Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum

Insectes Sociaux

Volumn 56, Issue 1, 2009, Pages 55-63

  Soro, A ^a,b   Ayasse, M ^c   Zobel, M U ^a   Paxton, R J ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c UNIVERSITY OF ULM   (Germany)

Author keywords

Eusociality; Foreign workers; Halictidae; Microsatellites; Relatedness

Indexed keywords

BEE; COMPLEXITY; EUSOCIALITY; GENETIC STRUCTURE; GEOGRAPHICAL DISTRIBUTION; INTERSPECIFIC VARIATION; INTRASPECIFIC VARIATION; LIFE CYCLE; MATING BEHAVIOR; NESTMATE RECOGNITION; POPULATION GENETICS; QUEEN; RELATEDNESS; SOCIAL ORGANIZATION; WORKER CASTE;

AUSTRIA; CENTRAL EUROPE; EICHKOGL; EURASIA; EUROPE; STYRIA;

APOIDEA; HALICTIDAE; HALICTINAE; LASIOGLOSSUM MALACHURUM;

EID: 60149101209     PISSN: 00201812     EISSN: 14209098     Source Type: Journal    
DOI: 10.1007/s00040-008-1037-y     Document Type: Article

References (59)

1. Andersson M. 1984. The evolution of eusociality. Annu. Rev. Ecol. Syst. 15: 165-190
2. Ayasse M. 1990. Odor based interindividual and nest recognition in the sweat bee Lasioglossum malachurum (Hymenoptera: Halictidae). In: Social Insects and the Environment (Veeresh G.K., Mallik B. and Viraktamath C.A. Eds.), Oxford & IBH, New Delhi, India. pp 511-512
3. Boomsma J.J. 2007. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17: R673-R683
4. Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351: 947-975
5. Bourke A.F.G. 1994. Worker matricide in social bees and wasps. J. Theor. Biol. 167: 283-292
6. Brady S.G., Sipes S., Pearson A. and Danforth B.N. 2006. Recent and simultaneous origins of eusociality in halictid bees. Proc. R. Soc. Lond. B 273: 1643-1649
7. Crozier R.H. and Pamilo P. 1996. Evolution of Social Insect Colonies. Sex Allocation and Kin Selection. Oxford University Press, Oxford, UK. 306 pp
8. Ellegren H. 2004. Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5: 435-447
9. Estoup A., Solignac M. and Cornuet J-M. 1994. Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc. R. Soc. Lond. B 258: 1-7
10. Hamilton W.D. 1964. The genetical evolution of social behaviour I. & II. J. Theor. Biol. 7: 1-16 & 17-52
11. Hamilton W.D. 1972. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3: 193-232
12. Hirata M. and Higashi S. 2008. Degree-day accumulation controlling allopatric and sympatric variations in the sociality of sweat bees, Lasioglossum (Evyleus) baleicum (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 62: 1239-1247
13. Hughes W.O.H., Oldroyd B.P., Beekman M. and. Ratnieks F.L.W. 2008a. Ancestral monogamy shows kin selection is key to the evolution of sociality. Science 320: 1213-1216
14. Hughes W.O.H., Ratnieks F.L.W and Oldroyd B.P. 2008b. Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera. J. Evol. Biol. 21: 1090-1095
15. Knerer G. 1992. The biology and social behaviour of Evylaeus malachurus (K.) (Hymenoptera; Halictidae) in different climatic conditions of Europe. Zool. Jb. Syst. 119: 261-290
16. Kukuk P.F. 1989. Evolutionary genetics of a primitively eusocial halictine bee, Dialictus zephyrus. In: The Genetics of Social Evolution (Breed M.D. and Page R.E. Eds), Westview Press, Boulder, Colorado, USA. pp183-202
17. Kukuk P.F., Eickwort G.C. and May B.P. 1987. Multiple maternity and multiple paternity in first generation brood from single foundress colonies of the sweat bee, Dialictus zephyrus. Insect. Soc. 34: 131-135
18. Lopez-Vaamonde C., Koning J.W., Brown R.M., Jordan W.C. and Bourke A.F.G. 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430: 557-560
19. Michener C.D. 1974. The Social Behavior of the Bees. A Comparative Study. Belknap Press of Harvard University Press, Cambridge, Massachusetts, USA. 404 pp
20. Moilanen A, Sundström L. and Pedersen J.V. 2004. MateSoft: a program for the deducing parental genotypes and estimating mating system statistics in haplodiploid species. Mol. Ecol. Notes 4: 795-797
21. Mueller U.G. 1991. Haplodiploidy and the evolution of facultative sex-ratios in a primitively eusocial bee. Science 254: 442-444
22. Mueller U.G., Eickwort G.C. and Aquadro C.F. 1994. DNA fingerprinting analysis of parent-offspring conflict in a bee. Proc. Natl. Acad. Sci. 91: 5143-5147
23. Nanork P., Chapman N.C., Wongsiri S., Lim J., Gloag R.S. and Oldroyd B.P. 2007. Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol. Ecol. 16: 1107-1114
24. Nanork P., Paar J., Chapman N.C., Wongsiri S. and Oldroyd B.P. 2005. Asian honeybees parasitize the future dead. Nature 437: 829
25. Nei M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590
26. Oldroyd B.P. and Fewell J.H. 2007. Genetic diversity promotes homeostasis in insect colonies. Trends Ecol. Evol. 22: 408-413
27. 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: 339-344
28. Packer L. and Knerer G. 1985. Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera;Halictidae). Behav. Ecol. Sociobiol. 17: 143-149
29. Palmer K.A., Oldroyd B. P., Quezada-Euán J.J.G., Paxton R.J. and May-Itza W.J. 2002. Paternity frequency and maternity of males in some stingless bee species. Mol. Ecol. 11: 2107-2113
30. Paxton R.J., Arévalo E. and Field J. 2003. Microsatellite loci for the eusocial Lasioglossum malachurum and other sweat bees (Hymenoptera, Halictidae). Mol. Ecol. Notes 3: 82-84
31. Paxton R.J., Ayasse M., Field J. and Soro A. 2002. Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee, Lasioglossum malachurum, as revealed by microsatellites. Mol. Ecol. 11: 2405-2416
32. Paxton R.J., Thorén P.A., Estoup A. and Tengö J. 2001. Queen-worker conflict over male production and the sex ratio in a facultatively polyandrous bumble bee, Bombus hypnorum: the consequences of nest usurpation. Mol. Ecol. 10: 2489-2498
33. Paxton R.J., Thorén P.A., Tengö J., Estoup A. and Pamilo P. 1996. Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera: Andrenidae), using microsatellites. Mol. Ecol. 5: 511-519
34. Pfeiffer K.J. and Crailsheim K. 1998. Drifting of honeybees. Insect. Soc. 45: 151-167
35. Plateaux-Quénu C. 1959. Un nouveau type de société d'insectes: Halictus marginatus Brullé (Hym., Apoidea). Ann. Biol. 35: 325-444
36. Queller D.C. and Goodnight K.F. 1989. Estimating relatedness using genetic markers. Evolution 43: 258-275
37. Queller D.C., Zacchi F., Cervo R., Turillazzi S., Henshaw M.T., Santorelli L.A. and Strassmann J. 2000. Unrelated helpers in a social insect. Nature 405: 784-787
38. Ratnieks F.L.W. and Wenseleers T. 2008. Altruism in insect societies and beyond: voluntary or enforced? Trends Ecol. Evol. 23: 45-52
39. Raymond, M. and Rousset F. 1995. GENEPOP (V. 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248-249
40. Richards M.H. 2000. Evidence for geographic variation in colony social organization in an obligately social sweat bee, Lasioglossum malachurum Kirby (Hymenoptera; Halictidae). Can. J. Zool. 78: 1259-1266
41. Richards M.H., French D. and Paxton R.J. 2005. It's good to be queen: classically eusocial colony structure and low worker fitness in a obligately social sweat bee. Mol. Ecol. 14: 4123-4133
42. Richards M.H., Packer L. and Seger J. 1995. Unexpected patterns of parentage and relatedness in a primitively eusocial bee. Nature 373: 239-241
43. Sakagami S.F. and Munakata M. 1972. Distribution and bionomics of a transpaleartic eusocial halictine bee, Lasioglossum (Evylaeus) calceatum, in Northern Japan, with reference to its solitary life cycle at high altitude. J. Fac. Sci. Hokkaido Univ. Zool. 18: 411-439
44. Schlötterer C. 1998. Microsatellites. In: Molecular Genetic Analysis of Populations (Hoelzel A.R. Ed), Oxford University Press, New York, USA. pp 237-261
45. Schwarz M.P., Richards M.H. and Danforth B.N. 2007. Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu. Rev. Entomol. 52: 127-150
46. Sorvari J., Theodora P., Turillazzi S., Hakkarainen H. and Sundström L. 2008. Food resources, chemical signaling, and nest mate recognition in the ant Formica aquilonia. Behav. Ecol. 19: 441-447
47. Soucy S.L. 2002. Nesting biology and socially polymorphic behavior of the sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Ann. Entomol. Soc. Am. 95: 57-65
48. Soucy S.L. and Danforth B.N. 2002. Phylogeography of the socially polymorphic sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Evolution 56: 330-341
49. Starr C.K. 1984. Sperm competition, kinship, and sociality in the aculeate Hymenoptera. In: Sperm Competition and the Evolution of Animal Mating Systems (Smith R.L. Ed), Academic Press, New York, USA. pp 427-464
50. Strassmann J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1-13
51. Strohm E. and Bordon-Hauser A. 2003. Advantages and disadvantages of large colony size in the halictid bee: the queen's perspective. Behav. Ecol. 14: 546-553
52. Sumner S., Lucas E., Barker J. and Isaac N. 2007. Radio-tagging technology reveals extreme nest-drifting behavior in a eusocial insect. Curr. Biol. 17: 140-145
53. Tregenza T. and Wedell N. 2002. Polyandrous females avoid costs of inbreeding. Nature 415: 71-73
54. Wenseleers T. and Ratnieks F.L.W. 2006. Enforced altruism in insect societies. Nature 444: 50
55. Westrich P. 1989. Die Wildbienen Baden Württembergs. Verlag Eugen Ulmer, Stuttgart, Germany. 972 pp
56. Wilson E.O. 1971. The Insect Societies. Belknap Press of Harvard University Press, Cambridge, Massachusetts, USA. 548 pp
57. Wyman L.M. and Richards M.H. 2003. Colony social organization of Lasioglossum malachurum Kirby (Hymenoptera; Halictidae) in southern Greece. Insect. Soc. 50: 1-12
58. Zanette L.R.S. and Field J. 2008. Genetic relatedness in early associations of Polistes dominulus: from related to unrelated helpers. Mol. Ecol. 17: 2590-2597
59. Zobel M. and Paxton R.J. 2007. Is big the best? Queen size, usurpation and nest closure of a primitively eusocial sweat bee (Lasioglossum malachurum). Behav. Ecol. Sociobiol. 61: 435-447