Peter K. Endress

Diversity and evolutionary biology of tropical flowers

1. Introduction 2. Floral organisation (bauplan, groundplan) 3. Floral construction (architecture, gestalt) 4. Floral adaptations to different pollinators (floral styles) 5. Special differentiations associated with pollinator attraction 6. Special differentiations associated with the breeding system 7. The process of anthesis 8. Floral structure: biology of selected systematic groups in the tropics 9. Aspects of flower evolution 10. Prospects Index.

Hydatellaceae identified as a new branch near the base of the angiosperm phylogenetic tree

Although the relationship of angiosperms to other seed plants remains controversial, great progress has been made in identifying the earliest extant splits in flowering-plant phylogeny, with the discovery that the New Caledonian shrub Amborella trichopoda, the water lilies (Nymphaeales), and the woody Austrobaileyales constitute a basal grade of lines that diverged before the main radiation in the clade. By focusing attention on these ancient lines, this finding has re-written our understanding of angiosperm structural and reproductive biology, physiology, ecology and taxonomy. The discovery of a new basal lineage would lead to further re-evaluation of the initial angiosperm radiation, but would also be unexpected, as nearly all of the ∼460 flowering-plant families have been surveyed in molecular studies. Here we show that Hydatellaceae, a small family of dwarf aquatics that were formerly interpreted as monocots, are instead a highly modified and previously unrecognized ancient lineage of angiosperms. Molecular phylogenetic analyses of multiple plastid genes and associated noncoding regions from the two genera of Hydatellaceae identify this overlooked family as the sister group of Nymphaeales. This surprising result is further corroborated by evidence from the nuclear gene phytochrome C (PHYC), and by numerous morphological characters. This indicates that water lilies are part of a larger lineage that evolved more extreme and diverse modifications for life in an aquatic habitat than previously recognized.

Morphological Phylogenetic Analysis of Basal Angiosperms: Comparison and Combination with Molecular Data

We have amassed structural data for 108 characters and 52 taxa of magnoliids and basal monocots and eudicots, including observations by P. K. Endress and A. Igersheim on flowers. These data were analyzed separately and in combination with rbcL, 18S, and atpB sequences. Besides confirming agreements between previous analyses of both kinds of data (reduction of Magnoliales to six families; relation of Piperaceae, Saururaceae, Lactoris, and Aristolochiaceae), trees based on this data set show shifts toward molecular results (separation of Illiciaceae and Schisandraceae from Winteraceae and of Amborella, Austrobaileya, Trimeniaceae, and Chloranthaceae from Laurales; relation of Winteraceae and Canellaceae) plus continued conflicts (association of Chloranthaceae with Amborella and Trimeniaceae and of Nymphaeales with monocots). In cases where molecular and morphological trees conflict, combined analyses of morphological and molecular data generally yield the same topologies as molecular analyses, but morphology overcomes weak molecular evidence in indicating that Chloranthaceae belong just above the basal grade, that monocots are related to Piperales, and that Lauraceae are linked with Hernandiaceae. If angiosperms are rooted by molecular data, chloranthoid leaf teeth, two‐trace nodes, columellar (not granular) pollen, and ascidiate carpels sealed by secretion are ancestral. Vesselless xylem is primitive in Amborella but secondary in Winteraceae and Trochodendraceae.

Symmetry in Flowers: Diversity and Evolution

This article traces research on floral symmetry back to its beginnings. It brings together recent advances from different fields that converge in floral symmetry and new unpublished material on diversity and development of floral symmetry. During floral development, symmetry may change: monosymmetric flowers may have a polysymmetric early phase; polysymmetric flowers may have a monosymmetric or even asymmetric early phase; more than one symmetry change is also possible. In Lamiales s.l. (comprising the model plant Antirrhinum, where the cycloidea gene produces monosymmetric flowers with the adaxial side of the androecium reduced), taxa also occur in which the androecium is reduced on both sides, adaxial and abaxial. As a trend in asymmetric flowers, enantiomorphy (with two mirror‐image morphs) at the level of individuals seems to occur only in groups in which the flowers are predominantly of a relatively simple construction. In contrast, one morph is fixed at the level of species or higher taxa in groups with more complicated flowers. This is indicated by the apparent lack of enantiomorphy in corolla contortion in asterids but its predominance in rosids with contort flowers, or by the apparent lack of enantiomorphy in the pollination organs of asymmetric flowers in Faboideae but its presence in asymmetric flowers in Caesalpinioideae. To study the evolution of the diverse symmetry patterns, a concerted approach from different fields including molecular developmental genetics, pollination biology, and comparative diversity research is necessary.

The Flowers in Extant Basal Angiosperms and Inferences on Ancestral Flowers

This is a combination of a review and original data on floral structure, development, and biology of representatives of all families of the ANITA grade and, in addition, Chloranthaceae and Ceratophyllaceae. Since the ANITA grade has been identified as the basalmost grade of extant angiosperms based on molecular studies by a number of authors, it has become possible to search for potential plesiomorphies among flowers of extant basal angiosperms. They may include the following traits: flowers small, pollination by small insects (dipters, thrips, moths); flowers with moderate or low number of floral organs, in spiral (or whorled) arrangement, with a tendency to form organ series in Fibonacci numbers (3, 5, 8); flowers bisexual (but easily becoming unisexual because of low level of synorganization between organs), protogynous; tepals (in spiral flowers) with gradual transitions between bractlike, sepal‐like, and petal‐like forms; stamens with short filaments, anthers with a connective tip, with more or less bulging disporangiate thecae; thecae opening by a longitudinal slit and not by valves. Carpels free, styleless, extremely ascidiate, with one or only few anatropous ovules, sealed by secretion and not by postgenital fusion; stigmas wet, with multicellular protrusions. Among members of the ANITA grade, there is a trend to form extragynoecial compita. In those taxa with the relatively most complicated gynoecium architecture (including an extragynoecial compitum), there is a concomitant trend to have less strongly ascidate to almost plicate carpels (Nymphaeaceae, Schisandraceae, Illiciaceae).

Gynoecium Structure and Evolution in Basal Angiosperms

A comparative study on gynoecium structure in basal angiosperms revealed new features relevant to systematics. In addition, based on the new phylogenetic framework on basal angiosperms gained by molecular systematics, an evolutionary evaluation of gynoecial character states has become possible. Angiospermy patterns are diverse and are here tentatively grouped into four types according to the mode of carpel closure: (1) by secretion, without postgenital fusion; (2) with a continuous secretory canal but partial postgenital fusion at the periphery; (3) with an incomplete secretory canal and complete postgenital fusion at the periphery; (4) by complete postgenital fusion. In most basal angiosperms the carpels are free, and the inner space of each carpel is occluded from the outside by secretion and not by postgenital fusion (angiospermy type 1). Correlated with this feature is a pronounced ascidiate shape of the carpels. The carpels tend to be shortly stipitate. In relatively many basal clades with pluricarpellate gynoecia an extragynoecial compitum is present. Stigmas are secretory and tend to have pluricellular papillae. Ethereal oil cells at the surface of the carpels (probably intrusive) are present in Illiciales (including Trimeniaceae), Chloranthaceae, Piperales s.l. (including Aristolochiales), and Acoraceae. Ovule structure is diverse. Ovules are predominantly anatropous. Although Amborellaceae, the phylogenetically earliest branching extant angiosperm, has orthotropous ovules, it is argued that the anatropous condition is basal in angiosperms. Crassinucellar ovules are predominant in basal angiosperms. However, there are apomorphic tendencies toward ovule reduction: weakly crassinucellar (Nymphaeales, some Alismatales), pseudocrassinucellar (Acorales, some Alismatales, some Ranunculales), and tenuinucellar (some Piperales s.l., including Aristolochiales, Rafflesiales, some Alismatales). Lobation of the inner integument and semiannular shape of the outer integument are variously present or absent. They appear to be due to architectural constraints in ovule development and not to constitute archaic features. In contrast to anatropous ovules, orthotropous ovules often have an outer integument that is thinner than the inner one. This may be due to a function of the outer integument in ovule curvature as indicated by molecular developmental genetics. On the other hand, the presence of an outer integument that is thinner than the inner one characterizes the majority of the Piperales s.l. (including Aristolochiales), irrespective of presence or absence of ovule curvature.

Reconstructing the ancestral angiosperm flower and its initial specializations.

Increasingly robust understanding of angiosperm phylogeny allows more secure reconstruction of the flower in the most recent common ancestor of extant angiosperms and its early evolution. The surprising emergence of several extant and fossil taxa with simple flowers near the base of the angiosperms-Chloranthaceae, Ceratophyllum, Hydatellaceae, and the Early Cretaceous fossil Archaefructus (the last three are water plants)-has brought a new twist to this problem. We evaluate early floral evolution in angiosperms by parsimony optimization of morphological characters on phylogenetic trees derived from morphological and molecular data. Our analyses imply that Ceratophyllum may be related to Chloranthaceae, and Archaefructus to either Hydatellaceae or Ceratophyllum. Inferred ancestral features include more than two whorls (or series) of tepals and stamens, stamens with protruding adaxial or lateral pollen sacs, several free, ascidiate carpels closed by secretion, extended stigma, extragynoecial compitum, and one or several ventral pendent ovule(s). The ancestral state in other characters is equivocal: e.g., bisexual vs. unisexual flowers, whorled vs. spiral floral phyllotaxis, presence vs. absence of tepal differentiation, anatropous vs. orthotropous ovules. Our results indicate that the simple flowers of the newly recognized basal groups are reduced rather than primitively simple.

Evolutionary diversification of the flowers in angiosperms

Angiosperms and their flowers have greatly diversified into an overwhelming array of forms in the past 135 million years. Diversification was shaped by changes in climate and the biological environment (vegetation, interaction with other organisms) and by internal structural constraints and potentials. This review focuses on the development and structural diversity of flowers and structural constraints. It traces floral diversification in the different organs and organ complexes (perianth, androecium, gynoecium) through the major clades of extant angiosperms. The continuously improved results of molecular phylogenetics provide the framework for this endeavor, which is necessary for the understanding of the biology of the angiosperms and their flowers. Diversification appears to work with innovations and modifications of form. Many structural innovations originated in several clades and in special cases could become key innovations, which likely were hot spots of diversification. Synorganization between organs was an important process to reach new structural levels, from which new diversifications originated. Complexity of synorganization reached peaks in Orchidaceae and Apocynaceae with the independent evolution of pollinaria. Such a review throughout the major clades of angiosperms also shows how superficial and fragmentary our knowledge on floral structure in many clades is. Fresh studies and a multidisciplinary approach are needed.

Gunnerales are sister to other core eudicots: implications for the evolution of pentamery

Phylogenetic relationships among many lineages of angiosperms have been clarified via the analysis of large molecular data sets. However, with a data set of three genes (18S rDNA, rbcL, and atpB), relationships among lineages of core eudicots (Berberidopsidales, Caryophyllales, Gunnerales, Santalales, Saxifragales, asterids, rosids) remain essentially unresolved. We added 26S rDNA sequences to a three-gene matrix for 201 eudicots (8430 base pair aligned nucleotides per taxon). Parsimony analyses provided moderate (84%) jackknife support for Gunnerales, which comprise the two enigmatic families Gunneraceae and Myrothamnaceae, as sister to all other core eudicots. This position of Gunnerales has important implications for floral evolution. A dimerous or trimerous perianth is frequently encountered in early-diverging eudicots (e.g., Buxaceae, Proteales, Ranunculales, Trochodendraceae), whereas in core eudicots, pentamery predominates. Significantly, dimery is found in Gunneraceae and perhaps Myrothamnaceae (the merosity of the latter has also been interpreted as labile). Parsimony reconstructions of perianth merosity demonstrate lability among early-diverging eudicots and further indicate that a dimerous perianth could be the immediate precursor to the pentamerous condition characteristic of core eudicots. Thus, the developmental canalization that yielded the pentamerous condition of core eudicots occurred after the node leading to Gunnerales.

Phylogenomics and a posteriori data partitioning resolve the Cretaceous angiosperm radiation Malpighiales

The angiosperm order Malpighiales includes ∼16,000 species and constitutes up to 40% of the understory tree diversity in tropical rain forests. Despite remarkable progress in angiosperm systematics during the last 20 y, relationships within Malpighiales remain poorly resolved, possibly owing to its rapid rise during the mid-Cretaceous. Using phylogenomic approaches, including analyses of 82 plastid genes from 58 species, we identified 12 additional clades in Malpighiales and substantially increased resolution along the backbone. This greatly improved phylogeny revealed a dynamic history of shifts in net diversification rates across Malpighiales, with bursts of diversification noted in the Barbados cherries (Malpighiaceae), cocas (Erythroxylaceae), and passion flowers (Passifloraceae). We found that commonly used a priori approaches for partitioning concatenated data in maximum likelihood analyses, by gene or by codon position, performed poorly relative to the use of partitions identified a posteriori using a Bayesian mixture model. We also found better branch support in trees inferred from a taxon-rich, data-sparse matrix, which deeply sampled only the phylogenetically critical placeholders, than in trees inferred from a taxon-sparse matrix with little missing data. Although this matrix has more missing data, our a posteriori partitioning strategy reduced the possibility of producing multiple distinct but equally optimal topologies and increased phylogenetic decisiveness, compared with the strategy of partitioning by gene. These approaches are likely to help improve phylogenetic resolution in other poorly resolved major clades of angiosperms and to be more broadly useful in studies across the Tree of Life.