The bee genera Haplomelitta and Samba (Hymenoptera : Anthophila : Melittidae): phylogeny, biogeography and host plants
Denis Michez A E , Connal Eardley B , Michael Kuhlmann C , Kim Timmermann D and Sébastien Patiny AA University of Mons, Laboratory of Zoology, Place du parc 20, 7000 Mons, Belgium.
B Agricultural Research Council, Private Bag X134, 0121 Queenswood, Pretoria, South Africa/School of Biological and Conservation Science, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg 3209, South Africa.
C Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.
D Institute of Landscape Ecology, University of Münster, Robert-Koch-Str. 26, D-48149 Münster, Germany.
E Corresponding author. Email: denis.michez@umons.ac.be
Invertebrate Systematics 24(4) 327-347 https://doi.org/10.1071/IS10008
Submitted: 3 March 2010 Accepted: 3 September 2010 Published: 13 December 2010
Abstract
Recent molecular phylogenetic data showed the Melittidae as the likely sister group to all other bees and indicated that proto-melittids could have been host-plant specialists originating in Africa. However, robust phylogenetic data at generic and species level are now needed for all melittid clades to test these hypotheses and investigate early melittid and bee evolution in general. The bee genera Haplomelitta and Samba, which comprise the former tribe Sambini (Hymenoptera : Melittidae), are revised here. The genera are endemic to the Afrotropical region, occurring in eastern and southern Africa. Previous studies hypothesised that Samba rendered Haplomelitta paraphyletic but a conclusive taxonomic decision was not proposed. By performing a comprehensive phylogenetic analysis based on five nuclear genes (28S, CAD, EF-1α (F2 copy), long-wavelength rhodopsin (opsin) and RNA polymerase II (RNAp); total 4179 bp) and morphological characters (34 characters), we here synonymise Haplomelitta with Samba. The genus is now subdivided into six subgenera containing 10 species, four of which are here described as new, namely: S. ascheri, S. gessorum, S. spinosa and S. rubigoinis. Moreover, we also considered biogeography, phenology and floral visitation data. Samba seems to have originated in southern Africa and later colonised eastern Africa. The ancestral host-plant foraging strategy was probably specialisation on one plant family (e.g. oligolectism). This result supports the hypothesis that the ancestor of bees arose in Africa and was a host-plant specialist.
Additional keywords: Afrotropical region, host specialisation, new species.
References
Alexander, B. A., and Michener, C. D. (1995). Phylogenetic studies of the families of short-tongued bees (Hymenoptera : Apoidea). The University of Kansas Science Bulletin 55, 377–424.Ascher, J. S., and Pickering, J. (2010). Bee species guide (Hymenoptera: Apoidea: Anthophila). Available at http://www.discoverlife.org/mp/20q?guide=Apoidea_species [accessed 10 November 2010].
Barbier, Y., and Rasmont, P. (2000). ‘Carto Fauna-Flora 2.0. Guide d’utilisation.’ (University Mons-Hainaut: Mons, Belgium.)
Barbier, Y., Rasmont, P., Dufrêne, M., and Sibert, J. M. (2000). ‘Data Fauna-Flora. Guide d’utilisation.’ (University Mons-Hainaut: Mons, Belgium.)
Bobe, R. (2006). The evolution of arid ecosystems in eastern Africa. Journal of Arid Environments 66, 564–584.
| The evolution of arid ecosystems in eastern Africa.Crossref | GoogleScholarGoogle Scholar |
Cameron, S. A., and Mardulyn, P. (2001). Multiple molecular data sets suggest independent origins of highly eusocial behavior in bees (Hymenoptera : Apinae). Systematic Biology 50, 194–214.
| Multiple molecular data sets suggest independent origins of highly eusocial behavior in bees (Hymenoptera : Apinae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVOgsw%3D%3D&md5=7125ffc2f032024f687b9e714e3f162aCAS | 12116928PubMed |
Cane, J. H., and Sipes, S. D. (2006). Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In ‘Specialization and Generalization in Plant-pollinator Interactions’. (Eds Waser, N. M. and Ollerton, J.) pp. 99–122. (University of Chicago Press: Chicago, IL.)
Chang, B. S. W., Ayers, D., Smith, W. C., and Pierce, N. E. (1996). Cloning of the gene encoding honeybee long-wavelength rhodopsin: a new class of insect visual pigments. Gene 173, 215–219.
| Cloning of the gene encoding honeybee long-wavelength rhodopsin: a new class of insect visual pigments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xlsl2gtLw%3D&md5=de4c51212c7170ccd594a82b3f3757e9CAS | 8964502PubMed |
Cockerell, T. D. A. (1932). Descriptions and records of bees. CXXXII. Annals & Magazine of Natural History 10, 447–458.
Cockerell, T. D. A. (1934). Descriptions and records of bees. CXLVIII. Annals & Magazine of Natural History 10, 444–456.
Danforth, B. N. (1999). Phylogeny of the bee genus Lasioglossum (Hymenoptera : Halictidae) based on mitochondrial COI sequence data. Systematic Entomology 24, 377–393.
| Phylogeny of the bee genus Lasioglossum (Hymenoptera : Halictidae) based on mitochondrial COI sequence data.Crossref | GoogleScholarGoogle Scholar |
Danforth, B. N., and Ji, S. (1998). Elongation factor-1 alpha occurs as two copies in bees: implications for phylogenetic analysis of EF-1 alpha sequences in insects. Molecular Biology and Evolution 15, 225–235.
| 1:CAS:528:DyaK1cXhtlyit74%3D&md5=2978ba50cbbc3cc191a65d6c5f35a2beCAS | 9501490PubMed |
Danforth, B. N., Fang, J., and 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. Molecular Phylogenetics and Evolution 39, 358–372.
| Analysis of family-level relationships in bees (Hymenoptera : Apiformes) using 28S and two previously unexplored nuclear genes: CAD and RNA polymerase II.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvF2msLs%3D&md5=53d587cba7b528e749957379e9ae5d8bCAS | 16412668PubMed |
Danforth, B. N., Sipes, S. D., Fang, J., and 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.
| The history of early bee diversification based on five genes plus morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFais7vF&md5=9da91c38b8a6e2b8d9c5ef87db384640CAS | 17015826PubMed |
Ebmer, A. W. (1984). Die westpaläarktischen Arten der Gattung Dufourea Lepeletier 1841 mit illustrierten Bestimmungstabellen (Insecta : Hymenoptera : Apoidea : Halictidae : Dufoureinae). Senckenbergiana Biologica 64, 313–379.
Engel, M. S. (2001). A monograph of the Baltic Amber bees and evolution of the Apoidea (Hymenoptera). Bulletin of the American Museum of Natural History 259, 1–192.
| A monograph of the Baltic Amber bees and evolution of the Apoidea (Hymenoptera).Crossref | GoogleScholarGoogle Scholar |
Friese, H. (1908). Neue Bienenarten aus Ostafrika. Deutsche Entomologische Zeitschrif 1908, 567–572.
Gess, S. K., and Gess, F. W. (2004). A comparative overview of flower visiting by non-Apis bees in the semi-arid to arid areas of southern Africa. Journal of the Kansas Entomological Society 77, 602–618.
| A comparative overview of flower visiting by non-Apis bees in the semi-arid to arid areas of southern Africa.Crossref | GoogleScholarGoogle Scholar |
Harris, R. A. (1979). A glossary of surface sculpturing. Occasional Papers in Entomology 28, 1–31.
Hines, H. M., Cameron, S. A., and Williams, P. H. (2006). Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera : Apidae : Bombus) with insights into gene utility for lower-level analysis. Invertebrate Systematics 20, 289–303.
| Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera : Apidae : Bombus) with insights into gene utility for lower-level analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFaqtr4%3D&md5=6ab79796a89660d46fbd0205c90d0de4CAS |
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=b68ec6b52214288e4845de02a156f7c7CAS | 11524383PubMed |
Kjer, K. M. (1995). Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Molecular Phylogenetics and Evolution 4, 314–330.
| Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptFShur0%3D&md5=25b5597619098358e2c7b4e289d69962CAS | 8845967PubMed |
Larkin, L. L., Neff, J. L., and Simpson, B. B. (2006). Phylogeny of the Callandrena subgenus of Andrena (Hymenoptera : Andrenidae) based on mitochondrial and nuclear DNA data: polyphyly and convergent evolution. Molecular Phylogenetics and Evolution 38, 330–343.
| Phylogeny of the Callandrena subgenus of Andrena (Hymenoptera : Andrenidae) based on mitochondrial and nuclear DNA data: polyphyly and convergent evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFCktA%3D%3D&md5=c87f2ec8dd3162d6bb7c9f30603bc2c7CAS | 16343953PubMed |
Maddison, W. P., and Maddison, D. R. (2007). Mesquite: a modular system for evolutionary analysis. Version 2.0. Available at http://mesquiteproject.org
Michener, C. D. (1981). Classification of the bee family Melittidae with a review of species of Meganomiinae. Contributions of the American Entomological Institute 18, 1–135.
Michener, C. D. (2007). ‘The bees of the world, second edition.’ (The Johns Hopkins University Press: Baltimore, USA.)
Michez, D., and Eardley, C. D. (2007). Monographic revision of the bee genus Melitta Kirby 1802 (Hymenoptera : Apoidea : Melittidae). Annales de la Société entomologique de France (n. s.) 43, 379–440.
Michez, D., and Patiny, S. (2006). Review of the bee genus Eremaphanta Popov 1940 (Hymenoptera : Melittidae), with the description of a new species. Zootaxa 1148, 47–68.
Michez, D., Terzo, M., and Rasmont, P. (2004a). Révision des espèces ouest-paléarctiques du genre Dasypoda Latreille 1802 (Hymenoptera, Apoidea, Melittidae). Linzer biologische Beiträge 36, 847–900.
Michez, D., Terzo, M., and Rasmont, P. (2004b). Phylogénie, biogéographie et choix floraux des abeilles oligolectiques du genre Dasypoda Latreille 1802 (Hymenoptera, Apoidea, Melittidae). Annales de la Société entomologique de France (n. s.) 40, 421–435.
Michez, D., Eardley, C. D., Kuhlmann, M., and Patiny, S. (2007). Revision of the bee genus Capicola (Hymenoptera : Apoidea : Melittidae) distributed in the Southwest of Africa. European Journal of Entomology 104, 311–340.
Michez, D., Patiny, S., Rasmont, P., Timmermann, K., and Vereecken, N. (2008). Phylogeny and host-plant evolution in Melittidae s.l. (Hymenoptera : Apoidea). Apidologie 39, 146–162.
| Phylogeny and host-plant evolution in Melittidae s.l. (Hymenoptera : Apoidea).Crossref | GoogleScholarGoogle Scholar |
Michez, D., Patiny, S., and Danforth, B. N. (2009). Phylogeny of the bee family Melittidae (Hymenoptera : Anthophila) based on combined molecular and morphological data. Systematic Entomology 34, 574–597.
| Phylogeny of the bee family Melittidae (Hymenoptera : Anthophila) based on combined molecular and morphological data.Crossref | GoogleScholarGoogle Scholar |
Müller, A. (1996). Host-plant specialization in Western Palearctic anthidiine bees (Hymenoptera : Apoidea : Megachilidae). Ecological Monographs 66, 235–257.
| Host-plant specialization in Western Palearctic anthidiine bees (Hymenoptera : Apoidea : Megachilidae).Crossref | GoogleScholarGoogle Scholar |
Müller, A., and Kuhlmann, M. (2008). Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera : Colletidae) : the Asteraceae paradox. Biological Journal of the Linnean Society. Linnean Society of London 95, 719–733.
| Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera : Colletidae) : the Asteraceae paradox.Crossref | GoogleScholarGoogle Scholar |
Nixon, K. C. (2002). ‘WinClada version 1.00.08.’ (Published by the author: Ithaca, NY, USA.)
Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author.
Patiny, S. (2004). Analysis of the Panurginae distribution in West-Africa and report of new data for Meliturgula scriptifrons (Walker 1871) in Mali (Hymenoptera, Apoidea, Andrenidae). Linzer biologische Beiträge 36, 901–906.
Patiny, S., and Michez, D. (2007). Biogeography of bees (Hymenoptera, Apoidea) in Sahara and the Arabian deserts. Insect Systematics & Evolution 38, 19–34.
Patiny, S., Michez, D., and Danforth, B. N. (2008). Phylogenetic relationships and host-plant evolution within the basal clade of Halictidae (Hymenoptera, Apoidea). Cladistics 24, 255–269.
| Phylogenetic relationships and host-plant evolution within the basal clade of Halictidae (Hymenoptera, Apoidea).Crossref | GoogleScholarGoogle Scholar |
Pauly, A. (1990). ‘Classification des Nomiinae Africains (Hymenoptera, Apoidea, Halictidae)’. (Musée royal de l’Afrique centrale: Tervuren, Belgium.)
Pesenko, Y. A., and Pauly, A. (2005). Monograph of the bees of the subfamily Nomioidinae (Hymenoptera : Apoidea) of Africa (excluding Madagascar). Annales de la Société entomologique de France (n.s.) 41, 129–236.
Posada, D., and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=f75bd0275a00f02a5b59a1df4084c599CAS | 9918953PubMed |
Praz, C. J., Müller, A., Danforth, B. N., Griswold, T. L., Widmer, A., and Dorn, S. (2008). Phylogeny and biogeography of bees of the tribe Osmiini (Hymenoptera : Megachilidae). Molecular Phylogenetics and Evolution 49, 185–197.
| Phylogeny and biogeography of bees of the tribe Osmiini (Hymenoptera : Megachilidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOltrzJ&md5=a076a977350b4aa7ad74e4c7ee795a8fCAS | 18675365PubMed |
Roig-Alsina, A., and Michener, C. D. (1993). Studies of the phylogeny and classification of long-tongued bees (Hymenoptera : Apoidea). The University of Kansas Science Bulletin 55, 123–173.
Rozen, J. G. (1974). The biology of two African melittid bees (Hymenoptera, Apoidea). New York Entomological Society 82, 6–13.
Rozen, J. G., and McGingley, R. J. (1974). Phylogeny and systematics of Melittidae based on the mature larvae (Insecta, Hymenoptera, Apoidea). American Museum Novitates 2545, 1–31.
Saghai-Maroof, M. A., Soliman, K. M., Jorgensen, R. A., and Allard, R. W. (1984). Ribosomal DNA spacer-length polymorphism in barley. Proceedings of the National Academy of Sciences of the United States of America 81, 8014–8018.
| Ribosomal DNA spacer-length polymorphism in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXptlWitg%3D%3D&md5=f49d2bf6898b5fc58ef51ec622894dbcCAS | 6096873PubMed |
Sipes, S. D., and Tepedino, V. (2005). Pollen-host specificity and evolutionary patterns of host switching in a clade of specialist bees (Apoidea : Diadasia). Biological Journal of the Linnean Society. Linnean Society of London 86, 487–505.
| Pollen-host specificity and evolutionary patterns of host switching in a clade of specialist bees (Apoidea : Diadasia).Crossref | GoogleScholarGoogle Scholar |
Stage, G. I. (1966). Biology and systematics of the American species of the genus Hesperapis Cockerell. (Ph-D, University of California: Berkley, USA.)
Stevens, P. F. (2001). Angiosperm Phylogeny Website. Version 9, March 2010. http://www.mobot.org/MOBOT/research/APweb
Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Ver.4b10.’ (Sinauer Associates: Sunderland, MA.)
Westrich, P. (1990). ‘Die Wildbienen Baden-Württembergs.’ (Ulmer Verlag: Stuttgart, Germany.)
Westrich, P., and Schmidt, K. (1986). Methoden und Anwendungsgebiete der Pollenanalyse bei Wildbienen (Hymenoptera, Apoidea). Linzer biologische Beiträge 18, 341–360.