Homology and Evolution of Petals in the Core Eudicots Louis P. Ronse De Craene Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, U.K. (l.ronsedecraene@rbge.ac.uk) Communicating Editor: Daniel Potter Abstract—Seventeen morphological characters are described and plotted on a phylogeny of the eudicots. The distribution of perianth characters demonstrates that the currently held view that petals originated from stamens in the core eudicots is not consistent with the predominance of bract-derived petals (bracteopetals). Petals in the core eudicots have the same morphological affinities and structure as sepals or bracts, with a few notable exceptions. Depending on the most likely topology, Berberidopsidales may represent the plesiomorphic perianth condition in the core eudicots, giving rise to pentamerous flowers with sepals and petals of a similar tepaline origin. Within the core eudicots several divergent trends have led to a wide variety of perianth morphologies involving to different degrees the presence of a calyx and corolla. Different factors contribute to the development of a biseriate perianth, including the upward shift of bracts and their absorption in the flower and a progressive differentiation of tepals through shifts in petaloidy. A number of correlations in perianth evolution are highlighted, such as petaloid sepals linked with loss of petals and presence of a hypanthium, a reversal to tepal-like petals with secondary polymery in the androecium and gynoecium, or the loss of sepals linked with the development of stamen-petal tubes. The relationship between petal morphology and the molecular basis for petaloidy is discussed. Keywords—andropetals, Berberidopsidales, bracteopetals, evo-devo, petaloidy, perianth. Angiosperm phylogenies based on large data sets, includ- ing molecular and more rarely morphological characters (e.g. Nandi et al. 1998; Doyle and Endress 2000; Soltis et al. 2000, 2003; APG 2003; Hilu et al. 2003; Kim et al. 2004) present a useful framework for investigating the evolution of floral structures, such as petals. The core eudicots are characterized as having basically pentamerous flowers, mostly with five green sepals and five alternating showy petals, five stamens or ten stamens in two whorls (or fewer by reduction, or more through a secondary increase), and a single whorl of two to five carpels. This floral Bauplan is almost unique for the core eudicots and is fundamentally different from that of early- diverging eudicots (except for some pentamerous Ranunucu- lales), magnoliids and monocots, where spiral, dimerous or trimerous flower types predominate, and where the floral organs often fluctuate in number and organization (e.g. En- dress 1990, 2004; Drinnan et al. 1994; Ronse De Craene and Smets 1998a; Magallón et al. 1999; Doyle and Endress 2000; Zanis et al. 2003; Ronse De Craene et al. 2003). Discussions on the origin of the perianth are as old as plant morphology (reviewed in Weberling 1989; Endress 1994; Al- bert et al. 1998; Ronse De Craene and Smets 2001a; Kramer et al. 2003; Zanis et al. 2003) and center on whether the perianth was derived from bracts, from stamens, from bracts and sta- mens, or had a de novo origin. The issue of petal origin has been dominated by the classic view that petals evolved sev- eral times, either centripetally through the transformation of bract-like phyllomes (bracteopetals), or centrifugally from ster- ile stamens (andropetals; e.g. Celakovsky 1896, 1900; Worsdell 1903; Hallier 1912; Troll 1927; Puri 1951; Eames 1961; Hiepko 1965; Walker and Walker 1984, Friis and Endress 1990; Takhtajan 1991). The fact that the basalmost angiosperms (e.g. Amborella- ceae, Austrobaileyales, Nymphaeales; the ANITA grade) do not possess distinctive petals and that the basal angiosperms mostly have undifferentiated organs acting as petals, led to the general acceptance that petals in a bipartite perianth are de facto derived from stamens “as highly elaborated stami- nodes with special optical attraction function” (Endress 1994 p. 25). Within the context of Cronquist’s classification system Walker and Walker (1984 p. 516) interpreted perianth evolu- tion as a gradual series, stating that “the staminodial petals of the Rosidae-Dilleniidae-Asteridae are apparently not ho- mologous with the more primitive tepalar petals of the ‘Lower Magnoliidae’, Nymphaeales and monocots”. In the absence of petals in the fossils from the Early Cretaceous, early stamens often combined attraction with reward (Crepet et al. 1992; Crepet and Nixon 1996; Friis and Endress 1990; Friis et al. 2000) and this has been used as evidence to inter- pret petals as derived from staminodes in some groups of the rosids and Saxifragales (e.g. Crepet et al. 1992; Crepet and Nixon 1996; Gandolfo et al. 1998). Nectar leaves of Ranuncu- lales, especially Ranunculaceae (e.g. Tamura 1965, 1993; Ko- suge 1994; Endress 1995; Erbar et al. 1998), have also been presented as direct evidence of staminodial petals for the core eudicots. Staminodial petals are thus widely accepted as an undisputable reality. Endress (1994) rightly pointed to the importance of the relationship between function in the flower and determina- tion of the perianth. The differentiation of the perianth into sepals and petals rests on ecological grounds: sepals or outer perianth parts are protective structures enveloping the bud, while petals or the inner perianth parts function as at- tractants to pollinators. Although the distinction between se- pals and petals appears firmly settled, especially in the core eudicots (Table 1), transference of function can lead to dra- matic changes in the morphology of the perianth, including the loss of sepals or petals and the transformation of the remaining organs (Endress, 1994). In some cases functions can change during the lifetime of the perianth organs, de- pending on the stage of development (e.g. Helleborus L. in Ranunculaceae: Herrera 2005; Coriariaceae: Matthews and Endress 2004). Protection and attraction were originally com- bined by pigmentation of the whole perianth of the flower, as is evident in several taxa of the basal angiosperms (e.g. Illi- ciaceae, Lauraceae). This is the most economic way to obtain petals (in a structural-evolutionary context) and is a wide- spread condition for the basal angiosperms and monocots. A progressive differentiation of outer (protective) organs and inner petaline showy organs became evident at later stages of evolution and involved different developmental factors (larger flowers necessitating a longer period of maturation, seasonality, the elaboration of inflorescences with bracts, etc.). Systematic Botany (2008), 33(2): pp. 301–325 © Copyright 2008 by the American Society of Plant Taxonomists 301