Abstract
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 long-standing ‘division of labour' hypothesis, which posits that some anthers are specialized as food rewards for bees whereas others 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 probably evolved through indirect male–male competition for siring success.
Highlights
Bee pollination poses an intriguing conflict for plants; plants rely on bees to transfer their pollen for sexual reproduction, the bees collect pollen to provision their nests
0.5 inner anthers outer anthers pistil inner anthers and removed removed removed pistil removed pollen exported to stigmas available pollen
Staggered dehiscence between anther types suggests heteranthery is a way for the flowers to gradually present their pollen to bees
Summary
Bee pollination poses an intriguing conflict for plants; plants rely on bees to transfer their pollen for sexual reproduction, the bees collect pollen to provision their nests. Instead of dividing labour between pollinating and feeding functions during a bee visit, we propose that the inconspicuous colour and deflection of the outer anther whorl make it cryptic until the conspicuous inner whorl has dehisced, at which point the outer anthers move to the center of the flower and gradually release pollen. Our study design allowed us to test one possible alternative explanation for gradual pollen dehiscence—that pollen released at the end of the male phase could assure seed set through pollinator attraction and/or autogamy during female phase We considered this explanation unlikely because stigmas open 2–7 days after outer anther dehiscence begins, at which time pollen is typically no longer present on the shriveled anthers, and styles elongate beyond the anthers at the time of receptivity [17].
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