The evolution of flower development: current understanding and future challenges.

One of the most fascinating questions in evolutionary biology is understanding how novelties such as new organs or novel body plans arise. Answering this question is all the more challenging as obvious predecessors cannot always be identified in the incomplete fossil record. Evolutionary developmental (evo-devo) studies address this issue by examining how developmental mechanisms have evolved over time. To undertake such studies, rigorous assessment of trait homology (i.e. inherited from a common ancestral trait) is necessary, and this can now be conducted in a robust phylogenetic framework thanks to the remarkable recent progress in molecular systematics (e.g. APG III, 2009; Moore et al., 2010). Close examination of the sequence of developmental events underlying homologous traits, and the genes regulating developmental changes, is critical to our understanding of the present state and evolution of biodiversity. Indeed, the emergence of novel body plans or organs very often coincides with the rise of a wealth of new species, suggesting that evo-devo concepts can revolutionize our understanding of macro-evolutionary events. The flower is doubtlessly the most beautiful example of an evolutionary innovation that is believed to have been a major contributor to the diversification of angiosperms. Flowering plants nowadays dominate terrestrial ecosystems and, as a major food source, are of outstanding importance for mankind. Floral structure is generally conserved with four main organ types (sepals, petals, stamens and carpel); however, the variation on this theme is breathtaking. The types of variation include abortion of organs, radial versus bilateral symmetry, whorled or spiral phyllotaxis, dramatic variations in the colour, arrangement, number or size of floral organs, or even evolution of extra floral organs, such as, for example, in the genus Aquilegia. In recognition of the recent advances in our understanding of the mechanisms involved in the evolution of floral phenotypes, this issue gathers together eleven articles contributing to the field of ‘flower evo-devo’, which represent diverse approaches ranging from morphological and developmental comparative studies, to phylogenetic analyses of important developmental regulators, and gene function analysis in non-model plants. Beyond their remarkable appearance and diversity that enchant our eyes (Fig. 1), flowers function as the angiosperm reproductive system. The amazing morphological diversity results from the interplay of selection and developmental constraints; however, evaluating the relative importance of these two evolutionary forces is not straightforward. Traits that have evolved several times independently provide interesting frameworks for addressing this issue. For instance, bilateral symmetry appears to be an adaptive trait that has probably evolved jointly with specialized pollinators, increasing precision in pollen deposition on the pollinator’s body and thus resulting in better cross-pollination efficiency (e.g. Citerne et al., 2010). Symmetry characteristics involved in flower–pollinator interactions are often clade-specific but with conserved general trends (e.g. bilaterally symmetrical flowers exist in Orchidaceae and Fabaceae but with different architectures: Fig. 1C, H). Bilateral floral symmetry probably emerged repeatedly as a result of selection for increased reproductive efficiency, and involved the evolutionary tinkering of inherited genetic networks (Jacob, 1977). The molecular network controlling flower symmetry is beginning to be characterized in distantly related taxa of core eudicots, revealing both shared and different factors (Costa et al., 2005; Wang et al., 2008). Similarly, selfing has evolved multiple times from outbreeding, with associated changes in several floral traits. In this Special Issue, Sicard and Lenhard (2011) examine the selfing syndrome, with a specific focus on sex allocation to male vs. female function and flower morphology. The molecular bases of these traits are still largely unknown, but this system appears promising for examining the importance of genetic constraints in evolution, especially in the early stages of the transition to selfing when selection associated with outbreeding is expected to be relieved. Homeotic mutants in model organisms have been crucial for the discovery of genes controlling key steps in developmental processes. The evolutionary potential of homeotic mutants is still strongly debated. Goldschmidt (1940) was the first to propose the concept of ‘hopeful monsters’, which has been strongly challenged by the tenants of the Synthetic Theory of evolution. It seems, however, that discrete phenotypical differences between species cannot always be explained by the accumulation of small changes and that, in at least some cases, evolution may have proceeded in a saltationist rather than a gradualist way (Rudall and Bateman, 2003; Theißen, 2009). Gould underlined that mutations in key developmental genes could result in drastic phenotypical changes in adult forms without conflicting with the Darwinian theory, and that the evolutionary potential of such phenotypes could not be simply dismissed (Gould, 1980). In plants, few mutants of floral phenotype are known (e.g. the ‘peloria’ flower in Linaria; Gustafsson, 1979): in this issue, Wang et al. (2011,