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

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.

Keywords: Clarkia; Darwin; bee pollination; heteranthery; intrasexual selection; pollen presentation.

Figure 1.

A selection of Clarkia flowers exhibiting heteranthery. Flowers are recently opened, showing the erect conspicuous inner anther whorl and the inconspicuous and reflexed pink, purple or red outer anther whorl. Photos by K. Kay and D. Tataru.

Figure 2.

The consensus phylogeny of diploid Clarkia shows a single evolution of heteranthery in a predominantly bee-pollinated clade. There are two independent losses of heteranthery in autogamous species (C. epilobioides and C. heterandra, the latter of which has sterile inner anthers), whereas one autogamous species (C. modesta) retains both heteranthery and anther movement. (Online version in colour.)

Figure 3.

Timing and duration of inner and outer anther dehiscence since anthesis for six Clarkia species with heteranthery (top) and five without (bottom), as determined by time lapse photography. Clarkia breweri and C. concinna only have one anther whorl, and C. epilobioides anthers fully dehisce prior to flower opening. Heterantherous species have significantly less overlap between anther whorls in the timing of pollen release. (Online version in colour.)

Figure 4.

The proportion of purple (outer anther) pollen found on bee scopae and plant stigmas does not differ but does increase with total pollen counts in a natural population of C. cylindrica. Flowers produce a higher proportion of purple pollen (dashed line, estimated from greenhouse-grown plants) than is typically found on either stigmas or bees.

Figure 5.

Green contrast values from flower colour reflectance from six heterantherous Clarkia species. In freshly opened flowers, undehisced outer anthers are significantly less conspicuous than the exposed pollen from inner anthers.

Figure 6.

(a) Field photos (K. Kay) of C. unguiculata flowers used as experimental controls. In the morning, newly opened flowers had inner anthers beginning to release pollen and outer anthers reflexed, whereas in the afternoon inner anthers were shriveled and outer anthers were erect and releasing pollen. (b) Proportional reduction in bee visitation compared to control flowers (horizontal black line) for altered C. unguiculata flowers in the morning (closed circles) and afternoon (open circles; *p < 0.05, **p < 0.01, ***p < 0.001). Photos of modified flowers are found in electronic supplementary material, figure S1. (Online version in colour.)

Figure 7.

Although dosing C. unguiculata flowers expose far less pollen than fully dehisced flowers (a), similar amounts are exported to stigmas (b).