Dual origins of social parasitism in North American Dialictus (Hymenoptera: Halictidae) confirmed using a phylogenetic approach.

Jason Gibbs, Jennifer Albert, Laurence Packer
Author Information
  1. Jason Gibbs: Department of Entomology, Cornell University, 3119 Comstock Hall, Ithaca, NY, USA.
  2. Jennifer Albert: Department of Biology, York University, 4700 Keele St., Toronto, ON, Canada.
  3. Laurence Packer: Department of Biology, York University, 4700 Keele St., Toronto, ON, Canada.

Abstract

The bee subgenus Dialictus (Halictidae: Lasioglossum) displays a large array of behaviours including solitary behaviour, eusociality, and social parasitism. Socially parasitic Dialictus share a suite of morphological traits; these could result from shared ancestry, but given their functional significance, could also have resulted from adaptive convergence. A combined morphological and molecular phylogenetic approach was used to test for monophyly of North American socially parasitic Dialictus. Two data sets were used in the phylogenetic analyses. First, short mitochondrial DNA sequences from previous taxonomic studies of North American Dialictus, including six social parasites, were used because of the broad taxon sampling they provide. These data were analysed in combination with a set of 40 morphological characters, including a large proportion of characters associated with social parasitism. Phylogenetic analysis of the combined DNA barcode and morphology data set resolves two distinct lineages of social parasite. The second data set was based on three genes (cytochrome c oxidase subunit 1, elongation factor 1α, and long-wavelength rhodopsin), but with sparser taxon sampling, including one representative from each putative social parasite-lineage. This also supported dual origins of social parasitism among North American Dialictus. The evolution of social parasitism is discussed. © The Willi Hennig Society 2011.

Associated Data

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References

  1. Alexander, B., 1990. A cladistic analysis of the nomadine bees (Hymenoptera: Apoidea). Syst. Entomol. 15, 121-152.
  2. Arduser, M.S., Michener, C.D., 1987. An African genus of cleptoparasitic halictid bees (Hymenoptera, Halictidae). J. Kansas Entomol. Soc. 60, 324-329.
  3. Ascher, J.S., Pickering, J., 2011. Discover life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20q?guide=Apoidea_species [last accessed 13 July 2011].
  4. Augusto, S.C., Garofalo, C.A., 1998. Behavioral aspects of Hoplostelis bilineolata (Spinola) (Hymenoptera, Megachilidae), a cleptoparasite of Euglossa cordata (Linnaeus) (Hymenoptera, Apidae), and behavior of the host in parasitized nests. Revta. Bras. Ent. 41, 507-515.
  5. Batra, S.W.T., Sakagami, S.F., Maeta, Y., 1993. Behavior of the Indian allodapine bee Braunsapis kaliago, a social parasite in the nests of B. mixta (Hymenoptera: Anthophoridae). J. Kansas Entomol. Soc. 66, 345-360.
  6. Beekman, M., Oldroyd, B.P., 2008. When workers disunite: intraspecific parasitism by eusocial bees. Annu. Rev. Entomol. 53, 19-37.
  7. Biani, N.B., Wcislo, W.T., 2007. Notes on the reproductive morphology of the parasitic bee Megalopta byroni (Hymenoptera: Halictidae), and a tentative new host record. J. Kansas Entomol. Soc. 80, 392-394.
  8. Birmingham, A.L., Hoover, S.E., Winston, M.L., Ydenberg, R.C., 2004. Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Can. J. Zool. 82, 1843-1853.
  9. Bourke, A.F.G., Franks, N.R., 1991. Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants. Biol. J. Linn. Soc. 43, 157-178.
  10. Brady, S.G., Sipes, S., Pearson, A., Danforth, B.N., 2006. Recent and simultaneous origins of eusociality in halictid bees. Proc. Roy. Soc. Lond. B. Biol. Sci 273, 1643-1649.
  11. Cameron, S.A., Hines, H.M., Williams, P.H., 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biol. J. Linn. Soc. 91, 161-188.
  12. Cardinal, S., Straka, J., Danforth, B.N., 2010. Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proc. Natl Acad. Sci. USA 107, 16207-16211.
  13. Carlin, N., 1988. Species, kin and other forms of recognition in the brood discrimination behaviour of ants. In: Trager, J.C. (Ed.), Advances in Myrmecology. E.J. Brill, Leiden, pp. 267-295.
  14. Carpenter, J.M., 1997. Phylogenetic relationships among European Polistes and the evolution of social parasitism (Hymenoptera: Vespidae, Polistinae). Mem. Mus. Natn. Hist. Nat. 173, 135-161.
  15. Carpenter, J.M., Perera, E.P., 2006. Phylogenetic relationships among yellowjackets and the evolution of social parasitism (Hymenoptera: Vespidae, Vespinae). Am. Mus. Novit. 3507, 1-19.
  16. Choudhary, M., Strassmann, J.E., Queller, D.C., Turillazzi, S., Cervo, R., 1994. Social parasites in polistine wasps are monophyletic: implications for sympatric speciation. Proc. Roy. Soc. Lond. B. Biol. Sci. 257, 31-35.
  17. Daly, H.V., Magnacca, K.N., 2003. Hawaiian Hylaeus (Nesoprosopis) bees (Hymenoptera: Apoidea). Insects of Hawaii, 17, [4] + 1-234.
  18. Danforth, B.N., Wcislo, W.T., 1999. Two new and highly apomorphic species of the Lasioglossum subgenus Evylaeus (Hymenoptera: Halictidae) form Central America. Ann. Entomol. Soc. Am. 92, 624-630.
  19. Danforth, B.N., Conway, L., Ji, S.Q., 2003. Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera : Halictidae). Syst. Biol. 52, 23-36.
  20. Danforth, B.N., Brady, S.G., Sipes, S.D., Pearson, A., 2004. Single copy nuclear genes recover Cretaceous age divergences in bees. Syst. Biol. 53, 309-326.
  21. Danforth, B.N., Eardley, C., Packer, L., Walker, K., Pauly, A., Randrianambinintsoa, F., 2008. Phylogeny of Halictidae with an emphasis on the endemic African Halictinae. Apidologie 39, 86-101.
  22. Eickwort, G.C., 1975. Gregarious nesting of the mason bee Hoplitis anthocopoides and the evolution of parasitism and sociality among megachilid bees. Evolution 29, 142-150.
  23. Eickwort, G.C., Eickwort, K.R., 1972. Aspects of the biology of Costa Rican halictine bees, III. Sphecodes kathleenae, a social cleptoparasite of Dialictus umbripennis. J. Kansas Entomol. Soc. 45, 529-541.
  24. Engel, M.S., Brooks, R.W., Yanega, D., 1997. New genera and subgenera of augochlorine bees. Sci. Pap. Nat. His. Mus. Univ. Kansas. 5, 1-21.
  25. Field, J., 1992. Intraspecific parasitism as an alternative reproductive tactic in nest-building wasps and bees. Biol. Rev. 67, 79-126.
  26. Fisher, R.M., 1984. Evolution and host specificity: dichotomous invasion success of Psithyrus citrinus (Hymenoptera: Apidae), a bumblebee social parasite in colonies of its two hosts. Can. J. Zool. 63, 977-981.
  27. Gibbs, J., 2009a. An integrative taxonomic approach reveals new (and old) species in the Lasioglossum (Dialictus) tegulare (Robertson) species group (Hymenoptera, Halictidae). Zootaxa 2032, 1-38.
  28. Gibbs, J., 2009b. A new cleptoparasitic Lasioglossum (Hymenoptera, Halictidae) from Africa. J. Hym. Res. 19, 74-79.
  29. Gibbs, J., 2009c. New species in the Lasioglossum petrellum species group identified through an integrative taxonomic approach. Can. Entomol. 141, 371-396.
  30. Gibbs, J., 2010. Revision of the metallic species of Lasioglossum (Dialictus) in Canada (Hymenoptera, Halictidae, Halictini). Zootaxa 2591, 1-382.
  31. Gibbs, J., 2011. Revision of the metallic Lasioglossum (Dialictus) of Eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa.
  32. Gibbs, J., Ascher, J.S., Packer, L., 2009. Proposal for precedence of Dialictus Robertson, 1902 and Evylaeus Robertson, 1902 over Hemihalictus Cockerell, 1897, Sudila Cameron, 1898 and Sphecodogastra, Ashmead, 1899 (Insecta, Hymenoptera). Bull. Zool. Nomen. 65, 147-157.
  33. Golding, G.B., Hanner, R., Hebert, P.D.N., 2009. Preface. Mol. Ecol. Resour 9 (S1), iv-vi.
  34. Goloboff, P.A., Farris, J.S., Nixon, K., 2003a. T.N.T.: Tree analysis using new technology. Available from: http://www.zmuc.dk/public/phylogeny.
  35. Goloboff, P.A., Farris, J.S., Källersjö, M., Boxelman, B., Ramírez, M.J., Szumik, C.A., 2003b. Improvements to resampling measures of group support. Cladistics 19, 324-332.
  36. Hajibabaei, M., deWaard, J.R., Ivanova, N.V., Ratnasingham, S., Dooh, R.T., Kirk, S.L., Mackie, P., Hebert, P.D.N., 2005. Critical factors for assembling a high volume of DNA barcodes. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360, 1959-1967.
  37. Hebert, P.D.N., Gregory, T.R., 2005. The promise of DNA barcoding for taxonomy. Syst. Biol. 54, 852-859.
  38. Hines, H.M., Cameron, S.A., 2010 The phylogenetic position of the bumble bee inquilines Bombus inexspectatus and implications for the evolution of social parasitism. Insect. Soc. 57, 379-383.
  39. Ivanova, N., deWaard, J., Hebert, P., 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol. Ecol. Notes 6, 998-1002.
  40. Knerer, G., 1980. Biologie und Sozialverhalten von Bienenarten der Gattung Halictus Latreille (Hymenoptera; Halictidae). Zool. Jahrb. Abt. Syst. Oekol. Geogr. Tiere 107, 511-536.
  41. Lopez-Vaamonde, C., Koning, J.W., Brown, R.M., Jordan, W.C., Bourke, A.F.G., 2004. Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430, 557-560.
  42. Lowe, R.M., Crozier, R.H., 1997. The phylogeny of bees of the socially parasitic Australian genus Inquilina and their Exoneura hosts (Hymenoptera, Anthophoridae). Insect. Soc. 44, 409-414.
  43. Lowe, R.M., Ward, S.A, Crozier, R.H., 2002. The evolution of parasites from their hosts: intra- and interspecific parasitism and Emery’s rule. Proc. R. Soc. Lond. B. 269, 1301-1305.
  44. Maddison, W.P., Maddison, D.R., 2010. Mesquite: a modular system for evolutionary analysis, ver. 2.7. http://mesquiteproject.org
  45. Michener, C.D., 1966. The bionomics of a primitively social bee, Lasioglossum versatum (Hymenoptera: Halictidae). J. Kansas Entomol. Soc. 39, 193-217.
  46. Michener, C.D., 1970. Social parasites among African allodapine bees (Hymenoptera, Anthophoridae, Ceratinini). Zool. J. Linn. Soc. 49, 199-225.
  47. Michener, C.D., 1974. The Social Behavior of the Bees. Belknap Press, Cambridge, MA.
  48. Michener, C.D., 1978. The parasitic groups of Halictidae (Hymenoptera, Apoidea). Univ. Kansas Sci. Bull. 51, 292-339.
  49. Michener, C.D., 2007. The Bees of the World, 2nd edn. Johns Hopkins University Press, Baltimore, MD.
  50. Miller, K.B., Alarie, Y., Wolfe, G.W., Whiting, M.F., 2005. Association of insect life stages using DNA sequences: the larvae of Philodytes umbrinus (Motschulsky) (Coleoptera: Dytiscidae). Syst. Entomol. 30, 499-509.
  51. Mitchell, T.B., 1960. Bees of the Eastern United States: volume I. NC. Agric. Exp. Stn. Tech. Bull. 141, 1-538.
  52. Moure, J.S., Hurd, P.D. Jr, 1987. An Annotated Catalog of the Halictid Bees of the Western Hemisphere (Hymenoptera: Halictidae). Smithsonian Institution Press, Washington, DC.
  53. Pabalan, N., Davey, K.G., Packer, L., 2000. Escalation of aggressive interactions during stage encounters in Halictus ligatus Say (Hymenoptera: Halictidae), with a comparison of circle tube behaviours with other halictine species. J. Insect Behav. 13, 627-650.
  54. Packer, L., 1986. The biology of a subtropical population of Halictus ligatus IV: a cuckoo-like caste. J. NY. Entomol. Soc. 94, 458-466.
  55. Pauly, A., 1984. Paradialictus, un nouveau genre cleptoparasite récolté au Parc National des Virungas (Zaire) (Hymenoptera, Apoidea, Halictidae). Rev. Zool. Afric. 98, 689-692.
  56. Pauly, A., 1997. Paraseladonia, nouveau genre cleptoparasite afrotropical (Hymenoptera, Apoidea, Halictidae). Bull. Ann. Soc. R. Belge Entomol. 133, 91-99.
  57. Plowright, R.C., Laverty, T.M., 1984. The ecology and sociobiology of bumblebees. Annu. Rev. Entomol. 29, 175-199.
  58. Plateaux-Quénu, C., 1960. Utilisation d’un nid de Halictus marginatus par une fondatrice de Halictus malachurus. Insect. Soc. 7, 349-352.
  59. Ratnasingham, S., Hebert, P.D.N., 2007. BOLD: the barcoding of life data system ( http://www.barcodinglife.org ). Mol. Ecol. Notes 7, 355-364.
  60. Robertson, C., 1901. Some new or little-known bees II. Can. Entomol. 33, 229-231.
  61. Robertson, C., 1926. Phenology of inquilines and nest-making bees. Psyche 33, 116-120.
  62. Roig-Alsina, A., Michener, C.D., 1993. Studies of the phylogeny and classification of long-tongued bees. Univ. Kansas Sci. Bull. 55, 124-162.
  63. Ronquist, F., Huelsenbeck, J.P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
  64. Rozen, J.G. Jr, 2000. Systematic and geographic distributions of neotropical cleptoparasitic bees, with notes on their modes of parasitism. In: Bitondi, M.M.G., Hartfelder, K. (Eds.), Anais do IV Encontro sobre Abehlhas. Ribeirão Preto, Brazil, pp. 204-210.
  65. Rozen, J.G. Jr, 2001. A taxonomic key to the mature larvae of cleptoparasitic bees (Hymenoptera: Apoidea). Am. Mus. Novit. 3309, 1-27.
  66. Rozen, J.G. Jr, 2003. Eggs, ovariole numbers, and modes of parasitism of cleptoparasitic bees, with emphasis on neotropical species. Am. Mus. Novit. 3413, 1-36.
  67. Savolainen, R., Vepsäläinen, K., 2003. Sympatric speciation through intraspecific social parasitism. Proc. Natl. Acad. Sci. USA 100, 7169-7174.
  68. Sheffield, C.S., Hebert, P.D.N., Kevan, P.G., Packer, L., 2009. DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Mol. Ecol. Resour. 9 (Suppl. 1), 196-207.
  69. Sick, M., Ayasse, M., Tengö, J., Engels, W., Lübke, G., Francke, W., 1994. Host-parasite relationships in six species of Sphecodes bees and their halictid hosts: nest intrusion, intranidal behaviour, and Dufour`s gland volatiles (Hymenoptera: Halictidae). J. Insect Behav. 7, 101-117.
  70. Smith, B.H., Weller, C., 1989. Social competition among gynes in halictine bees: the influence of bee size and pheromones on behaviour. J. Insect Behav. 2, 397-411.
  71. Smith, J.A., Tierney, S.M., Park, Y.C., Fuller, S., Schwarz, M.P., 2007. Origins of social parasitism: the importance of divergence ages in phylogenetic studies. Mol. Phylogenet. Evol. 43, 1131-1137.
  72. Smith, M.A., Rodriguez, J.J., Whitfield, J.B., Deans, A.R., Janzen, D.H., Hallwachs, W., Hebert, P.D.N., 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc. Natl Acad. Sci. USA 105, 12359-12364.
  73. Starr, C.K., 1979. The origin and evolution of sociality: a review of modern theory. In: Hermann, H.R. (Ed.), Social Insects. Academic Press, New York, NY, pp. 35-79.
  74. Steiner, F.M., Schlick-Steiner, B.C., Konrad, H., Moder, K., Christian, E., Seifert, B., Crozier, R.H., Stauffer, C., Buschinger, A., 2006. No sympatric speciation here: multiple data sources show that the ant Myrmica microrubra is not a separate species but an alternate reproductive morph of Myrmica rubra. J. Evol. Biol. 19, 777-787.
  75. Straka, J., Bogusch, P., 2007. Phylogeny of the bees of the family Apidae based on larval characters with focus on the origin of cleptoparasitism (Hymenoptera: Apiformes). Syst. Entomol. 32, 700-711.
  76. Sumner, S., Aanen, D.K., Delabie, J., Boomsma, J.J., 2004. The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery’s rule. Insect. Soc. 51, 37-42.
  77. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G., 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
  78. Tierney, S.M., Smith, J.A., Chenoweth, L., Schwarz, M.P., 2008. Phylogenetics of allodapine bees: a review of social evolution, parasitism and biogeography. Apidologie 39, 3-15.
  79. Ward, P.S., 1996 A new workerless social parasite in the ant genus Pseudomyrmex (Hymenoptera: Formicidae), with a discussion of the origin of social parasitism in ants. Syst. Entomol. 21, 253-263.
  80. Wcislo, W.T., 1987. The roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in Hymenoptera (Insecta), with special reference to bees (Apoidea). Biol. Rev. 62, 515-543.
  81. Wcislo, W.T., 1997. Invasion of nests of Lasioglossum imitatum by a social parasite, Paralictus asteris (Hymenoptera: Halictidae). Ethology 103, 1-11.
  82. Wcislo, W.T., 1999. Transvestism hypothesis: a cross-sex source of morphological variation for the evolution of parasitism among sweat bees (Hymenoptera: Halictidae)? Ann. Entomol. Soc. Am. 92, 239-242.
  83. Wcislo, W.T., Cane, J.H., 1996. Floral resource utilization by solitary bees (Hymenoptera: Apoidea) and exploitation of their stored foods by natural enemies. Annu. Rev. Entomol. 41, 257-286.
  84. West-Eberhard, M.J., 1986. Alternative adaptations, speciation and phylogeny. Evolution 83, 1388-1392.
  85. Wilson, E.O., 1971. The Insect Societies. Harvard University Press, Cambridge, MA.
  86. Wong, E., Hanner, R.H., 2008. DNA barcoding detects market substitution in North American seafood. Food Res. Int. 41, 828-837.

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