UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA

Authors: FREITAS, FELIPE - Universidade De Sao Paulo; Branstetter, Michael; FRANCESCHINI-SANTOS, VINICIUS - Universidade De Sao Paulo; DORCHIN, ACHICK - University Of Mons-Hainaut; WRIGHT, KAREN - Texas A&M University; LOPEZ-URIBE, MARGARITA - Pennsylvania State University; Griswold, Terry; SILVEIRA, FERNANDO - Universidade Federal De Minas Gerais; ALMEIDA, EDUARDO - Universidade De Sao Paulo

Submitted to: Insect Systematics and Diversity
Publication Type: Review Article
Publication Acceptance Date: 5/29/2023
Publication Date: 7/12/2023
Citation: Freitas, F., Branstetter, M.G., Franceschini-Santos, V.H., Dorchin, A., Wright, K., Lopez-Uribe, M., Griswold, T.L., Silveira, F., Almeida, E. 2023. UCE phylogenomics, biogeography, and classification of long-horned bees (Hymenoptera: Apidae: Eucerini), with insights on using specimens with extremely degraded DNA. Insect Systematics and Diversity. 7(4). Article 3. https://doi.org/10.1093/isd/ixad012.
DOI: https://doi.org/10.1093/isd/ixad012

Interpretive Summary: Long-horned bees (Apidae, Eucerini) are common worldwide, and they are important pollinators of diverse plant species, including squashes, which are economically valuable crops grown in the United States. The group is taxonomically diverse, with over 750 species and 30 genera, and it is challenging to work on due to species being very similar in appearance. Because of this challenge, there remains uncertainty regarding the taxonomic status of genera and subgenera and evolutionary relationships. Using genomic data from thousands of ultraconserved elements (UCEs), a type of genetic marker exhibiting high sequence conservation across distantly related species - and data from over 150 species, the phylogeny of this important group of bees was inferred with unprecedented precision, allowing for a re-assessment of taxonomic ranks and evolutionary origins. The results include significant taxonomic changes to tribes, genera, and subgenera; confirmation that the long-horned bees originated in southern South America before expanding to other regions; and new methods for better incorporating museum samples with high amounts missing data into analyses. Overall, the study improves the systematics of squash bees and their relatives, facilitating future ecological and biological research into this important group of pollinators.

Technical Abstract: Long-horned bees (Apidae, Eucerini) are commonly found in different biomes worldwide and include some important crop pollinators. At least in the New World, Eucerini has received extensive taxonomic study during the twentieth century, resulting in several revisions of its genera. In contrast, progress on eucerine phylogenetic research and genus-level classification has been slow, primarily due to the relatively homogeneous external morphology within the tribe and the rarity of many of its species in collections. Notable exceptions have been analyses based on molecular data of a few loci, which have shed light on the initial diversification of Eucerini and clarified relationships among some lineages of eucerine bees. Here, we present a comprehensive phylogenetic study of Eucerini based on ultraconserved elements that includes 153 species from nearly all genera and subgenera and from all biogeographic regions where these bees are known to occur. Largely agreeing with previous studies, we recovered seven main lineages and found most of the genera and subgenera to be reciprocally monophyletic. Using the updated phylogenetic framework, we: (1) propose taxonomic changes intending to make the classification more congruent with our phylogenetic understanding of Eucerini, including a new subtribal classification, and reorganized generic and subgeneric limits; (2) estimate divergence times using a recently proposed data-driven diversification prior (ddBD); and (3) conduct a detailed exploration of historical biogeography of long-horned bees. We find that eucerine lineages expanded their range onto most continents only after its initial diversification in southern South America during the Eocene. Finally, we discuss the challenges of working with specimens with highly degraded DNA and present insights into how to improve phylogenetic results for both species-tree and concatenation approaches.