Identification of a tetrahedral apical cell preserved within a fossilized fern fiddlehead

The gradual unfurling of fronds from tightly coiled tips, termed fiddleheads or croziers, is one of the most recognizable features of the fern lineage, but its evolutionary origin remains unclear. Here, we identify that fiddleheads and their development, termed circinate vernation,^1,2 are not ubiquitous across ferns. Instead, they are a synapomorphy of a clade we term the circinatophytes that includes extant marattioid and leptosporangiate ferns. Circinatophytes encompass the vast majority of extant ferns,³ and fossil evidence demonstrates the antiquity of the group at over 315 million years. Despite their overall conservation, a comparative investigation of extant species suggests that during fiddlehead evolution, there was a transition from a tetrahedral to a wedge-shaped apical cell in the leaf meristem. We predict that a tetrahedral leaf apical cell was likely ancestral in circinatophytes, despite being present in less than 2% of modern species,³ and that this cell mirrored the tetrahedral cell found in the shoots of all major groups of ferns. This is supported by our description of a tetrahedral apical cell in, to our knowledge, the oldest preserved fossil fern leaf meristem of the ca. 315-million-year-old fern Ankyropteris corrugata. We conclude that fiddleheads have been highly conserved in the circinatophytes, and the similarities in leaf and shoot apical cells in early diverging groups of ferns add support to the hypothesis that fern leaves evolved through the modification of shoots, as proposed by the telome theory.⁴.