Morphological phylogeny of Megachilini and the evolution of leaf-cutter behavior in bees (Hymenoptera: Megachilidae)

Evolution of leaf-cutter behavior in bees

Authors

  • Victor H. Gonzalez University of Kansas
  • Grey T Gustafson University of Kansas
  • Michael S Engel University of Kansas & American Museum of Natural History

DOI:

https://doi.org/10.17161/jom.v0i85.11541

Abstract

A unique feature among bees is the ability of some species of Megachile Latreille s.l. to cut and process fresh leaves for nest construction. The presence of a razor between the female mandibular teeth (interdental laminae) to facilitate leaf-cutting (LC) is a morphological novelty that might have triggered a subsequent diversification in this group. However, we have a limited understanding of the phylogeny of this group despite the large number of described species and the origins and patterns of variations of this mandibular structure are unknown. Herein, using a cladistic analysis of adult external morphological characters, we explored the relationships of all genera of Megachilini and the more than 50 subgenera of Megachile s.l. We coded 272 characters for 8 outgroups and 114 ingroup species. Depending on the weighting scheme (equal or implied weighting), our parsimony analyses suggested the monophyly of Megachile s.l. and that either Noteriades Cockerell or the clade Coelioxys Latreille + Radoszkowskiana Popov is the extant sister group of all other Megachilini. In addition, we conducted Bayesian total-evidence tip-dating analyses to examine other possible hypotheses of relationships and patterns of variation of the interdental lamina. Our analyses suggest that interdental laminae developed asynchronicaly from two different structures in the mandible, and differ in their phenotypic plasticity. Character correlation tests using phylogenetic pairwise comparisons indicated that the presence of interdental lamina is not associated with head size, mandible size and shape, and pubescence on the adductor interspace. We discuss the implications of our findings for the classification of Megachilini and the development of novel evolutionary, ecological, and functional hypotheses on this behavior. New taxa established are Pseudoheriadini Gonzalez & Engel, new tribe, Ochreriadini Gonzalez & Engel, new tribe, Cremnomegachile Gonzalez & Engel, new genus, Rozenapis Gonzalez & Engel, new genus, and Saucrochile Gonzalez & Engel, new genus, along with the following new combinations: Cremnomegachile dolichosoma (Benoist), new combination, Rozenapis ignita (Smith), new combination, and Saucrochile heriadiformis (Smith), new combination.

Metrics

Metrics Loading ...

References

Agnarsson, I., & J.A. Coddington. 2008. Quantitative tests of primary homology. Cladistics 24(1): 51–61.

Almeida, E.A.B. 2008. Revised species checklist of the Paracolletinae (Hymenoptera, Colletidae) of the Australian Region, with the description of new taxa. Zootaxa 1891: 1–24.

Almeida, E.A.B, & B.N. Danforth. 2009. Phylogeny of colletid bees (Hymenoptera: Colletidae) inferred from four nuclear genes. Molecular Phylogenetics and Evolution 50(2): 290–309.

Arcila, D., R.A. Pyron, J.C. Tyler, G. Ortí, & R. Betancur-R. 2015. An evaluation of fossil tip-dating versus node-age calibration in tetraodontiform fishes (Teleostei: Percomorphaceae). Molecular Phylogenetics and Evolution 82(A): 131–145.

Ascher, J.S., & J. Pickering. 2018. Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). [http://www.discoverlife.org/mp/20q?guide=Apoidea_species; last accessed 31 March 2018].

Astrin, J.J., X. Zhou, & B. Misof. 2013. The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. ZooKeys 365: 67–70.

Baker, D.B., & M.S. Engel. 2006. A new subgenus of Megachile from Borneo with arolia (Hymenoptera: Megachilidae). American Museum Novitates 3505: 1–12.

Banaszak, J., & L. Romasenko. 1998. Megachilid Bees of Europe (Hymenoptera, Apoidea, Megachilidae). Pedagogical University of Bydgoszcz; Bydgoszcz, Poland; 239 pp.

Benoist, R. 1962. Nouvelles espèces d’Apides malgaches [Hym.]. Bulletin de la Société Entomologique de France 67: 214–223.

Blaimer, B.B., M.W. Lloyd, W.X. Guillory, & S.G. Brady. 2016. Sequence capture and phylogenetic utility of genomic ultraconserved elements obtained from pinned insect specimens. PLoS ONE 11(8): [1–20] e0161531.

Brauns, H. 1926. V. Nachrag zu “Friese, Bienen Afrikas”. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Tiere 52: 187–230, +pl. 5.

Camargo, R.S., I.N. Hastenreiter, L.C. Forti, & J.F.S. Lopes. 2015. Relationship between mandible morphology and leaf preference in leaf-cutting ants (Hymenoptera: Formicidae). Revista Colombiana de Entomología 41(2): 241–244.

Cane, J.H. 2004. Exotic nonsocial bees (Hymenoptera: Apiformes) in North America: Ecological implications. In: Strickler, K.L., & J.H. Cane (Eds.), For Non-native Crops, Whence Pollinators of the Future?: 113–116. Thomas Say Publications in Entomology, Entomological Society of America; Lanham, MD; 204 pp.

Cardinal, S., & B.N. Danforth. 2013. Bees diversified in the age of eudicots. Proceedings of the Royal Society B (Biological Sciences) 280(1755): [1–9] 20122686.

Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17(4): 540–552.

Cockerell, T.D.A. 1907. Descriptions and records of bees—XV. Annals and Magazine of Natural History, Series 7 20(115): 59–68.

Cockerell, T.D.A. 1922. Descriptions and records of bees—XCV. Annals and Magazine of Natural History, Series 9 10(57): 265–269.

Dalla Torre, C.G., de [K.W., von]. 1896. Catalogus Hymenopterorum Hucusque Descriptorum Systematicus et Synonymicus. Vol. 10: Apidae (Anthophila). Engelmann; Lipsiae [Leipzig], Germany; viii+643 pp.

Dos Reis, M., & Z. Yang. 2013. The unbearable uncertainty of Bayesian divergence time estimation. Journal of Systematics and Evolution 51(1): 30–43.

Duckworth, R.A. 2009. The role of behavior in evolution: A search for mechanism. Evolutionary Ecology 23(4): 513–531.

Durante, S., & N. Cabrera. 2009. Cladistic analysis of Megachile (Chrysosarus) Mitchell and revalidation of Megachile (Dactylomegachile) Mitchell (Hymenoptera, Megachilidae). Zootaxa 2284: 48–62.

Durante, S.P., & A.H. Abrahamovich. 2006. Redescription of Chaetochile as subgenus of Megachile (Hymenoptera, Megachilidae). Transactions of the American Entomological Society 132(1): 103–109.

Eardley, C. 2012. A taxonomic revision of the southern African species of dauber bees in the genus Megachile Latreille (Apoidea: Megachilidae). Zootaxa 3460: 1–139.

Eardley, C. 2013. A taxonomic revision of the southern African leaf-cutter bees, Megachile Latreille sensu stricto and Heriadopsis Cockerell (Hymenoptera: Apoidea: Megachilidae). Zootaxa 3601(1): 1–133.

Eickwort, G.C., R.W. Matthews, & J. Carpenter. 1981. Observations on the nesting behavior of Megachile rubi and M. texana with a discussion of the significance of soil nesting in the evolution of megachilid bees (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 54(3): 557–570.

Engel, M.S. 1999. Megachile glaesaria, the first megachilid bee fossil from amber (Hymenoptera: Megachilidae). American Museum Novitates 3276: 1–13.

Engel, M.S. 2000. A new interpretation of the oldest fossil bee (Hymenoptera: Apidae). American Museum Novitates 3296: 1–11.

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.

Engel, M.S. 2005. Family-group names for bees (Hymenoptera: Apoidea). American Museum Novitates 3476: 1–33.

Engel, M.S. 2007. Ferdinand Meunier and the destruction of his Hymenoptera collections. Entomologist’s Gazette 58(3): 183–184.

Engel, M.S. 2017. Replacement names for bees in the tribe Megachilini (Hymenoptera: Megachilidae). Journal of Melittology 70: 1–5.

Engel, M.S., & D.B. Baker. 2006. A remarkable new leaf-cutter bee from Thailand (Hymenoptera: Megachilidae). Beiträge zur Entomologie 56(1): 69–74.

Engel, M.S., & V.H. Gonzalez. 2011. Alocanthedon, a new subgenus of Chalicodoma from Southeast Asia (Hymenoptera, Megachilidae). ZooKeys 101: 51–80.

Engel, M.S, & E.E. Perkovsky. 2006. An Eocene bee in Rovno amber, Ukraine (Hymenoptera: Megachilidae). American Museum Novitates 3506: 1–12.

Friese, H. 1898. Species aliquot novæ vel minus cognitæ generis Megachile Latr. (et Chalicodoma Lep.). Természetrajzi Füzetek 21(1–2): 198–202.

Friese, H. 1899. Die Bienen Europa’s (Apidae europaeae) nach ihren Gattungen, Arten und Varietäten auf vergleichend morphologisch-biologischer Grundlage. Theil V: Solitäre Apiden: Genus Lithurgus, Genus Megachile (Chalicodoma). C. Lampe; Innsbruck, Austria; 228 pp.

Friese, H. 1909. Die Bienen Afrikas nach dem Stande unserer heutigen Kenntnis. In: Schultze, L. (Ed.), Zoologische und anthropologische Ergebnisse einer Forschungsreise im westlichen und zentralen Südafrika ausgefuhrt in den Jahren 1903–1905 mit Unterstützung der Kgl. [Königlichen] Preussischen Akademie der Wissenschaften zu Berlin [Band 2, Lieferung 1, X Insecta (3te Serie): Jenaische Denkschriften 14]: 83–476, pls. ix–x. Gustav Fischer; Jena, Germany.

Friese, H. 1911a. Apidae I. Megachilinae. In: Schulze, F.E. (Ed.), Das Tierreich: Eine Zusammenstellung und Kennezeichnung der rezenten Tierformen. Lieferung 28: Hymenoptera: v–xxvi+1–440. Friedländer und Sohn; Berlin, Germany; xxvi+440 pp.

Friese, H. 1911b. Nachtrag zu “Bienen Afrikas”. Zoologische Jahrbücher, Abteilung für Systematik, Geographie und Biologie der Tiere 30(6): 651–670.

Gerstaecker, A. 1869. Beiträge zur näheren Kenntniss einiger Bienen-Gattugen. Entomologische Zeitung 30(4–6): 315–367.

Goloboff, P.A. 1993. Estimating character weights during tree search. Cladistics 9(1): 83–91.

Goloboff, P.A. 2008. Calculating SPR distances between trees. Cladistics 24(4): 591–597.

Goloboff, P.A., J.S. Farris, & K. Nixon. 2003a. T.N.T.: Tree analysis using new technology. Program and documentation. [http://www.lillo.org.ar/phylogeny/tnt/; last accessed 1 December 2018].

Goloboff, P.A., J.S. Farris, M. Källersjö, B. Oxelman, M.J. Ramírez, & C.A. Szumik. 2003b. Improvements to resampling measures of group support. Cladistics 19(4): 324–332.

Goloboff, P.A., A. Torres, & J.S. Arias. 2018. Weighted parsimony outperforms other methods of phylogenetic inference under models appropiate for morphology. Cladistics 34(4): 407–437.

Gonzalez, V.H. 2008. Phylogeny and classification of the bee tribe Megachilini (Hymenoptera: Apoidea, Megachilidae), with emphasis on the genus Megachile. Doctoral dissertation, University of Kansas; Lawrence, KS; 274 pp.

Gonzalez, V.H. 2013. Taxonomic comments on Megachile subgenus Chrysosarus (Hymenoptera: Megachilidae). Journal of Melittology 5: 1–6.

Gonzalez, V.H., & M.S. Engel. 2012. African and Southeast Asian Chalicodoma (Hymenoptera: Megachilidae): New subgenus, new species, and notes on the composition of Pseudomegachile and Largella. Annales Zoologici 62(4): 599–617.

Gonzalez, V.H., & T. Griswold. 2013. Wool carder bees of the genus Anthidium in the Western Hemisphere (Hymenoptera: Megachilidae): Diversity, host plant associations, phylogeny, and biogeography. Zoological Journal of the Linnean Society 168(2): 221–425.

Gonzalez, V.H., M.S. Engel, & I.A. Hinojosa-Díaz. 2010. A new species of Megachile from Pakistan, with taxonomic notes on the subgenus Eutricharaea (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 83(1): 58–67.

Gonzalez, V.H., T. Griswold, C.J. Praz, & B.N. Danforth. 2012. Phylogeny of the bee family Megachilidae (Hymenoptera: Apoidea) based on adult morphology. Systematic Entomology 37(2): 261‒286.

Gonzalez, V.H., T. Griswold, & M.S. Engel. 2013. Obtaining a better taxonomic understanding of native bees: Where do we start? Systematic Entomology 38(4): 645–653.

Gonzalez, V.H., T.L. Griswold, & M.S. Engel. 2018. South American leaf-cutter bees (genus Megachile) of the subgenera Rhyssomegachile and Zonomegachile, with two new subgenera (Hymenoptera: Megachilidae). Bulletin of the American Museum of Natural History 425: 1–73.

Griswold, T.L. 1985. A generic and subgeneric revision of the Heriades genus-group (Hymenoptera: Megachilidae). Doctoral dissertation, Utah State University; Logan, UT; xii+165 pp.

Griswold, T.L. 1994. A review of Ochreriades (Hymenoptera: Megachilidae: Osmiini). Pan-Pacific Entomologist 70(4): 318‒321.

Griswold, T., & V.H. Gonzalez. 2011. New species of the Eastern Hemisphere genera Afroheriades and Noteriades (Hymenoptera, Megachilidae), with keys to species of the former. ZooKeys 159: 65–80.

Heath, T.A., J.P. Huelsenbeck, & T. Stadler. 2014. The fossilized birth-death process for coherent calibration of divergence-time estimates. Proceedings of the National Academy of Sciences, U.S.A. 111(29): E2957–E2966.

Horne, M. 1995. Leaf area and toughness: Effects on nesting material preference of Megachile rotundata (Hymenoptera: Megachilidae). Annals of the Entomological Society of America 88(6): 868–875.

Huelsenbeck, J.P., B. Larget, & M.E. Alfaro. 2004. Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molecular Biology and Evolution 21(6): 1123–1133.

Kalyaanamoorthy, S., B.Q. Minh, T.K.F. Wong, A. von Haeseler, & L.S. Jermiin. 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589.

Kambli, S.S., M.S. Aiswarya, K. Manoj, S. Varma, G. Asha, T.P. Rajesh, & P.A. Sinu. 2017. Leaf foraging sources of leafcutter bees in a tropical environment: Implications for conservation. Apidologie 48(4): 473–482.

Katayama, E. 2004. Nesting biology of Megachile pseudomonticola Hedicke, with special reference to the manipulation and adhesion of leaf pieces used for cell construction. Japanese Journal of Entomology 7(1): 1–10. [In Japanese].

Katoh, K., & H. Toh. 2008. Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9: [1–13] 212.

Katoh, K., & D.M. Standley. 2013. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780.

Kim, J. 1992. Nest dimensions of two leaf-cutter bees (Hymenoptera: Megachilidae). Annals of the Entomological Society of America 85(1): 85–90.

Kim, Y.-H., & K.-J. Ahn. 2016. Phylogeny of the Homalotina (Coleoptera: Staphylinidae: Aleocharinae) based on morphology. Systematic Entomology 41(2): 323–338.

King, J. 1994. The bee family Megachilidae (Hymenoptera: Apoidea) in Australia. I. Morphology of the genus Chalicodoma Lepeletier, and a revision of the subgenus Hackeriapis Cockerell. Invertebrate Taxonomy 8(6): 1373–1419.

Krombein, K.V., & B.B. Norden. 1995. Notes on the behavior and taxonomy of Megachile (Xeromegachile) brimleyi Mitchell and its probable cleptoparasite, Coelioxys (Xerocoelioxys) galactiae Mitchell (Hymenoptera: Megachilidae). Proceedings of the Entomological Society of Washington 97(1): 86–89.

Labandeira, C.C. 2002. Paleobiology of middle Eocene plant-insect associations from the Pacific Northwest: A preliminary report. Rocky Mountain Geology 37(1): 31–59.

Lanfear, R., B. Calcott, S.Y. Ho, & S. Guindon. 2012. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analysis. Molecular Biology and Evolution 29(6): 1695–1701.

Lanfear, R., P.B. Frandsen, A.M. Wright, T. Senfeld, & B. Calcott. 2016. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34(3): 772–773.

Lapiedra, O., D. Sol, S. Carranza, & J.M. Beaulieu. 2013. Behavioural changes and the adaptive diversification of pigeons and doves. Proceedings of the Royal Society B (Biological Sciences) 280(1755): [1–9] 20122893.

Laroca, S., Corbella, E., Varela, G. 1992. Biologia de Dactylomegachile affabilis (Hymenoptera, Apoidea): I. Descrição do ninho. Acta Biológica Paranaense 21(1–5): 23–29.

Latreille, P.A. 1802. Histoire naturelle des fourmis, et recueil de memoires et d’observations sur les abeilles, les araignées, les faucheurs, et autres insectes. Crapelet; Paris, France; xvi+445 pp.

Lepeletier de Saint Fargeau, A.L.M. 1841. Histoire Naturelle des Insectes—Hyménoptères. Tome Second. Roret; Paris, France; 680 pp.

Litman, J.R., B.N. Danforth, C.D. Eardley, & C.J. Praz. 2011. Why do leafcutter bees cut leaves? New insights into the early evolution of bees. Proceedings of the Royal Society B (Biological Sciences) 278(1724): 3593–3600.

MacIvor, J.S. 2016. DNA barcoding to identify leaf preference of leafcutting bees. Royal Society Open Science 3(3): [1–13] 150623.

Maddison, W.P., & D.R. Maddison. 2018. Mesquite: A modular system for evolutionary analysis. Version 3.40. [http://mesquiteproject.org; last accessed on 1 March 2018]

Maeta, Y. 2005. Substitutional use of the two species of indigenous megachilids bees for seed production of alfalfa (Hymenoptera, Megachilidae). Chugoku Kontyu 19: 27–36. [In Japanese].

Marín, M.A., C. Peña, S.I. Uribe, & A.V.L. Freitas. 2017. Morphology agrees with molecular data: Phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae). Systematic Entomology 42(4): 768–785.

Mavromoustakis, G.A. 1956. On the bees (Hymenoptera, Apoidea) of Siria [sic], Part I. Eos 32: 215–229.

Medler, J.T. 1965. A note on Megachile mendica Cresson in trap-nests in Wisconsin (Hymenoptera: Megachilidae). Proceedings of the Entomological Society of Washington 67(2): 113–116.

Meunier, F. 1888. Megachillidae [sic]. Naturalista Siciliano: Organo della Società Siciliana di Scienze Naturali 7(6): 152.

Michener, C.D. 1944. Comparative external morphology, phylogeny, and a classification of the bees (Hymenoptera). Bulletin of the American Museum of Natural History 82(6): 153–326.

Michener, C.D. 1953. The biology of a leafcutter bee (Megachile brevis) and its associates. University of Kansas Science Bulletin 35(16): 1659–1748.

Michener, C.D. 1962. Observations on the classification of the bees commonly placed in the genus Megachile (Hymenoptera: Apoidea). Journal of the New York Entomological Society 70(1): 17–29.

Michener, C.D. 1965. A classification of the bees of the Australian and South Pacific regions. Bulletin of the American Museum of Natural History 130: 1–362.

Michener, C.D. 1983. The classification of the Lithurginae (Hymenoptera: Megachilidae). Pan-Pacific Entomologist 59(1–4): 176–187.

Michener, C.D. 1996. The first South American dioxyine bee and a generic review of the tribe Dioxyini (Hymenoptera, Megachilidae). Memoirs of the Entomological Society of Washington 17: 142–152.

Michener, C.D. 2000. The Bees of the World. Johns Hopkins University Press; Baltimore, MD; xiv+[i]+913 pp., +16 pls.

Michener, C.D. 2007. The Bees of the World [2nd Edition]. Johns Hopkins University Press; Baltimore, MD; xvi+[i]+953 pp., +20 pls.

Michener, C.D., & A. Fraser. 1978. A comparative anatomical study of mandibular structure in bees. University of Kansas Science Bulletin 51(14): 463–482.

Michez, D., M. Vanderplanck, & M.S. Engel. 2012. Fossil bees and their plant associates. In: Patiny, S. (Ed.), Evolution of Plant-Pollinator Relationships: 103–164. Cambridge University Press; Cambridge, UK; xv+477+[6] pp.

Minckley, R.L. 1998. A cladistic analysis and classification of the subgenera and genera of the large carpenter bees, tribe Xylocopini (Hymenoptera: Apidae). Scientific Papers, Natural History Museum, University of Kansas 9: 1–47.

Minh, B.Q., M.A.T. Nguyen, & A. von Haeseler. 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30(5): 1188–1195.

Mirande, J.M. 2009. Weighted parsimony phylogeny of the family Characidae (Teleostei: Characiformes). Cladistics 25(6): 574–613.

Mitchell, T.B. 1924. New megachilid bees. Journal of the Elisha Mitchell Scientific Society 40(3–4): 154–165.

Mitchell, T.B. 1933 [1934]. A revision of the genus Megachile in the Nearctic region. Part I. Classification and descriptions of new species (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 59(4): 295–361, +2 pls. [pls. xx–xxi].

Mitchell, T.B. 1935a. A revision of the genus Megachile in the Nearctic region. Part II. Morphology of the male sternites and genital armature and the taxonomy of the subgenera Litomegachile, Neomegachile and Cressoniella (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 61(1): 1–44, +1 pl. [pl. i].

Mitchell, T.B. 1935b. A revision of the genus Megachile in the Nearctic region. Part III. Taxonomy of subgenera Anthemois and Delomegachile (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 61(3): 155–205, +2 pls. [pls. viii–ix].

Mitchell, T.B. 1936a. A revision of the genus Megachile in the Nearctic region. Part IV. Taxonomy of subgenera Xanthosarus, Phaenosarus, Megachiloides and Derotropis (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 62(2): 117–166, +4 pls. [pls. viii–xi].

Mitchell, T.B. 1936b [1937]. A revision of the genus Megachile in the Nearctic Region. Part V. Taxonomy of subgenus Xeromegachile (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 62(4): 323–382, +5 pls. [pls. xxii–xxvi].

Mitchell, T.B. 1937a. A revision of the genus Megachile in the Nearctic Region. Part VI. Taxonomy of subgenera Argyropile, Leptorachis, Pseudocentron, Acentron and Melanosarus (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 63(1): 45–83, +2 pls. [pls. v–vi].

Mitchell, T.B. 1937b. A revision of the genus Megachile in the Nearctic Region. Part VII. Taxonomy of the subgenus Sayapis (Hymenoptera: Megachilidae). Transactions of the American Entomological Society 63(2): 175–206, +2 pls. [pls. xii–xiii].

Mitchell, T.B. 1937c. A revision of the genus Megachile in the Nearctic region. Part VIII. Taxonomy of the subgenus Chelostomoides, addenda and index (Hymenoptera: Megachilidae).Transactions of the American Entomological Society 63(4): 381–425, +4 pls. [pls. xxvi–xxix].

Mitchell, T.B. 1943. On the classification of neotropical Megachile (Hymenoptera: Megachilidae). Annals of the Entomological Society of America 36(4): 656–671.

Mitchell, T.B. 1980. A Generic Revision of the Megachiline Bees of the Western Hemisphere. North Carolina State University; Raleigh, NC; [ii]+95 pp.

Moure, J.S., G.A.R. Melo, & A. DalMolin. 2007. Megachilini Latreille, 1802. In: Moure, J.S., D. Urban, & G.A.R. Melo (Eds.), Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region: 917–1001. Sociedade Brasileira de Entomologia; Curitiba, Brazil; xiv+1058 pp.

Nguyen, L.-T., H.A. Schmidt, A. von Haeseler, & B.Q. Minh. 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–274.

Nixon, K.C. 1999. WINCLADA, version 0.9.99tuc.13, beta. Cornell University; Ithaca, NY.

O’Reilly, J.E., & P.C.J. Donoghue. 2016. Tips and nodes are complementary not competing approaches to the calibration of molecular clocks. Biology Letters 12(4): 637–650.

O’Reilly, J.E., M. dos Reis, & P.C.J. Donoghue. 2015. Dating tips for divergence-time estimation. Trends in Genetics 31(11): 637–650.

Ornosa, C., F.J. Ortiz-Sánchez, & F. Torres. 2007. Catálogo de los Megachilidae del Mediterráneo occidental (Hymenoptera, Apoidea). II. Lithurgini y Megachilini. Graellsia 63(1): 111–134.

Orr, M.C., Z.M. Portman, & T. Griswold. 2015. Megachile (Megachile) montivaga (Hymenoptera: Megachilidae) nesting in live thistle (Asteraceae: Cirsium). Journal of Melittology 48: 1–6.

Packer, L. 2003. Comparative morphology of the skeletal parts of the sting apparatus of bees (Hymenoptera: Apoidea). Zoological Journal of the Linnean Society 138(1): 1–38.

Packer, L. 2004. Morphological variation in the gastral sterna of female Apoidea (Insecta: Hymenoptera). Canadian Journal of Zoology 82(1): 130–152.

Pasteels, J.J. 1965. Revision des Megachilidae (Hymenoptera Apoidea) de l’Afrique Noire. I. Les genres Creightoniella [sic], Chalicodoma et Megachile (s. str.). Koninklijk Museum voor Midden-Afrika, Tervuren, België, Annalen, Reeks In-8°, Zoologische Wetenschappen 137: ix+1–579.

Pasteels, J.J., & J.M. Pasteels. 1971. Etude au microscope électronique à balayage des plages glandulaires tergales chez des espèces du genre Megachile (Hymenoptera, Apoïda, Megachilidae). Comptes Rendus de l’Académie des Sciences, Série D (Sciences Naturelles) 273: 1481–1483.

Pauly, A., R.W. Brooks, A. Nilsson, Y.A. Pesenko, C.D. Eardley, M. Terzo, T. Griswold, M. Schwarz, S. Patiny, J. Munzinger, & Y. Barbier. 2001. Hymenoptera Apoidea de Madagascar et des îles voisines. Koninklijk Museum voor Midden-Afrika, Tervuren, België, Annalen Zoologische Wetenschappen 286: 1–390, +16 pls.

Peters, D.S. 1970. Pseudoheriades n. gen., Afroheriades n. subgen., Pseudoheriades primus n. sp., neue Formen aus der Familie Megachilidae (Hymenoptera: Apoidea). Entomologische Zeitschrift 80(16): 153–160.

Pitts-Singer, T.L., & J.H. Cane. 2011. The alfalfa leafcutting bee, Megachile rotundata: The world’s most intensively managed solitary bee. Annual Review of Entomology 56: 221–237.

Praz, C.J. 2017. Subgeneric classification and biology of leafcutter and dauber bees (genus Megachile Latreille) of the western Palearctic (Hymenoptera, Apoidea, Megachilidae). Journal of Hymenoptera Research 55: 1–54.

Praz, C.J., A. Müller, B.N. Danforth, T. Griswold, A. Widmer, & S. Dorn. 2008. Phylogeny and biogeography of bees of the tribe Osmiini (Hymenoptera: Megachilidae). Molecular Phylogenetics and Evolution 49(1): 185–197.

Provancher, L. 1882. Faune Canadienne. Les Insectes—Hyménoptères. Naturaliste Canadien 13(152): 225–242.

Pyron, R.A. 2011. Divergence time estimation using fossils as terminal taxa and the origins of Lissamphibia. Systematic Biology 60(4): 446–481.

Radoszkowsky, O.B. 1874. Supplément indispensable à l’article publié par M. Gerstaecker en 1869, sur quelques genres d’Hyménoptères (Suite). Bulletin de la Société Impériale des Naturalistes de Moscou 46(3): 133-151, +1 pl.

Rambaut, A., M. Suchard, D. Xie, & A.J. Drummon. 2014. Tracer v1.6 [http://tree.bio.ed.ac.uk/software/tracer/; last accessed on 1 March 2018].

Rasmussen, C., A.L. Carríon, R. Castro-Urgal, S. Chamorro, V.H. Gonzalez, T.L. Griswold, H.W. Herrera, C.K. McMullen, J.M. Olesen, & A. Traveset. 2012. Megachile timberlakei Cockerell (Hymenoptera: Megachilidae): Yet another adventive bee species to the Galápagos Archipelago. Pan-Pacific Entomologist 88(1): 98‒102.

Raw, A. 2006. A new subgenus and three new species of leafcutter bees, Megachile (Austrosarus) (Hymenoptera, Megachilidae) from central Brazil. Zootaxa 1228(1): 25–34.

Reemer, M. 2012. Unravelling a hotchpotch: Phylogeny and classification of the Microdontinae (Diptera: Syrphidae). Doctoral dissertation, Leiden University; Leiden, The Netherlands; 384 pp.

Reemer, M., & G. Ståhls. 2013. Phylogenetic relationships of Microdontinae (Diptera: Syrphidae) based on molecular and morphological characters. Systematic Entomology 38(4): 661–688.

Remane, A. 1952. Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. Geest and Portig; Leipzig, Germany; vi+400 pp.

Rieppel, O., & M. Kearney. 2002. Similarity. Biological Journal of the Linnean Society 75(1): 59–82.

Robertson, C. 1901. Some new or little known bees. Canadian Entomologist 33(8): 229–231.

Robertson, C. 1903. Synopsis of Megachilidae and Bombinae. Transactions of the American Entomological Society 29(2): 163–178.

Rocha Filho, L.C.D., & L. Packer. 2017. Phylogeny of the cleptoparasitic Megachilini genera Coelioxys and Radoszkowskiana, with the description of six new subgenera in Coelioxys (Hymenoptera: Megachilidae). Zoological Journal of the Linnean Society 180(2): 354–413.

Roig-Alsina, A., & C.D. Michener. 1993. Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apoidea). University of Kansas Science Bulletin 55(4): 123–162.

Ronquist, F., S. Klopfstein, L. Vilhelmsen, S. Schulmeister, D.L. Murray, & A.P. Rasnitsyn. 2012a. A total-evidence approach to dating with fossils, applied to the early radiation of Hymenoptera. Systematic Biology 61(6): 973–999.

Ronquist, F., M. Teslenko, P. van der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard, & J.P. Huelsenbeck. 2012b. MrBayes version 3.2: Efficient Bayesian phylogenetic inference and model choice, across a large model space. Systematic Biology 61(3): 539–542.

Rozen, J.G., Jr., & S.M. Kamel. 2007. Investigations on the biologies and immature stages of the cleptoparasitic bee genera Radoszkowskiana and Coelioxys and their Megachile host (Hymenoptera: Apoidea: Megachilidae: Megachilini). American Museum Novitates 3573: 1–43.

Rozen, J.G., Jr., H. Özbek, J.S. Ascher, C. Sedivy, C. Praz, A. Monfared, & A. Müller. 2010. Nest, petal usage, floral preferences, and immatures of Osmia (Ozbekosmia) avosetta (Megachilidae: Megachilinae: Osmiini), including biological comparisons with other osmiine bees. American Museum Novitates 3680: 1–22.

Rozen, J.G., Jr., J.S. Ascher, S.M. Kamel, & K.M. Mohamed. 2016. Larval diversity in the bee genus Megachile (Hymenoptera: Apoidea: Megachilidae). American Museum Novitates 3863: 1–16.

Sarzetti, L.C., C.C. Labandeira, & J.F. Genise. 2008. A leafcutter bee trace fossil from the middle Eocene of Patagonia, Argentina, and a review of megachilid (Hymenoptera) ichnology. Palaeontology 51(4): 933–941.

Schofield, R.M.S., M.H. Nesson, & K.A. Richardson. 2002. Tooth hardness increases with zinc-content in mandibles of young adult leaf-cutter ants. Naturwissenschaften 89(12): 579–583.

Schultz, T.R., & S.G. Brady. 2008. Major evolutionary transitions in ant agriculture. Proceedings of the National Academy of Science, U.S.A. 105(14): 5435–5440.

Schwarz, H.F. 1948. Stingless bees (Meliponidae) of the Western Hemisphere: Lestrimelitta and the following subgenera of Trigona: Trigona, Paratrigona, Schwarziana, Parapartamona, Cephalotrigona, Oxytrigona, Scaura, and Mourella. Bulletin of the American Museum of Natural History 90: i–xvii, 1–546, +8 pls.

Sereno, P.C. 2007. Logical basis for morphological characters in phylogenetics. Cladistics 23(6): 565–587.

Sheffield, C.S., & S.M. Westby. 2007. The male of Megachile nivalis Friese, with an updated key to members of the subgenus Megachile s.str. (Hymenoptera: Megachilidae) in North America. Journal of Hymenoptera Research 16(1): 178–191.

Silveira, F.A., G.A.R. Melo, & E.A.B. Almeida. 2002. Abelhas Brasileiras: Sistemática e Identificação. Editora IDMAR; Belo Horizonte, Brazil; 253 pp.

Sinu, P.A., & J.L. Bronstein. 2018. Foraging preferences of leafcutter bees in three contrasting geographical zones. Diversity and Distributions 24(5): 621–628.

Slater, G.J., & L.J. Harmon. 2013. Unifying fossils and phylogenies for comparative analyses of diversification and trait evolution. Methods in Ecology and Evolution 4(8): 699–702.

Smith, F. 1853. Catalogue of the Hymenopterous Insects in the Collection of the British Museum. Part 1. Andrenidae and Apidae. British Museum; London, UK; [i]+198 pp., +pls. i–vi.

Smith, F. 1865. Descriptions of some new species of hymenopterous insects belonging to the families Thynnidae, Masaridae and Apidae. Transactions of the Entomological Society of London, Series 3 2(5): 389–399, +pl. xxi.

Soh, E.J.Y. 2014. Diversity and trap-nesting studies of Singaporean Megachile bees to inform monitoring and management of tropical pollinators. Honours thesis, National University of Singapore; Singapore, Singapore; iv+68+[36] pp.

Talavera, G., & J. Castresana. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56(4): 564–577.

Taschenberg, E. 1883. Die Gattungen der Bienen (Anthophila). Berliner Entomologische Zeitschrift 27(1): 37–100.
Thomson, C.G. 1872. Skandinaviens Hymenoptera. 2:a Delen, Innehållande Slägtet Apis Lin. Berlingska Boktryckeriet; Lund, Sweden; 286 pp.

Torretta, J.P., S.P. Durante, & A.M. Basilio. 2014. Nesting ecology of Megachile (Chrysosarus) catamarcensis Schrottky (Hymenoptera: Megachilidae), a Prosopis-specialist bee. Journal of Apicultural Research 53(5): 590–598.

Trunz, V., L. Packer, J. Vieu, N. Arrigo, & C.J. Praz. 2016. Comprehensive phylogeny, biogeography and new classification of the diverse bee tribe Megachilini: Can we use DNA barcodes in phylogenies of large genera? Molecular Phylogenetics and Evolution 103: 245–259.

Wedmann, S., T. Wappler, & M.S. Engel. 2009. Direct and indirect fossil records of megachilid bees from the Paleogene of central Europe (Hymenoptera: Megachilidae). Naturwissenschaften 96(6): 703–712.

West-Eberhard, M.J. 2003. Developmental Plasticity and Evolution. Oxford University Press; Oxford, UK; xx+794 pp.

Whiting, M.F., S. Bradler, & T. Maxwell. 2003. Loss and recovery of wings in stick insects. Nature 421(6920): 264–267.

Whitlock, J.A., & J.A. Wilson. 2013. Character distribution maps: A visualization method for comparative cladistics. Acta Zoologica 94(4): 490–499.

Williams, H.J., M.R. Strand, G.W. Elzen, S.B. Vinson, & J.S. Merritt. 1986. Nesting behavior, nest architecture, and use of Dufour’s gland lipids in nest provisioning by Megachile integra and M. mendica mendica (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 59(4): 588–597.

Williams, N.M., & K. Goodell. 2000. Association of mandible shape and nesting material in Osmia Panzer (Hymenoptera: Megachilidae): A morphometric analysis. Annals of the Entomological Society of America 93(2): 318–325.

Winston, M.L. 1979. The proboscis of the long-tongued bees: A comparative study. University of Kansas Science Bulletin 51(22): 631–667.

Wittmann, D., & B. Blochtein. 1995. Why males of leafcutter bees hold the females’ antennae with their front legs during mating. Apidologie 26(3): 181–196.

Zhang, C., T. Stadler, S. Klopfstein, T.A. Heath, & F. Ronquist. 2016. Total-evidence dating under the fossilized birth-death process. Systematic Biology 65(2): 228–249.

Zillikens, A., & J. Steiner. 2004. Nest architecture, life cycle and cleptoparasite of the Neotropical leaf-cutting bee Megachile (Chrysosarus) pseudanthidioides Moure (Hymenoptera: Megachilidae). Journal of the Kansas Entomological Society 77(3): 193–202.

Downloads

Published

03-07-2019

How to Cite

Gonzalez, V. H., Gustafson, G. T., & Engel, M. S. (2019). Morphological phylogeny of Megachilini and the evolution of leaf-cutter behavior in bees (Hymenoptera: Megachilidae): Evolution of leaf-cutter behavior in bees. Journal of Melittology, 85, 1-123. https://doi.org/10.17161/jom.v0i85.11541

Most read articles by the same author(s)

1 2 > >>