Ovule inversion in the earliest conifers

Recent investigations of ovulate conifer cones from southem Europe and midcontinent North America have independently documented that certain Paleozoic walchians have inverted ovules, rather than the erect ovules previously thought to characterize the most primitive conifers. Reinvestigation and consideration of other walchian conifers, including Moyliostrobus and Lebachia piniformis (sensu Florin), reveals that they also had inverted ovules. These different patterns of ovule orientation demonstrate that the nature and the polarity of the character states are dramatically different than popularly believed, and the shift from megasporophyll to ovuliferous cone-scale occurred within the Paleozoic walchians. WALCHIANS are the most ancient and presumably most primitive true conifers known. They appear first in Westphalian sediments in Europe and equivalent age deposits in North America, and are popularly perceived as a relatively homogeneous clade throughout the Carboniferous and basal Permian. Florin's landmark studies of Upper Paleozoic compression conifers clearly demonstrated the homology between ovulate cones of extant conifers and those of the earliest conifers and cordaites, and provided the basis upon which two generations of plant systematists have interpreted conifer phylogeny and evolution. Florin recognized that the ovuliferous seedscale, or cone-scale of modem conifers (e.g., Pinus) is not just a simple megasporophyll, but represents a phylogenetically modified fertile shoot (Florin, 1938-45, 195 1). Support for that view is provided by developmental study of modem ovulate conifer cones, and by documentation of a morphological series of fossil conifers whose ovulate shoots/fertile scales appear progressively fused and flattened through time. The cordaites and some walchian conifers bore their ovules on actual sporophylls, on individual fertile leaves or megasporophylls that are sometimes referred to as "fertile scales." Those simple scales, therefore, are homologous to only a portion of an ovuliferous cone-scale, I Received for publication 1 1 August 1986; revision accepted 11 December 1986. I especially appreciate J. A. Clement-Westerhof and J. H. F. Kerp, of the Laboratory of Paleobotany and Palynology, University of Utrecht, The Netherlands, for generously sharing ideas and discussions throughout this investigation. I also thank G. W. Rothwell for ongoing dialogue, and C. N. Miller and C. J. Felix for their suggestions in review. This work was initiated during tenure of a National Science Foundation Visiting Professorship of Women award with C. B. Beck, Museum of Paleontology, University of Michigan, Ann Arbor, MI. which represents an entire, reduced axillary fertile shoot. The latter is considerably more derived, and characterizes some walchians, voltzialeans, and all extant conifers. In the literature, the term "fertile scale" is also sometimes used in reference to the ovuliferous cone-scale, leading to potential confusion regarding the homologies of the described structures. In this paper I refer to sporophylls or to cone-scales, and suggest fertile scale be abandoned entirely, or limited to fertile structures with unknown homology. Florin's rather straight line view of conifer evolution emphasized themes of reduction and fusion, with particular focus in the ovulate cones on character state changes from radial to bilateral shoot symmetry, from numerous discrete parts to smaller numbers of combined elements, and from terminal, erect ovules to laterally attached, inverted ovules. This paper considers the last feature, inverted ovules, and its significance in early conifer biology and systematics. HISTORICAL CONTEXT-Currently, the most widely accepted model of a primitive early conifer is Lebachia piniformis (sensu Florin = Walchia in Clement-Westerhof, 1984), with compact, compound ovulate cones comprising a central axis and helically arranged bracts and axillary fertile shoots. Individual axillary shoots are described as radially symmetrical with numerous sterile scales, and one fertile scale with a single, erect, terminal ovule. Ovules of L. piniformis were characterized by Florin as bilaterally symmetrical, with a prominent bilobed micropyle directed distally toward the cone periphery. In contrast, recent investigations of ovulate conifer cones from the Italian Alps (ClementWesterhof, 1984) and Kansas (Mapes and Rothwell, 1984) have independently revealed