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
s

(1/ 3)

 Tij 

i  j 
= (1/ 6) 
 T 
ij 

i  j 
1.94
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
L
R
L
R
L
R
L
R
B Inflorescence level
C Plant level
random
L
L
R
R
L
R
L
L
L
L
L
L
L
L R
L R
L R
R
MONOMORPHIC ENANTIOSTYLY
R
R
R
R
L
L
L
L
L
L
L
L
R
R
R
R
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
NNNN
NNNN
NNNN
Straight-styled
R
L/R L/R L/R L/R
L/R L/R L/R L/R
L/R L/R L/R L/R
L/R L/R L/R L/R
M-enantiostyly
L
R
L
R
R
L
R
L
L
R
L
R
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
FA
• Small anthers attract and feed pollinators
(feeding anthers, FA)
• Large anther exports pollen to other plants
(pollinating anther, PA)
F. Müller 1883 Nature
Testing Muller’s “Division of Labour” Hypothesis
Experiments on Solanum rostratum
by Mario Vallejo-Marín
Pollinator behaviour and Pollen transfer
Methods
• 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
PA
5.1%
ab
30
35
P < 0.05
a
20
25
b
15
FA
94.8%
10
Visit length (seconds)
40
Pollen extraction effort (buzzing)
C
Control
only
FAFAonly
only
PAPAonly
J. Evolutionary Biology
(2009) 22: 828-839
Pollen from pollinating anthers is
preferentially transferred to stigmas
Recipient
5e-04
4e-04
2e-04
3e-04
P < 0.05
0e+00 1e-04
Donor
Pollendeposited/removed
deposited/Pollen removed
Pollen
2) Pollen export:
Control
Control
Heteranthery an adaptation to
resolve conflict of using male
gametes as food for pollinators
FAFAonly
only
PA
PAonly
only
Treatment
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
cpDNA 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 & cpDNA 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
QuickTime™ and a
TIFF (LZW) decompressor
are needed to see this picture.
“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 SelfFertilisation”
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 BayesDiscrete (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