The evolution of ﬂoral sonication,
a pollen foraging behavior used by bees
Stephen L. Buchmann,
and Avery L. Russell
Canadian National Collection of Insects, Agriculture and Agri-Food Canada, Ottawa, Ontario K1A 0C6, Canada
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
Received March 14, 2017
Accepted January 26, 2018
Over 22,000 species of biotically pollinated ﬂowering plants, including some major agricultural crops, depend primarily on bees
capable of ﬂoral sonication for pollination services. The ability to sonicate (“buzz”) ﬂowers is widespread in bees but not ubiquitous.
Despite the prevalence of this pollinator behavior and its importance to natural and agricultural systems, the evolutionary history
of ﬂoral sonication in bees has not been previously studied. Here, we reconstruct the evolutionary history of ﬂoral sonication
in bees by generating a time-calibrated phylogeny and reconstructing ancestral states for this pollen extraction behavior. We
also test the hypothesis that the ability to sonicate ﬂowers and thereby efﬁciently access pollen from a diverse assemblage of
plant species, led to increased diversiﬁcation among sonicating bee taxa. We ﬁnd that ﬂoral sonication evolved on average 45
times within bees, possibly ﬁrst during the Early Cretaceous (100–145 million years ago) in the common ancestor of bees. We ﬁnd
that sonicating lineages are signiﬁcantly more species rich than nonsonicating sister lineages when comparing sister clades, but a
probabilistic structured rate permutation on phylogenies approach failed to support the hypothesis that ﬂoral sonication is a key
driver of bee diversiﬁcation. This study provides the evolutionary framework needed to further study how ﬂoral sonication by
bees may have facilitated the spread and common evolution of angiosperm species with poricidal ﬂoral morphology.
Bee phylogeny, buzz pollination, diversiﬁcation, ﬂoral sonication, pollen foraging.
The complex interaction between flowering plants (angiosperms)
and their pollinators has resulted in notable cases of convergent
evolution (e.g., Cook et al. 2004; Vallejo-Mar
ın et al. 2010),
coevolution (e.g., Pellmyr and Thompson 1992; Anderson and
Johnson 2007; Thompson et al. 2013), and shifts in floral diversi-
fication (e.g., Sargent 2004; van der Niet and Johnson 2012). An-
giosperms have repeatedly evolved floral morphologies that con-
ceal floral rewards, including pollen and nectar, and concealment
is hypothesized to promote effective pollinator services (Harder
and Barclay 1994; Hargreaves et al. 2009 and references within).
To extract these concealed rewards, pollinators must frequently
use complex flower handling behavioral routines (e.g., Macior
1968; Laverty 1980; Buchmann 1983; Laverty and Plowright
1988; Lewis 1993; Westerkamp 1999). Among the best studied of
these interactions is floral sonication by bees, commonly referred
to as buzz pollination. Approximately 6% of the world’s estimated
352,000 species of flowering plants conceal their pollen within
tube-like poricidal anthers or, occasionally, corollas, and depend
primarily on sonicating bees for pollination services (Buchmann
1983; De Luca and Vallejo-Mar
ın 2013; Corbet and Huang 2014).
Plant species with such poricidal floral morphology
(>22,000 species) are widely distributed across at least 27 an-
giosperm orders, 72 families, and 544 genera (Buchmann 1983).
Commonly grown agricultural crops that require floral sonica-
tion include blueberries, cranberries, kiwis, chili peppers, egg-
plants, and tomatoes. The evolution and diversification of pori-
cidal angiosperms is thought to reflect selection by sonicating
bees (De Luca and Vallejo-Mar
ın 2013; Russell et al. 2017). Yet
2018 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited and is not used for commercial purposes.
Evolution 72-3: 590–600