A flat petal as ancestral state for Ranunculaceae

Abstract

Ranunculaceae comprise ca. 2,500 species (ca. 55 genera) that display a broad range of floral diversity, particularly at the level of the perianth. Petals, when present, are often referred to as "elaborate" because they have a complex morphology. In addition, the petals usually produce and store nectar, which gives them a crucial functional role in the interaction with pollinators. Its morphological diversity and species richness make this family a particularly suitable model group for studying the evolution of complex morphologies. Our aims are (1) to reconstruct the ancestral form of the petal and evolutionary stages at the scale of Ranunculaceae, (2) to test the hypothesis that there are morphogenetic regions on the petal that are common to all species and that interspecific morphological diversity may be due to differences in the relative proportions of these regions during development. We scored and analyzed traits (descriptors) that characterize in detail the complexity of mature petal morphology in 32 genera. Furthermore, we described petal development using high resolution X-Ray computed tomography (HRX-CT) in six species with contrasting petal forms (Ficaria verna, Helleborus orientalis, Staphisagria picta, Aconitum napellus, Nigella damascena, Aquilegia vulgaris). Ancestral state reconstruction was performed using a robust and dated phylogeny of the family, allowing us to produce new hypotheses for petal evolution in Ranunculaceae. Our results suggest a flat ancestral petal with a short claw for the entire family and for the ancestors of all tribes except Adonideae. The elaborate petals that are present in different lineages have evolved independently, and similar morphologies are the result of convergent evolution.

Keywords: Ranunculaceae; ancestral state reconstruction; elaborate petals; floral morphology; petal development.

FIGURE 1

Phylogenetic tree of Ranunculaceae, including representatives of all tribes of the family. Phylogenetic tree and tribal classification are adapted from Zhai et al. (2019). Species names missing are: Anemone raddeana, Anemone chinensis, Actaea dahurica, Actaea vaginata, Actaea asiatica, Trollius chinensis, Trollius saniculifolia, Aquilegia ecalcara, Aquilegia coerulea. On the right, schematic line drawings of a selection of petals displaying the morphological diversity of petals in Ranunculaceae. Letters a-n refer to the position of the species in the phylogenetiv tree.

FIGURE 2

Three-dimensional models of six petals summarizing the morphological diversity of Ranunculaceae petals. The petals are oriented in space according to their insertion on the floral receptacle, and divided in three equal zones: proximal, median, and distal. The red dot indicates the insertion on the floral receptacle.

FIGURE 3

Bayesian ancestral state reconstructions for the character “Outgrowth on adaxial side.” Character states include “Absence,” “Presence,” “NA” (non-applicable, i.e., petals absent). (A) The character is coded for the petal as a whole, notwithstanding the zonation. Outgrowths are given in yellow in the line drawing. (B) The same character is coded for each zone (proximal, median, distal) separately.

FIGURE 4

Comparison of petal development sequences of the six species representative of the morphological diversity using fertile organ development as reference. (A) Pistil and stamen development. Developmental stages of stamens: (1–2) Increase of the primordium size (2–3) filament/anther differentiation (3–4) differentiation of the two thecae (4–5) Connective differentiation (5–6) Stamen form is acquired, formation of the pollen sacs (6–7) Stamen elongation. Developmental stages of pistil: (3–4) Acquisition of the form (4–5) Ovules in the process of formation. (B) In yellow, development of bulges in the adaxial side. In gray, development of a depression in the abaxial side. (C) Example of a virtual section from a 3D floral bud reconstruction of Staphisagria picta.

FIGURE 5

Phylogeny of the Ranunculaceae (adapted from Zhai et al., 2019) with the mapping of functional characters. (a) Perianth differentiation, (b) nectar in flowers, (c) location of nectar production. Color code for tribes as in Figure 3.