O. H., B. P. Oldroyd, M. Beekman, and F. L. W. Ratnieks. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213-1216.
34. Huth-Schwarz, A., A. León, R. Vandame, R. F. A. Moritz, and F. B. Kraus. 2011. Workers dominate male production in the neotropical bumblebee Bombus wilmattae (Hymenoptera: Apidae). Front. Zool. 8:13. doi:10.1186/1742-9994-8-13.
35. Kikuta, N., and K. Tsuji. 1999. Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav. Ecol. Sociobiol. 46:180-189.
36. Lopez-Vaamonde, C., J. W. Koning, W. C. Jordan, and A. F. G. Bourke. 2003. No evidence that reproductive bumblebee workers reduce the production of new queens. Anim. Behav. 66:577-584.
37. Lopez-Vaamonde, C., J. W. Koning, R. M. Brown, W. C. Jordan, and A. F. G. Bourke. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557-560.
38. Lopez-Vaamonde, C., N. E. Raine, J. W. Koning, R. M. Brown, J. J. M. Pereboom, T. C. Ings, O. Ramos-Rodriguez, W. C. Jordan, and A. F. G. Bourke. 2009. Lifetime reproductive success and longevity of queens in an annual social insect. J. Evol. Biol. 22:983-996.
39. Marshall, T. C., J. Slate, L. E. B. Kruuk, and J. M. Pemberton. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7:639-655.
40. Nanork, P., J. Paar, N. C. Chapman, S. Wongsiri, and B. P. Oldroyd. 2005. Asian honeybees parasitize the future dead. Nature 437:829.
41. Nanork, P., S. Wongsiri, and B. P. Oldroyd. 2007. Preservation and loss of the honey bee (Apis) egg-marking pheromone signal across evolutionary time. Behav. Ecol. Sociobiol. 61:1509-1514.
42. Ohtsuki, H., and K. Tsuji. 2009. Adaptive reproduction schedule as a cause of worker policing in social Hymenoptera: a dynamic game analysis. Am. Nat. 173:747-758.
43. Oldroyd, B. P., L. A. Halling, G. Good, W. Wattanachaiyingcharoen, A. B. Barron, P. Nanork, S. Wongsiri, and F. L. W. Ratnieks. 2001. Worker policing and worker reproduction in Apis cerana. Behav. Ecol. Sociobiol. 50:371-377.
44. Paxton, R. J., P. A. Thorén, A. Estoup, and J. Tengö. 2001. Queen-worker conflict over male production and the sex ratio in a facultatively polyandrous bumblebee, Bombus hypnorum: the consequences of nest usurpation. Mol. Ecol. 10:2489-2498.
45. Payne, C. M., T. M. Laverty, and M. A. Lachance. 2003. The frequency of multiple paternity in bumble bee (Bombus) colonies based on microsatellite DNA at the B10 locus. Insectes Soc. 50:375-378.
46. Peeters, C., and J. Liebig. 2009. Fertility signaling as a general mechanism regulating reproductive division of labor in ants. Pp. 220-242 in J. Gadau and J. Fewell, eds. Organization of insect societies: from genome to sociocomplexity. Harvard Univ. Press, Cambridge, MA.
47. Pirk, C. W. W., P. Neumann, and F. L. W. Ratnieks. 2003. Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav. Ecol. 14:347-352.
48. Pirk, C. W. W., P. Neumann, and H. R. Hepburn. 2007. Nestmate recognition for eggs in the honeybee (Apis mellifera L.). Behav. Ecol. Sociobiol. 61:1685-1693.
49. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
50. Ratnieks, F. L. W. 1988. Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am. Nat. 132:217-236.
51. Ratnieks, F. L. W., and P. K. Visscher. 1989. Worker policing in the honeybee. Nature 342:796-797.
52. Ratnieks, F. L. W., and T. Wenseleers. 2008. Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol. Evol. 23:45-52.
53. Rousset, F. 2008. GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Res. 8:103-106.
54. Saigo, T., and K. Tsuchida. 2004. Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc. R. Soc. Lond. B 271:S509-S512.
55. Sauter, A., M. J. F. Brown, B. Baer, and P. Schmid-Hempel. 2001. Males of social insects can prevent queens from multiple mating. Proc. R. Soc. Lond. B 268:1449-1454.
56. Schmid-Hempel, R., and P. Schmid-Hempel. 2000. Female mating frequencies in Bombus spp. from Central Europe. Insectes Soc. 47:36-41.
57. Sramkova, A., C. Schulz, R. Twele, W. Francke, and M. Ayasse. 2008. Fertility signals in the bumblebee Bombus terrestris (Hymenoptera: Apidae). Naturwissenschaften 95:515-522.
58. Starr, C. K. 1984. Sperm competition, kinship, and sociality in the Aculeate Hymenoptera. Pp. 427-464 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, Orlando, FL.
59. Stroeymeyt, N., E. Brunner, and J. Heinze. 2007. "Selfish worker policing" controls reproduction in a Temnothorax ant. Behav. Ecol. Sociobiol. 61:1449-1457.
60. Takahashi, J., M. Itoh, I. Shimizu, and M. Ono. 2008. Male parentage and queen mating frequency in the bumblebee Bombus ignitus (Hymenoptera: Bombinae). Ecol. Res. 23:937-942.
61. Takahashi, J., S. J. Martin, M. Ono, and I. Shimizu. 2010. Male production by non-natal workers in the bumblebee, Bombus deuteronymus (Hymenoptera: Apidae). J. Ethol. 28:61-66.
62. Trivers, R. L., and H. Hare. 1976. Haplodiploidy and the evolution of the social insects. Science 191:249-263.
63. Truett, G. E., P. Heeger, R. L. Mynatt, A. A. Truett, J. A. Walker, and M. L. Warman. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29:52-54.
64. Van der Blom, J. 1986. Reproductive dominance within colonies of Bombus terrestris (L.). Behaviour 97:37-49.
65. Van Doorn, A., and J. Heringa. 1986. The ontogeny of a dominance hierarchy in colonies of the bumblebee Bombus terrestris (Hymenoptera, Apidae). Insectes Soc. 33:3-25.
66. Van Honk, C. G. J., P.-F. Röseler, H. H. W. Velthuis, and J. C. Hoogeveen. 1981. Factors influencing the egg laying of workers in a captive Bombus terrestris colony. Behav. Ecol. Sociobiol. 9:9-14.
67. Velthuis, H. H. W., D. De Araujo Alves, V. Imperatriz-Fonseca, and M. J. Duchateau. 2002. Worker bees and the fate of their eggs. Pp. 97-102 in J. Bruin, ed. Proceedings of the section experimental and applied entomology of the Netherlands Entomological Society (NEV), Vol. 13. NEV, Amsterdam.
68. Visscher, P. K. 1989. A quantitative study of worker reproduction in honey bee colonies. Behav. Ecol. Sociobiol. 25:247-254.
69. Visscher, P. K., and R. Dukas. 1995. Honey bees recognize development of nestmates' ovaries. Anim. Behav. 49:542-544.
70. Wenseleers, T., and F. L. W. Ratnieks. 2006. Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am. Nat. 168:E163-E179.
71. Wenseleers, T., A. Tofilski, and F. L. W. Ratnieks. 2005. Queen and worker policing in the tree wasp Dolichovespula sylvestris. Behav. Ecol. Sociobiol. 58:80-86.
72. Woyciechowski, M., and A. Lomnicki. 1987. Multiple mating of queens and the sterility of workers among eusocial Hymenoptera. J.Theor. Biol. 128:317-327.