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The Evolutionary Significance of Homeosis in Flowers: A Morphological Perspective

Louis P. Ronse De Craene
International Journal of Plant Sciences
Vol. 164, No. S5, Flowers—Diversity, Development, and EvolutionA conference organized and held at the Institute of Systematic Botany, University of Zurich, Switzerland, July 5–7, 2002 (September 2003), pp. S225-S235
DOI: 10.1086/376878
Stable URL: http://www.jstor.org/stable/10.1086/376878
Page Count: 11
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The Evolutionary Significance of Homeosis in Flowers: A Morphological Perspective


Homeosis is the result of a developmental process where attributes of one structure are transferred to the position normally occupied by a different structure. The importance of homeotic mutations in the evolution of flowers and their impact on the whole pollination strategy is discussed from a morphological perspective, with special reference to the development of floral organs and the underlying genetics. Three case studies are presented where transformations of organs in flowers have important evolutionary implications, and these are related to the genetic background that is causal for these changes. I hypothesize that petals in the Rosaceae are derived from stamens through homeosis. The petals usually occupy an apical position in a complex multistaminate androecium. Evidence is derived from the similar primordial morphology of petals, their occasional replacement by stamens, obhaplostemonous androecia without petals, and the position of the family next to Rhamnaceae and Urticales. It is postulated that petals and stamens are homologous structures in the Rosaceae, but they are expressed morphologically and functionally in a different way. As most members of the nearest sister groups of Rosaceae (especially Urticales) are wind pollinated, the transformation of stamens into petals led to a sudden expansion of the family through the development of better pollinator attraction. The Papaveraceae mostly have a multistaminate androecium of many whorls and three perianth whorls of bracteolar origin differentiated into sepals and petals; the outer stamens are arranged in alternation with the two inner perianth whorls. Two opposite evolutionary trends are believed to have occurred in the family. In Sanguinaria, the outer stamen whorl has been replaced by petals; in Macleaya, the two petal whorls have been replaced by stamens. Petals and stamens are nonhomologous structures, but their boundaries become shifted with the replacement of one or the other organ. In Macleaya the pollen load is increased for wind pollination, while in Sanguinaria insect attraction is enhanced by an increased number of petals. A third example is represented by Lacandonia. The stamens and carpels switch position while retaining their identity. The number of parts remains unchanged. The homeotic transformation in Lacandonia represents a unique event in evolution. The three case studies correspond with the expression of three different gene categories. Homeosis is either the result of a progressive transformation, i.e., a relocation of genetic influences (cf. the ABC model as in the Rosaceae) or a sudden mutation, i.e., a shift in boundaries in Papaveraceae or the upsetting of the bauplan of the flower in Lacandonia, leading to saltational evolution. Breeding mechanisms are likely to influence the extent of homeosis, with transformations of stamens into petals linked to an increased insect pollination through positive discrimination and the reverse transformation being related to wind pollination.

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