Reconstructing the ancestral angiosperm flower and its initial specializations

Abstract

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.

Ancestral traits and specializations in the flowers of the basal grade of living angiosperms

“…However, in the combined morphological and molecular analysis of Doyle & Endress (2000), which did not include Ceratophyllum, Chloranthaceae were the sister group of all other mesangiosperms, and when Endress & Doyle (2009) added Ceratophyllum to the tree it formed a clade with Chloranthaceae. This clade has also been found in a growing number of molecular analyses (Antonov & al., 2000;Duvall & al., 2006Duvall & al., , 2008Qiu & al., 2006Qiu & al., , 2010Moore & al., 2011;Zhang & al., 2012;Zeng & al., 2014;Sun & al., 2015), although its position varies greatly.…”

“…Parsimony optimization of the carpel form character on both trees used by Endress & Doyle (2009) indicates that pronouncedly ascidiate carpels are ancestral (Fig. 4).…”

“…Reviews on floral structure with different foci and various new results were provided by Endress (2001Endress ( , 2004), Endress Doyle (2009), andDoyle &Endress (2011). In the last two articles we used parsimony to reconstruct (optimize) the course of evolution of characters on two reference trees, chosen to represent the range of current phylogenetic results.…”

“…-Another commonly asked question is whether flowers of the ancestral angiosperm were bisexual or unisexual. Because Amborella has unisexual flowers, the ancestral state is equivocal in terms of parsimony (Endress & Doyle, 2009). However, although functionally unisexual flowers occur in six of the nine families considered here, there are only two families, Hydatellaceae and Ceratophyllaceae (with 16 species in total), in which all flowers are unisexual.…”

“…In a whorled flower, we can consider the number of parts per whorl (merism) and the number of whorls, but these measures are not applicable in flowers with spiral phyllotaxis. In Doyle & Endress (2000) and Endress & Doyle (2009), we treated number of whorls as comparable to number of so called series (sets of parts that fill the Version of Record circumference of the flower) in spiral flowers. Under this treatment, the ancestral angiosperm flower had more than two whorls or series in both the perianth and androecium, and if it was whorled it was trimerous.…”