Fern vascular architecture reveals how developmental constraint can generate novel morphology

The origin of variation is essential for evolution. Understanding how novel phenotypes arise is thus of principal importance in biology. Although some traits evolve independently,^1,2 organisms are integrated wholes, not sums of individually evolving parts.^3,4,5,6,7,8 Therefore, to fully understand the generation of new form, it is critical to consider how modification in one part of an organism developmentally influences another.^9,10 This is the concept of "developmental constraint," and it is usually invoked to describe the limitations on phenotypes.^11,12,13 However, this covariation can also provide a route for generating new form.^7,14 Using ferns as a system, and leveraging phylogenetic comparative methods with traditional histology and micro-computed tomography, I show how shifts in leaf arrangement (phyllotaxy) can developmentally reshape the organization of vascular patterns in the stem (stelar morphology). Specifically, transitions from spiral to non-spiral phyllotaxy directly lead to shifts from radial to dorsiventral stem vascular arrangement-a novel stelar configuration in ferns. Mechanistically, this occurs by direct modification of leaf primordia, which alters hormonal patterning and, in turn, reorganizes stem vascular arrangement. Ecologically, the dorsiventral stele is overrepresented in stem-climbing ferns, where it may have been selected upon for substrate connection. However, based on phylogenetic analyses, selection seems to have acted directly on phyllotaxy, not on novel vascular variants, in the evolution of the stem-climbing habit. These insights highlight how shifts in one pattern of growth can induce changes in another, emphasizing the role of developmental constraint in generating novel phenotypes and the origin of variation.