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Building the Monocot Tree of Death

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Building the Monocot Tree of Death Received Date: Revised Date: Accepted Date: Article Type: Special Issue Article 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 Short Title: Building the monocot tree of death Building the monocot tree of death: progress and challenges emerging from the macrofossil-rich Zingiberales 1,2,4,6 1,3 1,4 5 Selena Y. Smith , William J. D. Iles , John C. Benedict , and Chelsea D. Specht Manuscript received 1 November 2017; revision accepted 2 May 2018. 1 Department of Earth & Environmental Sciences, University of Michigan, Ann Arbor, MI 48109 USA 2 Museum of Paleontology, University of Michigan, Ann Arbor, MI 48109 USA 3 Department of Integrative Biology and the University and Jepson Herbaria, University of California, Berkeley, CA 94720 USA 4 Program in the Environment, University of Michigan, Ann Arbor, MI 48109 USA 5 School of Integrative Plant Sciences, Section of Plant Biology and the Bailey Hortorium, Cornell University, Ithaca, NY 14853 USA 6 Author for correspondence (e-mail: [email protected]); ORCID id 0000-0002-5923-0404 Author Manuscript This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/ajb2.1123 This article is protected by copyright. All rights reserved Smith et al.–Building the monocot tree of death Citation: Smith, S. Y., W. J. D. Iles, J. C. Benedict, and C. D. Specht. 2018. Building the monocot tree of death: progress and challenges emerging from the macrofossil-rich Zingiberales. American Journal of Botany 105(8): XXX. DOI: XXXX PREMISE OF THE STUDY: Inclusion of fossils in phylogenetic analyses is necessary in order to construct a comprehensive “tree of death” and elucidate evolutionary history of taxa; however, such incorporation of fossils in phylogenetic reconstruction is dependent on the availability and interpretation of extensive morphological data. Here, the Zingiberales, whose familial relationships have been difficult to resolve with high support, are used as a case study to illustrate the importance of including fossil taxa in systematic studies. METHODS: Eight fossil taxa and 43 extant Zingiberales were coded for 39 morphological seed characters, and these data were concatenated with previously published molecular sequence data for analysis in the program MrBayes. KEY RESULTS: Ensete oregonense is confirmed to be part of Musaceae, and the other seven fossils group with Zingiberaceae. There is strong support for Spirematospermum friedrichii, Spirematospermum sp. ‘Goth’, S. wetzleri, and Striatornata sanantoniensis in crown Zingiberaceae while “Musa” cardiosperma, Spirematospermum chandlerae, and Tricostatocarpon silvapinedae are best considered stem Zingiberaceae. Inclusion of fossils explains how different topologies from morphological and molecular data sets is due to 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 Author Manuscript tomography will help to build the tree of death and ultimately improve our understanding of the evolutionary history of monocots. This article is protected by copyright. All rights reserved Smith et al.–Building the monocot tree of death KEY WORDS: anatomy; digital morphology; Ensete oregonense; Spirematospermum; Striatornata; Tricostatocarpon Monocot flowering plants represent ca. 22% of flowering plant species, encompassing a large diversity of morphology, habit, and ecologies. This group is economically important, including many of our staple food crops such as grains (maize, wheat, rice, sorghum), coconuts, plantains; pasture feed for animals; materials produced from species such as bamboo or abaca; spices such as ginger, turmeric, and saffron; and many ornamentals such as spring bulbs, irises, and orchids. Monocots are also ecologically important, forming dominant components of grassland, savanna, fynbos, wetland, and seagrass ecosystems, as well as important parts of tropical forest understories. At an ordinal level, the monocot phylogeny has been relatively stable compared to other groups (APG, 1998, 2016), making them useful for broader studies. Most studies find monocots to be ca. 135 Ma (e.g., Janssen and Bremer, 2004: 134 Ma; Magallón et al., 2015: 135.7 Ma). Monocots represent a good model group for elucidating the patterns and processes of evolution, and understanding their evolutionary history is fundamentally important to human nutrition and well-being. Data from fossil taxa need to be included to obtain the most comprehensive results when inferring phylogenetic relationships and investigating trait evolution, geographic histories, and other aspects of evolution for a lineage. In most cases, fossils are simply considered as constraints on the ages of nodes (e.g., Ho and Duchêne, 2014; but see Ronquist et al., 2012a; Heath et al., 2014; Zhang et al., 2016) within a molecular phylogeny. Either the clade(s) including the fossil(s) or even the entire tree is fixed or constrained: in topology, and inferred ages are dependent on the sequence data, calibration priors, and the model of rate variation used but not uncertainty in the tree or the fossil placement per se. In these cases, morphological data and fossils do not inform the topology of the inferred phylogeny, but rather conform to placements dictated by the researcher. Fossil placements among and within lineages are therefore Author Manuscript not tested as part of the tree-building process. However, we know that present-day diversity in all lineages is a result of complex interactions on geological time scales of extinction, speciation, ecology, morphology, and genetics (e.g., Barnosky, 2001; McElwain and Punyasena, 2007; This article is protected by copyright. All rights reserved Smith et al.–Building the monocot tree of death Escapa and Pol, 2011; Green et al., 2011; Swenson, 2011; Wiens, 2017). Incorporating morphological data from the fossil record is the only objective way of characterizing extinct lineages and determining where they may fit in the evolutionary history of a lineage. With fossils included as terminal units in the phylogenetic analysis, biogeographic patterns, trait evolution, and impact of environmental and ecological changes across lineages can be examined with greater generality compared to studies based only on extant species with molecular sequence data. There are many cases where the fossil record preserves morphological, spatiotemporal (e.g., Prasad et al., 2005, 2011; Smith et al., 2008, 2009b; Wilf and Escapa, 2015) and even climatic/environmental data (e.g., Wing and Greenwood, 1993; Greenwood and Wing, 1995) that could not be predicted, or would not be considered when only extant lineages are evaluated. Rather than only relying on the information present in extant species to understand patterns of evolution and diversification across the entire history of a clade, including fossils will improve our inferences by incorporating a temporal component to studies of trait evolution, biogeographic patterns, and phylogenies. <h2>Reading the fossil record of monocots Numerous reviews regarding the fossil record of monocots (Doyle, 1973; Daghlian, 1981; Collinson et al., 1993; Herendeen and Crane, 1995; Gandolfo et al., 2000; Greenwood and Conran, 2000; Stockey, 2006; Smith et al., 2010; Friis et al., 2011; Smith, 2013) have discussed the challenges of working with monocot fossils, adding complications to building a monocot “tree of death”, i.e., a tree of life that includes both extant and extinct taxa to resolve overall patterns of phylogenetic relationships. Monocots generally have a low preservation potential because they are often small and herbaceous, lacking “woody” and highly lignified tissues, and have persistent senescent organs, so they either rot in place or never contribute to sediments and thus, do not enter the fossil record (Herendeen and Crane, 1995; Smith, 2013). The lineages of monocots that are better represented tend to be those that are more lignified (e.g., palms) or grow in habitats that are near good depositional environments, such as quiet bodies of fresh water. First and foremost, the study and accurate naming of fossil taxa is a key component of Author Manuscript building a reliable and accurate tree of death. Taxonomy is a vital and dynamic process, and assigning a name and rank to a fossil provides a taxonomic and phylogenetic framework for the taxon in question; we recommend not using unnamed fossils for dating phylogenies (e.g., Bell et This article is protected by copyright. All rights reserved Smith et al.–Building the monocot tree of death al., 2010; Smith et al., 2010; Zanne et al., 2014; Tank et al., 2015), as the lack of a name suggests the need for careful evaluation of described morphology and/or ambiguity in phylogenetic placement based on characters analyzed. In addition, one must be cognizant of the framework within which taxa were named as this can influence where they are assumed
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