Evolutionary significance of granular exine structure in the light of phylogenetic analyses

Abstract

In 1973 Van Campo and Lugardon recognized granular structure as a third major type of exine structure in seed plants, in addition to columellar (restricted to angiosperms) and alveolar (restricted to other seed plants, such as cycads and saccate conifers). Because they found granular structure both in other seed plants (non-saccate conifers, Gnetales) and in angiosperms (some Magnoliales, monocots, and “Amentiferae”), they suggested it might be ancestral in angiosperms. This suggestion was elaborated by other workers and supported by studies of Le Thomas and Lugardon on Annonaceae (Magnoliales), which appeared to show origin of columellae by various modifications of granules. Phylogenetic (cladistic) analyses of seed plants based on morphological and molecular data modify this scheme considerably but reaffirm the systematic interest of granular structure. In conifers and Gnetales (which probably form a clade), granular structure appears to be derived from alveolar (as in Pinaceae, Podocarpaceae and extinct outgroups of conifers). Molecular analyses root the phylogenetic tree of angiosperms among Amborella, Nymphaeales, and Austrobaileyales, which have columellar and related exine structures, implying that granular exines were derived within angiosperms. This contradicts earlier views that granular structure provides evidence for a relationship between angiosperms and outgroups such as Gnetales and Bennettitales. Phylogenetic analyses indicate that granular structure was derived from columellar within Magnoliales and Laurales, in each of which it is an important synapomorphy of a major subgroup; the same may also be true for Fagales. However, phylogenetic analyses of Annonaceae confirm that granular structure is ancestral in this group and columellar is derived, essentially as a reversal to the ancestral state in angiosperms. In Fagales granular structure is associated with wind pollination, but not in Magnoliales and Laurales; however, in all three cases it may be correlated with reduction in exine thickness.