Phylogenetic relationships and the evolution of host preferences in the largest clade of brood parasitic bees (Apidae: Nomadinae)

Authors: SLESS, TREVOR - Cornell University; Branstetter, Michael; GILLUNG, JESSICA - McGill University - Canada; Krichilsky, Erin; Tobin, Kerrigan; STRAKA, JAKUB - Charles University, Czech Republic; ROZEN, JEROME - American Museum Of Natural History; FREITAS, FELIPE - Universidad De Sao Paulo; MARTINS, ALINE - University Of Brasilia; BOSSERT, SILAS - Cornell University; SEARLE, JEREMY - Cornell University; DANFORTH, BRYAN - Cornell University

Submitted to: Molecular Phylogenetics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2021
Publication Date: 11/1/2021
Citation: Sless, T.J., Branstetter, M.G., Gillung, J.P., Krichilsky, E., Tobin, K.B., Straka, J., Rozen, J.G., Freitas, F.V., Martins, A.C., Bossert, S., Searle, J.B., Danforth, B.N. 2021. Phylogenetic relationships and the evolution of host preferences in the largest clade of brood parasitic bees (Apidae: Nomadinae) . Molecular Phylogenetics and Evolution. 166. https://doi.org/10.1016/j.ympev.2021.107326.
DOI: https://doi.org/10.1016/j.ympev.2021.107326

Interpretive Summary: Ultraconserved elements (UCEs) illuminate the phylogeny of the largest group of brood parasitic bees (Apidae: Nomadinae): Brood parasites (also known as cleptoparasites) represent a substantial fraction of global bee diversity. The oldest and most speciose parasitic clade is the subfamily Nomadinae (Apidae), and despite significant interest, the phylogenetic relationships among brood parasitic Apidae both within and outside the Nomadinae have not been fully resolved. Using ultraconserved element (UCE) molecular sequence data and extensive taxon sampling the phylogeny of the Nomadinae was investigated and greatly improved. The resulting phylogeny was used to expand the definition of the Nomadinae to include all parasitic species within the family Apidae and to improve the internal classification of the group, including the description of a new bee tribe. The phylogeny was also used to examine the evolution of host-parasite associations and it was found that host breadth broadened over time, supporting the idea that hosts are usually closely related to their parasites.

Technical Abstract: Brood parasites (also known as cleptoparasites) represent a substantial fraction of global bee diversity. Rather than constructing their own nests, these species instead invade those of host bees to lay their eggs. Larvae then hatch and consume the food provisions intended for the host’s offspring. While this life history strategy has evolved numerous times across the phylogeny of bees, the oldest and most speciose parasitic clade is the subfamily Nomadinae (Apidae). However, the phylogenetic relationships among brood parasitic apids both within and outside the Nomadinae have not been fully resolved. Here, we present new findings on the phylogeny of this diverse group of brood parasites based on ultraconserved element (UCE) sequence data and extensive taxon sampling. We suggest a broader definition of the subfamily Nomadinae to describe a clade that includes almost all parasitic members of the family Apidae. The tribe Melectini forms the sister group to all other Nomadinae, while the remainder of the subfamily is composed of two sister clades: a “nomadine line” representing the former Nomadinae sensu stricto, and an “ericrocidine line” that unites several, mostly Neotropical, lineages. We find the tribe Osirini Handlirsch to be polyphyletic, and divide it into three lineages, including the newly described Parepeolini trib. nov. In addition to our taxonomic findings, we use our phylogeny to explore the evolution of different modes of parasitism, detecting two independent transitions from closed-cell to open-cell parasitism. Finally, we examine how nomadine host-parasite associations have evolved over time. In support of Emery’s rule, which suggests close relationships between hosts and parasites, we confirm that the earliest nomadines were parasites of their close free-living relatives within the family Apidae, but that over time their host range broadened to include more distantly related hosts spanning the diversity of bees.