The evolutionary history of bees in time and space

Authors: ALMEIDA, EDUARDO A. - Universidad De Sao Paulo; BOSSERT, SILAS - Cornell University; DANFORTH, BRYAN - Cornell University; PORTO, DIEGO - Universidade De Sao Paulo; FREITAS, FELIPE - Universidade De Sao Paulo; DAVIS, CHARLES - Harvard University; MURRAY, ELIZABETH - Smithsonian Institute; BLAIMER, BONNIE - Washington State University; SPASOJEVIC, TAMARA - Smithsonian Institute; STROHER, PATRICIA - Universidade Federal Do Parana; ORR, MICHAEL - Stuttgart State Museum Of Natural History; PACKER, LAURENCE - York University; BRADY, SEAN - Smithsonian Institute; KUHLMANN, MICHAEL - University Of Kiel; Branstetter, Michael; PIE, MARCIO - Universidade Federal Do Parana

Submitted to: Current Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/4/2023
Publication Date: 7/27/2023
Citation: Almeida, E.A.B., Bossert, S., Danforth, B.N., Porto, D.S., Freitas, F.V., Davis, C.C., Murray, E.A., Blaimer, B.B., Spasojevic, T., Stroher, P.R., Orr, M.C., Packer, L., Brady, S.G., Kuhlmann, M., Branstetter, M.G., Pie, M.R. 2023. The evolutionary history of bees in time and space. Current Biology. 33:1-14. https://doi.org/10.1016/j.cub.2023.07.005.
DOI: https://doi.org/10.1016/j.cub.2023.07.005

Interpretive Summary: As the most important pollinators of flowering plants, bees are believed to have played a key role 3 in angiosperm diversification over the past 120 million years. Bees are hypothesized to have 4 originated in western Gondwana (Africa and South America), but the diversification and spread of 5 bee lineages around the world was a gradual process involving dispersal, extinction, and 6 cladogenesis layered on the shifting interconnections among the continents. How bee lineages 7 spread around the world has not been conclusively established even though resolving bee 8 biogeographic history has important implications for the diversification of flowering plants and for 9 the evolution of angiosperm pollination syndromes. To reconstruct the spatial and temporal 10 patterns of bee biogeographic history, we inferred relationships among 216 bee species from all 11 seven families using ultraconserved element phylogenomics. With the addition of 185 fossil taxa, 12 we estimated the timing of cladogenetic events. We then analyzed spatial patterns of bee 13 dispersal, extinction and cladogenesis using a Bayesian implementation of the DEC model. 14 Based on our analysis, bees originated in the Early Cretaceous, and the breakup of western 15 Gondwanan landmasses influenced their evolutionary history. All major lineages are associated 16 with the African and South American land masses. We show that the arrival of bees on northern 17 continents occurred later, probably around the Late Cretaceous or early Paleogene. The fauna 18 associated with other large Gondwanan landmasses—Australia and India—was assembled 19 relatively late, during the Cenozoic, which has important implications for understanding the assembly of local floras and diverse modes of pollination in these regions.

Technical Abstract: As the most important pollinators of flowering plants, bees are believed to have played a key role 3 in angiosperm diversification over the past 120 million years. Bees are hypothesized to have 4 originated in western Gondwana (Africa and South America), but the diversification and spread of 5 bee lineages around the world was a gradual process involving dispersal, extinction, and 6 cladogenesis layered on the shifting interconnections among the continents. How bee lineages 7 spread around the world has not been conclusively established even though resolving bee 8 biogeographic history has important implications for the diversification of flowering plants and for 9 the evolution of angiosperm pollination syndromes. To reconstruct the spatial and temporal 10 patterns of bee biogeographic history, we inferred relationships among 216 bee species from all 11 seven families using ultraconserved element phylogenomics. With the addition of 185 fossil taxa, 12 we estimated the timing of cladogenetic events. We then analyzed spatial patterns of bee 13 dispersal, extinction and cladogenesis using a Bayesian implementation of the DEC model. 14 Based on our analysis, bees originated in the Early Cretaceous, and the breakup of western 15 Gondwanan landmasses influenced their evolutionary history. All major lineages are associated 16 with the African and South American land masses. We show that the arrival of bees on northern 17 continents occurred later, probably around the Late Cretaceous or early Paleogene. The fauna 18 associated with other large Gondwanan landmasses—Australia and India—was assembled 19 relatively late, during the Cenozoic, which has important implications for understanding the assembly of local floras and diverse modes of pollination in these regions.