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Rich Zingiberales RESEARCH ARTICLE INVITED SPECIAL ARTICLE For the Special Issue: The Tree of Death: The Role of Fossils in Resolving the Overall Pattern of Plant Phylogeny Building the monocot tree of death: Progress and challenges emerging from the macrofossil- rich Zingiberales Selena Y. Smith1,2,4,6 , William J. D. Iles1,3 , John C. Benedict1,4, and Chelsea D. Specht5 Manuscript received 1 November 2017; revision accepted 2 May PREMISE OF THE STUDY: Inclusion of fossils in phylogenetic analyses is necessary in order 2018. to construct a comprehensive “tree of death” and elucidate evolutionary history of taxa; 1 Department of Earth & Environmental Sciences, University of however, such incorporation of fossils in phylogenetic reconstruction is dependent on the Michigan, Ann Arbor, MI 48109, USA availability and interpretation of extensive morphological data. Here, the Zingiberales, whose 2 Museum of Paleontology, University of Michigan, Ann Arbor, familial relationships have been difficult to resolve with high support, are used as a case study MI 48109, USA to illustrate the importance of including fossil taxa in systematic studies. 3 Department of Integrative Biology and the University and Jepson Herbaria, University of California, Berkeley, CA 94720, USA METHODS: Eight fossil taxa and 43 extant Zingiberales were coded for 39 morphological seed 4 Program in the Environment, University of Michigan, Ann characters, and these data were concatenated with previously published molecular sequence Arbor, MI 48109, USA data for analysis in the program MrBayes. 5 School of Integrative Plant Sciences, Section of Plant Biology and the Bailey Hortorium, Cornell University, Ithaca, NY 14853, USA KEY RESULTS: Ensete oregonense is confirmed to be part of Musaceae, and the other 6 Author for correspondence (e-mail: [email protected]) seven fossils group with Zingiberaceae. There is strong support for Spirematospermum Citation: Smith, S. Y., W. J. D. Iles, J. C. Benedict, and C. D. friedrichii, Spirematospermum sp. ‘Goth’, S. wetzleri, and Striatornata sanantoniensis in Specht. 2018. Building the monocot tree of death: Progress and crown Zingiberaceae while “Musa” cardiosperma, Spirematospermum chandlerae, and challenges emerging from the macrofossil- rich Zingiberales. Tricostatocarpon silvapinedae are best considered stem Zingiberaceae. Inclusion of fossils American Journal of Botany 105(8): 1389–1400. explains how different topologies from morphological and molecular data sets is due to doi:10.1002/ajb2.1123 shared plesiomorphic characters shared by Musaceae, Zingiberaceae, and Costaceae, and most of the fossils. CONCLUSIONS: Inclusion of eight fossil taxa expands the Zingiberales tree and helps explain the difficulty in resolving relationships. Inclusion of fossils was possible in part due to a large morphological data set built using nondestructive microcomputed tomography data. Collaboration between paleo- and neobotanists and technology such as microcomputed tomography will help to build the tree of death and ultimately improve our understanding of the evolutionary history of monocots. KEY WORDS anatomy; digital morphology; Ensete oregonense; Spirematospermum; Striatornata; Tricostatocarpon. Monocot flowering plants represent ca. 22% of flowering plant from species such as bamboo or abaca; spices such as ginger, tur- species, encompassing a large diversity of morphology, habit, and meric, and saffron; and many ornamentals such as spring bulbs, ecologies. This group is economically important, including many of irises, and orchids. Monocots are also ecologically important, form- our staple food crops such as grains (maize, wheat, rice, sorghum), ing dominant components of grassland, savanna, fynbos, wetland, coconuts, plantains; pasture feed for animals; materials produced and seagrass ecosystems, as well as important parts of tropical forest American Journal of Botany 105(8): 1389–1400, 2018; http://www.wileyonlinelibrary.com/journal/AJB © 2018 Botanical Society of America • 1389 1390 • American Journal of Botany understories. At an ordinal level, the monocot phylogeny has been Crane, 1995; Smith, 2013). The lineages of monocots that are better relatively stable compared to other groups (APG, 1998, 2016), mak- represented tend to be those that are more lignified (e.g., palms) or ing them useful for broader studies. Most studies find monocots to grow in habitats that are near good depositional environments, such be ca. 135 Ma (e.g., Janssen and Bremer, 2004: 134 Ma; Magallón as quiet bodies of fresh water. et al., 2015: 135.7 Ma). Monocots represent a good model group First and foremost, the study and accurate naming of fossil taxa for elucidating the patterns and processes of evolution, and under- is a key component of building a reliable and accurate tree of death. standing their evolutionary history is fundamentally important to Taxonomy is a vital and dynamic process, and assigning a name and human nutrition and well- being. rank to a fossil provides a taxonomic and phylogenetic framework Data from fossil taxa need to be included to obtain the most for the taxon in question; we recommend not using unnamed fos- comprehensive results when inferring phylogenetic relationships sils for dating phylogenies (e.g., Bell et al., 2010; Smith et al., 2010a; and investigating trait evolution, geographic histories, and other as- Zanne et al., 2014; Tank et al., 2015), as the lack of a name suggests pects of evolution for a lineage. In most cases, fossils are simply con- the need for careful evaluation of described morphology and/or sidered as constraints on the ages of nodes (e.g., Ho and Duchêne, ambiguity in phylogenetic placement based on characters analyzed. 2014; but see Ronquist et al., 2012a; Heath et al., 2014; Zhang et al., In addition, one must be cognizant of the framework within which 2016) within a molecular phylogeny. Either the clade(s) including taxa were named as this can influence where they are assumed to be the fossil(s) or even the entire tree is fixed or constrained: in topol- placed within a phylogenetic context. There has been a paradigm ogy, and inferred ages are dependent on the sequence data, calibra- shift in paleobotany regarding taxonomy. In the early 20th century, tion priors, and the model of rate variation used but not uncertainty attempts were made to place as many fossils as possible into extant in the tree or the fossil placement per se. In these cases, morpho- genera. Subsequently, thinking of fossils as extinct taxa that may logical data and fossils do not inform the topology of the inferred or may not be directly related to (or nested within) modern taxa phylogeny, but rather conform to placements dictated by the re- became more acceptable and encouraged. While some previously searcher. Fossil placements among and within lineages are therefore described fossils have been transferred to new extinct genera and not tested as part of the tree- building process. However, we know relationships to other fossils and to extant taxa were subsequently that present- day diversity in all lineages is a result of complex in- re- evaluated (e.g., “Viburnum” leaves from the Paleogene of North teractions on geological time scales of extinction, speciation, ecol- America and Asia that are now classified in the extinct genera ogy, morphology, and genetics (e.g., Barnosky, 2001; McElwain and Amersinia and Beringiaphyllum; Manchester et al., 1999), many Punyasena, 2007; Escapa and Pol, 2011; Green et al., 2011; Swenson, more have not been reinvestigated. Fossils assigned to extant genera 2011; Wiens, 2017). Incorporating morphological data from the should therefore be approached with particular caution, as the evi- fossil record is the only objective way of characterizing extinct line- dence for placing them in an extant genus (or even species) needs to ages and determining where they may fit in the evolutionary history be tested; however, these are very good candidates for further study. of a lineage. With fossils included as terminal units in the phyloge- Additionally, researchers should keep in mind that while presumed netic analysis, biogeographic patterns, trait evolution, and impact affinities and phylogenetic placement may change once re- evaluated, of environmental and ecological changes across lineages can be ex- the name of the taxon is often retained and reflects an incorrect amined with greater generality compared to studies based only on relationship. An example of this is the pollen genus Pandaniidites extant species with molecular sequence data. There are many cases Elsik, which was described from isolated grains that bore a resem- where the fossil record preserves morphological, spatiotemporal blance to Pandanus Parkinson (Pandanaceae), and given a name (e.g., Prasad et al., 2005, 2011; Smith et al., 2008, 2009b; Wilf and that reflected those observations, was classified as Pandanaceae. Escapa, 2015) and even climatic/environmental data (e.g., Wing Subsequently, the grains were found in situ in Pandaniidites that and Greenwood, 1993; Greenwood and Wing, 1995) that could not had aroid affinities, demonstrating they belong to Araceae and not be predicted, or would not be considered when only extant lineages Pandanaceae (Stockey et al., 1997): the name, however, using the are evaluated. Rather than only relying on the information present International Code of Nomenclature for algae, fungi, and plants, did in extant species to understand patterns of evolution and diversi- not change. Thus, usingPandaniidites to calibrate a Pandanaceae
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