Charles Darwin and the Origins of Plant Evolutionary Developmental Biology

Abstract

Much has been written of the early history of comparative embryology and its influence on the emergence of an evolutionary developmental perspective. However, this literature, which dates back nearly a century, has been focused on metazoans, without acknowledgment of the contributions of comparative plant morphologists to the creation of a developmental view of biodiversity. We trace the origin of comparative plant developmental morphology from its inception in the eighteenth century works of Wolff and Goethe, through the mid nineteenth century discoveries of the general principles of leaf and floral organ morphogenesis. Much like the stimulus that von Baer provided as a nonevolutionary comparative embryologist to the creation of an evolutionary developmental view of animals, the comparative developmental studies of plant morphologists were the basis for the first articulation of the concept that plant (namely floral) evolution results from successive modifications of ontogeny. Perhaps most surprisingly, we show that the first person to carefully read and internalize the remarkable advances in the understanding of plant morphogenesis in the 1840s and 1850s is none other than Charles Darwin, whose notebooks, correspondence, and (then) unpublished manuscripts clearly demonstrate that he had discovered the developmental basis for the evolutionary transformation of plant form.

Resolving Distinct Genetic Regulators of Tomato Leaf Shape within a Heteroblastic and Ontogenetic Context

“…As previously indicated, Goethe's prescient insight into the serial homology of lateral organs in plants was neither evolutionary nor developmental (Friedman and Diggle, 2011). Rather, in metaphorically declaring the leaf "Proteus," Goethe was demonstrating that the underlying, archetypal leaf is mutable, rather than singular and unchanging (Goebel, 1900;Ashby, 1948).…”

“…Goethe, 1952). Although referring to the more dramatic "metamorphosis" of lateral organs from leaves to floral organs within a single individual (Friedman and Diggle, 2011), "protean" aptly describes the mutable succession of not only shape but epidermal features and size of leaves iteratively produced by the shoot apical meristem during the transitions from juvenile to adult to reproductive development (Kerstetter and Poethig, 1998). The succession of leaf types produced during plant development is termed "heteroblasty," reflecting internal changes in the state of the shoot apical meristem manifest in lateral organ development (Goebel, 1900;Ashby, 1948;Poethig, 1990Poethig, , 2010.…”

The significance and scope of evolutionary developmental biology: a vision for the 21st century

“…Although having antecedents prior to Darwin (see Gould 1977;Friedman and Diggle 2011), evo-devo was made possible in large part by the emerging power of molecular biology to contrast gene sequences, and subsequently gene functions, across taxa (e.g., Ohno 1970;King and Wilson 1975;Jacob 1977;Bonner 1981). Although having antecedents prior to Darwin (see Gould 1977;Friedman and Diggle 2011), evo-devo was made possible in large part by the emerging power of molecular biology to contrast gene sequences, and subsequently gene functions, across taxa (e.g., Ohno 1970;King and Wilson 1975;Jacob 1977;Bonner 1981).…”

A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape

“…As the default archetype from which other organs are derived (Goethe, 1817;Friedman and Diggle, 2011), the developmental genetic programs that regulate leaf shape can globally impact the morphology of lateral organs throughout a plant. Because of the central importance of leaves, natural variation in leaf shape can constrain phenotypes in disparate organs.…”