The Good, The Bad, The Ugly: Using Naturally Occurring Terata to Distinguish the Possible from the Impossible in Orchid Floral Evolution

Abstract

We interpret extensive field observations of terata in the context of recent insights into monocot phylogeny and evolutionary–developmental genetics to explore the evolution of the orchid flower. Our arguably typological classification of floral terata focuses on natural occurrences of three contrasting modes of peloria (restoration of actinomorphy in a formerly zygomorphic perianth) and three contrasting modes of pseudopeloria (lessening of the degree of zygomorphy shown by the evolutionarily preceding perianth). Dynamic evolutionary transitions in floral morphology are assigned to recently revised concepts of heterotopy (including homeosis: evolutionary transitions in position of expression) and heterochrony (evolutionary transitions in timing of expression), seeking patterns that delimit developmental constraints and allow inferences regarding underlying genetic controls. Lateral heterotopy, occurring within the whorl of three petals (including the labellum) or within the adjacent whorl of three sepals, is more frequent than acropetal heterotopy, and full basipetal heterotopy does not occur. Pseudopeloria is more likely than peloria to generate a radically altered yet functional perianth, but is also more likely to cause acropetal modification of the fused filaments and style that constitute the characteristic gynostemium of orchids. We infer that at least one gene or gene complex controls style– stamen fusion, which requires the preadaptation of strongly developed epigyny, and another determines both stamen suppression and labellum formation adaxially. Our earlier hypothesis implicating genes of the TCP family has recently been challenged by empirical evidence of complex interactions between several MADS-box genes. Many transitions are highly iterative, and some are reversible (atavistic). Once heritability has been demonstrated, the most effective criteria for determining the most appropriate taxonomic status of a novel morph are the profundity of the phenotypic shift that it represents, the number and uniformity of the resulting populations, and whether the novel morph subsequently diversified to generate further morphs that retain the innovative features. Although morphological transitions attributable to heterochrony may be a more common driver of speciation than those attributable to heterotopy, we demonstrate that arguably all of the modes of instantaneous floral transition described in this paper have the ability to generate prospecies.