Darwin’s abominably ‘‘perplexing phenomenon’’
William L. Crepet*
Department of Plant Biology, 228 Plant Science Building, Cornell University, Ithaca, NY 14853-4301
To Charles Darwin the suddenness of the angiosperm appearance and their rapid rise to dominance in the fossil record was both a “perplexing phenomenon” to “those who believe in extremely gradual evolution” and an “abominable mystery” (1). It has been 125 years since Darwin's letter to Heer and for most of this time the investigation of the mystery has been in the domain of comparative morphology, traditional taxonomy, and the fossil record, principally of pollen and leaves. These approaches have failed to illuminate the mystery that has now grown to include major aspects of angiosperm phylogeny, evolutionary success, and origin (2). But lately, exciting new methods and data are available that have enormous potential to resolve this set of problems. New kinds of fossils have been discovered from critical times (2–4); new algorithms are available for the rapid comparative analysis of all kinds of data (5), and molecular genetics is providing data on nucleic acid sequences and homeotic genes like the MADS family (6–12). These allow invaluable insights into homology of floral organs.
How then have these changes in the landscape of evolutionary biology affected our understanding of the set of problems often grouped under “Darwin's Abominable Mystery?” And, for that matter, are these problems of sufficient stature to be worthy of this continuing attention? With respect to the latter, the answer is yes. The angiosperms dominate the terrestrial biota with between 300,000 and 400,000 species (13). They are vital sources of foods and drugs and are the primary constituents of the tropical rain forests, and they provide important three-dimensional structural definition for terrestrial ecosystems at most latitudes. In addition to addressing one of the greatest fundamental gaps in our understanding of evolutionary history, an understanding of precise relationships within the angiosperms would have remarkable practical value and relevance. It would allow a better understanding of species distributions and their ecological implications. It would facilitate more efficient phylogenetic context-guided searches for natural drugs and provide a precise framework within which to intelligently direct and ethically evaluate the inevitable, if controversial, bioengineering of plants for agricultural and medicinal purposes. Finally, knowledge of relationships has the potential for allowing more informed decision making on biodiversity conservation issues by permitting comparisons of the explicit uniqueness of taxa in situations involving difficult choices.
Molecular data have provided the potential to transcend subjective limitations on assessments of homology in morphological features at the very time when new algorithms provide tools necessary for large, previously intractable, data sets to be analyzed very quickly (5). Only 2 years ago it seemed that a consensus, based on molecular data, would emerge on angiosperm relationships within 10 years (14). One year later the New York Times reported that “evolutionary biologists have at last answered a question so difficult that Darwin himself called it the ‘abominable mystery”’ (15). Actually the article referred to a consensus of independent studies of extant angiosperms. This consensus included four independent analyses that pointed to the same result: Amborella at the base of the flowering plants (7–12). Although not all scientists were convinced that the matter of the basal angiosperm was settled, the response was dramatic with one morphologist heralding the identification of a basal angiosperm as “the answer” (15), even though it conflicted with his own previous analyses (16).
Now a year later, in this issue of PNAS Barkman et al. (17) report yet another but more detailed and extensive analysis of genes from all three compartments and includes and accommodates the discovery of an additional copy of the atpA gene in Amborella. The results of the Barkman et al. analysis suggest a different and significant basal arrangement of flowering plants with Nymphaea, a water lily, sharing the first branch with Amborella. This difference has implications for identifying an angiosperm ancestor. It suggests that such an ancestor might share characters with Nymphaea as well as with Amborella—a decided contrast because Nymphaea has vessels and bisexual flowers (13).
(a) A typical morphology-based phylogeny of existing seed plants (plus the extinct Bennettitales) illustrating (in bold type) the anthophyte clade. (b) A composite phylogeny illustrating the realignment of Bennettitales and Gnetales based on ITS and new morphological data (21).
A three-dimensionally preserved Cretaceous (Turonian) flower similar to modern Nymphaea (scanning electron micrograph by Jennifer Svitko).
(a) A reconstruction of Paleoclusia, a Cretaceous relative of modern Clusiaceae, a family closely associated with meliponine bee pollinators. (b) A reconstruction of an extinct (Cretaceous, Turonian) ericalean flower typical of a complex that includes several adaptations for pollination by derived anthophilous insects clawed petals and pollen in polyads. (Reconstructions by Michael Rothman.) (c) Appearance of floral innovations (●) during the Aptian (Ap)-Albian (Ab)-Cenomanian (C)-Turonian (T) interval vs. appearance of new floral characters/million years (○). (d) Angiosperm radiation in the Aptian–Turonian interval (based on ref. 32; ○) vs. rate of appearance of new floral characters during the same interval (●).