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Commentary Progress in understanding angiosperm history, success, and relationships: Darwin’s abominably ‘‘perplexing phenomenon’’ William L. Crepet* Department of Plant Biology, 228 Plant Science Building, Cornell University, Ithaca, NY 14853-4301 o Charles Darwin the suddenness of the Tangiosperm 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 taxon- omy, and the fossil record, principally of Fig. 1. (a) A typical morphology-based phylogeny of existing seed plants (plus the extinct Bennettitales) pollen and leaves. These approaches have illustrating (in bold type) the anthophyte clade. (b) A composite phylogeny illustrating the realignment failed to illuminate the mystery that has now of Bennettitales and Gnetales based on ITS and new morphological data (21). grown to include major aspects of angiosperm phylogeny, evolutionary success, and origin (2). But lately, exciting new methods and provide a precise framework within answer’’ (15), even though it conflicted and data are available that have enormous which to intelligently direct and ethically with his own previous analyses (16). potential to resolve this set of problems. evaluate the inevitable, if controversial, bio- Now a year later, in this issue of PNAS New kinds of fossils have been discovered engineering of plants for agricultural and Barkman et al. (17) report yet another but COMMENTARY from critical times (2–4); new algorithms are medicinal purposes. Finally, knowledge of more detailed and extensive analysis of available for the rapid comparative analysis relationships has the potential for allowing genes from all three compartments and of all kinds of data (5), and molecular more informed decision making on biodi- includes and accommodates the discovery genetics is providing data on nucleic acid versity conservation issues by permitting of an additional copy of the atpA gene in sequences and homeotic genes like the comparisons of the explicit uniqueness of Amborella. The results of the Barkman et MADS family (6–12). These allow invalu- taxa in situations involving difficult choices. al. analysis suggest a different and signif- able insights into homology of floral organs. Molecular data have provided the po- icant basal arrangement of flowering How then have these changes in the land- tential to transcend subjective limitations plants with Nymphaea, a water lily, sharing scape of evolutionary biology affected our on assessments of homology in morpho- the first branch with Amborella. This dif- understanding of the set of problems often logical features at the very time when new ference has implications for identifying an grouped under ‘‘Darwin’s Abominable algorithms provide tools necessary for angiosperm ancestor. It suggests that such Mystery?’’ And, for that matter, are these large, previously intractable, data sets to an ancestor might share characters with problems of sufficient stature to be worthy be analyzed very quickly (5). Only 2 years Nymphaea as well as with Amborella—a of this continuing attention? With respect to ago it seemed that a consensus, based on decided contrast because Nymphaea has the latter, the answer is yes. The angio- vessels and bisexual flowers (13). molecular data, would emerge on angiosperms dominate the terrestrial biota with But even when The New York Times was sperm relationships within 10 years (14). between 300,000 and 400,000 species (13). highlighting the ‘‘consensus’’ on angiosperm One year later the New York Times re- They are vital sources of foods and drugs relations (15), another well-established con- ported that ‘‘evolutionary biologists have and are the primary constituents of the sensus, on angiosperm relations to other at last answered a question so difficult that tropical rain forests, and they provide im- seed plants, was beginning to erode. Virtu- portant three-dimensional structural defini- Darwin himself called it the ‘abominable ally all morphology-based analyses of seed tion for terrestrial ecosystems at most lati- mystery’’’ (15). Actually the article re- plants have included a monophyletic group tudes. In addition to addressing one of the ferred to a consensus of independent stud- consisting of the angiosperms ϩ Gnetales ϩ greatest fundamental gaps in our under- ies of extant angiosperms. This consensus Bennettitales—the so-called anthophytes standing of evolutionary history, an under- included four independent analyses that (16, 18, 19). However, even 2 years ago gene standing of precise relationships within the pointed to the same result: Amborella at sequence data were suggesting that that angiosperms would have remarkable prac- the base of the flowering plants (7–12). Gnetales might more properly be placed tical value and relevance. It would allow a Although not all scientists were convinced with the remainder of the gymnosperms and better understanding of species distribu- that the matter of the basal angiosperm tions and their ecological implications. It was settled, the response was dramatic would facilitate more efficient phylogenetic with one morphologist heralding the iden- See companion article on page 13166. context-guided searches for natural drugs tification of a basal angiosperm as ‘‘the *E-mail: [email protected]. PNAS ͉ November 21, 2000 ͉ vol. 97 ͉ no. 24 ͉ 12939–12941 Downloaded by guest on September 24, 2021 plant relationships promise to further alter on Amborella alone. What of complemen- the landscape of seed plant relationships by tary projections derived from analyses of removing the Bennettitales from the antho- seed plant relationships? Do these analyses phytes and eliminating the anthophyte con- point toward likely archetypal angiosperms cept (23) (Fig. 1). This analysis differs from or angiosperm ancestors? No. Not when we previous ones in the broader sampling of incorporate the recent analyses challenging extant cycads, the more precise analysis of the validity of the anthophytes. Instead, fossil bennettitalean characters, and the angiosperms become more distantly related treatment of poorly understood fossils pur- to all existing seed plants, leaving a gap ported to be links between Bennettitales populated only by extinct taxa that may or and Gnetales despite their ambiguous char- may not be represented in the fossil record. acter associations. The results suggest that That brings us full circle to the kind of the Bennettitales are actually rather basal evidence that first allowed Darwin to rec- seed plants and sister group to the cycads ognize the perplexing phenomenon in the (Fig. 1) despite the superficial similarity of first place: the fossil record. How does the the reproductive structures to those of clas- record impinge on our understanding of sically archetypal angiosperms. within angiosperm relationships, angio- Where then do we stand? A more re- sperm success, and angiosperm origins? solved and, as a result of the recent Barkman An improved understanding of the angio- Fig. 2. A three-dimensionally preserved Creta- et al. study, a more compelling picture of sperm fossil record has resulted from crit- ceous (Turonian) ﬂower similar to modern Nym- relationships within the flowering plants is ical analysis of the leaf and pollen records phaea (scanning electron micrograph by Jennifer now emerging based on molecular data. (25), but most dramatically from a new Svitko). And although the results of this most recent emphasis on well-preserved fossil angio- analysis are not consistent with phylogenies sperm flowers (2, 3, 26). One obvious based on morphological data sets (16, 19, ͞ application of these new data and result- that any valid structural life cycle gnetalean 24), there is no consensus among the exclu- ant pattern would be to test hypotheses of similarities to angiosperms were convergent sively morphology-based sets. With both phylogeny based on extant taxa for corre- (20, 21). Subsequent research has supported Nymphaea and Amborella at the base of the spondence with the observed temporal this conclusion based on genomic studies latest angiosperm tree, a wider range of progression of angiosperm taxa in the and analyses of MADS box genes (6, 22). characters might be expected in archetypal fossil record. There is no exact congru- Now, morphology-based and combined angiosperms or angiosperm sister groups ence between any angiosperm phylogeny morphology͞molecular analyses of seed than that implied by the previous consensus based on existing taxa and angiosperm fossil history. It is too early to make too much of this because the pace of paleo- botanical discovery is forcing ongoing re- assessments of pattern. There is rough consistency between the fossil record and the Barkman et al. phylogeny, but this is also true for some other estimations of flowering plant relationships. Regretta- bly, there is no confirmation of the basal angiosperm taxon based on an unequivo- cal progression of discrete identifiable taxa early in angiosperm history. Instead, reliable evidence of early Cretaceous angiosperms suggests a rapid initial diversi- fication with ‘‘eudicots’’ immediately fol- lowing magnoliids (2). Among earliest recognizable taxa are the families Chlo- ranthaceae and Winteraceae (14). These families (and others) are basal in several morphology-derived

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