Darwin's Vexing Contrivance: a New Hypothesis for Why Some Flowers Have Two Kinds of Anther

Overview

Journal Proc Biol Sci

Specialty Biology

Date 2020 Dec 22

PMID 33352073

Citations 6

Authors

Kathleen M Kay

Tania Jogesh

Diana Tataru

Sami Akiba

Affiliations

Soon will be listed here.

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 (Onagraceae) and study plant-pollinator interactions in two heterantherous 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.

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References

Briscoe A, Chittka L . The evolution of color vision in insects. Annu Rev Entomol. 2000; 46:471-510. DOI: 10.1146/annurev.ento.46.1.471. View

Harder L . Behavioral responses by bumble bees to variation in pollen availability. Oecologia. 2017; 85(1):41-47. DOI: 10.1007/BF00317341. View

Peitsch D, Fietz A, Hertel H, de Souza J, Ventura D, Menzel R . The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A. 1992; 170(1):23-40. DOI: 10.1007/BF00190398. View

Peach K, Mazer S . Heteranthery in Clarkia: pollen performance of dimorphic anthers contradicts expectations. Am J Bot. 2019; 106(4):598-603. DOI: 10.1002/ajb2.1262. View

Bateman A . Intra-sexual selection in Drosophila. Heredity (Edinb). 1948; 2(Pt. 3):349-68. DOI: 10.1038/hdy.1948.21. View

Amorim T, Marazzi B, Soares A, Forni-Martins E, Muniz C, Westerkamp C . Ricochet pollination in Senna (Fabaceae) - petals deflect pollen jets and promote division of labour among flower structures. Plant Biol (Stuttg). 2017; 19(6):951-962. DOI: 10.1111/plb.12607. View

Tonnabel J, David P, Pannell J . Do metrics of sexual selection conform to Bateman's principles in a wind-pollinated plant?. Proc Biol Sci. 2019; 286(1905):20190532. PMC: 6599987. DOI: 10.1098/rspb.2019.0532. View

Briscoe Runquist R, Grossenbacher D, Porter S, Kay K, Smith J . Pollinator-mediated assemblage processes in California wildflowers. J Evol Biol. 2016; 29(5):1045-58. DOI: 10.1111/jeb.12845. View

Vorobyev M, Brandt R, Peitsch D, Laughlin S, Menzel R . Colour thresholds and receptor noise: behaviour and physiology compared. Vision Res. 2001; 41(5):639-53. DOI: 10.1016/s0042-6989(00)00288-1. View

10.

Kay K, Jogesh T, Tataru D, Akiba S . Darwin's vexing contrivance: a new hypothesis for why some flowers have two kinds of anther. Proc Biol Sci. 2020; 287(1941):20202593. PMC: 7779490. DOI: 10.1098/rspb.2020.2593. View

11.

Vallejo-Marin M, Manson J, Thomson J, Barrett S . Division of labour within flowers: heteranthery, a floral strategy to reconcile contrasting pollen fates. J Evol Biol. 2009; 22(4):828-39. DOI: 10.1111/j.1420-9101.2009.01693.x. View

12.

Thomson J . Tactics for male reproductive success in plants: contrasting insights of sex allocation theory and pollen presentation theory. Integr Comp Biol. 2011; 46(4):390-7. DOI: 10.1093/icb/icj046. View

13.

Tang L, Huang S . Evidence for reductions in floral attractants with increased selfing rates in two heterandrous species. New Phytol. 2007; 175(3):588-595. DOI: 10.1111/j.1469-8137.2007.02115.x. View

14.

Thomson J . When is it mutualism?. Am Nat. 2003; 162(4 Suppl):S1-9. DOI: 10.1086/378683. View

15.

Lloyd D, Yates J . INTRASEXUAL SELECTION AND THE SEGREGATION OF POLLEN AND STIGMAS IN HERMAPHRODITE PLANTS, EXEMPLIFIED BY WAHLENBERGIA ALBOMARGINATA (CAMPANULACEAE). Evolution. 2017; 36(5):903-913. DOI: 10.1111/j.1558-5646.1982.tb05462.x. View

16.

Charnov E . Simultaneous hermaphroditism and sexual selection. Proc Natl Acad Sci U S A. 1979; 76(5):2480-4. PMC: 383626. DOI: 10.1073/pnas.76.5.2480. View

17.

Barrett S . Darwin's legacy: the forms, function and sexual diversity of flowers. Philos Trans R Soc Lond B Biol Sci. 2010; 365(1539):351-68. PMC: 2838255. DOI: 10.1098/rstb.2009.0212. View

18.

Castellanos M, Wilson P, Keller S, Wolfe A, Thomson J . Anther evolution: pollen presentation strategies when pollinators differ. Am Nat. 2006; 167(2):288-96. DOI: 10.1086/498854. View

19.

Vallejo-Marin M, Da Silva E, Sargent R, Barrett S . Trait correlates and functional significance of heteranthery in flowering plants. New Phytol. 2010; 188(2):418-25. DOI: 10.1111/j.1469-8137.2010.03430.x. View

20.

van der Kooi C, Dyer A, Kevan P, Lunau K . Functional significance of the optical properties of flowers for visual signalling. Ann Bot. 2018; 123(2):263-276. PMC: 6344213. DOI: 10.1093/aob/mcy119. View