Advertisement

Behavioral Ecology and Sociobiology

, Volume 67, Issue 2, pp 331–340 | Cite as

Foundress polyphenism and the origins of eusociality in a facultatively eusocial sweat bee, Megalopta genalis (Halictidae)

  • Karen M. Kapheim
  • Adam R. Smith
  • Peter Nonacs
  • William T. Wcislo
  • Robert K. Wayne
Original Paper

Abstract

The reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality.

Keywords

Alternative reproductive behavior Facultative eusociality Maternal manipulation Social evolution Polyphenism 

Notes

Acknowledgments

KMK was supported by a short-term fellowship from STRI, a 10-week and pre-doctoral fellowship from the Smithsonian Institution, a Holmes O. Miller grant and a George Bartholomew fellowship from UCLA EEB, a Joan Wright Goodman award from American Women in Science, a GAANN fellowship from the US Department of Education, a graduate mentor fellowship from the UCLA graduate division, a graduate fellowship from the Center for Society and Genetics, and an NSF doctoral dissertation improvement grant. KMK and PN were also supported by NSF grant IOS-0642085. ARS was supported by grant COL 06-030 from the Secretaria Nacional de Ciencia, Tecnología e Innovación (SENACYT) of Panama to WTW and ARS, a fellowship to ARS from the NSF International Research Fellowship Program, and a Smithsonian Institution post-doctoral fellowship. STRI provided additional support through general research funds to WTW. We would like to thank Margarita Lopez-Uribe, Michael Reiser, Ricardo Cossio, Dyana La Rosa, Julian Medina Gutierrez, Sandra Bernal, Damien Ramirez Garcia, and Tim Alvey for the assistance in the field. Oris Acevedo, Belkys Jimenez, and Orelis Arosemena and the rest of the STRI staff provided valuable logistic support. Research on BCI was conducted with permission from the Autoridad Nacional del Ambiente under permit # SEX/A-34-09, in accordance with the laws of the Republic of Panama. We are thankful to Greg Grether, Torrey Rodgers, Simon Tierney, and Smadar Gilboa for the helpful comments on the manuscript. Earlier drafts of this manuscript were greatly improved by suggestions from Andrew Bourke and two anonymous reviewers.

Supplementary material

265_2012_1453_MOESM1_ESM.pdf (232 kb)
ESM 1 (PDF 231 KB)

References

  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Arneson L, Wcislo WT (2003) Dominant–subordinate relationships in a facultatively social, nocturnal bee, Megalopta genalis (Hymenoptera: Halictidae). J Kansas Entomol Soc 76:183–193Google Scholar
  3. Boomsma JJ, Eickwort GC (1993) Colony structure, provisioning and sex allocation in the sweat bee Halictus ligatus (Hymenoptera, Halictidae). Biol J Linn Soc 48:355–377CrossRefGoogle Scholar
  4. Bull NJ, Schwarz MP (2001) Brood insurance via protogyny: a source of female biased sex allocation. Proc Roy Soc Lond, B 268:1869–1874CrossRefGoogle Scholar
  5. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  6. Eickwort GC, Eickwort JM, Gordon J, Eickwort MA (1996) Solitary behavior in a high altitude population of the social sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Behav Ecol Sociobiol 38:227–233CrossRefGoogle Scholar
  7. Field J, Paxton R, Soro A, Craze P, Bridge C (2012) Body size, demography and foraging in a socially plastic sweat bee: a common garden experiment. Behav Ecol Sociobiol 66:743–756CrossRefGoogle Scholar
  8. Field J, Paxton RJ, Soro A, Bridge C (2010) Cryptic plasticity underlies a major evolutionary transition. Curr Biol 20:2028–2031PubMedCrossRefGoogle Scholar
  9. Field J, Shreeves G, Sumner S (1999) Group size, queuing and helping decisions in facultatively eusocial hover wasps. Behav Ecol Sociobiol 45:378–385CrossRefGoogle Scholar
  10. Fisher RA (1958) The genetical theory of natural selection. Dover Publications, New YorkGoogle Scholar
  11. Gadagkar R (1990) Evolution of eusociality—the advantage of assured fitness returns. Phil Trans R Soc B - Biol Sci 329:17–25CrossRefGoogle Scholar
  12. Godfray HCJ, Grafen A (1988) Unmatedness and the evolution of eusociality. Am Nat 131:303–305CrossRefGoogle Scholar
  13. Grafen A (1986) Split sex ratios and the evolutionary origins of eusociality. J Theor Biol 122:95–121CrossRefGoogle Scholar
  14. Kapheim KM, Bernal SP, Smith AR, Nonacs P, Wcislo WT (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae). Behav Ecol Sociobiol 65:1179–1190PubMedCrossRefGoogle Scholar
  15. Kapheim KM, Pollinger JP, Wcislo WT, Wayne RK (2009) Characterization of 12 polymorphic microsatellite markers for a facultatively eusocial sweat bee (Megalopta genalis). Mol Ecol Resour 9:1527–9PubMedCrossRefGoogle Scholar
  16. Kapheim KM, Smith AR, Ihle KE, Amdam GV, Nonacs P, Wcislo WT (2012) Physiological variation as a mechanism for developmental caste-biasing in a facultatively eusocial sweat bee. Proc R Soc Lond, B, Biol Sci 279:1437–1446CrossRefGoogle Scholar
  17. Landi M, Queller DC, Turillazzi S, Strassmann JE (2003) Low relatedness and frequent queen turnover in the stenogastrine wasp Eustenogaster fraterna favor the life insurance over the haplodiploid hypothesis for the origin of eusociality. Insect Soc 50:262–267CrossRefGoogle Scholar
  18. Leigh EG Jr (1999) Tropical forest ecology: a view from Barro Colorado Island. Oxford University Press, OxfordGoogle Scholar
  19. Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. Oxford University Press, OxfordGoogle Scholar
  20. Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University. Press, CambridgeGoogle Scholar
  21. Meunier J, West SA, Chapuisat M (2008) Split sex ratios in the social Hymenoptera: a meta-analysis. Behav Ecol 19:382–390CrossRefGoogle Scholar
  22. Michener CD (1961) Social polymorphism in Hymenoptera. In: Kennedy JS (ed) Insect Polymorphism. Symposia of the Royal Entomological Society of London Bartholomew Press, Surrey, pp 43–56Google Scholar
  23. Michener CD (1974) The social behavior of the bees. Harvard University Press, CambridgeGoogle Scholar
  24. Michener CD (1990) Reproduction and castes in social halictine bees. In: Engels W (ed) Social insects: an evolutionary approach to castes and reproduction. Springer, New YorkGoogle Scholar
  25. Michener CD, Brothers DJ (1974) Were workers of eusocial Hymenoptera initially altruistic or oppressed. Proc Natl Acad Sci U S A 71:671–674PubMedCrossRefGoogle Scholar
  26. Mitesser O, Weissel N, Strohm E, Poethke H (2007) Optimal investment allocation in primitively eusocial bees: a balance model based on resource limitation of the queen. Insect Soc 54:234–241CrossRefGoogle Scholar
  27. Mueller UG, Eickwort GC, Aquadro CF (1994) DNA-fingerprinting analysis of parent-offspring conflict in a bee. Proc Natl Acad Sci U S A 91:5143–5147PubMedCrossRefGoogle Scholar
  28. Nonacs P (1991) Alloparental care and eusocial evolution—the limits of Queller head-start advantage. Oikos 61:122–125CrossRefGoogle Scholar
  29. Nonacs P (2011) Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation. Proc Natl Acad Sci U S A 108:10808–10815PubMedCrossRefGoogle Scholar
  30. Packer L (1990) Solitary and eusocial nests in a population of Augochlorella striata (Provancher) (Hymenoptera; Halictidae) at the northern edge of its range. Behav Ecol Sociobiol 27:339–344CrossRefGoogle Scholar
  31. 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 67:2871–2877CrossRefGoogle Scholar
  32. Plateaux-Quenu C, Plateaux L, Packer L (2000) Population-typical behaviours are retained when eusocial and non-eusocial forms of Evylaeus albipes (F.) (Hymenoptera, Halictidae) are reared simultaneously in the laboratory. Insect Soc 47:263–270CrossRefGoogle Scholar
  33. Queller DC (1989) The evolution of eusociality—reproductive head starts of workers. Proc Natl Acad Sci U S A 86:3224–3226PubMedCrossRefGoogle Scholar
  34. Rehan SM, Richards MH (2010) The influence of maternal quality on brood sex allocation in the small carpenter bee, Ceratina calcarata. Ethology 116:876–887Google Scholar
  35. Schwarz MP, Richards MH, Danforth BN (2007) Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu Rev Entomol 52:127–50PubMedCrossRefGoogle Scholar
  36. Simpson SJ, Sword Gregory A, Lo N (2011) Polyphenism in insects. Curr Biol 21:R738–R749PubMedCrossRefGoogle Scholar
  37. Smith A, Wcislo W, O’Donnell S (2008) Body size shapes caste expression, and cleptoparasitism reduces body size in the facultatively eusocial bees Megalopta (Hymenoptera: Halictidae). J Insect Behav 21:394–406CrossRefGoogle Scholar
  38. 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 78:1043–1050CrossRefGoogle Scholar
  39. Smith AR, Kapheim KM, Pérez-Ortega B et al (2012) Juvenile hormone levels reflect social opportunities in the facultatively eusocial bee Megalopta genalis (Hymenoptera: Halictidae). Horm Behav. doi: 10.1016/j.yhbeh.2012.08.012
  40. 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 54:14–21CrossRefGoogle Scholar
  41. Smith AR, Wcislo WT, O'Donnell S (2007) Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae). Behav Ecol Sociobiol 61:1111–1120CrossRefGoogle Scholar
  42. Soucy SL (2002) Nesting biology and socially polymorphic behavior of the sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Ann Entomol Soc Am 95:57–65CrossRefGoogle Scholar
  43. Soucy SL, Danforth BN (2002) Phylogeopgraphy of the socially polymorphic sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Evolution 56:330–341PubMedGoogle Scholar
  44. Strohm E, Bordon-Hauser A (2003) Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective. Behav Ecol 14:546–553CrossRefGoogle Scholar
  45. Tierney SM, Fischer CN, Rehan SM et al (in revision) Facultative social nesting does not vary across a climate gradient, despite disparity in brood production and body sizeGoogle Scholar
  46. Wcislo WT (1997a) Behavioral environments of sweat bees (Halictinae) in relation to variability in social organization. In: Choe JC, Crespi BJ (eds) Social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 316–332Google Scholar
  47. Wcislo WT (1997b) Behavioral environments of sweat bees (Halictinae) in relation to variability in social organization. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 316–332Google Scholar
  48. Wcislo WT (2000) Environmental hierarchy, behavioral contexts, and social evolution in insects. In: Martins RP, Lewinsohn TM, Barbeitos MS (eds) Ecologia e comportameno de insetos. PPGE-UFRJ, Rio de Janeiro, BrasilGoogle Scholar
  49. Wcislo WT, Arneson L, Roesch K, Gonzalez V, Smith A, Fernandez H (2004) The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? Biol J Linn Soc 83:377–387CrossRefGoogle Scholar
  50. Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474PubMedCrossRefGoogle Scholar
  51. Wcislo WT, Gonzalez VH (2006) Social and ecological contexts of trophallaxis in facultatively social sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera, Halictidae). Insect Soc 53:220–225CrossRefGoogle Scholar
  52. Wcislo WT, Tierney SM (2009) Behavioural environments and niche construction: the evolution of dim-light foraging in bees. Biol Rev Camb Philos Soc 84:19–37PubMedCrossRefGoogle Scholar
  53. Weissel N, Mitesser O, Poethke HJ, Strohm E (2012) Availability and depletion of fat reserves in halictid foundress queens with a focus on solitary nest founding. Insect Soc 59:67–74CrossRefGoogle Scholar
  54. West-Eberhard MJ (1986) Alternative adaptations, speciation, and phylogeny. Proc Natl Acad Sci U S A 83:1388–1392PubMedCrossRefGoogle Scholar
  55. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, OxfordGoogle Scholar
  56. West Eberhard MJ (1978) Polygyny and the evolution of social behavior in wasps. J Kansas Entomol Soc 51:832–856Google Scholar
  57. Willmer PG, Stone GN (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. In: Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ, Brockmann HJ, Naguib M (eds) Advances in the study of behavior. Elsevier Science & Technology Books, San Diego, pp 347–466Google Scholar
  58. Wolf JB, Wade MJ (2001) On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J Evol Biol 14:347–356CrossRefGoogle Scholar
  59. Yanega D (1997) Demography and sociality in halictine bees (Hymenoptera: Halictidae). In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 293–315Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Karen M. Kapheim
    • 1
    • 2
    • 3
  • Adam R. Smith
    • 2
    • 4
  • Peter Nonacs
    • 1
  • William T. Wcislo
    • 2
  • Robert K. Wayne
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California, Los AngelesLos AngelesUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  3. 3.Department of EntomologyInstitute for Genomic BiologyUrbanaUSA
  4. 4.Department of Biological SciencesGeorge Washington UniversityWashingtonUSA

Personalised recommendations