A royally mangled fern and a handle of evolution

If genes are the blueprint for the body plan, development is the architect. From the smallest insect to the tallest pine, all organisms develop. Animals do it quite differently from plants though. Most development in animals occurs early in life. As an animal reaches maturity development stops; some organisms like fish can still continue to grow in size, but they don't continue to develop much.

Plants on the other hand, continue development throughout their life. New leaves, stems, roots, and reproductive structures are produced over their phenological stages. At the same time leaves fall off, branches die back, and shoots sprout from new limbs. Death and rebirth, united in one. The 19th century German botanist Matthias Jakob Schleiden got it right, “Here there is nothing firm, nothing consistent; an endless becoming and unfolding, and a continual death and destruction, side by side and integrated—such is the plant! It has a history, not only of its formation, but also of its existence, not merely of its origin, but of its persistence.” Translated to English by Arthur Henfrey in The Plant; a Biography (1858). I have to give credit where it is due, I was first introduced to an abridged version of this quote when I was an introductory botany teaching assistant for Elena Kramer, Harvard’s preeminent plant developmental biologist. It wasn’t until now that I explored Schleiden’s writing for myself, and I was not disappointed.

Schleiden was a brilliant scientist, pioneering important advances like the cell theory and even promoting early evolutionary thought—a cogent explanation of this latter point was made by Ned Friedman, whose work on early evolutionists I highly recommend. Schleiden was also a science communicator—a nonexistent concept back then—who followed a line of those savvy in the craft. He wrote scientifically accurate (for his time) but accessible botanical books for the general public, such as Poetry of the Vegetable World: A Popular Exposition of the Science of Botany, and Its Relations to Man. He opens this book with an explanation, “I have sought, therefore, in the present discourses, to bring within the sphere of general comprehension, the more important problems of the real science of Botany, to point out how closely it is connected with almost all the most abstruse branches of philosophy and natural science, and to show how almost every fact or larger group of facts tends, as well in Botany as in every other branch of human activity, to suggest the most earnest and weighty questions and to carry mankind forward.” In other words, studying plants can enrich your life and provide meaning and insight to all other aspects of it. If he were alive today, we would be lucky to have him on the board of Let’s Botanize. We can forgive his run on sentence, it was stylistic of the time and we were forewarned: “The following essays… were by no means intended for publication.”

On Ned Friedman’s comprehensive, but cogent, webpage on early evolutionists I noticed another Schleiden quote that references his idea on how one species can transmute into another (i.e., evolution). He states, “How, then, if the same influences which have called forth an aberration from the original form of the plant, continue to act in the same way, not for centuries or tens of centuries, but for ten or a hundred thousand years, will not at last, as the variety thus becomes a sub-species, so also, this, become so permanent, that we shall and must describe it as a species.” The point that got me thinking was his use of the word aberration. In this context, he is describing how mutations and divergence over time can eventually lead to new species. I was less curious about the process of speciation, but more focused on aberrations in development.

While modifications of the blueprint (genetic mutations) can cause catastrophic issues, the architect (development) can equally blunder the implementation of the design. For instance, a polydactylous cat with six toes or a fruit fly with legs for antennas. The study of developmental malfunctions is called teratology and it is these aberrations and their implications for evolution which form the central theme of this essay.

During a botanizing trip in Tennessee’s Cumberland Plateau, I stumbled upon the royal fern (Osmunda spectabilis, Osmundaceae). Usually, this species has leaves that are hemidimorphic, meaning they divide the labor of photosynthesis and reproduction into different segments of a leaf. The lower leaflets (pinna) are completely vegetative and lack spore producing structures (sporangia), and they are only used for photosynthesis. In contrast, the top leaflets lack photosynthetic lamina and are anointed with a crown of reproductive leaflets that produce spores—the developmental namesake of this fern’s common name. This hemidimorphic growth form is contrasted with two other forms: monomorphism, the production of spores on the same leaves used for reproduction (most common in ferns); and holodimorphism, the production of two separate leaves for reproduction and photosynthesis, as found in the cinnamon fern (Osmundastrum cinnamomeum).

Normal form of Osmunda spectabilis fertile frond. The upper portion of the leaf is crowned with reproductive leaflets.

Sometimes the line between fertile and sterile portions of the leaf becomes blurred. In the individual leaf I observed, the developmental switch to reproduction occurred two thirds of the way up the leaf, and then seemed to switch back to vegetative. This led to the development of fertile leaflets sandwiched by sterile photosynthesizing leaflets. These modified fertile leaves are called hemiphyllodes, according to Beitel and colleagues (1981). In the 17th and 18th century these abnormalities would be technically called monstrosities, modifications in the normal course of development.

Hemiphyllodes of Osmunda spectabilis frond. Vegetative leaves and leaflet switch to reproductive and then back.

These developmental aberrations are often disregarded in evolutionary biology as mere random events, idiosyncratic processes that do not, and should not, tell us about how evolution of form can proceed. This stems, in part, from criticisms of 20th century German geneticist Richard Goldschmidt’s idea of “hopeful monsters.” His work on mutant organisms led him to the hypothesis that evolution could occur through large mutational shifts, or saltations. He is most famous for his claim that the generation of new species (speciation) occurs in this way—mutations affecting development lead to abnormal teratological “monsters,” some of which are “hopeful” and selected for, leading to a new species. His work was vehemently bashed by organizers of the modern synthesis, specifically Mayr and Dobzhansky, who heralded the concept that small mutations lead to variation which spreads through populations over time—not macromutations abruptly leading to new species. It is now generally accepted that speciation mostly occurs through the divergence of ancestral populations over time, usually by limitations in reproduction from geographic or other barriers—not from major events occurring within single individuals.

But, Goldschmidt was not a kook, his focused and detailed studies of mutant organisms and development led him to his ideas. I am not supporting his claims of speciation by macromutation, but there are still interesting implications of his hopeful monsters that merit deep thought, especially when thinking about the origin of novel form. Specifically, Goldschmidt thought that mutations in the genes that are important for development are critical for understanding how new forms arise. By and large, this is not a crazy idea. Genetic changes that affect important developmental processes are much more likely to lead to drastic changes in form than small point mutations that shift narrow individual traits. This idea forms the basis for some lines of research in the field of evolutionary-development (evo-devo), and has been implicated in studies of fruit fly body segmentation and limb evolution in vertebrates.

In the case of this royal fern, the monstrous leaves may mean nothing, another parochial event in the polity of nature. In fact, the developmental aberrations of these leaves are likely not even genetic, but environmentally induced, meaning they are not heritable so cannot be passed on through generations. However, we should not discard them entirely; in the millions of potential ways new forms could arise, these hemiphyllodes exist. These monstrosities occur. They provide a set of observable and realized events, where the developmental processes were modified leading to a plant with somewhat different looking leaves. It is far easier to break the intricate web of coordinated molecular events that build an organ, than to modify it piece by piece in a new, yet viable, way. These perturbations in the system are noteworthy because they still build a coherent and functioning plant structure. I am not making the claim that developmental aberrations are always, or even ever, the path taken in the evolution of new forms. But, these aberrations generate a set of testable hypotheses on how variation in new morphology can arise.

Interestingly, the hemiphyllodes of the royal fern lead to a fascinating morphological form that mimics the fertile leaf type of its relative, the interrupted fern (Claytosmunda claytoniana). This species produces leaves where the bottom portion is vegetative, the middle is reproductive, and the upper portion is vegetative again, like our royal monster. It is thus conceivable that genomic modifications could occur that lead to similar developmental aberrations of the observed hemiphyllodes. This would then be heritable, providing one potential route for the evolution of different fertile leaf forms. If we can pinpoint the developmental shifts underlying the unusual hemiphyllodes O. spectabilis, we may gain insight into how variation in fertile leaf morphology evolves.

Fertile fronds of interrupted fern (Claytosmunda claytoniana), showing fertile leaflets sandwiched by sterile leaflets.

At the end of the day, for evolution to occur, a particular mutation (large or small) must spread through the population—whether it be by natural selection or other mechanisms of drift and random chance. Understanding which changes can arise, or have arisen, can help generate hypotheses on morphological transitions and evolution. Development is a powerful lever for evolution to pull. Small modifications of genes that regulate the developmental process could have massive ramifications for downstream structure, function, and survival of an individual and thus evolution itself. We should perhaps pay a bit more attention to the monsters, however they form, as they show us one observable path in the origin of variation.

August 31, 2025

References

Beitel, Joseph M., Warren H. Wagner Jr, and Kerry S. Walter. "Unusual Frond Development in Sensitive Fern Onoclea sensibilis L." American Midland Naturalist (1981): 396-400.

Dietrich, Michael R. "Richard Goldschmidt: hopeful monsters and other'heresies'." Nature Reviews Genetics 4.1 (2003): 68-74.

Goldschmidt, Richard. The material basis of evolution. Yale University Press, 1982.

Schleiden, Matthias Jacob. The Plant; a Biography: In a Series of Popular Lectures. H. Bailliere, 1848.

Schleiden, Matthias Jacob. Poetry of the vegetable world. Moore, Anderson, Wilstach & Keys, 1853.

Schölch, A. "Relations between submarginal and marginal sori in ferns IV. The sori of Osmunda and selected Schizaeaceae and their morphological relations." Plant Systematics and Evolution 263.3 (2007): 227-251.