Fossils and Plant Phylogeny1

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Fossils and Plant Phylogeny1 American Journal of Botany 91(10): 1683±1699. 2004. FOSSILS AND PLANT PHYLOGENY1 PETER R. CRANE,2,5 PATRICK HERENDEEN,3 AND ELSE MARIE FRIIS4 2Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK; 3Department of Biological Sciences, The George Washington University, Washington DC 20052 USA; 4Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, S-104 05 Stockholm, Sweden Developing a detailed estimate of plant phylogeny is the key ®rst step toward a more sophisticated and particularized understanding of plant evolution. At many levels in the hierarchy of plant life, it will be impossible to develop an adequate understanding of plant phylogeny without taking into account the additional diversity provided by fossil plants. This is especially the case for relatively deep divergences among extant lineages that have a long evolutionary history and in which much of the relevant diversity has been lost by extinction. In such circumstances, attempts to integrate data and interpretations from extant and fossil plants stand the best chance of success. For this to be possible, what will be required is meticulous and thorough descriptions of fossil material, thoughtful and rigorous analysis of characters, and careful comparison of extant and fossil taxa, as a basis for determining their systematic relationships. Key words: angiosperms; fossils; paleobotany; phylogeny; spermatophytes; tracheophytes. Most biological processes, such as reproduction or growth distic context, neither fossils nor their stratigraphic position and development, can only be studied directly or manipulated have any special role in inferring phylogeny, and although experimentally using living organisms. Nevertheless, much of more complex models have been developed (see Fisher, 1994; what we have inferred about the large-scale processes of plant Huelsenbeck, 1994), these have not been widely adopted. But evolution, and much of what we know about the plant diver- fossils do provide additional information on the diversity of sity to which those processes gave rise, is based on preserved plants, which must be accounted for by any comprehensive samples taken from living organisms. These samples, brought understanding of plant phylogeny and evolution (e.g., Doyle together in the collections of museums and herbaria around and Donoghue, 1987). They also provide evidence on the tim- the world, are crucial to attempts to name, characterize, sys- ing of evolutionary events that is useful to develop and test tematize, and understand the origin of the variety of plant life. ideas on how the variety of plant life may have arisen (e.g., They are also the starting point for any investigation of plant Doyle and Donoghue, 1993; Crane et al., 1995). phylogeny. Preserved specimens are the essential samples and In this paper, we discuss the contributions of paleobotanical indispensable reference points on which knowledge of botan- data to understanding large-scale evolutionary patterns in the ical diversity and large-scale processes of plant evolution are plant kingdom. We begin with a brief consideration of the based. nature of the paleobotanical record and the temporal infor- Fossils, like herbarium specimens and leaf fragments kept mation it provides. We then review three key areas of plant in silica gel for DNA analysis, are the remains of once-living phylogeny with a particular focus on the contributions of pa- organisms gathered at a particular time and from a particular leobotanical data: the origin and diversi®cation of vascular place. There is no essential difference between a dried speci- plants, the origin and diversi®cation of seed plants, and the men collected a decade ago and a fossil specimen entombed origin and diversi®cation of ¯owering plants. The many other within rocks for millions of years. Neither is a perfect sample contributions of paleobotanical data, to areas of science as di- of a complex living organism, but combined with knowledge verse as global environmental change, biostratigraphy, and pa- from other samples of plant diversity and supplemented by leogeography, are not considered in this paper. information from living plants, both can help answer questions about the form of the botanical tree of life and the processes FOSSIL PLANTS AND CHARACTERS FOR by which it has come about. PHYLOGENETIC ANALYSIS Even relatively recently, paleontological data have been considered by some (e.g., Hughes, 1976, 1994) to be the ®nal Fossil plants are generally more poorly known than their arbiters in any effort to understand plant phylogeny. We do living counterparts. However, perhaps surprisingly, they are not subscribe to this view. Recent advances in systematic the- sometimes exquisitely well preserved. In many cases, they ory have developed a more sophisticated perspective and have provide a level of structural detail that cannot be retrieved helped to clarify exactly what information fossils can and can- from living plants without signi®cant investment of time and not deliver (e.g., Hill and Crane, 1982; Crane and Hill, 1987; effort. For example, permineralized plant fossils from classic Patterson, 1981; Doyle and Donoghue, 1987; Gauthier et al., localities such as the Eocene Princeton Chert preserve near- 1988; Donoghue et al., 1989). The result is a straightforward perfect anatomical details of stems, fruits, and seeds (e.g., and uncompromising view of paleontological data. In a cla- Cevallos-Ferriz and Stockey, 1991; Pigg and Stockey, 1996; Stockey et al., 1998). Equivalent information for the extant 1 Manuscript received 21 January 2004; revision accepted 17 June 2004. relatives of these plants is frequently not readily available. The authors thank Jeffrey A. Palmer, Douglas E. Soltis, and Mark W. Chase Similarly, the quality of preservation of morphological and for the invitation to contribute to this special issue and James A. Doyle for anatomical details in charcoali®ed ¯owers from Cretaceous his valuable comments on the manuscript. Many of these issues have been discussed during meetings of the ``Deep Time'' Research Coordination Net- fossil ¯oras may exceed that seen in standard herbarium spec- work (NSF grant RCN-0090283). imens (e.g., Friis, 1990; Herendeen et al., 1994, 1995; Keller 5 E-mail: [email protected]. et al., 1996; MagalloÂn-Puebla et al., 1997, 2001; SchoÈnenber- 1683 1684 AMERICAN JOURNAL OF BOTANY [Vol. 91 ger et al., 2001; Friis et al., 2003b). In both these cases, de- ships with living and other fossil organisms. It is self-evident tailed comparison of fossil and extant material often requires that it is of no value to know that a fossil is of a particular extensive morphological and anatomical surveys of different age unless it can also be linked to a previously recognized organs from living plants. These, and many other examples, group of plants at some level. show that frequently it is not the quality of preservation of In broad terms, establishing the age of fossil plants is not fossil material that limits comparison with extant taxa. Often problematic. Decades of geological and paleontological re- it is simply that detailed comparative, morphological, and an- search have established that the fossil record is strongly inter- atomical studies of the relevant living plants have not been nally consistent, just as there is pattern and internal consisten- done. cy in the distribution of character states among organisms. A much more signi®cant problem, at least for most fossils This is well corroborated by many millions of individual ob- of large and complex plants (e.g., shrubs or trees), is that the servations of plant and animal fossils, as well as by geological different organs derived from the same living plant rarely oc- evidence from superposition, correlation, and large-scale strati- cur in attachment in fossil assemblages. Thus while the leaves, graphic and structural geological patterns. Our current under- seeds, pollen grains, stems, and other parts of fossil plants can standing of the geological column is supported by a wealth of often be extremely well preserved, a central dif®culty is de- interlocking geological data. The large-scale patterns of geo- termining which of these dispersed plant organs were pro- logical succession are well known. This is not to say that cur- duced by the same fossil species. Trying to understand which rent knowledge of geology is infallible and should not be sub- leaf ``belongs to'' which seed or pollen grain is not a straight- ject to revision in light of information from biology or pale- forward undertaking. ontology. But to overthrow a signi®cant body of geological Because attachment between different organs in the fossil data, inferences from biology or paleontology will themselves record is the exception rather than the rule, attempts to recon- need to be highly corroborated and unambiguous. struct fossil plants generally lean heavily on a variety of in- However, it is also the case that determining the age of fossil direct inferences (see for example the arguments used to re- assemblages is generally most straightforward for marine de- construct various fossil angiosperms; Dilcher and Crane, 1984; posits where correlation is possible over large distances. Long- MagalloÂn-Puebla et al., 1997; Manchester et al., 1999). Unless distance correlation is more dif®cult in nonmarine situations done extremely carefully, such inferences are potentially sub- (e.g., river deposits, lake basins). Unfortunately, plant fossils ject to signi®cant error, with obvious consequences
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