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Phylogeny of the Genus Apis

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Honeybees of Asia

Abstract

The early historical background of honeybee phylogeny and systematics are reviewed and then proceed through the important contributions of von Buttel-Reepen (Mitt Zool Mus Berl 3, 117–201, 1906), Skorikov (Rep Appl Entomol Leningrad 4:249–264, 1929) through Maa (Treubia 21:525–640, 1953) and the first modern analysis of Lindauer (Z Vgl Physiol 38:521–557, 1956). The importance of chromosomes, geotaxis, the dance language and cavity nesting are analysed at length. Contemporary discussions focus on molecular approaches to honeybee phylogeny and various attempts at consensus tree structure are considered. Similarly, the persistent difficulties of polarity on Apis evolution are probed as are the evolutionary significance of worker size in the context of the fossil record.

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References

  • Alexander BA (1991) Phylogenetic analysis of the genus Apis (Hymenoptera: Apidae). Ann Entomol Soc Am 84:137–149

    Google Scholar 

  • Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae; Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35

    Article  CAS  PubMed  Google Scholar 

  • Ashmead WH (1904) Remarks on honeybees. Proc Entomol Soc Wash 6:120–123

    Google Scholar 

  • Cameron SA, Derr JN, Austin AD, Woollwy JB, Wharton RA (1992) The application of nucleotide sequence data to phylogeny of Hymenoptera: a review. J Hymenopt Res 1:63–79

    Google Scholar 

  • Cornuet JM, Garnery L (1991) Mitochondrial DNA variability in honeybees and its phylogeographic implications. Apidologie 22:627–642

    Article  CAS  Google Scholar 

  • Crozier RH, Crozier YC (1992) The Cytochrome-b and ATPase genes of honeybee mitochondrial DNA. Mol Biol Evol 9:474–482

    CAS  PubMed  Google Scholar 

  • Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133:97–117

    CAS  PubMed  Google Scholar 

  • Crozier RH, Crozier YC, Mackinlay AG (1989) The CO-I and CO-II region of honeybee mitochondrial DNA: evidence for variation in insect mitochondrial evolutionary rates. Mol Biol Evol 6:399–411

    CAS  PubMed  Google Scholar 

  • Crozier YC, Koulianos S, Crozier RH (1991) An improved test for Africanized honeybee mitochondrial DNA. Experientia 47:968–969

    Article  CAS  PubMed  Google Scholar 

  • Danforth BN, Ji SQ (1998) Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. Mol Biol Evol 15:225–235

    CAS  PubMed  Google Scholar 

  • Deodikar GB, Thakar CV (1966) Cyto-genetics of Indian honeybees and bearing on taxonomic and breeding problems. Indian J Genet 36A:386–393

    Google Scholar 

  • Dyer FC (1991) Comparative studies of dance communication: analysis of phylogeny and function. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 177–198

    Google Scholar 

  • Dzierzon J (1849) Neue verbesserte Bienenzucht des Pfarrers Dzierzon. Publ. by author [in German]

    Google Scholar 

  • Engel MS (1998) Fossil honey bees and evolution in the genus Apis (Hymenoptera: Apidae). Apidologie 29:265–281

    Article  Google Scholar 

  • Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J Hymenopt Res 8:165–196

    Google Scholar 

  • Engel MS (2006) A giant honey bee from the Middle Miocene of Japan (Hymenoptera: Apidae). Am Mus Novitat 3504:1–12

    Article  Google Scholar 

  • Engel MS, Schultz TTR (1997) Phylogeny and behaviour in honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 90:43–53

    Google Scholar 

  • Engel MS, Hinojosa-Diaz IA, Rasnitsyn AP (2009) A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae). Proc Calif Acad Sci 60:23–38

    Google Scholar 

  • Fabricius JC (1787) Supplemental list of insects setting out recently discovered species together with their generic characteristics, specific distinguishing features, emendations and remarks. Hafniae, Proft, Copenhagen [in Latin]

    Google Scholar 

  • Fabricius JC (1793) Systematic description of nature in accordance with the three natural kingdoms, according to classes, orders, genera and species with their distinguishing characteristics, alternative names and habitats. Hafniae, Proft Copenhagen [in Latin]

    Google Scholar 

  • Fahrenhorst H (1977) Nachweis übereinstimmender Chromosomen-Zahlen (n=16) bei allen 4 Apis-Arten. Apidologie 8:89–100 [in German]

    Article  Google Scholar 

  • Friese H (1923) Die europäischen Bienen (Apidae). Walter de Gruyter, Berlin

    Google Scholar 

  • Garnery L, Vautrin D, Cornuet JM, Solignac M (1991) Phylogenetic relationships in the genus Apis inferred from mitochondrial DNA sequence data. Apidologie 22:87–92

    Article  CAS  Google Scholar 

  • Garnery L, Cornuet JM, Solignac M (1992) Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol Ecol 1:145–154

    Article  CAS  PubMed  Google Scholar 

  • Gerstäcker CEA (1862) Über die die geographische Verbreitung und die Abänderungen der Honigbiene nebst Bemerkungen über die ausländischen Honigbienen der alten Welt. Festschrift XI Wanderversammlungdeutsch. Bienenwirthe. Potsdam, Kraemer [in German]

    Google Scholar 

  • Hall HG, Smith DR (1991) Distinguishing African and European honeybee matrilines using amplified mitochondrial DNA. Proc Natl Acad Sci 88:4548–4552

    Article  CAS  PubMed  Google Scholar 

  • Horn EP (1975) Mechanisms of gravity processing by leg and abdominal gravity receptors in bees. J Insect Physiol 21:673–679

    Article  Google Scholar 

  • Horne C (1870) Notes on the habits of some hymenopterous insects of the north-west provinces of India. Trans Zool Soc Lond 7:161–196

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jander R, Jander U (1970) Über die Phylogenie der Geotaxis innerhalb der Bienen (Apoidea). Z Vgl Physiol 66:355–368 [in German]

    Article  Google Scholar 

  • Koeniger N (1976) Neue Aspekte der Phylogenie innerhalb der Gattung Apis. Apidologie 7:357–366 [in German]

    Article  Google Scholar 

  • Koeniger N, Koeniger G (1980) Observations and experiments on migration and dance communication of Apis dorsata in Sri Lanka. J Apic Res 19:21–34

    Google Scholar 

  • Koeniger N, Koeniger G (1991) An evolutionary approach to mating behaviour and drone copulatory organs in Apis. Apidologie 22:581–590

    Article  Google Scholar 

  • Koeniger N, Weiss J, Maschwitz U (1979) Alarm pheromones of the sting in the genus Apis. J Insect Physiol 25:467–476

    Article  CAS  Google Scholar 

  • Koeniger G, Koeniger N, Mardan M, Otis GW, Wongsiri S (1991) Comparative anatomy of male genital organs in the genus Apis. Apidologie 22:539–552

    Article  Google Scholar 

  • Koeniger G, Koeniger N, Mardan M, Wongsiri S (1993) Variance in weight of sexuals and workers within and between four Apis species (Apis florea, Apis dorsata, Apis cerana and Apis mellifera). In: Proceedings of the 1st international conference on Asian honeybees bee mites, Bangkok, Wicwas, Cheshire, pp 104–109

    Google Scholar 

  • Koeniger N, Koeniger G, Tingek S (2010) Honey bees of Borneo – exploring the center of Apis diversity. Nat. History Publ. (Borneo) Kota Kinabalu pp 262

    Google Scholar 

  • Leelamanit W, Neelasaewee S, Boonyom R, Panyim S, Hayashi T, Yasue H, Amano K (2004) The NADH dehydrogenase genes of Apis mellifera, A. cerana, A. dorsata, A. laboriosa and A. florea: sequence comparison and genetic diversity. J Anim Genet 31:3–12

    Google Scholar 

  • Lindauer M (1956) Über die Verständigung bei indischen Bienen. Z Vgl Physiol 38:521–557 [in German]

    Article  Google Scholar 

  • Linnaeus C (1758) Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. 10th edn. Holmiae (Laurentii Salvii) [in Latin]

    Google Scholar 

  • Liu H, Beckenbach A (1992) Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol Phylogenet Evol 1:41–52

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia, New York

    Google Scholar 

  • Michener CD (2000) The bees of the world. John Hopkins University Press, Baltimore, London

    Google Scholar 

  • Moritz RFA, Hawkins CF, Crozier RH, Mackinley AG (1986) A mitochondrial DNA polymorphism in honeybees (Apis mellifera L). Experientia 42:322–324

    Article  CAS  Google Scholar 

  • Oldroyd BP, Wongsiri S (2006) Asian honey bees. Harvard University Press, Cambridge

    Google Scholar 

  • Pollmann A (1879) Wert der verschiedenen Bienenrassen und deren Varietäten, 2nd edn. Voigt, Berlin

    Google Scholar 

  • Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol 43:543–552

    Article  CAS  PubMed  Google Scholar 

  • Ruttner F (1988) Biogeography and taxonomy of honey bees. Springer, Berlin

    Google Scholar 

  • Schmiedeknecht O (1907) Die Hymenopteren Mitteleuropas. Fischer, Jena [in German]

    Google Scholar 

  • Seeley TD (1985) Honeybee ecology. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Seeley TD, Seeley RH, Akratanakul P (1982) Colony defence strategies of the honeybee in Thailand. Ecol Monogr 52:43–63

    Article  Google Scholar 

  • SenSarma M, Fuchs S, Werber C, Tautz J (2002) Worker piping triggers hissing for coordinated colony defence in the dwarf honeybee Apis florea. Zoology 105:215–223

    Article  Google Scholar 

  • Sheppard WS, Rinderer TE, Mazzoli JA, Stelzer JA, Shimanuki H (1991a) Gene flow between African-derived and European derived honey bee populations in Argentina. Nature 349:782–784

    Article  Google Scholar 

  • Sheppard WS, Soares AAE, Dejong D, Shimanuki H (1991b) Hybrid status of honey bee populations near the historic origin of Africanization in Brazil. Apidologie 22:643–652

    Article  Google Scholar 

  • Skorikov AS (1929) Eine neue Basis für eine Revision der Gattung Apis L. Rep Appl Entomol Leningrad 4:249–264 [in German]

    Google Scholar 

  • Smith F (1858) Catalogue of the hymenopterous insects collected at Sarawak, Borneo; Mount Ophir, Malacca; and at Singapore, by A.R. Wallace. Proc Linn Soc Lond 2:42–130

    Google Scholar 

  • Smith F (1861) Descriptions of new species of hymenopterous insects collected by A.R. Wallace at Celebes. Proc Linn Soc Lond 5:57–93

    Google Scholar 

  • Smith F (1865) On the species and varieties of the honey-bees belonging to the genus Apis. Ann Mag Nat Hist 15:372–380

    Google Scholar 

  • Smith F (1871) A catalogue of the aculeate Hvmenoptcra and Ichneumonidae of India and the eastern Archipelago. J Linn Soc 11:285–415

    Article  Google Scholar 

  • Smith DR (1991a) African bees in the Americas - insights from biogeography and genetics. Trends Ecol Evol 6:17–21

    Article  Google Scholar 

  • Smith DR (1991b) Mitochondrial DNA and honey bee biogeography. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 131–176

    Google Scholar 

  • Smith DR, Brown WM (1988) Polymorphisms in mitochondrial DNA of European and Africanized honeybees (Apis mellifera). Experientia 44:257–260

    Article  CAS  PubMed  Google Scholar 

  • Smith DR, Brown WM (1990) Restriction endonuclease cleavage site and length polymorphisms in mitochondrial DNA of Apis mellifera mellifera and A. m. carnica (Hymenoptera: Apidae). Ann Entomol Soc Am 83:81–88

    CAS  Google Scholar 

  • Smith DR, Palopoli MF, Taylor BR, Garnery L, Cornuet JM, Solignac M, Brown WM (1991) Geographical overlap of 2 mitochondrial genomes in Spanish honeybees (Apis mellifera iberica). J Hered 82:96–100

    CAS  PubMed  Google Scholar 

  • Spinola M (1806) Insectorum Liguriae species novae aut rariores, quas in agro Ligustico nuper detexit descripsit, et iconibus illustravit adjecto catalogo specierum auctoribus jam enumeratarum, quae in cadem regione passim occurrunt. Yves Gravier, Genuae [in Latin]

    Google Scholar 

  • Thakar CV, Deodikar GB (1966) Chromosome number in Apis florea Fab. Curr Sci 7:186

    Google Scholar 

  • Tingek S, Mardan M, Rinderer TE, Koeniger N, Koeniger G (1988) Rediscovery of Apis vechti (Maa 1953): the Saban honey bee. Apidologie 19:97–102

    Article  Google Scholar 

  • Tirgari S (1971) Biology and behavioural characteristics of the Iranian dwarf honeybee. Proc Int Beekeep Congr 23:344–345

    Google Scholar 

  • Torchio PF, Torchio DM (1975) Larvae of the Apidae (Hymenoptera: Apoidea), part 1. Apini, Apis. Agric Exp Stn. Utah State Univ Res Rep 10:1–36

    Google Scholar 

  • von Berlepsch A (1873) Die Biene und ihre Zucht mit beweglichen Wabenin Gegenden ohne Spätsommertracht. J. Schneider, Mannheim [in German]

    Google Scholar 

  • von Buttel-Reepen H (1906) Contributions to the systematics biology as well as the historical and geographical distribution of honeybees (Apis mellifica L) their variability and other Apis species. Mitt Zool Mus Berl 3:117–201 [in German]

    Google Scholar 

  • von Frisch K (1965) Tanzsprache und Orientierung der Bienen. Springer, Berlin [in German]

    Google Scholar 

  • von Siebold BTE (1856) Wahre Parthenogenese bei Schmetterlingen und Bienen. Engelmann, Leipzig [in German]

    Google Scholar 

  • Walldorf U, Hovemann BT (1990) Apis mellifera cytoplasmic elongation factor 1-alpha (EF-1-alpha) is closely related to Drosophila melanogaster EF-1-alpha. FEBS Lett 267:245–249

    Article  CAS  PubMed  Google Scholar 

  • Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol Phylogenet Evol 1:169–178

    Article  CAS  PubMed  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Wu Y, Kuang B (1987) Two species of small honeybee: a study of the genus Micrapis. Bee World 68:153–155

    Google Scholar 

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Koeniger, N., Koeniger, G., Smith, D. (2011). Phylogeny of the Genus Apis . In: Hepburn, H., Radloff, S. (eds) Honeybees of Asia. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-16422-4_2

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