Investigating Eusociality in Bees while Trusting the Uncertainty

Authors

  • Eduardo A. B. Almeida Universidade de Sao Paulo FFCLRP/USP - Dept.Biologia
  • Diego Sasso Porto Universidade de Sao Paulo FFCLRP/USP - Dept.Biologia

DOI:

https://doi.org/10.13102/sociobiology.v61i4.355-368

Keywords:

Apini, social behavior, Comparative Biology, divergence time, Meliponina, phylogeny

Abstract

Phylogenetic hypotheses and estimates of divergence times have already been used to investigate the evolution of social behavior in all lineages of bees. The interpretation of the number of origins of eusocial behavior and the timing these events depends on reliable phylogenetic hypotheses for the clades in which these lineages are nested. Three to six independent origins of eusocial behavior are interpreted to have occurred in bee taxa that differentiated in the Late Cretaceous, or much later in the Paleogene. Only two groups of bees exhibit the behaviors that qualify their members to be considered obligate eusocial, the honey bees (Apina) and the stingless bees (Meliponina). The evolutionary history of corbiculate bees remains uncertain in many respects, but phylogenetic research has been paving the path for comprehensive comparative approaches likely to shed light on the origin of diversity of forms and behaviors of these bees. In total, corbiculate bees encompass about 1000 species, roughly 5% of the described species diversity of bees. These bees are rather heterogeneous in terms of social organization, particularly stingless bees and orchid bees, which display a fascinating range of behavioral variation. Using phylogenetic tools, it has been possible to infer that caste polymorphism, division of labor and other traits of corbiculate bees probably started evolving over 80 million years ago. Phylogenetic hypotheses must be interpreted as more or less uncertain scenarios for studying the biological diversity, but when trusted they can provide powerful tools to investigate the evolution of social behaviors.

Author Biographies

Eduardo A. B. Almeida, Universidade de Sao Paulo FFCLRP/USP - Dept.Biologia

Associate Professor

Diego Sasso Porto, Universidade de Sao Paulo FFCLRP/USP - Dept.Biologia

Master's student

References

Abonyi, S. (1903). Morphologische und physiologische Beschreibung des Darmkanals der Honigbiene (Apis mellifica). Ablatt Közlem., II: 137-168.

Albrecht, M., Schmid, B., Hautier, Y. & Muller, C.B. (2012). Diverse pollinator communities enhance plant reproductive success. Proc. Biol. Sci., 279, 4845–4852. DOI: 10.1098/rspb.2012.1621

Alexander, B. A. & Michener, C. D. (1995). Phylogenetic studies of the families of short-tongued bees (Hymenoptera: Apoidea). Univ. Kansas Sci. Bul. 55, 377–424.

Almeida, E. A. B., Pie, M. R., Brady, S. G. & Danforth, B. N. (2012). Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world. J. Biogeogr. 39: 526-544. DOI: 10.1111/j.1365-2699.2011.02624.x

Alves, D. A., Menezes, C., Imperatriz-Fonseca, V. L., & Wenseleers, T. (2010). First discovery of a rare polygyne colony in the stingless bee Melipona quadrifasciata (Apidae, Meliponini). Apidologie. 42: 211-213. DOI: 10.1051/apido/2010053

Alves, D. A., Imperatriz-Fonseca, V. L., Francoy, T. M., Santos-Filho, P. S., Nogueira-Neto, P., Billen, J. and Wenseleers, T. (2009). The queen is dead—long live the workers: intraspecific parasitism by workers in the stingless bee Melipona scutellaris. Molec. Ecol., 18: 4102–4111. DOI: 10.1111/j.1365-294X.2009.04323.x

Andrade-Silva, A. C. R. & Nascimento, F. S. (2012). Multifemale nests and social behavior in Euglossa melanotricha (Hymenoptera, Apidae, Euglossini). J. Hymen. Res. 26: 1–16. DOI: 10.3897/JHR.26.1957

Ascher, J. S., Danforth, B. N. & Ji, S. (2001). Phylogenetic utility of the major opsin in bees (Hymenoptera: Apoidea): a reassessment. Mol. Phylogenet. Evol. 19: 76-93. DOI: 10.1006/mpev.2001.0911

Ascher, J. S. & Pickering, J. (2014). Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). [Accessed: October 25, 2014] URL: http://www.discoverlife.org/mp/20q?guide=Apoidea_species

Arnhart, L. (1906). Anatomie und Physiologie der Honigbiene. Wien: M. Perles, 99 p.

Augusto, S. C. & Garófalo, C. A. (2009). Bionomics and sociological aspects of Euglossa fimbriata (Apidae, Euglossini). Genet. Mol. Res. 8 (2): 525-538. DOI: 10.4238/vol8-2keer004

Augusto, S. C. & Garófalo, C. A. (2011). Task allocation and interactions among females in Euglossa carolina nests (Hymenoptera, Apidae, Euglossini). Apidologie 42: 162-173. DOI: 10.1051/apido/2010040

Bartomeus, I., Park, M. G., Gibbs, J., Danforth, B. N., Lakso, A. N. & Winfree, R. (2013). Biodiversity ensures plant–pollinator phenological synchrony against climate change. Ecol. Letters 16: 1331–1338. DOI: 10.1111/ele.12170

Bennett, F. D. (1965). Notes on a nest of Eulaema terminata Smith (Hymenoptera, Apoidea) with a suggestion of the occurrence of a primitive social system. Insect. Soc. 12: 81-92.

Blair, J. E. (2009). Animals (Metazoa). In Hedges, S. B. & Kumar, S. (Eds.), The Timetree of Life (pp. 223-230). New York: Oxford University Press.

Bordas, L. (1894). Anatomie du tube digestif des Hyménoptères. Comptes Kendus de I'Acad. des Sci., CXVIII: 1423-1425.

Bourke, A. F. G. (1999). Colony size, social complexity and reproductive conflict in social insects. J. Evol. Biol. 12: 245-257. DOI: 10.1046/j.1420-9101.1999.00028.x

Brady, S. G., Schultz, T. R., Fisher, B. L. & Ward, P. S. (2006a). Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc. Natl. Acad. Sci. USA 103: 18172–18177. DOI: 10.1073/pnas.0605858103

Brady, S. G., Sipes, S., Pearson, A. & Danforth, B. N. (2006b). Recent and simultaneous origins of eusociality in halictid bees. Proc. R. Soc. B 273, 1643-1649. DOI: 10.1098/rspb.2006.3496

Briant, T. J. (1884). On the anatomy and functions of the tongue of the honey bee (worker). Journ. Linn. Soc. London Zool.: 408-417.

Camargo, J. M. F. & Pedro, S. R. M. (1992a). Sistemática de Meliponinae (Hymenoptera, Apidae): sobre a polaridade e significado de alguns caracteres morfológicos. In: “Anais do Encontro Brasileiro sobre Biologia de Abelhas e outros Insetos Sociais.” Naturalia, num. esp., p. 45-49.

Camargo, J. M. F. & Pedro, S. R. M. (1992b). Systematics, phylogeny and biogeography of the Meliponinae (Hymenoptera: Apidae): a mini-review. Apidologie 23: 509-522. DOI: 10.1051/apido:19920603

Camargo, J. M. F. & Pedro, S. R. M. (2003) Sobre as relações filogenéticas de Trichotrigona Camargo & Moure (Hymenoptera, Apidae, Meliponini). In Melo, G. A. R. & Alves-dos-Santos, I. (Eds.), Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure (pp. 45-49). Criciúma: Editora UNESC.

Camargo, J. M. F. & Pedro, S. R. M. (2013). Meliponini Lepeletier, 1836. In Moure, J. S., Urban, D. & Melo, G. A. R. (Orgs). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. Available at http://www.moure.cria.org.br/catalogue. Accessed Oct/25/2014

Camargo, J. M. F. & Roubik, D. W. (2005). Neotropical Meliponini: Paratrigonoides mayri, new genus and species from western Colombia (Hymenoptera, Apidae, Apinae) and phylogeny of related genera. Zootaxa 1081: 33-45.

Cameron, S. A. (1991). A new tribal phylogeny of the Apidae inferred from mitochondrial DNA sequences. In Smith, D. R. (Ed.), Diversity in the Genus Apis (pp. 71-87). Oxford: Westview Press.

Cameron, S. A. (1993). Multiple origins of advanced eusociality in bees inferred from mitochondrial DNA sequences. Proc. Natl. Acad. Sci. USA 90: 8687-8691.

Cameron, S. A. (2004). Phylogeny and biology of Neotropical orchid bees (Euglossini). Annu. Rev. Entomol. 49: 377-404. DOI: 10.1146/annurev.ento.49.072103.115855

Cameron, S. A., Lozier, J. D., Strange, J. P., Koch, J. B., Cordes, N., Solter, L. F. & Griswold, T. L. (2010). Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA 108(2): 662–667. DOI: 10.1073/pnas.1014743108

Cameron, S. A. & Mardulyn, P. (2001). Multiple molecular data sets suggest independent origins of highly eusocial behavior in bees (Hymenoptera: Apinae). Syst. Biol. 50 (2): 194-214. DOI: 10.1080/10635150120230

Cardinal, S. & Danforth, B. N. (2011). The antiquity and evolutionary history of social behavior in bees. PLoS ONE 6(6): e21086. DOI: 10.1371/journal.pone.0021086

Cardinal, S. & Danforth, B. N. (2013). Bees diversified in the age of eudicots. Proc R Soc B 280: 20122686. DOI: 10.1098/rspb.2012.2686

Cardinal, S. & Packer, L. (2007). Phylogenetic analysis of corbiculate Apinae based on morphology of the sting apparatus (Hymenoptera: Apidae). Cladistics 23: 99-118. DOI: 10.1111/j.1096-0031.2006.00137.x

Cardinal, S., Straka, J. & Danforth, B. N. (2010). Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proc. Nat. Acad. Sci. USA 107: 16207-16211. DOI: 10.1073/pnas.1006299107

Carlet, G. (1884). Sur les muscles de I'abdomen de I'abeille. Comptes Rendus de I'Acad. des Sci. de Paris, XCVIII: 758-759.

Canevazzi, N. C. S. & Noll, F. B. (2014). Cladistic analysis of self-grooming indicates a single origin of eusociality in corbiculate bees (Hymenoptera: Apidae). Cladistics: 16 pp. DOI: 10.1111/cla.12077

Chavarría, G. & Carpenter, J. M. (1994). “Total evidence” and evolution of highly social bees. Cladistics 10: 229-258. DOI: 10.1111/j.1096-0031.1994.tb00177.x

Chenoweth, L. B., Tierney, S. M., Smith, J. A., Cooper, S. J. B. & Schwarz, M. P. (2007). Social complexity in bees is not sufficient to explain lack of reversions to solitary living over long time scales. BMC Evol. Biol. 7: 246(9). DOI: 10.1186/1471-2148-7-246

Costa, M. A., del Lama, M. A., Melo, G. A. R. & Sheppard, W. S. (2003). Molecular phylogeny of the stingless bees (Apidae, Apinae, Meliponini) inferred from mitochondrial 16S rDNA sequences. Apidologie 34: 73-84. DOI: 10.1051/apido:2002051

Crespi, B. J. & Yanega, D. (1994). The definition of eusociality. Behav. Ecol. 6: 109-115. DOI: 10.1093/beheco/6.1.109

Cronin, A.L., Molet, M., Doums, C., Monnin, T. & Peeters, C. (2013). Recurrent evolution of dependent colony foundation across eusocial insects. Annu. Rev. Entomol. 58:37–55. DOI: 10.1146/annurev-ento-120811-153643

Crozier, R. H. & Crozier, Y. C. (1993). The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics, 133(1): 97-117.

Danforth, B. N., Cardinal, S., Praz, C., Almeida, E. A. B. & Michez, D. (2013). The impact of molecular data on our understanding of bee phylogeny and evolution. Annu. Rev. Entomol. 58: 57-78. DOI: 10.1146/annurev-ento-120811-153633

Danforth, B.N., Fang, J. & Sipes S. D. (2006a). Analysis of family level relationships in bees (Hymenoptera: Apiformes) using 28S and two previously unexplored nuclear genes: CAD and RNA polymerase II. Molec. Phylogen. Evol. 39: 358–372. DOI: 10.1016/j.ympev.2005.09.022

Danforth, B. N., Sipes, S.D., Fang, J. & Brady, S. G. (2006b). The history of early bee diversification based on five genes plus morphology. Proceedings of the National Academy of Sciences of the United States of America 103: 15118–15123. DOI: 10.1073/pnas.0604033103

Debevec, A. H., Cardinal, S. & Danforth, B. N. (2012) Identifying the sister group to the bees: a molecular phylogeny of Aculeata with an emphasis on the superfamily Apoidea. Zool. Scripta, 41: 527–535. DOI: 10.1111/j.1463-6409.2012.00549.x

Dodson, C. H. (1966). Ethology of some bees of the tribe Euglossini (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 39: 607-629.

Edgecombe, G. D., Giribet, G., Dunn, C. W., Hejnol, A., Kristensen, R. M., Neves, R. C., Rouse, G. W., Worsaae, K. & Sørensen, M. V. (2011). Higher-level metazoan relationships: recent progress and remaining questions. Org. Divers. Evol. 11, 151-172. DOI: 10.1007/s13127-011-0044-4

Engel, M.S. (2001a). A monograph of the Baltic amber bees and evolution of the Apoidea (Hymenoptera). Bull. Am. Mus. Nat. Hist. 259: 1–192. DOI: http://dx.doi.org/10.1206/0003-0090(2001)259<0001:AMOTBA>2.0.CO;2

Engel, M. S. (2001b). Monophyly and extensive extinction of advanced eusocial bees: Insights from an unexpected Eocene diversity. Proc. Natl Acad. Sci. USA 98: 1661–1664. DOI: 10.1073/pnas.98.4.1661

Engel, M. S. (2011). Systematic melittology: where to from here? Syst. Entomol. 36: 2-15. DOI: 10.1111/j.1365-3113.2010.00544.x

Engel, M. S., Hinojosa-Díaz, I. A. & Rasnitsyn, A. R. (2009). A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae: Apini). Proc. Calif. Acad. Sci. (4)60: 23-38.

Engels, W. & Imperatriz-Fonseca, V. L. (1990). Caste development, reproductive strategies and control of fertility in honey bees and stingless bees. In Engels, W. (Ed.), Social Insects: An Evolutionary Approach to Caste and Reproduction (pp. 167-230). Heidelberg: Springer Berlin.

Faustino, C. D., Silva-Matos, E. V., Mateus, S. & Zucchi, R. (2002). First record of emergency queen rearing in stingless bees (Hymenoptera, Apinae, Meliponini), Insectes Soc. 49: 111–113. DOI: 10.1007/s00040-002-8287-x

Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Syst. Biol. 27(4): 401-410.

Fittkau, E. J. & Klinge, H. (1973). On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica 5: 2-14.

Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M., Ghazoul, J., Greenleaf, S., Hipólito, J., Holzschuh, A., Howlett, B., Isaacs, R., Javorek, S. K., Kennedy, C. M., Krewenka, K. M., Krishnan, S., Mandelik, Y., Mayfield, M. M., Motzke, I., Munyuli, T., Nault, B. A., Otieno, M., Petersen, J., Pisanty, G., Potts, S. G., Rader, R., Ricketts, T. H., Rundlöf, M., Seymour, C. L., Schüepp, C., Szentgyörgyi, H., Taki, H., Tscharntke, T., Vergara, C. H., Viana, B. F., Wanger, T. C., Westphal, C., Williams, N. & Klein, A. M. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339: 1608-1611. DOI: 10.1126/science.1230200

Garófalo, C. A., Camillo, E., Augusto, S. C., Jesus, B. M. V. & Serrano, J. C. (1998). Nest structure and communal nesting in Euglossa (Glossura) annectans Dressler (Hymenoptera, Apidae, Euglossini). Revta. Bras. Zool. 15(3): 589-596.

Gibbs, J., Brady, S. G., Sipes, S., Kanda, K. & Danforth, B. N. (2012). Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Molec. Phylogen. Evol. 65: 926-939. DOI: 10.1016/j.ympev.2012.08.013

Girdwoyn, M. (1876). Anatomie et physiologie de I'abeille. Paris: Mem. de la Soc. Polonaise des Sci. Exac., VI, 39 p.

Grimaldi, D. A. & Engel, M. S. (2005). Evolution of the Insects. New York: Cambridge University Press 755 p.

Hartfelder, K. (2000). Insect juvenile hormone: from "status quo" to high society. Brazilian Journal of Medical and Biological Research, 33(2), 157-177. Retrieved October 25, 2014, from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-879X2000000200003&lng=en&tlng=en. 10.1590/S0100-879X2000000200003.

Hartfelder, K. & Engels, W. (1998). Social insect polymorphism: Hormonal regulation of plasticity in development and reproduction in the honeybee. Current Topics in Developmental Biology 40: 45-77.

Hartfelder, K., Market, G. R., Judice, C. C., Pereira, G. A. G., Santana, W. C., Dallacqua, R. & Bitondi, M. M. G. (2006). Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37: 144–163. DOI: 10.1051/apido:2006013

Hedke, S. M., Patiny, S. & Danforth, B. N. (2013) The bee tree of life: a supermatrix approach to apoid phylogeny and biogeography. BMC Evol. Biol., 13:138. DOI: 10.1186/1471-2148-13-138

Hines, H. M., Hunt, J. H., O'Connor, T. K., Gillespie, J. J. & Cameron, S. A. (2007). Multigene phylogeny reveals eusociality evolved twice in vespid wasps. Proc. Natl. Acad. Sci. USA 104: 3295-3299. DOI: 10.1073/pnas.0610140104

Hölldobler, B. & Wilson, E. O. (1990). The Ants. Cambridge: Harvard Univ. Press, 732 p.

Hommell, R. (1904). Anatomie et physiologie de I'abeille domestique. Le Microg. Prép., XII: 49-60.

Hommell, R. (1905). Anatomie et physiologie de I'abeille domestique. Le Microg. Prép., XIII: 15-25, 60-67.

'Honeybee Genome Sequencing Consortium' (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114): 931-949. DOI: 10.1038/nature05260

Ihering, H. v. (1903). Biologie der stachellosen Honigbienen Brasiliens, Zool. Jahrb., Abt. Syst., Geogr. Biol. der Tiere. 19, 179-287, pl. 110–122.

Ihering H. v. (1930). Biologia das abelhas melliferas do Brasil, Bol. Agric. (São Paulo) 31, 435–506; 649–714.

Imperatriz-Fonseca, V. L. & Zucchi R. (1995). Virgin queens in stingless bee (Apidae, Meliponinae) colonies: a review. Apidologie 26: 231-244. DOI: 10.1051/apido:19950305

Jarvis, J. U. (1981). Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212: 571-573. DOI: 10.1126/science.7209555

Kamakura, M. (2011). Royalactin induces queen differentiation in honeybees. Nature 473: 478–483. DOI: 10.1038/nature10093

Kawakita, A., Ascher, J. S., Sota, T., Kato, M. & Roubik, D. W. (2008). Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein-coding genes (Hymenoptera: Apoidea: Apidae). Apidologie 39: 163-175. DOI: 10.1051/apido:2007046

Kerr, W. E. (1948). Estudos sôbre o gênero Melipona, An. Esc. Sup. Agricult. “Luiz de Queiroz” 5: 181-276.

Kerr, W. E. (1969). Some aspects of the evolution of social bees (Apidae). Evol. Biol. 3: 119-175.

Kerr, W. E. (1987). Sex determination in bees. XVII. Systems of caste determination in the Apinae, Meliponinae and Bombinae and their phylogenetic implications. Rev. Bras. Genet. 10: 685–694.

Kimsey, L. S. (1984). The behavioral and structural aspects of grooming and related activities in euglossine bees (Hymenoptera: Apidae). J. Zool. 204: 541-50.

Koulianos, S., Schmid-Hempel, R., Roubik, D. W. & Schmid-Hempel, P. (1999). Phylogenetic relationships within the corbiculate Apinae (Hymenoptera) and the evolution of eusociality. J. Evol. Biol. 12: 380-384.

Laidlaw, H. H., Jr., Pimentel-Gomes, F. & Kerr, W. E. (1956). Estimation of the number of lethal alleles in a panmitic population of Apis mellifera L. Genetics 41: 179-188.

Lee, C. Y. (2002). Subterranean termite pests and their control in the urban environment in Malaysia. Sociobiology 40: 3-10.

Lindauer, M. & Kerr, W. E. (1960). Communication between the workers of stingless bees. Bee World 41: 29–71.

Lockhart, P. G. & Cameron, S. A. (2001). Trees for bees. Trends Ecol. Evol. 16: 84-88. DOI: http://dx.doi.org/10.1016/S0169-5347(00)02054-1

Maa, T. (1953). An inquiry into the systematics of the tribus Apidini or honeybees (Hym.). Treubia 21: 525–640.

Macloskie, G. (1881). The endocranium and maxillary suspensorium of the bee. Amer. Nat., XV: 353-362.

Mardulyn, P. & Cameron, S. A. (1999). The major opsin in bees (Insecta: Hymenoptera): a promising nuclear gene for higher level phylogenetics. Mol. Phylogenet. Evol. 12: 168–176. DOI: 10.1006/mpev.1998.0606

Martins, A. C., Melo, G. A. R. & Renner, S. S. (2014). The corbiculate bees arose from New World oil-collecting bees: Implications for the origin of pollen baskets. Molec. Phylogen. Evol. 80, 88–94. DOI: 10.1016/j.ympev.2014.07.003

Michener, C. D. (1944). Comparative external morphology, phylogeny, and a classification of the bees (Hymenoptera). Bull. Am. Mus. Nat. Hist. 82: 151-326.

Michener, C. D. (1974). The Social Behavior of the Bees: A Comparative Study. Cambridge: Belknap, 404 p.

Michener, C. D. (1990). Classification of Apidae (Hymenoptera). Univ. Kansas Sci. Bull. 54: 75-164.

Michener, C. D. (2007). The Bees of the World (2nd Ed). Baltimore: John Hopkins University Press, 953 p.

Moreau, C. S., Bell, C. D., Vila, R., Archibald, S. B. & Pierce N. E. (2006). Phylogeny of the ants: Diversification in the age of angiosperms. Science 312: 101–104. DOI: 10.1126/science.1124891

Moure, J. S. (1961). A preliminary supra-specific classification of the Old World Meliponinae bees (Hymenoptera, Apoidea). Studia Entomol. 4, 181-242.

Moure, J. S., Melo, G. A. R. & Faria, L. R. R., Jr. (2012). Euglossini Latreille, 1802. In Moure, J. S., Urban, D. & Melo, G. A. R. (Orgs). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version. Available at http://www.moure.cria.org.br/catalogue. Accessed Oct/25/2014

Nixon, K. C. & Carpenter, J. M. (2012). On homology. Cladistics 28: 160–169. DOI: 10.1111/j.1096-0031.2011.00371.x

Noll, F. B. (2002). Behavioral phylogeny of corbiculate Apidae (Hymenoptera; Apinae), with special reference to social behavior. Cladistics 18: 137-153. DOI: 10.1006/clad.2001.0191

Oldroyd, B. P. (2007). What's killing american honey bees? PLoS Biol 5(6): e168. DOI:10.1371/journal.pbio.0050168

Page, R. E., Jr. (2013). The Spirit of the Hive: The Mechanisms of Social Evolution. Cambridge: Harvard University Press, 240 p.

Patel, A., Fondrk, M. K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K. & Amdam, G. V. (2007). The Making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE 2(6): e509. doi:10.1371/journal.pone.0000509

Payne, A. (2013). Resolving the relationships of apid bees (Hymenoptera: Apidae) through a direct optimization sensitivity analysis of molecular, morphological, and behavioral characters. Cladistics: 1-15. DOI: 10.1111/cla.12022

Pech, M. E. C., May-Itzá, W. de J., Medina, L. A. M. & Quezada-Euán, J. J. G. (2008). Sociality in Euglossa (Euglossa) viridissima Friese (Hymenoptera, Apidae, Euglossini). Insect. Soc. 55: 428-433. DOI: 10.1007/s00040-008-1023-4

Peixoto, E. B. M. I. & Serrão, J. E. (2001). A comparative study of the cardia and cardiac valves in the corbiculate bees (Hymenoptera: Apinae). Sociobiology 37: 707-721.

Pereira-Martins, S. R., Kerr, W. E. (1991). Biologia de Eulaema nigrita. 1. Construcão de células, oviposicão e desenvolvimento. Pap. Avuls. Zool. 37: 227-235.

Plant, J. D. & Paulus, H. F. (1987). Comparative morphology of the postmentum of bees (Hymenoptera: Apoidea) with special remarks on the evolution of the lorum. Zeitschrift fur Zoologische Systematik und Evolutionsforchung 25: 81-103.

Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P. & Schweiger, O. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25(6): 345-353. DOI: 10.1016/j.tree.2010.01.007

Prentice, M. (1991). Morphological analysis of the tribes of Apidae. In Smith, D. R. (Ed.), Diversity in the Genus Apis (pp. 51-69). Oxford: Westview Press.

Ramírez, S. R., Roubik, D. W., Skov, C. & Pierce, N. E. (2010). Phylogeny, diversification patterns and historical biogeography of euglossine orchid bees (Hymenoptera: Apidae). Biol. J. Linn. Soc. 100: 552-572. DOI: 10.1111/j.1095-8312.2010.01440.x

Ramírez-Arriaga, E., Cuadriello-Aguilar, J. I. & Hernández, E. M. (1996). Nest structure and parasite of Euglossa atroveneta Dressler (Apidae: Bombinae: Euglossini) at Unión Juárez, Chiapas, México. J. Kans. Entomol. Soc.69: 144-152

Rasmussen, C. & Cameron, S. A. (2010). Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol. J. Linn. Soc. 99: 206-232. DOI: 10.1111/j.1095-8312.2009.01341.x

Reeve, H. K. & Keller, L. (1999). Levels of Selection in Evolution. Princeton: Princeton University Press, 318p.

Roig-Alsina, A. & Michener, C. D. (1993). Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apoidea). Univ. Kansas Sci. Bull. 55: 123-160.

Roubik, D. W., Segura, J. A. L. & Camargo, J. M. F. (1997). New stingless bee genus endemic to Central American cloudforests: phylogenetic and biogeographical implications (Hymenoptera: Apidae: Meliponini). Syst. Entomol. 22: 67–80.

Sakagami S. F. (1982). Stingless bees. In Hermann H.R. (Ed.), Social insects (pp. 361–423). New York: Academic Press.

Sakagami, S. F. & Maeta, Y. (1984). Multifemale nests and rudimentary castes in the normally solitary bee Ceratina japonica (Hymenoptera: Xylocopidae). J. Kans. Entomol. Soc. 57: 639-656.

Santos-Filho, P. de S., Alves, D. de A., Eterovic, A., Imperatriz-Fonseca, V. L. & Kleinert, A. de M. P. (2006). Numerical investment in sex and caste by stingless bees (Apidae: Meliponini): a comparative analysis. Apidologie 37: 207–221.

Schmid, A. & Kleine, G. (1861). Umrisse zur anatomie und physiologie der bienen. Die Bienenzeitung, I: 498-525.

Schultz, T. R., Engel, M. S. & Prentice, M. (1999). Resolving conflict between morphological and molecular evidence for the origin of eusociality in the “corbiculate” bees (Hymenoptera: Apidae): a hypothesis-testing approach. Uni. Kans. Nat. Hist. Mus. Spec. Publ. 24: 125-138.

Schwarz, M. P., Richards, M. H. & Danforth, B. N. (2007). Changing paradigms in insect social evolution: insights from halictine and allodapine bees. Annu. Rev. Entomol. 52: 127–150. DOI: 10.1146/annurev.ento.51.110104.150950

Seeley, T. D. (1995). The Wisdom of the Hive: the social physiology of honey bee colonies. Cambridge: Harvard University Press, 318p.

Seeley, T. D. (2010). Honeybee Democracy. Princeton: Princeton University Press, 280 p.

Serrão, J. E. (2001). A comparative study of the proventricular structure in corbiculate apinae (Hymenoptera: Apidae). Micron 32: 379-385. DOI: 10.1016/S0968-4328(00)00014-7

Sheppard, W. S. & McPheron, B. A. (1991). Ribosomal DNA diversity in Apidae. In Smith, D. R. (Ed.), Diversity in the genus Apis (pp. 89-102). Oxford: Westview Press.

Snodgrass, R. E. (1910). The Anatomy of the Honey Bee. Washington: Government Printing Office, 236 p.

Snodgrass, R. E. (1935). Principles of insect morphology. New York: McGraw-Hill Book Co., ix + 667 p.

Snodgrass, R. E. (1942). The skeleto-muscular mechanisms of the honey bee. Smithson. misc. Coll. 103(2): 1-120.

Snodgrass, R. E. (1956). Anatomy of the Honey Bee. Ithaca: Cornell University Press., i-xiv + 334 p.

Soucy, S. L., Giray, T. & Roubik, D. W. (2003). Solitary and group nesting in the orchid bee Euglossa hyachintina (Hymenoptera, Apidae). Insect. Soc. 50: 248-255. DOI: 10.1007/s00040-003-0670-8

Sullivan, J. P., Jassim, O., Fahrbach, S. E. & Robinson, G. E. (2000). Juvenile hormone paces behavioral development in the adult worker honey bee. Hormones and behavior, 37(1): 1-14. DOI: 10.1006/hbeh.1999.1552

Tarpy, D. R. & Gilley. D.C. (2004). Group decision making during queen production in colonies of highly eusocial bees. Apidologie 35: 207–216. DOI: 10.1051/apido:2004008

Toth, A. L., Varala, K., Newman, T. C., Miguez, F. E., Hutchison, S. K., Willoughby, D. A., Simons, J. F., Egholm, M., Hunt, J. H., Hudson, M. E. & Robinson, G. E. (2007). Wasp gene expression supports an evolutionary link between maternal behavior and eusociality. Science 318: 441. DOI: 10.1126/science.1146647

Tóth, E., Queller, D. C., Dollin, A. & Strassmann, J. E. (2004). Conflict over male parentage in stingless bees. Insect. Soc. 51: 1-11. DOI: 10.1007/s00040-003-0707-z

Trivers, R. L. & Hare H. (1976). Haplodiploidy and the evolution of the social insects. Science. 191: 249-263. DOI: 10.1126/science.1108197

Von Frisch, K. (1946). Die Tänze der Bienen. Österreichische Zoolog. Zeitsch. 1: 1-48

Ware, J. L., Grimaldi, D. A. & Engel, M. S. (2010). The effects of fossil placement and calibration on divergence times and rates: An example from the termites (Insecta: Isoptera). Arthropod Struct. Dev. 39: 204–219. DOI: 10.1016/j.asd.2009.11.003

Weaver, N. (1955). Rearing of honeybee larvae on royal jelly in the laboratory. Science 121: 509-510. DOI: 10.1126/science.121.3145.509

Wille, A. (1979). Phylogeny and relationships among the genera and subgenera of stingless bees (Meliponinae) of the world. Rev. Biol. Trop. 27: 241–277.

Wilson. E. O. (1971). The Insect Societies. Cambridge: The Belknap Press of Harvard University Press, x + 548 p.

Wilson, E. O. & Hölldobler, B. (2005). Eusociality: Origin and consequences. Proc. Natl. Acad. Sci. USA 102(38):13367–13371. DOI: 10.1073/pnas.0505858102

Winston, M. L. (1987). The Biology of the Honey Bee. Cambridge: Harvard University Press, 294 p.

Winston, M. L. & Michener, C. D. (1977). Dual origin of highly social behavior among bees. Proc. Natl. Acad. Sci. USA 74: 1135-1137.

Woodard, S. H., Fischman, B. J., Venkat, A., Hudson, M. E., Varala, K., Cameron, S. A., Clark, A. G. & Robinson, G. E. (2014). Genes involved in convergent evolution of eusociality in bees. Proc. Natl Acad. Sci. USA 108: 7472–7477. DOI: 10.1073/pnas.1103457108

Zucchi, R., Sakagami, S.F. & Camargo, J.M.F. (1969). Biological observations on a neotropical parasocial bee, Eulaema nigrita, with a review on the biology of Euglossinae (Hymenoptera: Apidae). A comparative study. J. Fac. Sci. Hokkaido Univ., Zool. 17: 271-380.

Downloads

Published

2014-12-29

How to Cite

Almeida, E. A. B., & Porto, D. S. (2014). Investigating Eusociality in Bees while Trusting the Uncertainty. Sociobiology, 61(4), 355–368. https://doi.org/10.13102/sociobiology.v61i4.355-368

Issue

Section

Review

Most read articles by the same author(s)