Recent advances in molecular phylogenetics and a series of important palaeobotanical discoveries have revolutionized our understanding of angiosperm diversification. Yet, the origin and early evolution of their most characteristic feature, the flower, remains poorly understood. In particular, the structure of the ancestral flower of all living angiosperms is still uncertain. Here we report model-based reconstructions for ancestral flowers at the deepest nodes in the phylogeny of angiosperms, using the largest data set of floral traits ever assembled. We reconstruct the ancestral angiosperm flower as bisexual and radially symmetric, with more than two whorls of three separate perianth organs each (undifferentiated tepals), more than two whorls of three separate stamens each, and more than five spirally arranged separate carpels. Although uncertainty remains for some of the characters, our reconstruction allows us to propose a new plausible scenario for the early diversification of flowers, leading to new testable hypotheses for future research on angiosperms.

No abstract

The staggering diversity of angiosperms and their flowers has fascinated scientists for centuries. However, the quantitative distribution of floral morphological diversity (disparity) among lineages and the relative contribution of functional modules (perianth, androecium and gynoecium) to total floral disparity have rarely been addressed. Focusing on a major angiosperm order (Ericales), we compiled a dataset of 37 floral traits scored for 381 extant species and nine fossils. We conducted morphospace analyses to explore phylogenetic, temporal and functional patterns of disparity. We found that the floral morphospace is organized as a continuous cloud in which most clades occupy distinct regions in a mosaic pattern, that disparity increases with clade size rather than age, and that fossils fall in a narrow portion of the space. Surprisingly, our study also revealed that among functional modules, it is the androecium that contributes most to total floral disparity in Ericales. We discuss our findings in the light of clade history, selective regimes as well as developmental and functional constraints acting on the evolution of the flower and thereby demonstrate that quantitative analyses such as the ones used here are a powerful tool to gain novel insights into the evolution and diversity of flowers.

In molecular phylogenetic studies, Actinidiaceae, Roridulaceae and Sarraceniaceae form a strongly supported clade, which is sister to the ericoid clade (Clethraceae, Cyrillaceae and Ericaceae). In pre-molecular classifications, the sarracenioid families were often not affiliated with other ericalean taxa or considered to be closely related with each other, as they differ conspicuously in their habit, mode of nutrient uptake and/or superficial floral structure. In order to interpret the findings of molecular phylogenetic analyses from a morphological point of view, a detailed comparative study of floral morphology, anatomy and histology of these three families is presented. In addition, earlier literature is reviewed. The three families share a series of general and, at the level of Ericales, most likely plesiomorphic floral features, including pentamery, actinomorphy and hypogyny. Other, more specialized features, such as polystemony, choripetaly and integument number, turn out to be homoplasious in the sarracenioid clade. A floral feature shared by the three families is late anther inversion, which, in Ericales, is restricted to the sarracenioids and ericoids. Potential synapomorphies for the sarracenioids include tanniferous floral tissue, vesicles that appear to contain condensed tannins in floral tissue, proximally thick petals, ovules with a nucellar hypostase and the presence of iridoid compounds. For the subclade of Actinidiaceae and Roridulaceae, potential synapomorphies include the presence of raphides and mucilage cells in floral tissue, a secretory inner surface in the gynoecium and the absence of synlateral vasculature in the ovary. Floral features in the clade are discussed and compared with the other families of Ericales. Further structural studies in other clades of Ericales and a well-resolved molecular phylogeny of the order are needed to test the systematic value of these features further. Some features may turn out to be true synapomorphies, whereas others may turn out to be widespread in Ericales and therefore plesiomorphic for the order.

The sarracenioid families (Actinidiaceae, Roridulaceae, Sarraceniaceae) were rarely affiliated with other ericalean taxa in pre‐molecular classifications and have seldom been considered closely related to each other. In molecular phylogenetic studies, the sarracenioids form a strongly supported clade and are sister to the ericoid clade (Clethraceae, Cyrillaceae, Ericaceae); the sarracenioids and ericoids together make up core Ericales. To date, no phylogenetic study has included all sarracenioid genera (Actinidia, Clematoclethra and Saurauia in Actinidiaceae; Roridula in Roridulaceae; Darlingtonia, Heliamphora and Sarracenia in Sarraceniaceae). In particular, the monophyly of Saurauia has not previously been tested using molecular characters. We shed light on the phylogenetic relationships within the sarracenioid clade and, based on ancestral state reconstructions, test floral characters previously suggested as potential synapomorphies for the sarracenioids and ericoids. Phylogenetic analysis was performed for the DNA regions ITS, rbcL, rpl32‐trnL, trnK and trnL‐F using RAxML, MrBayes and PAUP*. Our results support the monophyly of the sarracenioid clade as well as of all its families and non‐monotypic genera. Two distinct geographical lineages are identified in Saurauia; the two lineages are characterised by differences in petal union (choripetaly versus sympetaly), style union (free versus partially united), gynoecium merism and base chromosome numbers. Our analyses identify the following floral characters as synapomorphic for core Ericales: adaxial anther attachment, anther inversion and a depression at the ovary‐to‐style transition. Proximally thick to massive petals, the presence of a nucellar hypostase in ovules and polystemony are synapomorphies of the sarracenioid clade. The presence of calcium oxalate raphides, mucilage cells, a secretory inner gynoecium surface and the absence of synlateral vasculature in the ovary are synapomorphies of the Actinidiaceae‐Roridulaceae clade. A two‐whorled androecium is a synapomorphy of the ericoid clade.

The Hymenodicteae-Naucleeae clade is a predominantly Paleotropical group with 220 species in 28 genera. The phylogenetic relationships and generic limits within Naucleeae have previously been assessed using combined molecular-morphological data, however the status of some genera remains questionable. The evolutionary relationships within Hymenodictyeae have never been investigated before. We performed phylogenetic analyses of the Hymenodictyeae-Naucleeae clade using nuclear [nrETS; nrITS] and chloroplast [ndhF; rbcL; rps16; trnT-F] data and a large sampling of both tribes. Our study supports the monophyly of the tribes, all subtribes of Naucleeae (Adininae, Breoniinae, Cephalanthinae, Corynantheinae, Mitragyninae, Naucleinae, and Uncariinae), and the Hymenodictyeae genera Hymenodictyon and Paracorynanthe. In Naucleeae, the monotypic genera Adinauclea, Metadina, and Pertusadina are nested within Adina, Mitragyna within Fleroya, Ludekia, Myrmeconauclea, and Ochreinauclea within Neonauclea, and Burttdavya and Sarcocephalus within Nauclea. Corynanthe and Pausinystalia are mutually paraphyletic. We provisionally maintain the current generic status of Neonauclea and its allied genera, pending further study. In sum, we recognize 17 genera in Naucleeae:

Summary Morphological diversity (disparity) is an essential but often neglected aspect of biodiversity. Hence, it seems timely and promising to re‐emphasize morphology in modern evolutionary studies. Disparity is a good proxy for the diversity of functions and interactions with the environment of a group of taxa. In addition, geographical and ecological patterns of disparity are crucial to understand organismal evolution and to guide biodiversity conservation efforts. Here, we analyse floral disparity across latitudinal intervals, growth forms, climate types, types of habitats, and regions for a large and representative sample of the angiosperm order Ericales. We find a latitudinal gradient of floral disparity and a decoupling of disparity from species richness. Other factors investigated are intercorrelated, and we find the highest disparity for tropical trees growing in African and South American forests. Explanations for the latitudinal gradient of floral disparity may involve the release of abiotic constraints and the increase of biotic interactions towards tropical latitudes, allowing tropical lineages to explore a broader area of the floral morphospace. Our study confirms the relevance of biodiversity parameters other than species richness and is consistent with the importance of species interactions in the tropics, in particular with respect to angiosperm flowers and their pollinators.

The early floral development of Actinidia (A. arguta, A. callosa, A. chinensis and A. kolomikta; Actinidiaceae), Saurauia (S. montana, S. oldhamii, S. pittieri and S. subspinosa; Actinidiaceae), Roridula gorgonias (Roridulaceae) and Heliamphora nutans (Sarraceniaceae) was studied comparatively using scanning electron microscopy. Late stages of androecium development are additionally presented for Clematoclethra scandens (Actinidiaceae), Darlingtonia californica and Sarracenia leucophylla (Sarraceniaceae). Flowers are typically pentamerous and share a number of developmental features: perianth organs emerge in a clockwise or anticlockwise spiral sequence on the floral apex with relatively long plastochrons between successive organs, resulting in conspicuous size differences among perianth organs in early development; the perianth always consists of two differentiated whorls (unlike earlier interpretations of the perianth in Heliamphora); the androecium is polystemonous in most species and is initiated with leading stamens in alternipetalous positions; successive stamen primordia appear in a lateral succession until a ring‐like structure is formed; and the anthers become inverted shortly before anthesis. Later androecial development differs conspicuously between taxa and further proliferation may be centrifugal, centripetal and/or lateral. For Ericales, unusual features of floral development include: petals initiated in a spiral sequence (but later organized in a whorl) with comparatively long plastochrons between individual petals (except Saurauia); common occurrence of perianth organs in double positions in Actinidiaceae; and anthers that become inverted close to anthesis. The floral development in the sarracenioids is additionally compared with that of other families and clades in Ericales, further emphasizing the highly variable patterns of androecium development in the order.