Leaf variation in Ficus: an evolutionary perspective

Kandlikar Gau-LouNguyen Hai Huyen

Wu Wei-HuanYao Xin

Zeng Si-Jin28 November 2013

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Outline• Introduction to leaf diversity and Ficus• Our hypotheses• How we tested them• What we found • What it means

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Leaf diversity

• Leaves are the organs primarily responsible for photosynthesis

• Evolutionary patterns of leaf variation are not well understood (Jones et al. 2008)

Leaf variation in Pelargonium. Image from Nicotra et al. 2011

Introduction to Ficus• Ficus is a large pan-tropical genus with >800

species • Lot of variation in life history patterns and

ecology, with an equally complex evolutionary history (Harrison 2005)

• Leaves within the genus exhibit tremendous diversity

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Hemiepiphytic Ficus• Many Ficus species have a “hemi-epiphytic” life

style

• Epiphytic stage associated with water stress (Holbrook & Putz 1996, Hao et al. 2010)

Epiphytic and Terrestrial F. concinna, from Hao G.Y., et al. 2010

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Leaf variation in Ficus

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Leaf size variation• Large leaves require more “structure” to hold up

against gravity (Niklas 1999)

– Structure might come in many ways (Westbrook et al., 2012)

• For large leaves to evolve, ancestors needed to have leaves with greater structure

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Hypotheses

• HI: Hemiepiphytic figs have evolved to deal with water stressed environments– Prediction: Hemiepiphytic figs have smaller leaves

with lower specific leaf area (SLA), even when grown in common gardens with terrestrial figs

• HII: Large leaves are harder to hold up than small leaves; thus they need to be tougher– Prediction: Leaf size ~ Leaf lamina toughness– Prediction: Leaf size and leaf toughness show

patterns of correlated evolution

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Study site• Xishuangbanna Tropical Botanical Garden

Ficus collection= sampled individuals

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• Sampling intensity:– 2 trees/species; 3 leaves/tree

• Leaf traits measurements according to published protocols (Perez-Harguindeguy et al. 2013)– Leaf Area, Toughness, and SLA

• Life history data (i.e. epiphytic/terrestrial) collected from the Flora of China (eFloras 2008)

Methods

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Phylogenetic Methods

• Used a published Ficus phylogeny (Cruaud et al. 2012)

• Thirty species shared between XTBG Ficus collection and the phylogeny

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Data Analysis• Testing prediction 1– T-Tests to compare leaf area and SLA of HE/Ter

• Testing prediction 2 – Test for relationship between Leaf Area and

Toughness• Testing prediction 3– Ancestral Trait Reconstruction and Phylogenetically

Independent Contrasts (PICs) of Area and Toughness in R package phytools (Felsenstein 1985; Revell 2012)

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Results

• Prediction 1 (Hemiepiphytes ~ smaller leaves with low SLA)

Results

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Log Area of HE and Terrestrial Ficus species SLA of HE and Terrestrial Ficus species

p=0.90p=0.40

SLA

log

Are

a

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Results, cont.• Prediction 2 (Leaf area ~ Leaf toughness)

p=0.91

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Results, cont.

• Prediction 3 (Leaf area ~ Leaf toughness across the phylogeny)

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Reco

nstr

uctio

n of

log

Area

Reco

nstr

uctio

n of

Tou

ghne

ss

200 grams 1500 grams20 cm2 800 cm2

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• Prediction 3

Results, cont.

p = 0.34p=0.36

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Discussion• Prediction 1 (Hemiepiphytic figs ~ low leaf area and SLA)

– Not supported

– Environmental factors drive reported leaf variation (e.g. Holbrook & Putz 1996)

– Hemiepiphytes may have evolved other mechanisms to deal with water stress

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Discussion

• Prediction 2 (Leaf area ~ lamina toughness)– Not supported– Veins and petioles may be sufficient to support large

leaves. • Prediction 3 (Leaf area ~ lamina toughness across phylogeny)

– Not supported– Evolution of leaf size and toughness not correlated

across the phylogeny

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Discussion: Limitations• Sampling intensity may not have accounted for

intraspecific variation in leaf traits• Unbalanced data set to test Hypothesis I• Ficus phylogeny is still being developed (e.g. Yao

et al. 2013), and our methods are sensitive to the phylogeny used

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Future Directions• The evolutionary history of leaves is not well

understood• Ficus is an ideal group to study this diversity– Morphological, distributional, and life history

variation• Studies based on leaf morphology, structure,

venation, and architecture (Nicotra et al., 2011)

• Characterize leaf transcriptomes– Determine molecular basis for variation

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Acknowledgements• AFEC Instructors and Organizers– Liu Jing-Xin, Drs. Richard Corlett, Alice Hughes, Kyle

Tomlinson, Uromi Goodale, Eben Goodale, Ferry Slik– Other XTBG research groups, especially the

Evolutionary Ecology, Plant Ecophysiology, and Plant-Animal Interaction groups, and Pan Bo for helping with Ficus identification

• XTBG Ficus collection management staff• Numerous tutorials/guides to comparative

phylogenetics in R

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References• Cruaud, A., et al. 2012. An extreme case of plant-insect codiversification: figs and fig-

pollinating wasps. Systematic Botany 61(6), 1029-1047• Felsenstein K. 1985. Phylogenetics and the comparative method. American Naturalist 125, 1-

15..• Hao, G-Y., et al. 2010. Differentiation in leaf water flux and drought tolerance traits in

hemiepiphytic and non-hemiepiphytic Ficus tree species. Functional Ecology 24(4), 731-740• Harrison, R.D. 2005. Figs and the diversity of tropical rainforests. BioScience 55(12), 1053-

1064.• Holbrook, N.M., and Putz, F.E. 1996. From epiphyte to tree: differences in leaf structure and

leaf water relations associated with the transition in growth form in eight species of hemiepiphytes. Plant, Cell and Environment 19, 631-642.

• Jones, C.S., et al. 2008. Leaf shape evolution in the South African genus Pelargonium L’He’R. (Geraniaceae). Evolution 63-2, 479-497

• Niklas, K.J. A mechanical perspective on foliage leaf form and function. New Phytologist 143, 19-31.

• Nicotra, A.B., et al. The evolution and functional significance of leaf shape in the Angiosperms. Functional Plant Biology 38, 535-552

• Revell, L.J. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3(2), 217-223.

• Westbrook, J.W. et al. 2011. What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade tolerant woody species in a Neotropical forest. The American Naturalist 177(6), 800-811.

• Yao, X., et al. Exon-Primed Intron-Crossing (EPIC) Markers for Evolutionary Studies of Ficus and Other Taxa in the Fig Family (Moraceae). Appications in Plant Science 1(10).

251. South China Agricultural University 3,5. Xishuangbanna Tropical Botanical Garden2. University of Science, Vietnam National University 4. University of Minnesota

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Questions?

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F. hirta

F. cyrtophylla

F. auriculata

F. deltoidea

F. cyathistipula

F. hispida

F. ruficaulis

F. ischnopoda