Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses

Abstract

Phylogenetic analyses of molecular and morphological data, revised in this study, shed light on long‐standing controversies on the early evolution of angiosperm pollen. Although relationships between angiosperms and other seed plants remain uncertain, the robust rooting of the angiosperms among the “ANITA” groups (Amborella, Nymphaeales, Illiciales, Trimenia, and Austrobaileya) clarifies their original pollen morphology. Contrary to the view that the first angiosperms had boat‐shaped monosulcate pollen with granular or atectate exine structure, the ANITA rooting implies that globose monosulcate pollen with more or less columellar structure and a continuous tectum was ancestral and a foveolate‐reticulate tectum arose soon after. The oldest recognized Cretaceous angiosperm pollen may represent the latter grade of evolution. Structure described as granular evolved independently from columellar within Nymphaeales, Magnoliales, and Laurales. In Magnoliales, columellar Myristicaceae and Magnoliaceae diverge below Degeneria, Galbulimima, Eupomatia, and Annonaceae, which shifted to granular structure. Granular monosulcate pollen was ancestral in Annonaceae but gave rise to columellar monosulcates and permanent tetrads. In Laurales, reduction and granularization culminated in the fragile exines of Lauraceae. Although absence of a distinctly staining endexine in Magnoliales has been considered evidence that the laminated endexine of gymnosperms was lost before the origin of angiosperms, presence of a thin endexine now appears to be ancestral. These results refute the view that granular structure supports a relationship between angiosperms and Gnetales, Bennettitales, and Pentoxylon. Relationships with groups with alveolar exines (e.g., Caytonia, glossopterids) and/or reticulate‐columellar Triassic Crinopolles pollen now seem equally likely.