Geometric morphometrics of functionally distinct floral organs in Iris pumila: Analyzing patterns of symmetric and asymmetric shape variations

Sanja Radović, Aleksandar Urošević, Katarina Hočevar, Ana Vuleta, Sanja Manitašević Jovanović, Branka Tucić


The Iris flower is a complex morphological structure composed of two trimerous whorls of functionally distinct petaloid organs (the falls and the standards), one whorl of the stamens and one tricarpellary gynoecium. The petal-like style arms of the carpels are banded over the basal part of the falls, forming three pollination tunnels, each of which is perceived by the Iris pollinators as a single bilaterally symmetrical flower. Apart from the stamens, all petaloid floral organs are preferentially involved in advertising rewards to potential pollinators. Here we used the methods of geometric morphometrics to explore the shape variation in falls, standards and style arms of the Iris pumila flowers and to disentangle the symmetric and the asymmetric component of the total shape variance. Our results show that symmetric variation contributes mostly to the total shape variance in each of the three floral organs. Fluctuating asymmetry (FA) was the dominant component of the asymmetric shape variation in the falls and the standards, but appeared to be marginally significant in the style arms. The values of FA indexes for the shape of falls (insects’ landing platforms) and for the shape of standards (long-distance reward signals) were found to be two orders of magnitude greater compared to that of the style arms. Directional asymmetry appeared to be very low, but highly statistically significant for all analyzed floral organs. Because floral symmetry can reliably indicate the presence of floral rewards, an almost perfect symmetry recorded for the style arm shape might be the outcome of pollinator preferences for symmetrical pollination units.

Received: July 20, 2016; Revised: September 12, 2016; Accepted: September 21, 2016; Published online: October 5, 2016

How to cite this article: Radović S, Urošević A, Hočevar K, Vuleta A, Manitašević-Jovanović S, Tucić B. Geometric morphometrics of functionally distinct floral organs in Iris pumila: Analyzing patterns of symmetric and asymmetric shape variations. Arch Biol Sci. 2017;69(2):223-31.


directional asymmetry; geometric morphometrics; floral organ shape; fluctuating asymmetry; Iris pumila

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Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature. 1991;353(6339):31-7.

Weigel D, Meyerowitz EM. The ABCs of floral homeotic genes: Review Cell. 1994;78:203-9.

Rijpkema AS, Vandenbussche M, Koes R, Heijmans K, Gerats T. Variations on a theme: changes in the floral ABCs in angiosperms. Semin Cell Dev Biol. 2010;21(1):100-7.

Sauret-Güeto S, Schiessl K, Bangham A, Sablowski R, Coen E. JAGGED controls Arabidopsis petal growth and shape by interacting with a divergent polarity field. PLoS Biol. 2013;11(4):e1001550.

Gómez JM, Torices R, Lorite J, Klingenberg CP, Perfectti F. The role of pollinators in the evolution of corolla shape variation, disparity and integration in a highly diversified plant family with a conserved floral bauplan. Ann Bot. 2016;117(5):889-904.

Harder LD, Barrett SCH. Ecology and evolution of flowers. Oxford: Oxford University Press; 2006. 370 p.

Glover BJ. Understanding flowers and flowering: an integrated approach. Oxford, UK: Oxford University Press; 2007. 227 p.

Córdoba SA, Cocucci AA. Flower power: its association with bee power and floral functional morphology in papilionate legumes. Ann Bot. 2011;108(5):919-31.

Willmer P. Pollination and floral ecology. Princeton: Princeton University Press; 2011. 778 p.

Clarke D, Whitney H, Sutton G, Robert D. Detection and learning of floral electric fields by bumblebees. Science. 2013;340(6128):66-9.

Schiestl FP, Johnson SD. Pollinator-mediated evolution of floral signals. Trends Ecol Evol. 2013;28(5):307-15.

Gómez JM, Bosch J, Perfectti F, Fernández JD, Abdelaziz M, Camacho JPM. Association between floral traits and rewards in Erysimum mediohispanicum (Brassicaceae). Ann Bot. 2008;101(9):1413-20.

Gomez JM, Munoz-Pajares AJ, Abdelaziz M, Lorite J, Perfectti F. Evolution of pollination niches and floral divergence in the generalist plant Erysimum mediohispanicum. Ann Bot. 2014;113(2):237-49.

Gómez JM, Perfectti F, Camacho JPM. Natural selection on Erysimum mediohispanicum flower shape: insights into the evolution of zygomorphy. Am Nat. 2006;168(4):531-45.

Gómez JM, Verdú M, Perfectti F. Ecological interactions are evolutionarily conserved across the entire tree of life. Nature. 2010;465(7300):918-21.

Gómez JM, Perfectti F. Evolution of complex traits: the case of Erysimum corolla shape. Int J Plant Sci. 2010;171(9):987-98.

Møller AP. Bumblebee preference for symmetrical flowers. Proc Nat Acad Sci USA. 1995;92(6):2288-92.

Parsons PA. Fluctuating asymmetry: an epigenetic measure of stress. Biol Rev. 1990;65(2):131-45.

Lawing AM, Polly PD. Geometric morphometrics: recent applications to the study of evolution and development. J Zool. 2010;280(1):1-7.

Savriama Y, Klingenberg C. Beyond bilateral symmetry: geometric morphometric methods for any type of symmetry. BMC Evol Biol. 2011;11(1):280.

Savriama Y, Gómez JM, Perfectti F, Klingenberg CP. Geometric morphometrics of corolla shape: dissecting components of symmetric and asymmetric variation in Erysimum mediohispanicum (Brassicaceae). New Phytol. 2012;196(3):945-54.

Zelditch ML, Swiderski DL, Sheets HD. Geometric morphometrics for biologists: a primer. Amsterdam: Academic Press; 2012. 478 p.

Klingenberg CP, Duttke S, Whelan S, Kim M. Developmental plasticity, morphological variation and evolvability: A multilevel analysis of morphometric integration in the shape of compound leaves. J Evol Biol. 2012;25(1):115-29.

Gardner AG, Gerald JNF, Menz J, Shepherd KA, Howarth DG, Jabaily RS. Characterizing floral symmetry in the Core Goodeniaceae with geometric morphometrics. PLoS One. 2016;11(5):e0154736.

Klingenberg CP. Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet. 2010;11(9):623-35.

Adams DC, Rohlf FJ, Slice DE. A field comes of age: geometric morphometrics in the 21st century. Hystrix. 2013;24(1):7-14.

Mathew B. The Iris. Portland, OR: Timber Press; 1981.

Pande PC, Singh V. Floral development of Iris decora Wall. (Iridaceae). Bot J Linn Soc. 1981;83:41-56.

Proctor M, Yeo P. The pollination of flowers. New York: Taplinger Pub. Co.; 1973. 418 p.

Goldblatt P, Manning JC, Bernhardt P. Pollination biology of Lapeirousia subgenus Lapeirousia (Iridaceae) in southern Africa; floral divergence and adaptation for long-tongued fly pollination. Ann Missouri Bot Gard. 1995;517-34.

Sapir Y, Shmida A, Ne’eman G. Pollination of Oncocyclus irises (Iris: Iridaceae) by night-sheltering male bees. Plant Biol. 2005;7(04):417-24.

Sapir Y, Shmida A, Ne’eman G. Morning floral heat as a reward to the pollinators of the Oncocyclus irises. Oecologia. 2006;147(1):53-9.

Segal B, Sapir Y, Carmel Y. Fragmentation and pollination crisis in the self-incompatible Iris bismarckiana (Iridaceae), with implications for conservation. Isr J Ecol Evol. 2006;52(2):111-22.

Imbert E, Wang H, Anderson B, Hervouet B, Talavera M, Schatz B. Reproductive biology and colour polymorphism in the food-deceptive Iris lutescens (Iridaceae). Acta Bot Gall. 2014;161(2):117-27.

Lavi R, Sapir Y. Are pollinators the agents of selection for the extreme large size and dark color in Oncocyclus irises? New Phytol 2015;205(1):369-77.

Gajić M. The Flora of the Deliblato Sand. Novi Sad, Serbia: Fac Nat Sci Inst Biol Univ Novi Sad. 1983.

F. K. Iris. Stuttgart: Verlag Eugen Ulmer; 1981.

Tucić B, Milojković S, Vujčić S, Tarasjev A. Clonal diversity and dispersion in Iris pumila. Acta oecologica. 1988;9(2):211-9.

Manitašević Jovanović S, Tucić B, Matić G. Differential expression of heat-shock proteins Hsp70 and Hsp90 in vegetative and reproductive tissues of Iris pumila. Acta Physiol Plant. 2011;33(1):233-40.

Tucić B, Vuleta A, Manitašević Jovanović S. Exploring phenotypic floral integration in Iris pumila L.: a common-garden experiment. Arch Biol Sci. 2013;65:781-93.

Dryden IL, Mardia K V. Statistical shape analysis. Chichester, New York: John Wiley & Sons; 1998. 347 p.

Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011;11(2):353-7.

Klingenberg CP, Barluenga M, Meyer A. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution. 2002;56(10):1909-20.

Klingenberg CP. Analyzing fluctuating asymmetry with geometric morphometrics: Concepts, methods, and applications. Symmetry. 2015;7(2):843-934.

Leamy LJ, Klingenberg CP. The genetics and evolution of fluctuating asymmetry. Annu Rev Ecol Evol Syst. 2005;1-21.

Debat V, David P. Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol. 2001;16(10):555-61.

Palmer AR, Strobeck C. Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst. 1986;391-421.

Klingenberg CP, McIntyre GS. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution. 1998;52(5):1363-75.

Palmer AR, Strobeck C. Fluctuating asymmetry analyses revisited. In: Polak M, editor. Developmental instability. Causes and consequences. Oxford: Oxford Univ Press; 2003. p. 279-319.

Jojić V, Blagojević J, Vujošević M. B chromosomes and cranial variability in yellow-necked field mice (Apodemus flavicollis). J Mammal. 2011;92(2):396-406.

Debat V, Alibert P, David P, Paradis E, Auffray JC. Independence between developmental stability and canalization in the skull of the house mouse. Proc R Soc London B Biol Sci. 2000;267(1442):423-30.

Waddington CH. The strategy of the genes. A discussion of some aspects of theoretical biology. London: Allen & Unwin; 1957.

Palmer AR. Waltzing with asymmetry. Bioscience. 1996;46(7):518-32.

Klingenberg CP, Nijhout HF. Genetics of fluctuating asymmetry: a developmental model of developmental instability. Evolution. 1999;53(2):358-75.

Klingenberg CP. A developmental perspective on developmental instability: theory, models and mechanisms. In: Polak M, ed. Developmental instability: causes consequences. Oxford: Oxford University Press; 2003. p. 14-34.

Merlin F. Developmental noise: Explaining the specific heterogeneity of individual organisms. In: Braillard PA, Malaterre C, editors. Explanation in Biology. Netherlands: Springer; 2015. p. 91-110.

Nijhout HF, Davidowitz G. Developmental perspectives on phenotypic variation, canalization, and fluctuating asymmetry. In: Polak M, ed. Developmental instability: causes and consequences. Oxford: Oxford University Press; 2003. p. 3-13.

Yoshioka Y, Ohashi K, Konuma A, Iwata H, Ohsawa R, Ninomiya S. Ability of bumblebees to discriminate differences in the shape of artificial flowers of Primula sieboldii (Primulaceae). Ann Bot. 2007;99(6):1175-82.

Wilson P. Variation in the intensity of pollination in Drosera tracyi: Selection is strongest when resources are intermediate. Evol Ecol. 1995;9(4):382-96.

Møller AP, Sorci G. Insect preference for symmetrical artificial flowers. Oecologia. 1998;114(1):37-42.

West EL, Laverty TM. Effect of floral symmetry on flower choice and foraging behaviour of bumble bees. Can J Zool. 1998;76(4):730-9.


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