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.

Stamen dimorphism in bird‐pollinated flowers: Investigating alternative hypotheses on the evolution of heteranthery

“…Our results are in line with recent work by Kay et al. (2020), challenging the long‐standing view that the ‘pollen dilemma’ drove the evolution of heteranthery. While we are convinced that “division of labor” is one important functional aspect of heteranthery in pollen rewarding flowers, we call for rigorous testing of alternative functional and evolutionary hypotheses, especially in lineages with non‐pollen‐rewarding heterantherous flowers, to arrive at a more inclusive evolutionary perspective on this fascinating aspect of floral diversity and evolution.…”

“…This finding has important implications when thinking about male fitness and siring success (Kay et al. 2020) as well as about female fitness. Generally, reproductive success should be optimized if a pollinator delivers purely conspecific pollen loads, originating from several genetically different pollen donors (Paschke et al.…”

“…Kay et al. (2020) found, for example, that in Clarkia (Onagraceae), the showy stamen whorl is depleted before the inconspicuous one. Later in anthesis, however, pollinators will shift their foraging to the inconspicuous whorl.…”

“…Consequently, one may expect selection to act toward increasing the number of independent foraging trips to a flower, thereby maximizing chances of receiving different (ideally outcross) pollen loads (increasing both male and female fitness) and distributing pollen to many different vectors (increasing male fitness, Kay et al. 2020). If important, this strategy may occur both in pollen‐rewarding systems and in systems offering alternative rewards.…”

A sophisticated case of division of labour in the trimorphic stamens of theCassia fistula(Leguminosae) flower

“…Floral buds at different stages were collected and fixed in FAA 70 (formalin:acetic acid:alcohol; Johansen 1940 ), gradually dehydrated in an ethanol series and stored in 70 % ethanol. Then, the floral buds at several developmental stages were dissected to investigate the ontogeny of internal floral whorls, especially the androecium whorls, using a Leica MZ 75 stereomicroscope and a Leica S APO stereomicroscope.…”