Forms and Function of Flowers Darwin s Legacy

Forms and Function of Flowers Darwin’s Legacy

Darwin as a Reproductive Botanist • 1836 Beagle returns • 1839 marries Emma Wedgwood • 1842 moves to Down House, Kent “During the summer of 1839…I was led to attend to the crossfertilisation of flowers by the aid of insects” Charles Darwin at 31

“Plant Reproductive Biology Central” Darwin’s Home - Down House (1842 - 1882)

Why did Darwin devote more of his life to studying plants than any other group of organisms? • Family interest and influential mentors John S. Henslow and Joseph D. Hooker • Easy to observe at Down House, able to obtain seeds & preserved flowers from his many correspondents • Plants easy to grow and manipulate, facilitating experimental tests of his adaptive hypotheses • Not just curiosity, appealed to Darwin’s practical side numerous articles in Gardener’s Chronicle

Charles Darwin’s Three Books on Plant Reproductive Biology 1862 1876 1877

Outcrossing Mechanisms & Floral Function “I do not think anything in my scientific life has given me so much satisfaction as making out the meaning of the structure of heterostylous flowers” Darwin 1876

A Test of the Darwinian Hypothesis: Pollen Transfer in Pontederia l Average proficiency of legitimate transfer m P= 1. 94 s Evolution (1985) 37: 745 -760

Diverse Stylar Polymorphisms in Flowering Plants distyly enantiostyly Wachendorfia Primula tristyly flexistyly Alpinia Eichhornia stigma-height dimorphism inversostyly Hemimeris Narcissus

Enantiostyly & Heteranthery: Darwin’s enigma “. . . [I] have wasted enormous labour over them and cannot yet get a glimpse of the meaning of the parts. ” Letter to JD Hooker, October 14 1862 Letter to JE Todd, Darwin’s last scientific correspondence 9 days before his death

Forms of Enantiostyly - Mirror Image Flowers A Flower level non-random R L L R B Inflorescence level random L R R L L L L L R L R R R MONOMORPHIC ENANTIOSTYLY C Plant level L L L L R R R R DIMORPHIC ENANTIOSTYLY Nature Reviews Genetics (2002) 3: 274 -284

Function of Enantiostyly Experiments on Solanum rostratum by Linley Jesson L NNNN Straight-styled R L/R L/R L/R L/R M-enantiostyly L R L R L D-enantiostyly

Enantiostyly Promotes Cross-Pollination Outcrossing rate Between Floral Forms 1. 0 0. 8 0. 6 S 0. 4 A D 0. 2 Straight style Monomorphic enantiostyly Dimorphic enantiostyly Nature (2002) 417: 707 D = intermorph mating A = intramorph mating S = selfing

Function of Heteranthery? “Feeding” “Pollinating” © Barrett Xylocopa (Carpenter bee) visiting Cassia fistula - Caesalpinaceae

Heteranthery Anther differentiation within flowers • Occurs in ~ 23 families Solanum Cyanella • associated with enantiostyly, bee pollination and nectarless flowers • adaptation to resolve conflict of using male gametes as food for pollinators Monochoria Cassia

Fritz Müller’s “Division of Labour” Hypothesis PA • Small anthers attract and feed pollinators (feeding anthers, FA) • Large anther exports pollen to other plants (pollinating anther, PA) F. Müller 1883 Nature FA

Testing Muller’s “Division of Labour” Hypothesis Experiments on Solanum rostratum by Mario Vallejo-Marín Methods behaviour and Pollen transfer Pollinator • Solanum rostratum arrays • Free-foraging bumble bees (Bombus impatiens) • Block access to pollen • Three treatments: • FA only (PA glued shut) • PA only (FA glued shut) • Control (sham glue) • ~30 flower visits per trial; 22 trials J. Evolutionary Biology (2009) 22: 828 -839

Bees spend more time visiting and manipulating feeding anthers Visit length (seconds) Pollen extraction effort (buzzing) P < 0. 05 a PA 5. 1% ab b FA 94. 8% Control FA only PA only J. Evolutionary Biology (2009) 22: 828 -839

Pollen from pollinating anthers is preferentially transferred to stigmas Donor Recipient Pollen deposited/removed 2) Pollen export: P < 0. 05 Control Heteranthery an adaptation to resolve conflict of using male gametes as food for pollinators FA only PA only Treatment J. Evolutionary Biology (2009) 22: 828 -839

Sexual System Diversity in Plants “As far as the sexual relations of flowers are concerned, Linnaeus long ago divided them into hermaphroditic, monoecious, dioecious, and polygamous species…but the classification is artificial, and the groups often pass into one another” Darwin 1877 “Forms of Flowers” pg. 1

Sagittaria latifolia Three sexual phenotypes Two primary sexual systems Monoecy Ecological differentiation Marcel Dorken Dioecy

Continuous Sex-Ratio Variation Female frequency Dioecy N=116 populations sampled in eastern N. America Mixed populations most common at northern range limit of dioecy Sarah Yakimowski Hermaphrodite frequency Mixed Subdioecious Gynodioecious Androdioecious Male frequency Monoecy

Origins of “Mixed-Sex” Subdioecious Populations? Two hypotheses Monoecy Dioecy Sex Inconstancy Hybridization Mixed

Genetic Markers & Hypothesis Testing • Are monoecious and dioecious populations genetically differentiated? • If so, what are the genetic characteristics of mixed-sex populations? Increase in sex inconstancy Co-occurrence of monoecious & dioecious Hybridization

Genetic Markers & Sampling 11 SSR Markers Contemporary variation • Highly polymorphic markers: Average 28 alleles per locus 1172 individuals genotyped 10 Monoecious, 12 Dioecious, 14 Mixed populations Molecular Ecology Resources (2009) 9: 579 -581 cp. DNA Markers Historical Variation • Two haplotypes based on 5 variable PCR-RFLP loci Molecular Ecology (2008) 13: 2699 -2707 Haplotype M – monoecious populations Haplotype D – dioecious populations Sarah Yakimowski

Genetic Differentiation between Monoecious & Dioecious Populations Q: If individuals are assigned to two groups are they monoecy & dioecy? Monoecious Populations Dioecious Populations STRUCTURE (Pritchard et al 2000, Falush et al. 2003) 98% genome cluster M 93% individuals pure M 97% genome cluster D 91% individuals pure D Sarah Yakimowski

Evidence for Two Pathways to Subdioecy SSR & cp. DNA markers concur Mixed Populations % Individuals Hybrid Monoecious: 7% Dioecious: 9% Mixed: 35% Hybridization Sex Inconstancy Sarah Yakimowski

Evolution of Wind Pollination Occurs in 18% of angiosperm families At least 65 independent origins from animal pollination animal wind Thalictrum thalictroides Thalictrum dioicum

Wind Pollination and Self-Pollination as Alternative Means of Reproductive Assurance “If any entomophilous species ceased altogether to be visited by insects, it would probably perish unless it were rendered anemophilous, or acquired a full capacity for self-fertilisation” Charles Darwin 1876 p. 410 “Effects of Cross and Self. Fertilisation”

Correlated Evolution of Unisexual Flowers and Wind Pollination Unisexual flowers (LR=58. 32***) Unisexual plants (LR=53. 35***) Wind pollination evolves more often in diclinous taxa, either unisexual flowers (LR=13. 63***) or unisexual plants (LR=19. 30***) Methods - 560 species; 68 wind-pollinated; Phylogeny after Soltis et al (2000) Analysis using Bayes. Discrete (Pagel & Meade 2006) IJPS (2008) 169: 49 -58 Leucadendron rubrum

Why is there an association between unisexual flowers and wind pollination? Ancestral animalpollinated population Insufficient pollination causing pollen limitation Alternative outcomes same selection Self-fertilization Hermaphrodite Flowers SELECTION FOR REPRODUCTIVE ASSURANCE Wind pollination Unisexual Flowers ancestral condition determines outcome

Novel Outcrossing Mechanisms - Pollination of Babiana ringens by Malachite Sunbirds Specialized bird perch promotes outcrossing Nature (2005) 435: 41 -42

The function of whisker-like bracteoles and the case of “sapromyiophily” in Tacca chantrieri ? Amer J Bot 2005 92: 517 -524

Acknowledgements Function of heterostyly - Steven Price, Lorne Wolfe, Deborah Glover Function of enantiostyly & heteranthery - Linley Jesson, Mario Vallejo -Marín Evolution of sexual systems in Sagittaria - Marcel Dorken, Sarah Yakimowski Evolution of wind-pollination - Jannice Friedman Function of bird perches - Bruce Anderson, Bill Cole Function of pollination syndrome in Tacca - Ling Zhang, Qing-Jun Li Research funded by NSERC Discovery Grants, Canada Research Chair, Premier’s Discovery Award