[en] The mining bees (Andrenidae) are a major bee family of over 3000 described species with a nearly global distribution. They are a particularly significant component of northern temperate ecosystems and are critical pollinators in natural and agricultural settings. Despite their ecological and evolutionary significance, our knowledge of the evolutionary history of Andrenidae is sparse and insufficient to characterize their spatiotemporal origin and phylogenetic relationships. This limits our ability to understand the diversification dynamics that led to the second most species-rich genus of all bees, Andrena Fabricius, and the most species-rich North American genus, Perdita Smith. Here, we develop a comprehensive genomic dataset of 195 species of Andrenidae, including all major lineages, to illuminate the evolutionary history of the family. Using fossil-informed divergence time estimates, we characterize macroevolutionary dynamics, incorporate paleoclimatic information, and present our findings in the context of diversification rate estimates for all other bee tribes. We found that diversification rates of Andrenidae steeply increased over the past 15 million years, particularly in the genera Andrena and Perdita. This suggests that these two groups and the brood parasites of the genus Nomada Scopoli (Apidae), which are the primary cleptoparasitic counterparts of Andrena, are similar in age and represent the fastest diversifying lineages of all bees. Using our newly developed time frame of andrenid evolution, we estimate a late Cretaceous origin in South America for the family and reconstruct the past dispersal events that led to its present-day distribution.
Disciplines :
Entomology & pest control Zoology
Author, co-author :
Bossert, Silas ; Department of Entomology, Washington State University, Pullman, United States ; Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, United States
Patiny, Sébastien; Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Mons, Belgium
Michez, Denis ; Université de Mons - UMONS > Faculté des Sciences > Service de Zoologie
Almeida, Eduardo A. B. ; Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, Brazil
Minckley, Robert L. ; Department of Biology, University of Rochester, Rochester, United States
Packer, Laurence ; Department of Biology, York University, Toronto, Canada
Neff, John L. ; Central Texas Melittological Institute, Austin, United States
Copeland, Robert S. ; Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, United States ; ICIPE, International Centre of Insect Physiology and Ecology, Nairobi, Kenya
Straka, Jakub ; Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic
Pauly, Alain; Royal Belgian Institute of Natural Sciences, O.D. Taxonomy and Phylogeny, Brussels, Belgium
Griswold, Terry ; U.S. Department of Agriculture, Agricultural Research Service, Pollinating Insects Research Unit, Utah State University, Logan, United States
Brady, Seán G.; Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, United States
Danforth, Bryan N. ; Department of Entomology, Cornell University, Ithaca, United States
Murray, Elizabeth A. ; Department of Entomology, Washington State University, Pullman, United States ; Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, United States
Grantová Agentura České Republiky National Science Foundation of Sri Lanka
Funding text :
Fundação de Amparo á Pesquisa do Estado de São Paulo (FAPESP), Grant/Award Number: #2018/09666‐5; Grantová Agentura České Republiky, Grant/Award Number: 20‐14872S; National Science Foundation, Grant/Award Numbers: DEB‐1555905, DEB‐2127744, DEB‐2127745 Funding informationThis work was supported by U.S. National Science Foundation grants DEB‐1555905, DEB‐2127744 and DEB‐2127745, and a Cornell Entomology Griswold Grant to S. Bossert. S. Bossert and E.A. Murray were supported by Peter Buck fellowships at the Smithsonian Institution. R.S. Copeland thanks the director of ICIPE for her continuing support of our project on the biodiversity of Kenyan insects, and he gratefully acknowledges the ICIPE core funding provided by UK Aid from the Government of the United Kingdom; Swedish International Development Cooperation Agency; the Swiss Agency for Development and Cooperation; Federal Ministry for Economic Cooperation and Development, Germany; and the Kenyan Government. J. Straka was supported by the Czech Science Foundation grant (20‐14872S) and E.A.B. Almeida received funding from grant #2018/09666‐5 of the São Paulo Research Foundation (FAPESP). T.J. Wood is supported by an F.R.S.‐FNRS fellowship “Chargé de recherches”. We thank Bonnie Blaimer for her help with DNA extractions, Michael O. Dillon for the discussion on the antiquity of , and Michael R. May for advice on RevBayes. Parts of the laboratory work for this study was conducted in the L.A.B. facilities of the National Museum of Natural History, Smithsonian Institution. We acknowledge the usage of DNA extracts that were generated and deposited at Cornell University by John Ascher during his PhD education. We thank Katherine Parys (USDA‐ARS) for contributing specimens of . Computational resources were provided by the SI High‐Performance Computing cluster ( 10.25572/SIHPC ). Nolana Anthemurgus passifloraeThis work was supported by U.S. National Science Foundation grants DEB-1555905, DEB-2127744 and DEB-2127745, and a Cornell Entomology Griswold Grant to S. Bossert. S. Bossert and E.A. Murray were supported by Peter Buck fellowships at the Smithsonian Institution. R.S. Copeland thanks the director of ICIPE for her continuing support of our project on the biodiversity of Kenyan insects, and he gratefully acknowledges the ICIPE core funding provided by UK Aid from the Government of the United Kingdom; Swedish International Development Cooperation Agency; the Swiss Agency for Development and Cooperation; Federal Ministry for Economic Cooperation and Development, Germany; and the Kenyan Government. J. Straka was supported by the Czech Science Foundation grant (20-14872S) and E.A.B. Almeida received funding from grant #2018/09666-5 of the S?o Paulo Research Foundation (FAPESP). T.J. Wood is supported by an F.R.S.-FNRS fellowship ?Charg? de recherches?. We thank Bonnie Blaimer for her help with DNA extractions, Michael O. Dillon for the discussion on the antiquity of Nolana, and Michael R. May for advice on RevBayes. Parts of the laboratory work for this study was conducted in the L.A.B. facilities of the National Museum of Natural History, Smithsonian Institution. We acknowledge the usage of DNA extracts that were generated and deposited at Cornell University by John Ascher during his PhD education. We thank Katherine Parys (USDA-ARS) for contributing specimens of Anthemurgus passiflorae. Computational resources were provided by the SI High-Performance Computing cluster (10.25572/SIHPC).
Alexander, B.A. (1994) Species-groups and cladisitic analysis of the cleptoparasitic bee genus Nomada (Hymenoptera: Apoidea). University of Kansas Science Bulletin, 55, 175–238.
Alfaro, M.E., Brock, C.D., Banbury, B.L. & Wainwright, P.C. (2009) Does evolutionary innovation in pharyngeal jaws lead to rapid lineage diversification in labrid fishes? BMC Evolutionary Biology, 9, 255.
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. Journal of Biogeography, 39, 526–544.
Almeida, E.A.B., Packer, L., Melo, G.A.R., Danforth, B.N., Cardinal, S.C., Quinteiro, F.B. et al. (2019) The diversification of neopasiphaeine bees during the Cenozoic (Hymenoptera: Colletidae). Zoologica Scripta, 48, 226–242.
Amiet, F. & Krebs, A. (2012) Bienen Mitteleuropas - Gattungen, Lebensweise, Beobachtung. Bern: Haupt Verlag.
Ascher, J.S. (2003) Evidence for the phylogenetic position of Nolanomelissa from nuclear EF-1a sequence data. In: Melo, G.A.R. & Alves-dos-Santos, I. (Eds.) Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure. Criciúma: UNESC, pp. 17–19.
Ascher, J.S. (2004) Systematics of the bee family Andrenidae (Hymenoptera: Apoidea). PhD Thesis, Cornell University, 333 pp.
Ascher, J.S. & Pickering, J. (2021) Discover Life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). Available at: http://www.discoverlife.org/mp/20q?guide=Apoidea_species. Accessed January 2021
Ascher, J.S., Engel, M.S. & Griswold, T.L. (2006) A new subgenus and species of Oxaea from Ecuador (Hymenoptera: Andrenidae). Polskie Pismo Entomologiczne, 75, 539–552.
Ballantyne, G., Baldock, K.C.R., Rendell, L. & Willmer, P.G. (2017) Pollinator importance networks illustrate the crucial value of bees in a highly speciose plant community. Scientific Reports, 7, 8389.
Blaimer, B.B., LaPolla, J.S., Branstetter, M.G., Lloyd, M.W. & Brady, S.G. (2016) Phylogenomics, biogeography and diversification of obligate mealybug-tending ants in the genus Acropyga. Molecular Phylogenetics and Evolution, 102, 20–29.
Blaimer, B.B., Lloyd, M.W., Guillory, W.X. & Brady, S.G. (2016) Sequence capture and phylogenetic utility of genomic ultraconserved elements obtained from pinned insect specimens. PLoS One, 11, e0161531.
Blaimer, B.B., Mawdsley, J.R. & Brady, S.G. (2018) Multiple origins of sexual dichromatism and aposematism within large carpenter bees. Evolution, 72, 1874–1889.
Borowiec, M.L. (2016) AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ, 4, e1660.
Borowiec, M.L., Lee, E.K., Chiu, J.C. & Plachetzki, D.C. (2015) Extracting phylogenetic signal and accounting for bias in whole-genome data sets supports the Ctenophora as sister to remaining Metazoa. BMC Genomics, 16, 1–15.
Bossert, S., Copeland, R.S., Sless, T.J.L., Branstetter, M.G., Gillung, J.P., Brady, S.G. et al. (2020) Phylogenomic and morphological reevaluation of the bee tribes Biastini, Neolarrini, and Townsendiellini (Hymenoptera: Apidae) with description of three new species of Schwarzia. Insect Systematics and Diversity, 4, 1–29.
Bossert, S., Murray, E.A., Pauly, A., Chernyshov, K., Brady, S.G. & Danforth, B.N. (2021) Gene tree estimation error with ultraconserved elements: an empirical study on Pseudapis bees. Systematic Biology, 70, 803–821.
Botero, C.A., Dor, R., McCain, C.M. & Safran, R.J. (2014) Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Molecular Ecology, 23, 259–268.
Branstetter, M.G., Danforth, B.N., Pitts, J.P., Faircloth, B.C., Ward, P.S., Buffington, M.L. et al. (2017) Phylogenomic insights into the evolution of stinging wasps and the origins of ants and bees. Current Biology, 27, 1019–1025.
Cantrill, D.J. & Poole, I. (2012) The vegetation of Antarctica through geological time. Cambridge: Cambridge University Press.
Cardinal, S. (2018) Bee (Hymenoptera: Apoidea: Anthophila) diversity through time. In: Foottit, R.G. & Adler, P.H. (Eds.) Insect biodiversity: science and society, Vol. 2. Oxford, UK: John Wiley & Sons Ltd., pp. 851–867.
Cardinal, S. & Danforth, B.N. (2013) Bees diversified in the age of eudicots. Proceedings of the Royal Society B: Biological Sciences, 280, 1–9.
Cardinal, S., Buchmann, S.L. & Russell, A.L. (2018) The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila). Evolution, 72, 590–600.
Claramunt, S. & Cracraft, J. (2015) A new time tree reveals earth history's imprint on the evolution of modern birds. Science Advances, 1, e1501005.
Cockerell, T.D.A. (1904) New records of bees. The Entomologist, 37, 231–236.
Cockerell, T.D.A. (1906) Fossil Hymenoptera from Florissant, Colorado. Bulletin of the Museum of Comparative Zoology at Harvard College, 50, 33–58.
Cockerell, T.D.A. (1908) Descriptions and records of bees. XX. Annals and Magazine of Natural History, 8, 323–334.
Cockerell, T.D.A. (1909) Two fossil bees. Entomological News, 20, 159–161.
Cockerell, T.D.A. (1911) Fossil insects from Florissant, Colorado. Bulletin of the American Museum of Natural History, 30, 71–82.
Cockerell, T.D.A. (1913) Some fossil insects from Florissant, Colorado. Proceedings of the United States National Museum, 44, 341–346.
Cockerell, T.D.A. (1914) Miocene fossil insects. Proceedings of the Academy of Natural Sciences of Philadelphia, 66, 634–648.
Condamine, F.L., Rolland, J., Höhna, S., Sperling, F.A.H. & Sanmartín, I. (2018) Testing the role of the red queen and court jester as drivers of the macroevolution of Apollo butterflies. Systematic Biology, 67, 940–964.
Crawford, J.C. (1916) Nine new species of Hymenoptera. Insecutor Inscitiae Menstruus, 4, 101.
Danforth, B.N. (1996) Phylogenetic analysis and taxonomic revision of the Perdita subgenera Macrotera, Macroteropsis, Macroterella and Cockerellula (Hymenoptera: Andrenidae). The University of Kansas Science Bulletin, 55, 635.
Danforth, B.N., Fang, J. & Sipes, S. (2006) 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, 358–373.
Danforth, B.N., Sipes, S., Fang, J. & Brady, S.G. (2006) The history of early bee diversification based on five genes plus morphology. Proceedings of the National Academy of Sciences, 103, 15118–15123.
Danforth, B.N., Minckley, R.L. & Neff, J.L. (2019) The solitary bees: biology, evolution, conservation. Princeton: Princeton University Press.
Dehon, M., Michez, D., Nel, A., Engel, M.S. & De Meulemeester, T. (2014) Wing shape of four new bee fossils (Hymenoptera: Anthophila) provides insights to bee evolution. PLoS One, 9, e108865.
Dewulf, A., De Meulemeester, T., Dehon, M., Engel, M.S. & Michez, D. (2014) A new interpretation of the bee fossil Melitta willardi Cockerell (Hymenoptera, Melittidae) based on geometric morphometrics of the wing. ZooKeys, 389, 35–48.
Donoghue, M.J. & Sanderson, M.J. (2015) Confluence, synnovation, and depauperons in plant diversification. New Phytologist, 207, 260–274.
Eardley, C.D. & Schwarz, M. (1991) The Afrotropical species of Nomada Scopoli (Hymenoptera: Anthophoridae). Phytophylactica, 23, 17–28.
Eardley, C.D., Kuhlmann, M. & Pauly, A. (2010) The bee genera and subgenera of sub-Saharan Africa. Abc Taxa, 7, 1–139.
Engel, M.S. (2001) A monography 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. (2015) A review of the genera and subgenera of Oxaeinae (Hymenoptera: Andrenidae). Journal of Melittology, 52, 1–18.
Ezard, T.H.G., Aze, T., Pearson, P.N. & Purvis, A. (2011) Interplay between changing climate and species' ecology drives macroevolutionary dynamics. Science, 332, 349–351.
Faircloth, B.C. (2016) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics, 32, 786–788.
Faircloth, B.C., Branstetter, M.G., White, N.D. & Brady, S.G. (2015) Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera. Molecular Ecology Resources, 15, 489–501.
Foster, G.L., Royer, D.L. & Lunt, D.J. (2017) Future climate forcing potentially without precedent in the last 420 million years. Nature Communications, 8, 14845.
Gibbs, J., Brady, S.G., Kanda, K. & Danforth, B.N. (2012) Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Molecular Phylogenetics and Evolution, 65, 926–939.
Gonzalez, V.H., Rasmussen, C. & Engel, M.S. (2013) Incasarus garciai, a new genus and species of panurgine bees from the Peruvian Andes (Hymenoptera: Andrenidae). Journal of Melittology, 8, 1–9.
Grab, H., Branstetter, M.G., Amon, N., Urban-Mead, K.R., Park, M.G., Gibbs, J. et al. (2019) Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services. Science, 363, 282–284.
Gusenleitner, F., Schwarz, M. & Mazzucco, K. (2012) Apidae (Insecta: Hymenoptera). In: Schuster, R. (Ed.) 162 pp. Checklisten der Fauna Österreichs, No. 6. Wien: Österreichische Akademie der Wissenschaften.
Hansen, J., Sato, M., Russell, G. & Kharecha, P. (2013) Climate sensitivity, sea level and atmospheric carbon dioxide. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 371, 20120294.
Heath, T.A., Huelsenbeck, J.P. & Stadler, T. (2014) The fossilized birth-death process for coherent calibration of divergence-time estimates. Proceedings of the National Academy of Sciences of the United States of America, 111, E2957–E2966.
Hedtke, S.M., Patiny, S. & Danforth, B.N. (2013) The bee tree of life: a supermatrix approach to apoid phylogeny and biogeography. BMC Evolutionary Biology, 13, 1–13.
Hines, H.M. (2008) Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology, 57, 58–75.
Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q. & Vinh, L.S. (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35, 518–522.
Höhna, S. (2015) The time-dependent reconstructed evolutionary process with a key-role for mass-extinction events. Journal of Theoretical Biology, 380, 321–331.
Höhna, S., Landis, M.J., Heath, T.A., Boussau, B., Lartillot, N., Moore, B.R. et al. (2016) RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Systematic Biology, 65, 726–736.
Huang, X.-C., German, D.A. & Koch, M.A. (2020) Temporal patterns of diversification in Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization events. Annals of Botany, 125, 29–47.
Huelsenbeck, J.P., Larget, B. & Alfaro, M.E. (2004) Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Molecular Biology and Evolution, 21, 1123–1133.
Hunter, J.P. (1998) Key innovations and the ecology of macroevolution. Trends in Ecology & Evolution, 13, 31–36.
Hurd, P.D.J. & Linsley, E.G. (1976) The bee family Oxaeidae with a revision of the north American species (Hymenoptera, Apoidea). Smithsonian Contributions to Zoology, 220, 1–75.
Jetz, W., Thomas, G.H., Joy, J.B., Hartmann, K. & Mooers, A.O. (2012) The global diversity of birds in space and time. Nature, 491, 444–448.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587.
Kayaalp, P., Schwarz, M.P. & Stevens, M.I. (2013) Rapid diversification in Australia and two dispersals out of Australia in the globally distributed bee genus, Hylaeus (Colletidae: Hylaeinae). Molecular Phylogenetics and Evolution, 66, 668–678.
Keller, G. (2001) The end-cretaceous mass extinction in the marine realm: year 2000 assessment. Planetary and Space Science, 49, 817–830.
Kembel, S.W., Cowan, P.D., Helmus, M.R., Cornwell, W.K., Morlon, H., Ackerly, D.D. et al. (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26, 1463–1464.
Kergoat, G.J., Condamine, F.L., Toussaint, E.F.A., Capdevielle-Dulac, C., Clamens, A.-L., Barbut, J. et al. (2018) Opposite macroevolutionary responses to environmental changes in grasses and insects during the Neogene grassland expansion. Nature Communications, 9, 5089.
Klages, J.P., Salzmann, U., Bickert, T., Hillenbrand, C.D., Gohl, K., Kuhn, G. et al. (2020) Temperate rainforests near the south pole during peak cretaceous warmth. Nature, 580, 81–86.
Klein, A.-M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C. et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274, 303–313.
Krombein, K.V., Hurd, P.D., Smith, D.R. & Burks, B.D. (1979) Catalog of Hymenoptera in America north of Mexico. Washington, DC: Smithsonian Institution Press.
Labandeira, C.C., Johnson, K.R. & Wilf, P. (2002) Impact of the terminal cretaceous event on plant-insect associations. Proceedings of the National Academy of Sciences, 99, 2061–2066.
Lagomarsino, L.P., Condamine, F.L., Antonelli, A., Mulch, A. & Davis, C.C. (2016) The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytologist, 210, 1430–1442.
Landis, M.J., Matzke, N.J., Moore, B.R. & Huelsenbeck, J.P. (2013) Bayesian analysis of biogeography when the number of areas is large. Systematic Biology, 62, 789–804.
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
Lanfear, R., Calcott, B., Kainer, D., Mayer, C. & Stamatakis, A. (2014) Selecting optimal partitioning schemes for phylogenomic datasets. BMC Evolutionary Biology, 14, 82.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.
Lepage, T., Bryant, D., Philippe, H. & Lartillot, N. (2007) A general comparison of relaxed molecular clock models. Molecular Biology and Evolution, 24, 2669–2680.
Longrich, N.R., Bhullar, B.-A.S. & Gauthier, J.A. (2012) Mass extinction of lizards and snakes at the cretaceous-Paleogene boundary. Proceedings of the National Academy of Sciences, 109, 21396–21401.
Luo, A., Duchêne, D.A., Zhang, C., Zhu, C.-D. & Ho, S.Y.W. (2020) A simulation-based evaluation of tip-dating under the fossilized birth-death process. Systematic Biology, 69, 325–344.
Magallón, S. & Sanderson, M.J. (2001) Absolute diversification rates in angiosperm clades. Evolution, 55, 1762–1780.
Matzke, N.J. (2018, November 6) BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis with R scripts. version 1.1.1, published on GitHub.
Mayhew, P.J. (2007) Why are there so many insect species? Perspectives from fossils and phylogenies. Biological Reviews, 82, 425–454.
Michener, C.D. (1979) Biogeography of the bees. Annals of the Missouri Botanical Garden, 66, 277–347.
Michener, C.D. (1986) New Peruvian genus and a generic review of Andreninae (Hymenoptera: Apoidea: Andrenidae). Annals of the Entomological Society of America, 79, 62–72.
Michener, C.D. (2000) The bees of the world. Baltimore: The Johns Hopkins University Press.
Michener, C.D. (2007) The bees of the world. Baltimore: The Johns Hopkins University Press.
Michez, D., Vanderplanck, M. & Engel, M.S. (2012) Fossil bees and their plant associates. In: Patiny, S. (Ed.) Evolution of plant-pollinator relationships. Cambridge: Cambridge University Press, pp. 103–164.
Mikát, M., Matoušková, E. & Straka, J. (2021) Nesting of Ceratina nigrolabiata, a biparental bee. Scientific Reports, 11, 5026.
Milne, R.I. (2006) Northern hemisphere plant disjunctions: a window on tertiary land bridges and climate change? Annals of Botany, 98, 465–472.
Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. et al. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534.
Morlon, H. (2014) Phylogenetic approaches for studying diversification. Ecology Letters, 17, 508–525.
Ollerton, J. (2017) Pollinator diversity: distribution, ecological function, and conservation. Annual Review of Ecology, Evolution, and Systematics, 48, 353–376.
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C. et al. (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience, 51, 933–938.
Orr, M.C., Hughes, A.C., Chesters, D., Pickering, J., Zhu, C.-D. & Ascher, J.S. (2021) Global patterns and drivers of bee distribution. Current Biology, 31, 451–458.
Panero, J.L. & Crozier, B.S. (2016) Macroevolutionary dynamics in the early diversification of Asteraceae. Molecular Phylogenetics and Evolution, 99, 116–132.
Pardo, A. & Borges, P.A.V. (2020) Worldwide importance of insect pollination in apple orchards: a review. Agriculture, Ecosystems & Environment, 293, 106839.
Park, M.G., Raguso, R.A., Losey, J.E. & Danforth, B.N. (2016) Per-visit pollinator performance and regional importance of wild Bombus and Andrena (Melandrena) compared to the managed honey bee in New York apple orchards. Apidologie, 47, 145–160.
Patiny, S. (1999) Etude phylogénétique des Panurginae de l'Ancien Monde (Hymenoptera, Andrenidae). Linzer Biologische Beiträge, 31, 249–275.
Patiny, S. (2003) Phylogénie des espèces de Clavipanurgus Warncke, 1972 (Hymenoptera, Apoidea: Andrenidae). Annales de la Société Entomologique de France, 39, 229–234.
Peters, R.S., Krogmann, L., Mayer, C., Donath, A., Gunkel, S., Meusemann, K. et al. (2017) Evolutionary history of the Hymenoptera. Current Biology, 27, 1013–1018.
Pisanty, G., Richter, R., Martin, T., Dettman, J. & Cardinal, S. (2021) Molecular phylogeny and historical biogeography of andrenine bees (Hymenoptera: Andrenidae). Molecular Phylogenetics and Evolution, 107151. https://doi.org/10.1016/j.ympev.2021.107151
Plant, J.D. & Paulus, H.F. (2016) Evolution and phylogeny of bees - a review and a cladistic analysis in light of morphological evidence (Hymenoptera, Apoidea). Zoologica, 161, 1–364.
Portman, Z.M. & Tepedino, V.J. (2017) Convergent evolution of pollen transport mode in two distantly related bee genera (Hymenoptera: Andrenidae and Melittidae). Apidologie, 48, 461–472.
Praz, C.J. & Packer, L. (2014) Phylogenetic position of the bee genera Ancyla and Tarsalia (Hymenoptera: Apidae): a remarkable base compositional bias and an early Paleogene geodispersal from North America to the Old World. Molecular Phylogenetics and Evolution, 81, 258–270.
R Core Team. (2021) R: a language and environment for statistical computing. Vienna: R Core Team. Available at: http://www.r-project.org/
Rabosky, D.L. (2014) Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One, 9, e89543.
Rabosky, D.L. (2017) Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification. Philosophical Transactions of the Royal Society, B: Biological Sciences, 372, 20160417.
Rabosky, D.L., Slater, G.J. & Alfaro, M.E. (2012) Clade age and species richness are decoupled across the eukaryotic tree of life. PLoS Biology, 10, e1001381.
Rabosky, D.L., Grundler, M., Anderson, C., Title, P., Shi, J.J., Brown, J.W. et al. (2014) BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution, 5, 701–707.
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Systematic Biology, 67, 901–904.
Ramos, K.S. (2011) Relações filogenéticas entre as abelhas da subfamília Andreninae com ênfase nas tribos Calliopsini, Protandrenini e Protomelitturgini (Hymenoptera, Apidae). PhD Thesis, Universidade Federal do Paraná, Brazil, 156 pp.
Ramos, K.S. & Rozen, J.G. (2014) Psaenythisca, a new genus of bees from South America (Apoidea: Andrenidae: Protandrenini) with a description of the nesting biology and immature stages of one species. American Museum Novitates, 2014, 1–32.
Rannala, B. & Yang, Z. (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics, 164, 1645–1656.
Raup, D.M., Gould, S.J., Schopf, T.J.M. & Simberloff, D.S. (1973) Stochastic models of phylogeny and the evolution of diversity. The Journal of Geology, 81, 525–542.
Ree, R.H. & Sanmartín, I. (2018) Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. Journal of Biogeography, 45, 741–749.
Ree, R.H. & Smith, S.A. (2008) Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology, 57, 4–14.
Rehan, S.M., Leys, R. & Schwarz, M.P. (2013) First evidence for a massive extinction event affecting bees close to the K-T boundary. PLoS One, 8, e76683.
Ronquist, F. (1997) Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology, 46, 195–203.
Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D.L. & Rasnitsyn, A.P. (2012a) A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Systematic Biology, 61, 973–999.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S. et al. (2012b) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
Rozen, J.G. (1964) Phylogenetic-taxonomic significance of last instar of Protoxaea gloriosa fox, with descriptions of first and last instars (Hymenoptera: Apoidea). Journal of the New York Entomological Society, 72, 223–230.
Rozen, J.G. (1965) The biology and immature stages of Melitturga clavicornis (Latreille) and of Sphecodes albilabris (Kirby) and the recognition of the Oxaeidae at the family level (Hymenoptera, Apoidea). American Museum Novitates, 2224, 1–18.
Rozen, J.G. (1996) A new species of the bee Heterosarus from Dominican Amber (Hymenoptera: Andrenidae; Panurginae). Journal of the Kansas Entomological Society, 69, 346–352.
Rozen, J.G. (2003) A new tribe, genus, and species of south American panurgine bee (Andrenidae, Panurginae), oligolectic on Nolana (Nolanaceae). In: Melo, G.A.R. & Alves-dos-Santos, I. (Eds.) Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure, pp. Criciúma, Brazil: Editora da UNESC, 93–108.
Russo, L., Park, M.G., Blitzer, E.J. & Danforth, B.N. (2017) Flower handling behavior and abundance determine the relative contribution of pollinators to seed set in apple orchards. Agriculture, Ecosystems & Environment, 246, 102–108.
Ruz, L. (1986) Classification and phylogenetic relationships of the panurgine bees. PhD Thesis, University of Kansas, 312 pp.
Sahoo, R.K., Warren, A.D., Collins, S.C. & Kodandaramaiah, U. (2017) Hostplant change and paleoclimatic events explain diversification shifts in skipper butterflies (family: Hesperiidae). BMC Evolutionary Biology, 17, 1–9.
Sann, M., Niehuis, O., Peters, R.S., Mayer, C., Kozlov, A., Podsiadlowski, L. et al. (2018) Phylogenomic analysis of Apoidea sheds new light on the sister group of bees. BMC Evolutionary Biology, 18, 71.
Särkinen, T., Bohs, L., Olmstead, R.G. & Knapp, S. (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology, 13, 214.
Scheuchl, E. (1995) Illustrierte Bestimmungstabellen der Wildbienen Deutschlands und Österreichs. Band I: Anthophoridae. Velden: Eigenverlag.
Smith-Ramírez, C., Martinez, P., Nuñez, M., González, C. & Armesto, J.J. (2005) Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloé Island, Chile. Botanical Journal of the Linnean Society, 147, 399–416.
Spagarino, C., Martínez Pastur, G. & Peri, P. (2001) Changes in Nothofagus pumilio forest biodiversity during the forest management cycle. 1. Insects. Biodiversity & Conservation, 10, 2077–2092.
Stadler, T. (2010) Sampling-through-time in birth-death trees. Journal of Theoretical Biology, 267, 396–404.
Stanley, S.M. (1975) A theory of evolution above the species level. Proceedings of the National Academy of Sciences, 72, 646–650.
Sun, M., Folk, R.A., Gitzendanner, M.A., Soltis, P.S., Chen, Z., Soltis, D.E. et al. (2020) Recent accelerated diversification in rosids occurred outside the tropics. Nature Communications, 11, 3333.
Thompson, J.B., Dodd, H.O., Wills, M.A., & Priest, N.K. (2021) Speciation across the earth driven by global cooling in orchidoid orchids. bioRxiv [Preprint]. https://doi.org/10.1101/2021.02.06.430029. Accessed January 2021
Tiffney, B.H. (1985) The Eocene North Atlantic land bridge: its importance in tertiary and modern phytogeography of the northern hemisphere. Journal of the Arnold Arboretum, 66, 243–273.
Timberlake, P.H. (1975) The north American species of Heterosarus Robertson (Hymenoptera, Apoidea). University of California Publications in Entomology, 77, 1–57.
Title, P.O. & Rabosky, D.L. (2019) Tip rates, phylogenies and diversification: what are we estimating, and how good are the estimates? Methods in Ecology and Evolution, 10, 821–834.
Toussaint, E.F.A., Condamine, F.L., Kergoat, G.J., Capdevielle-Dulac, C., Barbut, J., Silvain, J.-F. et al. (2012) Palaeoenvironmental shifts drove the adaptive radiation of a noctuid stemborer tribe (Lepidoptera, Noctuidae, Apameini) in the Miocene. PLoS One, 7, e41377.
Trunz, V., Packer, L., Vieu, J., Arrigo, N. & Praz, C.J. (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.
Vázquez, D.P. & Simberloff, D. (2002) Ecological specialization and susceptibility to disturbance: conjectures and refutations. The American Naturalist, 159, 606–623.
Walker, K.L., Tattersall, M. & Houston, T.F. (2020) First host record for the Australian kleptoparasitic bee Nomada australensis (Perkins) (Hymenoptera: Apidae) and a new synonymy. The Australian Entomologist, 47, 285–300.
Warncke, K. (1972) Westpaläarktische Bienen der Unterfamilie Panurginae (Hym., Apidae). Polskie Pismo Entomologiczne, XLII, 53–108.
Westerhold, T., Marwan, N., Drury, A.J., Liebrand, D., Agnini, C., Anagnostou, E. et al. (2020) An astronomically dated record of Earth's climate and its predictability over the last 66 million years. Science, 369, 1383.
Westrich, P. (2006) Ein weiterer Beleg für den Bivoltinismus und das Wirt-Parasit-Verhältnis von Andrena bicolor (Fabricius 1804) und Nomada fabriciana (Kirby 1802)(Hym. Apidae). Linzer Biologische Beiträge, 38, 919–923.
Westrich, P. (2018) Die Wildbienen Deutschlands. Stuttgart: Eugen Ulmer KG.
Wood, T.J. & Cross, I. (2017) Camptopoeum (Camptopoeum) baldocki spec. Nov., a new panurgine bee species from Portugal and a description of the male of Flavipanurgus fuzetus Patiny (Andrenidae: Panurginae). Zootaxa, 4254, 285–293.
Zhang, C., Stadler, T., Klopfstein, S., Heath, T.A. & Ronquist, F. (2016) Total-evidence dating under the fossilized birth-death process. Systematic Biology, 65, 228–249.
Zhang, S.D., Jin, J.J., Chen, S.Y., Chase, M.W., Soltis, D.E., Li, H.T. et al. (2017) Diversification of Rosaceae since the late cretaceous based on plastid phylogenomics. New Phytologist, 214, 1355–1367.
Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. (2018) ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics, 19, 153.