Phylogeny and evolution of the horsetails: Evidence from spore wall ultrastructure

Abstract

A new comparative TEM study of the ultrastructure of the spores of the Carboniferous genus Calamites with those of Triassic Equisetites sp. and Schizoneura paradoxa, Jurassic Equisetum columnare and living Equisetum has allowed the recognition of an evolutionary series confirming that Calamites and Equisetum are closely related and belong to the same lineage. Such a relationship was previously proposed by Good [Good, C.W., 1975. Pennsylvanian-age calamitean cones, elater-bearing spores, and associated vegetative organs. Palaeontogr. Abt. B 153, 28–99.] on the basis of morphological and anatomical similarities. Indeed, this study clearly shows that the ultrastructure of the spores of Triassic and Jurassic Equisetales is intermediate between that of Carboniferous Calamites and modern Equisetum, demonstrating that Equisetum evolved from Calamites. The present study illustrates how Calamites spores of the Calamospora type progressively evolved into the quite different spores of living Equisetum. Indeed, it would not have been possible to understand how such a transition occurred without this TEM study. Similarly, it underscores the proclivity of the Equisetales to develop unusual structures in both their spores and their reproductive organs. Moreover, it demonstrates that the ultrastructural features of equisetalean spores changed greatly during their long evolutionary history, whereas those of other Pteridophytes groups, such as ferns and lycopsids, remained unchanged. However, the most striking outcome of this comparative TEM study is the demonstration that spores of the Triassic horsetails show many ultrastructural similarities with spores of the Ophioglossaceae, a living family of primitive ferns. According to Lugardon and Brousmiche Delcambre [Lugardon, B., Brousmiche-Delcambre, C., 1994. Exospore ultrastructure in Carboniferous sphenopsids. In: Kurmann, M.H., Doyle, J.A. (Eds.), Ultrastructure of fossil spores and pollen, pp. 53–66, Royal Botanic Gardens, Kew.], who made the same observations for the spores of Calamites, these similarities indicate that horsetails and ferns are closely related and have a common origin. These results are in agreement with those of a recent DNA analysis which shows that the horsetails and the ferns form a monophyletic group of plants. Moreover, they support and are in agreement with the phylogenetic analysis using cladistic principles of Stein et al. [Stein, W.E., Wight, D.C., Beck, C.B., 1984. Possible alternatives for the origin of Sphenopsida. Syst. Bot. 9 (1), 102–118.] which suggests that the sphenophytes and the ferns as a whole are descended from a common ancestor, the Devonian complex Cladoxylopsida including the Hyeniales. The fact that the Hyeniales combine sphenophyte and fern-like features would explain why the spores of the ferns and those of the ancient sphenophytes have the same ultrastructural features. Moreover, this study indicates that spore ultrastructure retains ancestral features for a longer time than the other parts of the plants which evolve and thus change more rapidly. This study provides a further demonstration that spore ultrastructure, particularly of those preserved in situ, is of great value in researching the evolutionary and phylogenetic relationships of plants.