Darwin’s vexing contrivance: A new hypothesis for why some flowers have two kinds of anther

Heteranthery, the presence of two or more anther types in the same flower,
is taxonomically widespread among bee-pollinated angiosperms, yet has
puzzled botanists since Darwin. We test two competing hypotheses for its
evolution: the longstanding “division of labour” hypothesis, which posits
that some anthers are specialized as food rewards for bees whereas other
are specialized for surreptitious pollination, and our new hypothesis that
heteranthery is a way to gradually release pollen that maximizes pollen
delivery. We examine the evolution of heteranthery and associated traits
across the genus Clarkia (Onagraceae) and study plant-pollinator
interactions in two heterantherous Clarkia species. Across species,
heteranthery is associated with bee pollination, delayed dehiscence and
colour crypsis of one anther whorl, and movement of that anther whorl upon
dehiscence. Our mechanistic studies in heterantherous species show that
bees notice, forage on, and export pollen from each anther whorl when it
is dehiscing, and that heteranthery promotes pollen export. We find no
support for division of labour, but multifarious evidence that
heteranthery is a mechanism for gradual pollen presentation that likely
evolved through indirect male-male competition for siring success.