Integrative Paleobotany: Affirming the Role of Fossils in Modern Plant Biology—Introduction and Dedication

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Previous articleNext article FreeSpecial Issue—Rothwell CelebrationIntegrative Paleobotany: Affirming the Role of Fossils in Modern Plant Biology—Introduction and DedicationIgnacio H. Escapa, Alexandru M.F. Tomescu, Michael T. Dunn, and Ruth A. StockeyIgnacio H. Escapa*Consejo Nacional de Investigaciones Científicas y Técnicas, Museo Paleontológico Egidio Feruglio, Trelew, Chubut 9100, Argentina Search for more articles by this author , Alexandru M.F. Tomescu†Department of Biological Sciences, Humboldt State University, Arcata, California 95521, USA1Author for correspondence; email: [email protected]. Search for more articles by this author , Michael T. Dunn‡Department of Agriculture, Biology, and Health Sciences, Cameron University, Lawton, Oklahoma 73505, USA Search for more articles by this author , and Ruth A. Stockey§Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331, USA Search for more articles by this author PDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinked InRedditEmailQR Code SectionsMoreIf you are interested in plant evolution, try this quick exercise: take a phylogenetic tree of the plant kingdom, close your eyes, and point your finger randomly to a node of the phylogeny. Irrespective of the clade to which you are pointing, there is one thing you should know about it: the living representatives of that clade have evolved as a result of a long process in which failed attempts are the rule, and as a result, the diversity of extinct forms accumulated in the fossil record far exceeds that recorded in the extant flora. From this simple concept, Gar W. Rothwell made his career. Because of that, here is a second thing you should know about the plant clade to which you pointed at random: Gar has, more likely than not, contributed information about evolution in that clade at some point in his career. Gar was one of the principal contributors to the revival of paleobotany from a largely descriptive discipline to a vibrant field of investigation at the forefront of modern evolutionary sciences that contributes crucial insights into plant evolution, equal in importance to those provided by genetics and molecular biology. Because of this, the impact of Gar’s scientific contributions reaches far beyond the field of paleobotany, with important implications for wide areas of plant biology, including anatomy and morphology, development, systematics, phylogeny, and evolution.Gar earned a master’s degree in the laboratory of Thomas N. Taylor (University of Illinois at Chicago, 1966) studying Paleozoic seeds in the genus Conostoma (Rothwell and Eggert 1970; Rothwell 1971a). He subsequently earned his PhD degree in the laboratory of Wilson N. Stewart (University of Alberta, 1973), where he reconstructed the plants in the seed fern genus Callistophyton (Rothwell 1972b, 1975, 1980, 1981). His work was instrumental in ushering in studies of fossil plants as whole living organisms, looking at both structure and development. These early experiences launched Gar on a career in plant evolutionary biology that stretched over a half century, during which he occupied positions at the University of Alberta, University of London–Chelsea College, Ohio University, and Oregon State University. Throughout his career, Gar’s scholarly work and contributions have been recognized by numerous awards and honors: the Isabel Cookson Award, the Edgar T. Wherry Award, the Michael A. Cichan Award, the Merit Award of the Botanical Society of America, and honorary membership in the International Organization of Palaeobotany, where he served for 12 years as secretary-treasurer and president.Gar is the author, with Wilson Stewart, of one of the most impactful and widely used textbooks in the field of paleobotany and plant evolution—Paleobotany and the Evolution of Plants. Published in 1993, this textbook explains in direct and engaging prose the crucial role of fossils, and of their anatomy and morphology, in understanding the origin and evolution of all major plant groups. For more than a quarter century it has provided inspiration to numerous paleobotanists and structural botanists worldwide.The results of the research program that Gar has led are reflected in the more than 250 peer-reviewed journal articles and book chapters published in more than 30 scientific journals that cover the fields of botany and paleobotany (e.g., International Journal of Plant Sciences, American Journal of Botany, and Review of Palaeobotany and Palynology) and the broader area of the natural sciences (e.g., Science and Nature). However, Gar’s influence in the field of plant biology cannot be reduced to a number of publications—it is best reflected in the quality, relevance, and impact of these contributions, which combine a classic perspective derived from detailed anatomical and morphological descriptions of fossil species with innovative methodologies and approaches. Gar conducted most of these studies in collaboration with his students and other fellow paleobotanists and plant biologists.Gar is a time traveler: the species he has described belong to a time slice that spans more than 400 million years. His studies have investigated plants and other organisms from the Paleozoic to the present and have addressed an incredibly large number of lineages, many of them described as new species, genera, families, and even classes. He has made detailed descriptions of prokaryotes, fungi, liverworts, mosses, lycopsids, sphenopsids, ferns of a wide variety of lineages, pteridosperms, conifers and coniferophytes, cycads, ginkgophytes, bennettitaleans, and angiosperms—nothing has escaped Gar’s inquisitive eye. These descriptions of fossil taxa, which led to the development of several now-classic whole-plant concepts, have always represented for Gar only the first step in understanding broader and deeper processes in plant evolution and development. Gar has also used these fossils to develop innovative ideas and approaches for documenting the natural history of species long extinct and to inform some of the most vexing unanswered questions in plant evolution and phylogeny. Over the past few decades, no scientist has been more influential in affirming and expanding the potential of paleobotany as an integral contributor to evolutionary plant biology than Gar. In terms of organismal biology and natural history, in landmark studies Gar documented several aspects of reproductive biology of the early seed plants, including the hydrasperman reproductive syndrome (Rothwell 1971a, 1971b, 1986; Rothwell and Scheckler 1988; Serbet and Rothwell 1995), pollination drops (Rothwell 1977) and pollen tubes (Rothwell 1972a) of Carboniferous seed ferns (pteridosperms), and seed dormancy in Paleozoic conifers (Mapes et al. 1989). Together with collaborators, Gar described what is still the oldest seed plant reconstructed as a whole plant, the pteridosperm Elkinsia (Rothwell et al. 1989; Rothwell and Serbet 1992; Serbet and Rothwell 1992). His studies of the apical organization of lepidodendralean rooting structures (rhizomorphs; Rothwell 1984; Rothwell and Pryor 1991), the lepidodendralean embryo anatomy (Stubblefield and Rothwell 1981; Pigg and Rothwell 1983b), and the body plan of the Chaloneriaceae (Pigg and Rothwell 1979, 1983a) led to a paradigm shift in our understanding of the structure and evolution of the body plan of isoetalean lycopsids (Rothwell and Erwin 1985). Gar’s continued exploration of coal ball floras put on firm footing the idea that the rise and the first major radiation of leptosporangiate ferns occurred in the Carboniferous (Rothwell 1978, 1987a, 1996, 1999; Trivett and Rothwell 1988; Rothwell and Good 2000; Tomescu et al. 2006; Rothwell and Stockey 2008). His studies spanning several decades also painstakingly documented the evolution of conifer reproductive structures, from the early conifers of the Paleozoic (Rothwell 1982; Mapes and Rothwell 1984, 1991, 1998; Rothwell et al. 1997, 2005, 2007; Hernandez-Castillo et al. 2001, 2009; Rothwell and Mapes 2001) to the origins of modern conifer families (Falder et al. 1998; Ratzel et al. 2001; Klymiuk et al. 2011; Rothwell et al. 2011, 2012; Serbet et al. 2013; Atkinson et al. 2014a, 2014b; Rothwell and Ohana 2016). In studies of broader scope, Gar surveyed the diversity of fossil and extant plants, contributing novel perspectives on the evolution of sporophyte body plans and branching patterns across the entire embryophyte clade (Rothwell 1995; Tomescu et al. 2014) and on the diversity and evolution of stelar architecture across the tracheophyte clade (Rothwell 1976; Beck et al. 1982).The inclusion of fossil plants in phylogenetic analyses ranks among Gar’s most important contributions to evolutionary biology. Extinct species exhibiting novel combinations of characters refashion our understanding of evolutionary relationships and are key to studies of deep phylogeny. Gar’s work has been at the forefront of the integration of fossils in studies of systematics and phylogeny. He was one of the pioneering paleobotanists to empirically address the influence of fossils on the resolution of phylogenetic relationships. Based on numerous analyses focused on different plant groups, Gar has repeatedly demonstrated that the inclusion of fossil species in a phylogenetic context, aside from broadening the scope of analyses, can change traditionally held views on the relationships of living organisms. Among the most relevant of these studies, Rothwell and Serbet (1994) undertook an analysis of lignophyte evolution, which supports the monophyly of seed plants and has been at the base of subsequent developments and discussions (e.g., Doyle 2006; Hilton and Bateman 2006; Toledo et al. 2018). In another study, Gar took on the depths of pteridophyte phylogeny, developing an extensive morphological matrix that included the broad diversity of extinct fern lineages alongside living ferns (Rothwell 1999). The study supports a paraphyletic grade of pteridophytes along the euphyllophyte backbone, providing a solid counterpoint to the results of studies based exclusively on living plants, which recover ferns, psilotophytes, and sphenopsids as a monophyletic group sister to the seed plants (revisited by Rothwell and Nixon in 2006). Branching off from many of Gar’s extensive studies of fossil gymnosperms and conifers are collaborative treatments of phylogeny within these groups, aimed at voltzialeans (Rothwell et al. 2005), Pinaceae (Ryberg et al. 2012; Gernandt et al. 2016; Smith et al. 2017), Cupressaceae (Rothwell et al. 2011), gnetophytes (Rothwell and Stockey 2013), and broader samplings across these groups (Rothwell and Stockey 2016). In the same vein, Rothwell et al. (2009) queried the Paleozoic and Mesozoic fossil record of seed plants, garnering renewed support for an anthophyte clade and, at the same time, emphasizing the need for total evidence analyses in the resolution of recalcitrant areas of plant phylogeny. The state of the art in the integrative assessment of plant phylogeny based on living, as well as fossil, diversity has been presented recently in a special issue of the American Journal of Botany in the article “Tree of Death: The Role of Fossils in Resolving the Overall Pattern of Plant Phylogeny” that Gar coedited with two of us (Rothwell et al. 2018a). Many of the articles in the special issue—to which Gar contributed an extensive treatment of marattialean phylogeny (Rothwell et al. 2018b)—are authored by his former students and collaborators.Another major direction pioneered by Gar involved integrating the extensive knowledge of the morphology and anatomy of fossil plants with the growing understanding of developmental regulation at the genetic and molecular levels to undertake “paleo-evo-devo” studies in plant biology (Rothwell 1987b). In doing this, Gar searched the fossil record for structural evidence supporting the action of specific genes and growth regulators. This type of anatomical evidence, which he introduced as “structural fingerprints” (Rothwell and Lev-Yadun 2005; Rothwell et al. 2014), allows for tracing the history of those mechanisms in phylogenetic space and time and is crucial to understanding the origin and evolution of the regulatory processes that these fingerprints reflect, thus refining our understanding of the patterns and processes of morphological evolution. Gar was the first paleobotanist to explore such structural fingerprints and the first to explicitly articulate and consistently pursue the integration of plant fossils in the evo-devo paradigm (Rothwell and Tomescu 2018). His studies that integrate data from the fossil record to address the evolution of lycophyte body plans (Rothwell and Erwin 1985), leaves (Sanders et al. 2007, 2009), polar auxin transport (Rothwell and Lev-Yadun 2005), gravitropism (Sanders et al. 2011), and secondary growth (Rothwell et al. 2008) are now classic landmarks for integrative studies of the evolution of plant morphology.This special issue is the outcome of both Garfest 2017, a joyful paleobotanical banquet held in Gar’s honor at the 2017 meeting of the Botanical Society of America in Fort Worth, Texas, and a daylong colloquium organized in recognition of Gar’s scientific achievements at the 2018 meeting of the Botanical Society of America in Rochester, Minnesota. The articles collected in this issue celebrate Gar’s prolific, wide-ranging, and far-reaching career and fittingly explore a very diverse array of plants, time periods, and questions. Our original idea was to publish a single volume including all the contributed articles. However, the large number of articles we received (27), a testament to the respect and appreciation that Gar commands among his peers, has required a change of plan. Thus, this issue contains a subset of those articles, selected solely based on the order in which they were accepted for publication. The remaining articles are scheduled for publication in Rothwell special sections that will be included in subsequent issues of the International Journal of Plant Sciences. Together, these articles cover a broad spectrum of plant and nonplant lineages (e.g., chytridiomycetes, bryophytes, lycopsids, sphenopsids, ferns, pteridosperms, coniferophytes, conifers, gnetophytes, and angiosperms) and address questions that range from ecology to anatomy and morphology of various plant parts, whole-plant reconstructions, systematics, phylogeny, developmental regulation, and the evolution of plant development. The studies investigate plants from throughout the geologic timescale (Paleozoic, Mesozoic, Cenozoic), as well as living plants, in all corners of the world: Australia, Argentina, Canada, China, Finland, Germany, Italy, Panama, Portugal, Russia, Scotland, Switzerland, Turkey, Venezuela, and the United States.As Andrew Knoll recounts: “Many years ago, I received a phone call from Gar. His opening words were, ‘I have a theory.’ Sensing the irony oozing down the phone line, I took the bait, ‘Gar, what’s your theory?’ ‘I think,’ replied Gar, ‘that my fossils were once living plants.’” Paleobotany is the science that endeavors to bring the terrific spectrum of extinct species back to life, and for several decades Gar has been one of its foremost luminaries. This collection of articles provides a crystal clear image of the impetus and relevance of the studies of fossil plants in today’s integrative world of plant biology. It is an honor and a great pleasure to dedicate it to our colleague, mentor, and friend, Gar Rothwell, for the legacy of his insatiable curiosity, his innovative ideas, and the abundant inspiration he has engendered throughout the discipline of botany. In closing, we rejoice that this is but one milestone in Gar’s story, which continues and never ceases to keep us guessing—or in Steve Manchester’s words: “Gar moves so gracefully up and down the stratigraphic column and across plant phylogeny that it can be difficult to know where he will strike next.” Wherever that may happen, we look forward to it! Gar Rothwell was named Distinguished Professor at Ohio University in 2004. Photo courtesy of Fred C. Tom of Lamborn’s Studio, Athens, Ohio.View Large ImageDownload PowerPointAcknowledgmentsWe thank all those who contributed their stories and thoughts on Gar in preparation of Garfest 2017 and the 2018 Botanical Society of America colloquium “Fossil Plants at the Intersection of Evo-Devo and Phylogeny: Celebrating the Contributions of Gar W. Rothwell to Biodiversity and Evolution.” We also thank all of Gar’s colleagues, both for contributing articles to the colloquium and to this special issue and for volunteering to review one or more of the 27 contributed articles. They are too numerous to be listed here. We are indebted to the editors of the International Journal of Plant Sciences, Christina Caruso and James Ellis, for their invaluable support and guidance. Fred C. Tom at Lamborn’s Studio (Athens, Ohio) graciously provided the photograph of Gar shown here.Literature CitedAtkinson BA, GW Rothwell, RA Stockey 2014a Hubbardiastrobus cunninghamioides gen. et sp. nov., evidence for a Lower Cretaceous diversification of cunninghamioid Cupressaceae. Int J Plant Sci 175:256–269.First citation in articleLinkGoogle Scholar——— 2014b Hughmillerites vancouverensis sp. nov. and the Cretaceous diversification of Cupressaceae. Am J Bot 101:2136–2147.First citation in articleCrossref MedlineGoogle ScholarBeck CB, R Schmid, GW Rothwell 1982 Stelar morphology and the primary vascular system of seed plants. Bot Rev 48:691–815.First citation in articleCrossrefGoogle ScholarDoyle JA 2006 Seed ferns and the origin of angiosperms. J Torrey Bot Soc 133:169–209.First citation in articleCrossrefGoogle ScholarFalder AB, GW Rothwell, G Mapes, RH Mapes, LA Doguzhaeva 1998 Pityostrobus milleri sp. nov., a pinaceous cone from the Lower Cretaceous (Aptian) of southwestern Russia. Rev Palaeobot Palynol 103:253–261.First citation in articleCrossrefGoogle ScholarGernandt DS, G Holman, C Campbell, M Parks, S Mathews, LA Raubeson, A Liston, RA Stockey, GW Rothwell 2016 Phylogenetics of extant and fossil Pinaceae: methods for increasing topological stability. Botany 94:863–884.First citation in articleCrossrefGoogle ScholarHernandez-Castillo GR, GW Rothwell, G Mapes 2001 Thucydiaceae fam. nov., with a review and reevaluation of Paleozoic walchian conifers. Int J Plant Sci 162:1155–1185.First citation in articleLinkGoogle ScholarHernandez-Castillo GR, RA Stockey, GW Rothwell, G Mapes 2009 Reconstructing Emporia lockardii (Voltziales: Emporiaceae) and initial thoughts on Paleozoic conifer ecology. Int J Plant Sci 170:1056–1074.First citation in articleLinkGoogle ScholarHilton J, RM Bateman 2006 Pteridosperms are the backbone of seed-plant phylogeny. J Torrey Bot Soc 133:119–168.First citation in articleCrossrefGoogle ScholarKlymiuk AA, RA Stockey, GW Rothwell 2011 The first organismal concept for an extinct species of Pinaceae: Pinus arnoldii Miller. Int J Plant Sci 172:294–313.First citation in articleLinkGoogle ScholarMapes G, GW Rothwell 1984 Permineralized ovulate cones of Lebachia from Late Palaeozoic limestones of Kansas. Palaeontology 27:69–94.First citation in articleGoogle Scholar——— 1991 Structure and relationships of primitive conifers. N Jahrb Geol Palaontol Abh 183:269–287.First citation in articleGoogle Scholar——— 1998 Primitive pollen cone structure in Upper Pennsylvanian (Stephanian) walchian conifers. J Paleontol 72:571–576.First citation in articleCrossrefGoogle ScholarMapes G, GW Rothwell, MT Haworth 1989 Evolution of seed dormancy. Nature 337:645–646.First citation in articleCrossrefGoogle ScholarPigg KB, GW Rothwell 1979 Stem-root transition of an Upper Pennsylvanian woody lycopsid. Am J Bot 66:914–924.First citation in articleCrossrefGoogle Scholar——— 1983a Chaloneria gen. nov.: heterosporus lycophytes from the Pennsylvanian of North America. Bot Gaz 144:132–147.First citation in articleLinkGoogle Scholar——— 1983b Megagametophyte development in the Chaloneriaceae fam. nov., permineralized Paleozoic Isoetales (Lycopsida). Bot Gaz 144:295–302.First citation in articleLinkGoogle ScholarRatzel SR, GW Rothwell, G Mapes, RH Mapes, LA Doguzhaeva 2001 Pityostrobus hokodzensis, a new species of pinaceous cone from the Cretaceous of Russia. J Paleontol 75:895–900.First citation in articleCrossrefGoogle ScholarRothwell GW 1971a Additional observations on Conostoma anglo-germanicum and C. oblongum from the Lower Pennsylvanian of North America. Palaeontogr Abt B 131:167–178.First citation in articleGoogle Scholar——— 1971b Ontogeny of the Paleozoic ovule, Callospermarion pusillum. Am J Bot 58:706–715.First citation in articleCrossrefGoogle Scholar——— 1972a Evidence of pollen tubes in Paleozoic pteridosperms. Science 175:772–774.First citation in articleCrossrefGoogle Scholar——— 1972b Pollen organs of the Pennsylvanian Callistophytaceae (Pteridospermopsida). Am J Bot 59:993–999.First citation in articleCrossrefGoogle Scholar——— 1975 The Callistophytaceae (Pteridospermopsida). I. Vegetative structures. Palaeontogr Abt B 151:171–196.First citation in articleGoogle Scholar——— 1976 Primary vasculature and gymnosperm systematics. Rev Palaeobot Palynol 22:193–206.First citation in articleCrossrefGoogle Scholar——— 1977 Evidence for a pollination-drop mechanism in Paleozoic pteridosperms. Science 198:1251–1252.First citation in articleCrossrefGoogle Scholar——— 1978 Doneggia complura gen. et sp. nov., a filicalean fern from the Upper Pennsylvanian of Ohio. Can J Bot 56:3096–3104.First citation in articleCrossrefGoogle Scholar——— 1980 The Callistophytaceae (Pteridospermopsida). II. Reproductive features. Palaeontogr Abt B 173:85–106.First citation in articleGoogle Scholar——— 1981 The Callistophytales (Pteridospermopsida): reproductively sophisticated Paleozoic gymnosperms. Rev Palaeobot Palynol 32:103–121.First citation in articleCrossrefGoogle Scholar——— 1982 New interpretations of the earliest conifers. Rev Palaeobot Palynol 37:7–28.First citation in articleCrossrefGoogle Scholar——— 1984 The apex of Stigmaria (Lycopsida), rooting organ of lepidodendrales. Am J Bot 71:1031–1034.First citation in articleCrossrefGoogle Scholar——— 1986 Classifying the earliest gymnosperms. Pages 137–161 in RA Spicer, BA Thomas, eds. Systematic and taxonomic approaches in paleobotany. Clarendon, Oxford.First citation in articleGoogle Scholar——— 1987a Complex Paleozoic filicales in the evolutionary radiation of ferns. Am J Bot 74:458–461.First citation in articleCrossrefGoogle Scholar——— 1987b The role of development in plant phylogeny: a paleobotanical perspective. Rev Palaeobot Palynol 50:97–114.First citation in articleCrossrefGoogle Scholar——— 1995 The fossil history of branching: implications for the phylogeny of land plants. Pages 71–86 in PC Hoch, AG Stephenson, eds. Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis.First citation in articleGoogle Scholar——— 1996 Phylogenetic relationships of ferns: a palaeobotanical perspective. Pages 395–404 in JM Camus, M Gibby, RJ Johns, eds. Pteridology in perspective. Royal Botanic Gardens, Kew.First citation in articleGoogle Scholar——— 1999 Fossils and ferns in the resolution of land plant phylogeny. Bot Rev 65:188–218.First citation in articleCrossrefGoogle ScholarRothwell GW, WL Crepet, RA Stockey 2009 Is the anthophyte hypothesis alive and well? new evidence from the reproductive structures of Bennettitales. Am J Bot 96:296–322.First citation in articleCrossrefGoogle ScholarRothwell GW, DA Eggert 1970 A Conostoma with tentacular sarcotesta from the Upper Pennsylvanian of Illinois. Bot Gaz 131:359–366.First citation in articleLinkGoogle ScholarRothwell GW, DM Erwin 1985 The rhizomorph apex of Paurodendron: implications for homologies among the rooting organs of Lycopsida. Am J Bot 72:86–98.First citation in articleCrossrefGoogle ScholarRothwell GW, IH Escapa, AMF Tomescu 2018a Tree of death: the role of fossils in resolving the overall pattern of plant phylogeny. Am J Bot 105:1239–1242.First citation in articleCrossrefGoogle ScholarRothwell GW, CW Good 2000 Reconstructing the Pennsylvanian-age filicalean fern Botryopteris tridentata (Felix) Scott. Int J Plant Sci 161:495–507.First citation in articleLinkGoogle ScholarRothwell GW, S Lev-Yadun 2005 Evidence of polar auxin flow in 375 million-year-old fossil wood. Am J Bot 92:903–906.First citation in articleCrossrefGoogle ScholarRothwell GW, G Mapes 2001 Barthelia furcata gen. et sp. nov., with a review of Paleozoic coniferophytes and a discussion of coniferophyte systematics. Int J Plant Sci 162:637–667.First citation in articleLinkGoogle ScholarRothwell GW, G Mapes, GR Hernandez-Castillo 2005 Hanskerpia gen. nov. and phylogenetic relationships among the most ancient conifers (Voltziales). Taxon 54:733–750.First citation in articleCrossrefGoogle ScholarRothwell GW, G Mapes, J Hilton, NT Hollingworth 2007 Pollen cone anatomy of Classostrobus crossii sp. nov. (Cheirolepidiaceae). Int J Coal Geol 69:55–67.First citation in articleCrossrefGoogle ScholarRothwell GW, G Mapes, RH Mapes 1997 Late Paleozoic conifers of North America: structure, diversity and occurrences. Rev Palaeobot Palynol 95:95–113.First citation in articleCrossrefGoogle ScholarRothwell GW, G Mapes, RA Stockey, J Hilton 2012 The seed cone Eathiestrobus gen. nov.: fossil evidence for a Jurassic origin of Pinaceae. Am J Bot 99:708–720.First citation in articleCrossrefGoogle ScholarRothwell GW, MA Millay, RA Stockey 2018b Resolving the overall pattern of marattialean fern phylogeny. Am J Bot 105:1304–1314.First citation in articleCrossrefGoogle ScholarRothwell GW, KC Nixon 2006 How does the inclusion of fossil data change our conclusions about the phylogenetic history of euphyllophytes? Int J Plant Sci 167:737–749.First citation in articleLinkGoogle ScholarRothwell GW, T Ohana 2016 Stockeystrobus gen. nov. (Cupressaceae), and the evolutionary diversification of sequoioid conifer seed cones. Botany 94:847–861.First citation in articleCrossrefGoogle ScholarRothwell GW, JS Pryor 1991 Developmental dynamics of arborescent lycophytes: apical and lateral growth in Stigmaria ficoides. Am J Bot 78:1740–1745.First citation in articleCrossrefGoogle ScholarRothwell GW, H Sanders, SE Wyatt, S Lev-Yadun 2008 A fossil record for growth regulation: the role of auxin in wood evolution. Ann Mo Bot Gard 95:121–134.First citation in articleCrossrefGoogle ScholarRothwell GW, SE Scheckler 1988 Biology of ancestral gymnosperms. Page 85–134 in CB Beck, ed. Origin and evolution of gymnosperms. Columbia University Press, New York.First citation in articleGoogle ScholarRothwell GW, SE Scheckler, WH Gillespie 1989 Elkinsia gen. nov., a late Devonian gymnosperm with cupulate ovules. Bot Gaz 158:170–189.First citation in articleLinkGoogle ScholarRothwell GW, R Serbet 1992 Pollination biology of Elkinsia polymorpha, implications for the origin of gymnosperms. Cour Forschungsinst Seckenb 147:225–231.First citation in articleGoogle Scholar——— 1994 Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Syst Bot 19:443–482.First citation in articleCrossrefGoogle ScholarRothwell GW, RA Stockey 2008 Phylogeny and evolution of ferns: a paleontological perspective. Pages 332–366 in TA Ranker, CH Haufler, eds. Biology and evolution of ferns and lycophytes. Cambridge University Press, Cambridge.First citation in articleGoogle Scholar——— 2013 Evolution and phylogeny of gnetophytes: evidence from the anatomically preserved seed cone Protoephedrites eamesii gen. et sp. nov. and the seeds of several bennettitalean species. Int J Plant Sci 174:511–529.First citation in articleLinkGoogle Scholar——— 2016 Phylogenetic diversification of Early Cretaceous seed plants: the compound seed cone of Doylea tetrahedrasperma. Am J Bot 103:923–937.First citation in articleCrossrefGoogle ScholarRothwell GW, RA Stockey, G Mapes, J Hilton 2011 Structure and relationships of the Jurassic conifer seed cone Hughmillerites juddii gen. et comb. nov.: implications for the origin and evolution of Cupressaceae. Rev Palaeobot Palynol 164:45–59.First citation in articleCrossrefGoogle ScholarRothwell GW, AMF Tomescu 2018 Structural fingerprints of development at the intersection of evo-devo and the fossil record. Page 30 in L Nuño de la Rosa, GB Muller, eds. Evolutionary developmental biology. Springer, New York. doi:10.1007/978-3-319-33038-9_169-1.First citation in articleGoogle ScholarRothwell GW, SE Wyatt, AMF Tomescu 2014 Plant evolution at the interface of paleontology and developmental biology: an organism-centered paradigm. Am J Bot 101:899–913.First citation in articleCrossrefGoogle ScholarRyberg PE, GW Rothwell, RA Stockey, J Hilton, G Mapes, JB Riding 2012 Reconsidering relationships among stem and crown group Pinaceae: oldest record of the genus Pinus from the Early Cretaceous of Yorkshire, United Kingdom. Int J Plant Sci 173:917–932.First citation in articleLinkGoogle ScholarSanders H, GW Rothwell, SE Wyatt 2007 Paleontological context for the developmental mechanisms of evolution. Int J Plant Sci 168:719–728.First citation in articleLinkGoogle Scholar——— 2009 Key morphological alterations in the evolution of leaves. Int J Plant Sci 170:860–868.First citation in articleLinkGoogle Scholar——— 2011 Parallel evolution of auxin regulation in rooting systems. Plant Syst Evol 291:221–225.First citation in articleCrossrefGoogle ScholarSerbet R, B Bomfleur, GW Rothwell 2013 Cunninghamia taylorii sp. nov., a structurally preserved cupressaceous conifer from the Upper Cretaceous (Campanian) Horseshoe Canyon Formation of western North America. Int J Plant Sci 174:471–488.First citation in articleLinkGoogle ScholarSerbet R, GW Rothwell 1992 Characterizing the most primitive seed ferns. I. A reconstruction of Elkinsia polymorpha. Int J Plant Sci 153:602–521.First citation in articleLinkGoogle Scholar——— 1995 Functional morphology and homologies of gymnospermous ovules: evidence from a new species of Stephanospermum. Can J Bot 73:650–661.First citation in articleCrossrefGoogle ScholarSmith SY, RA Stockey, GW Rothwell, SA Little 2017 A new species of Pityostrobus (Pinaceae) from the Cretaceous of California: moving towards understanding the Cretaceous radiation of Pinaceae. J Syst Palaeontol 15:69–81.First citation in articleCrossrefGoogle ScholarStewart WN, GW Rothwell 1993 Paleobotany and the evolution of plants. 2nd ed. Cambridge University Press, New York.First citation in articleGoogle ScholarStubblefield SP, GW Rothwell 1981 Embryogeny and reproductive biology of Bothrodendrostrobus mundus (Lycopsida). Am J Bot 68:625–634.First citation in articleCrossrefGoogle ScholarToledo S, AC Bippus, AMF Tomescu 2018 Buried deep beyond the veil of extinction: euphyllophyte relationships at the base of the spermatophyte clade. Am J Bot 105:1264–1285.First citation in articleCrossrefGoogle ScholarTomescu AMF, GW Rothwell, ML Trivett 2006 Kaplanopteridaceae fam. nov., additional diversity in the initial radiation of filicalean ferns. Int J Plant Sci 167:615–630.First citation in articleLinkGoogle ScholarTomescu AMF, SE Wyatt, M Hasebe, GW Rothwell 2014 Early evolution of the vascular plant body plan—the missing mechanisms. Curr Opin Plant Biol 17:126–136.First citation in articleCrossrefGoogle ScholarTrivett ML, GW Rothwell 1988 Modelling the growth architecture of fossil plants: a Paleozoic filicalean fern. Evol Trends Plants 2:25–29.First citation in articleGoogle Scholar Previous articleNext article DetailsFiguresReferencesCited by International Journal of Plant Sciences Volume 180, Number 6July/August 2019Special Issue: Rothwell Celebration Article DOIhttps://doi.org/10.1086/704242HistoryReceived May 2019Revised May 2019Published online May 31, 2019 © 2019 by The University of Chicago. 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