Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor

By Michael Krings and Gar W. Rothwell

Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor features the broadest possible spectrum of topics analyzing the structure, function and evolution of fossil plants, microorganisms, and organismal interactions in fossil ecosystems (e.g., plant paleobiography, paleoecology, early evolution of land plants, fossil fungi and microbial interactions with plants, systematics and phylogeny of major plant and fungal lineages, biostratigraphy, evolution of organismal interactions, ultrastructure, Antarctic paleobotany). The book includes the latest research from top scientists who have made transformative contributions.

Sections are richly illustrated, well concepted, and characterize and summarize the most up-to-date understanding of this respective and important field of study.

• Features electronic supplements, such as photographs, diagrams, tables, flowcharts and links to other websites
• Includes in-depth illustrations with diagrams, flowcharts and photographic plates (many in color for enhanced utility), tables and graphs

• Language: English
• Publisher: Academic Press
• Release date: Jul 14, 2018
• ISBN: 9780128130131

Book preview

Transformative Paleobotany

Papers to Commemorate the Life and Legacy of Thomas N. Taylor

Editors

Michael Krings

SNSB-Bavarian State Collection for Palaeontology and Geology Munich, Germany

Ludwig-Maximilians-Universität München Munich, Germany

The University of Kansas Lawrence, Kansas, United States

Carla J. Harper

The University of Kansas Lawrence, Kansas, United States

SNSB-Bavarian State Collection for Palaeontology and Geology Munich, Germany

Néstor Rubén Cúneo

Museo Paleontológico Egidio Feruglio, and National Research Council of Argentina Trelew, Chubut, Argentina

Gar W. Rothwell

Ohio University Athens, Ohio, United States Oregon State University Corvallis, Oregon, United States

Table of Contents

Cover image

Title page

Companion Website

Copyright

Contributors

About the Editors

Biography

Foreword

Acknowledgments

Section I. Early Land Plants: Innovations and Adaptations

Chapter 1. The Evolutionary Origin of the Plant Spore in Relation to the Antithetic Origin of the Plant Sporophyte

1. Introduction

2. The Antithetic Theory as a Scaffold for Interpreting the Fossil Record of the Algal–Plant Transition

3. Early Cryptospore Morphology

4. Cryptospores and the Origin of Meiosis in Plants

5. The Stratigraphic Record of the Cryptospores as a Record of Sporophyte Evolution

6. Interpreting Ordovician-Silurian Phytodebris as a Record of Sporophyte Evolution

7. Conclusion

Chapter 2. Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia

1. Introduction

2. Background

3. Previously Described Early Devonian Taxa

4. Comparisons

5. Discussion

6. Conclusions

Chapter 3. Using Architecture Modeling of the Devonian Tree Pseudosporochnus to Compute Its Biomass

1. Introduction

2. Material

3. Modeling Pseudosporochnus With AmapSim

4. Computing Biomass

5. Results

6. Discussion

7. Conclusions

Supplementary Figure

Chapter 4. The Advantages and Frustrations of a Plant Lagerstätte as Illustrated by a New Taxon From the Lower Devonian of the Welsh Borderland, UK

1. Introduction

2. Geological Background and Previous Research

3. New Research

4. The Limitations of Charcoalified Lagerstätten

5. Future Research

Chapter 5. Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies

1. Introduction

2. Materials and Methods

3. Results

4. Discussion

5. Conclusions

Appendices

Section II. Late Paleozoic and Mesozoic Plants and Floras

Chapter 6. Lower Permian Flora of the Sanzenbacher Ranch, Clay County, Texas

1. Introduction

2. Geology

3. Collections

4. Methods

5. Results

6. Discussion

7. Conclusions

Chapter 7. Permian Ginkgophytes of Angaraland

1. Introduction

2. Historical Background

3. Material and Methods

4. Results

5. Discussion

Chapter 8. Glossopterid Plant Remains in Permineralization: What Do They Tell Us?

1. Introduction

2. Material and Methods

3. Results

4. Discussion

Chapter 9. Pachytestopsis tayloriorum gen. et sp. nov., an Anatomically Preserved Glossopterid Seed From the Lopingian of Queensland, Australia

1. Introduction

2. Geological Setting

3. Material and Methods

4. Results

5. Discussion

6. Conclusions

Chapter 10. A Triassic Mystery Solved: Fertile Pekinopteris From the Triassic of North Carolina, United States

1. Introduction

2. Geological Setting

3. Material and Methods

4. Systematic Paleontology

5. Discussion

6. Conclusion

Chapter 11. Enigmatic, Structurally Preserved Stems From the Triassic of Central Europe: A Fern or Not a Fern?

1. Introduction

2. Historical Background

3. Geological Settings

4. Material and Methods

5. Systematic Paleontology

6. Results

7. Discussion

8. Conclusions

Section III. Paleobiogeography, Biology, and Phylogenetic Relationships of Plants

Chapter 12. A Comprehensive Assessment of the Fossil Record of Liverworts in Amber

1. Introduction

2. Material and Methods

3. Results

4. Discussion

5. Conclusions and Future Prospects

Chapter 13. Aerodynamics of Fossil Pollen: Implications for Understanding Pollination Biology in Extinct Plants

1. Introduction

2. Material and Methods

3. Results

4. Discussion

5. Conclusions

Chapter 14. Escapia gen. nov.: Morphological Evolution, Paleogeographic Diversification, and the Environmental Distribution of Marattialean Ferns Through Time

1. Introduction

2. Material and Methods

3. Systematic Paleontology

4. Discussion

5. Conclusions

Chapter 15. Heterosporous Ferns From Patagonia: The Case of Azolla

1. Introduction

2. Material and Methods

3. Results

4. Discussion

5. Conclusions

Chapter 16. Why Are Bryophytes So Rare in the Fossil Record? A Spotlight on Taphonomy and Fossil Preservation

1. Introduction

2. Challenges to Traditional Views of the Bryophyte Fossil Record

3. Bryophyte Taphonomy

4. Human Bias

5. Conclusions and Future Outlook

Chapter 17. Fossil Seeds With Affinities to Austrobaileyales and Nymphaeales From the Early Cretaceous (Early to Middle Albian) of Virginia and Maryland, USA: New Evidence for Extensive Extinction Near the Base of the Angiosperm Tree

1. Introduction

2. Geological Setting

3. Material and Methods

4. Results

5. Discussion

6. Conclusion

Section IV. Fossil Microorganisms

Chapter 18. Reactive Oxygen Defense Against Cellular Endoparasites and the Origin of Eukaryotes

1. Introduction

2. Frequent Invasion of Eukaryotic Cells by Diverse Microbes

3. Were Archaea Victims of Endoparasitism by Bacteria?

4. The Fossil Record of Endoparasitism

5. Reactive Oxygen Defense Response of the Host Cell

6. ER and NADPH-Oxidase

7. Membrane Sterols to Protect Eukaryote Membranes From Reactive Oxygen Damage

8. Evolution of the Cytoskeleton Network of Eukaryotic Cells

9. Evolution of the Nuclear Envelope

10. Evolution of Autophagy

11. Evolution of Mitochondria

12. Massive Genomes as a Legacy of Endoparasitism

13. Chloroplast Acquisition

14. Fungal Cell Walls as an Adaptation to Exclude Prokaryotic Endoparasites

15. Plant Cell Walls as Defense Against Endoparasitism

16. Endoparasitic Prokaryotes in Plants

17. Building on the Reactive Oxygen Defensive System in Animals

18. Multicellularity as Defense Against Endoparasites

19. Evolution of Apoptosis

20. Conclusions

Chapter 19. Fossils of Arbuscular Mycorrhizal Fungi Give Insights Into the History of a Successful Partnership With Plants

1. Introduction

2. The Early History of Mycorrhizal Fungi

3. Fungal Associations of Fossil Plants and Their Living Equivalents

4. Comparing Mycorrhizas in Fossil and Modern Land Plants

Chapter 20. Looking for Arbuscular Mycorrhizal Fungi in the Fossil Record: An Illustrated Guide

1. Introduction

2. Materials Used to Illustrate the Guide

3. Life Cycle of Extant AMF

4. Structural Characteristics of AMF

5. Fine Root Endophytes

6. Summary and Outlook

Chapter 21. Exceptional Preservation of Sessile, Long-Stalked Microorganisms in the Lower Devonian Windyfield Chert (Scotland)

1. Introduction

2. Geological Setting, Material, and Methods

3. Results

4. Discussion

5. Conclusions

Chapter 22. Morphological Convergence in Forest Microfungi Provides a Proxy for Paleogene Forest Structure

1. Introduction

2. Morphology, Distribution, and Ecology of Extant Calicioids

3. Fossil Calicioids Preserved in Amber

4. Discussion

Chapter 23. Ediacarans, Protolichens, and Lichen-Derived Penicillium: A Critical Reassessment of the Evolution of Lichenization in Fungi

1. Introduction

2. What Constitutes a (Fossil) Lichen?

3. Lichens and Lichen Symbiosis in the Fossil Record

4. Lichens in Time: The Fungal and Eukaryote Molecular Clock Revisited

5. Were the Ediacarans Lichens?

6. Protolichens: A Narrow Premise With Broad Implications?

7. Are Aspergillus and Penicillium Derived From Lichenized Ancestors?

8. Lichens: Multiple Gains of a Successful Lifestyle

9. Conclusions

Section V. Antarctic Paleobotany

Chapter 24. Polar Regions of the Mesozoic–Paleogene Greenhouse World as Refugia for Relict Plant Groups

1. Introduction

2. Material and Methods

3. Results

4. Discussion

5. Conclusions

Chapter 25. Leaf Venation Density and Calculated Physiological Characteristics of Fossil Leaves From the Permian of Gondwana

1. Introduction

2. Materials and Methods

3. Results

4. Discussion

5. Conclusions

Chapter 26. Functional Significance of Cambial Development in Vertebraria Roots: How Do Unusual Xylem Traits Serve Life at a High Latitude?

1. Introduction

2. Material and Methods

3. Results

4. Discussion

5. Conclusion

Chapter 27. Cretaceous to Paleogene Vegetation Transition in Antarctica

1. Introduction

2. Late Cretaceous Vegetation

3. Late Maastrichtian to Paleogene

4. Paleogene Vegetation

5. Discussion

6. Conclusions

Author Biographies

Index

Companion Website

Additional materials and information are available from the book’s companion website

https://www.elsevier.com/books-and-journals/book-companion/9780128130124

Copyright

Academic Press is an imprint of Elsevier

125 London Wall, London EC2Y 5AS, United Kingdom

525 B Street, Suite 1650, San Diego, CA 92101, United States

50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States

The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom

Copyright © 2018 Elsevier Inc. All rights reserved.

No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions.

This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein).

Notices

Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary.

Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility.

To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein.

Library of Congress Cataloging-in-Publication Data

A catalog record for this book is available from the Library of Congress

British Library Cataloguing-in-Publication Data

A catalogue record for this book is available from the British Library

ISBN: 978-0-12-813012-4

For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Andre Gerhard Wolff

Acquisitions Editor: Anna Valutkevich

Editorial Project Manager: Pat Gonzalez

Production Project Manager: Sreejith Viswanathan

Cover Designer: Mark Rogers

Typeset by TNQ Technologies

Contributors

Brian Axsmith,     University of South Alabama, Mobile, AL, United States

Jean-François Barczi,     AMAP, Université de Montpellier, Montpellier, France

Julia Bechteler,     Ludwig-Maximilians-Universität München, Munich, Germany

Marshall Bergen,     Rutgers University, New Brunswick, NJ, United States

Alexander C. Bippus,     Humboldt State University, Arcata, California, United States

Patrick Blomenkemper,     Westfälische Wilhelms-Universität Münster, Münster, Germany

Benjamin Bomfleur,     Westfälische Wilhelms-Universität Münster, Münster, Germany

Lara Brindisi,     Rutgers University, New Brunswick, NJ, United States

Mark C. Brundrett

University of Western Australia, Crawley, WA, Australia

Department of Biodiversity, Conservation and Attractions, Swan Region, WA, Australia

David J. Cantrill

Royal Botanic Gardens Victoria, Melbourne, VIC, Australia

The University of Melbourne, Parkville, VIC, Australia

Dan S. Chaney,     NMNH Smithsonian Institution, Washington, DC, United States

Xiaoqian Chang,     Rutgers University, New Brunswick, NJ, United States

Qiang Chen,     Rutgers University, New Brunswick, NJ, United States

Peter R. Crane

Oak Spring Garden Foundation, Upperville, VA, United States

Yale University, New Haven, CT, United States

William L. Crepet,     Cornell University, Ithaca, NY, United States

Néstor Rubén Cúneo,     Museo Paleontológico Egidio Feruglio, CONICET, Trelew, Argentina

Charles P. Daghlian,     Dartmouth College, Hanover, NH, United States

Anaëlle Dambreville,     AMAP, Université de Montpellier, Montpellier, France

Facundo De Benedetti,     Museo Paleontológico Egidio Feruglio, CONICET, Trelew, Argentina

Anne-Laure Decombeix

AMAP, Université de Montpellier, Montpellier, France

University of Kansas, Lawrence, KS, United States

Melanie L. DeVore,     Georgia College and State University, Milledgeville, GA, United States

William A. DiMichele,     NMNH Smithsonian Institution, Washington, DC, United States

Andrew N. Drinnan,     The University of Melbourne, Parkville, VIC, Australia

Dianne Edwards,     Cardiff University, Cardiff, United Kingdom

Kathrin Feldberg,     Ludwig-Maximilians-Universität München, Munich, Germany

Else Marie Friis,     Swedish Museum of Natural History, Stockholm, Sweden

Jean Galtier,     UMR AMAP, CIRAD, Montpellier, France

María A. Gandolfo,     Cornell University, Ithaca, NY, United States

Patricia G. Gensel,     University of North Carolina at Chapel Hill, Chapel Hill, NC, United States

Lisa Grega,     The College of New Jersey, Ewing, NJ, United States

Sébastien Griffon,     AMAP, Université de Montpellier, Montpellier, France

Carsten Gröhn,     Amber Study Group, c/o Geological-Palaeontological Museum of the University of Hamburg, Hamburg, Germany

Carla J. Harper

SNSB-Bavarian State Collection for Palaeontology and Geology, Munich, Germany

University of Kansas, Lawrence, KS, United States

Jochen Heinrichs,     Ludwig-Maximilians-Universität München, Munich, Germany (Deceased)

Robert W. Hook,     The University of Texas at Austin, Austin, TX, United States

Carol L. Hotton

NMNH Smithsonian Institution, Washington, DC, United States

National Institutes of Health, Bethesda, MD, United States

Hans Kerp,     Westfälische Wilhelms-Universität Münster, Münster, Germany

Kathryn Kingsley,     Rutgers University, New Brunswick, NJ, United States

Michael Krings

SNSB-Bavarian State Collection for Palaeontology and Geology, Munich, Germany

Ludwig-Maximilians-Universität München, Munich, Germany

University of Kansas, Lawrence, KS, United States

Evelyn Kustatscher

Ludwig-Maximilians-Universität München, Munich, Germany

Museum of Nature South Tyrol, Bozen/Bolzano, Italy

Cindy V. Looy,     University of California Berkeley, Berkeley, CA, United States

Robert Lücking,     Freie Universität Berlin, Berlin, Germany

Stephen McLoughlin,     Swedish Museum of Natural History, Stockholm, Sweden

Brigitte Meyer-Berthaud,     AMAP, Université de Montpellier, Montpellier, France

April Micci,     Rutgers University, New Brunswick, NJ, United States

Michael A. Millay,     Ohio University Southern, Ironton, OH, United States

Jennifer L. Morris,     Cardiff University, Cardiff, United Kingdom

Patrick Müller,     Amber Study Group, c/o Geological-Palaeontological Museum of the University of Hamburg, Hamburg, Germany

Serge V. Naugolnykh

Geological Institute, Russian Academy of Sciences, Moscow, Russia

Kazan Federal University, Kazan, Russia

Matthew P. Nelsen,     The Field Museum, Chicago, IL, United States

Karl J. Niklas,     Cornell University, Ithaca, NY, United States

Harufumi Nishida,     Chuo University, Tokyo, Japan

Adam Novotny,     The College of New Jersey, Ewing, NJ, United States

Jeffrey M. Osborn,     The College of New Jersey, Ewing, NJ, United States

Kaj R. Pedersen,     University of Aarhus, Aarhus C, Denmark

Kathleen B. Pigg,     Arizona State University, Tempe, AZ, United States

Christian Pott

Swedish Museum of Natural History, Stockholm, Sweden

LWL-Museum für Naturkunde, Münster, Germany

Ledis Regalado,     Ludwig-Maximilians-Universität München, Munich, Germany

Matthew A.M. Renner,     Royal Botanic Gardens and Domain Trust, Sydney, NSW, Australia

Hervé Rey,     AMAP, Université de Montpellier, Montpellier, France

John B. Richardson,     Natural History Museum, London, United Kingdom

Jouko Rikkinen,     Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland

Ronny Rößler

Museum für Naturkunde Chemnitz, Chemnitz, Germany

TU Bergakademie Freiberg, Freiberg, Germany

Gar W. Rothwell

Ohio University, Athens, OH, United States

Oregon State University, Corvallis, OR, United States

Nicholas P. Rowe,     AMAP, Université de Montpellier, Montpellier, France

Adolfina Savoretti,     Instituto de Botanica Darwinion, San Isidro and CONICET, Argentina

Alfons Schäfer-Verwimp,     Herdwangen-Schönach, Germany

Alexander R. Schmidt,     Geoscience Centre, University of Göttingen, Göttingen, Germany

Harald Schneider

Center for Integrative Conservation, Yunnan, China

Natural History Museum, London, United Kingdom

Andrew B. Schwendemann,     Lander University, Greenwood, SC, United States

Judith Skog,     George Mason University, Fairfax, VA, United States

Christopher Stabile,     The College of New Jersey, Ewing, NJ, United States

Ruth A. Stockey,     Oregon State University, Corvallis, OR, United States

Paul K. Strother,     Weston Observatory of Boston College, Weston, MA, United States

Wilson A. Taylor,     University of Wisconsin Eau Claire, Eau Claire, WI, United States

Edith L. Taylor,     University of Kansas, Lawrence, KS, United States

Mackenzie L. Taylor,     Creighton University, Omaha, NE, United States

Alexandru M.F. Tomescu,     Humboldt State University, Arcata, California, United States

Satish K. Verma

Rutgers University, New Brunswick, NJ, United States

Banaras Hindu University, Varanasi, India

Christopher Walker

University of Western Australia, Crawley, Australia

Royal Botanic Garden Edinburgh, Edinburgh, WA, United Kingdom

James F. White Jr. ,     Rutgers University, New Brunswick, NJ, United States

María del C. Zamaloa,     Universidad de Buenos Aires, Buenos Aires, Argentina

About the Editors

Michael Krings is the curator for fossil plants at the Bavarian State Collection for Palaeontology and Geology (SNSB-BSPG) in Munich, Germany, and a professor of plant paleobiology at the Ludwig-Maximilians-University Munich. He also holds an affiliate faculty position in the Department of Ecology and Evolutionary Biology at the University of Kansas. He received his PhD in botany from the University of Münster, Germany, and was an Alexander von Humboldt-Foundation postdoctoral fellow at the University of Kansas. He is author of the paleobotany textbook Paleobotany. The Biology and Evolution of Fossil Plants (T.N. Taylor, E.L. Taylor & M. Krings, 2009) and the paleomycology book Fossil Fungi (T.N. Taylor, M. Krings & E.L. Taylor, 2015). His research interests include Carboniferous, Permian, and Triassic seed plants and the biology and ecology of microorganisms in ancient ecosystems.

Néstor Rubén Cúneo is the Museo Paleontológico Egidio Feruglio director and principal researcher of the National Research Council, Trelew, Chubut, Argentina. He also was an invited researcher for several years at the U.S. Antarctic Program and invited professor at the University of Patagonia. He received his PhD in geology from the Universidad de Buenos Aires, Argentina, and had a postdoctoral position at Ohio State University under the guidance of Thomas N. Taylor. His research interests center on Gondwanan paleofloras, Patagonian Jurassic floras, and, more recently, Cretaceous ecosystems.

Carla J. Harper is a National Science Foundation (NSF) Zygomycetes Genealogy of Life (ZyGoLife)–the Conundrum of Kingdom Fungi postdoctoral research fellow at the Biodiversity Institute and Natural History Museum at the University of Kansas. She was an Alexander von Humboldt-Foundation postdoctoral research fellow (2015–17) at the Bavarian State Collection for Palaeontology and Geology (SNSB-BSPG) and Ludwig-Maximilians-University Munich, Germany, and currently holds a research associate position at SNSB-BSPG. She received her PhD in ecology and evolutionary biology from the University of Kansas. Her research interests include the biology and ecology of microorganisms and biotas in Permian–Jurassic ecosystems of Antarctica and late Paleozoic of Europe, symbiotic systems through time, as well as the biology, geochemistry, and evolution of fossil microbes.

Gar Rothwell is the Edwin and Ruth Kennedy Distinguished Professor of Environmental and Plant Biology, Emeritus, Ohio University, and Courtesy Professor of Botany and Plant Pathology, Oregon State University. He is past-president of the International Organisation of Palaeobotany, author of the paleobotany textbook Paleobotany and the Evolution of Plants (W.N. Stewart & G.W. Rothwell, 1993), and editor of six previous volumes of studies in plant paleontology. His research focuses on the role of development in evolution and on the patterns of organismal evolution and phylogeny among land plants, particularly lycophytes, equisetophytes, ferns, and seed plants.

Biography

Thomas N. Taylor (1937–2016)

Foreword

As natural history has progressively given way to newer approaches and avenues of inquiry in the fields of biology and geology during the past 60  years, the field of paleobotany has grown as a vibrant source of innovative science. To a certain extent, this resulted from the irreplaceable nature of data from the fossil record. Of perhaps greater importance, this period has witnessed an unprecedented stream of new paleobiological approaches and techniques that have energized collaborative efforts with a wide array of other disciplines. Together, these innovations have dramatically transformed traditional paleobotanical studies, fostered creative fusions of disciplines, and produced whole new avenues of scientific inquiry.

At the forefront of these transformative innovations are the studies of Thomas N. (Tom) Taylor, whose scholarship, insightful contributions, and scientific impact this compendium celebrates. Of perhaps even greater significance than the voluminous research personally developed and conducted by Tom Taylor are the colleagues he has influenced and students he has inspired to extend our understanding of the evolution of life and to chart the forthcoming directions of paleobiological research for the 21st century. Moreover, Tom was transformative in bringing together ideas and colleagues from different disciplines to approach paleobotany. He also had foresight in many areas; while he certainly was not the first to explore the topics of paleomycology or Antarctic paleobotany, he brought those areas to the forefront because he knew at the time that they had tremendous potential, and he brought people together beyond the traditional boundaries.

We envisage the present volume as a companion to Tom's most recent Paleobotany and Fossil Fungi books and to exemplify the vast body of accumulated research that is derived from Tom's influence. The included reports define and summarize the breadth of scholarship that has resulted from Tom's scientific contributions to organismal and evolutionary biology, to the early evolution of land plants, to our understanding of fossil fungi and other microorganisms, to systematics and phylogeny of plants and fungi, to biostratigraphy, to the evolution of organismal interactions, and to palynology and ultrastructure.

The volume is divided into five sections to emphasize the most promising avenues of investigation that Tom has opened and to highlight the fruitful contributions that his influence has engendered.

I. Early land plants: innovations and adaptations—Unanswered fundamental questions about the origin and early evolution of land plants underlie Tom Taylor's overall scientific interests. From his earliest studies on the evolution of primitive seeds, through his contributions to the evolution of spore and pollen ultrastructure, to his pioneering work on the paleontological progression of plant/microorganism interactions, his contributions have redefined the focus of early land plant studies. Tom's emphasis on evolutionary changes in structure/ultrastructure of Paleozoic spores is extended by Strother and W.A. Taylor, who use early Paleozoic evolution of embryophyte spores to emphasize life cycle changes leading to the origin of the sporophyte phase of the plant life cycle. The roles of key evolutionary innovations in tissue development such as the vascular cambium and in the architecture of the sporophyte and gametophyte plant bodies were major emphases of Tom's research. Advancements are extended by Gensel's focus on the origin of wood in Early Devonian plants, the architectural analysis of a Middle Devonian fern-like tree by Dambreville et al., and the characterization of a plant from a Lower Devonian Lagerstätte in the Welch Borderlands by Morris et al. As emphasized by Tom's focus on early land plant evolution, studies of these types rely heavily on our understanding of basic homologies, which is the focus of the final contribution in this section by Crepet and Niklas.

II. Late Paleozoic and Mesozoic plants and floras—When Tom started to work in paleobotany, it was not early land plants or microbial interactions he laid his eyes on, but rather the vast record of plant remains from the late Paleozoic and Mesozoic of North America and Europe that were readily accessible in great numbers, especially in the form of coal balls providing detailed insights into the internal organization and biology of Carboniferous coal swamp plants. He studied various ferns and sphenophytes but then found the reproductive biology of late Paleozoic seed plants fascinating and worked on Carboniferous seeds and pollen organs. The reports in this section emphasize Tom's interest in the diversity and biology of vascular cryptogams and seed plants in late Paleozoic and Mesozoic ecosystems. DiMichele et al. describe an Early Permian flora from Clay County, Texas, while Naugolnykh discusses the astonishingly diverse early fossil record of (putative) ginkgophytes in Angaraland. The third contribution in this section, by Nishida et al., discusses the value of permineralized glossopteridalean plant remains, and the fourth, by McLoughlin et al., harks back to Tom's interest in seed structure by describing a new glossopteridalean seed from Australia and naming it in honor of Tom. The last two reports in this section focus on plants that have remained mysteries since their first discovery and description. Axsmith et al. resolve the systematic affinities and reproductive biology of Pekinopteris based on fertile material from the North American Triassic, while Galtier et al. provide evidence suggesting that the permineralized stem Knorripteris from the Triassic of central Europe belongs to the ferns.

III. Paleobiogeography, biology, and phylogenetic relationships of plants—One of Tom's greatest contributions to the field was the integration of ideas and people from different fields of science to help answer paleobotanical questions and explain paleobotanical discoveries. Therefore, it comes as no surprise that one of the sections in this book brings together interdisciplinary studies with a focus on paleobotany concerning a wide range of different plant groups and their distribution in time and space. The section is headed by a report by Heinrichs et al. on the fossil record of liverworts in amber and the value of these fossils in phylogenetic and molecular clock analyses. Aerodynamics of fossil pollen (by Grega et al.) then shifts the focus to the connection between reproductive biology and biomechanics by assessing the aerodynamic effects of certain pollen characters through electron microscopy, mathematical modeling, and experiments using scaled-up physical models. Rothwell et al. summarize and elaborate on the morphological evolution, paleogeographic diversification, and environmental distribution of marattialean ferns through time based on a new genus, Escapia, from the Early Cretaceous Apple Bay flora of Canada. The paleogeographic distribution of certain ferns through time is also the focus of the next report (by De Benedetti et al.) that surveys the fossil record of Azolla in Patagonia. An entirely different question, raised by Tomescu et al., is connected thematically with the first paper of the section by addressing the overall scarcity of bryophytes in the fossil record. Finally, Friis et al. describe Early Cretaceous seeds of North America with affinities to Austrobaileyales and Nymphaeales that provide new evidence for extensive extinction near the base of the angiosperm tree.

IV. Fossil microorganisms—Examination, description, evaluation, and biological characterization of microorganisms, especially fungi and fungus-like organisms and their various levels of biological interactions with plants, animals, and other microorganisms from the Lower Devonian Rhynie chert and other sources of histological preservation, were among Tom's favorite topics during the later years of his career. Microorganisms are key drivers in past and present-day ecosystems, and other organisms would not exist in the way they do without microorganisms. As a result, understanding the evolution of fossil plants for Tom required detailed attention to the microorganisms associated with the plants. Noteworthy among Tom's many contributions on Rhynie chert microorganisms, which he first studied with Winifred Remy of Münster, Germany, are the accounts on the endomycorrhizas in sporophytes and gametophytes of the land plant Aglaophyton majus. Because the Rhynie chert was one of Tom's greatest scientific affections, it is not surprising that one of the contributions in this section (by Krings et al.) presents new findings from the Rhynie chert and the nearby, coeval Windyfield chert, while another, by Brundrett et al., uses the fossil record of arbuscular mycorrhizas to elucidate the history of this successful partnership between fungi and plants. The next contribution, by Walker et al., looks at the characteristics of present-day mycorrhizas and mycorrhizal fungi, and the chances of recognizing these characteristics in fossils. Moreover, Tom's 1997 report on the Rhynie chert lichen Winfrenatia reticulata represents a benchmark contribution in the field of lichen evolution. The contribution by Lücking and Nelson in this section takes the discussion of the origin and early evolution of lichen symbioses yet a step further. The two remaining contributions in this section are great examples of how cooperation between paleobiologists and neomicrobiologists has produced intellectual cross-fertilization resulting in an expanded knowledge base about the evolutionary history of eukaryotes (by White et al.) and Paleogene forest structure (by Rikkinen and Schmidt).

V. Antarctic paleobotany—The diversity of fossil remains from Antarctica and the excellence of preservation of many of these fossils at some point caught Tom Taylor's interest and, in the course of several expeditions to the ice that he and his wife Edie planned and conducted, Antarctica and Antarctic paleobotany developed into one of Tom's great scientific love affairs. Permian and Triassic chert (permineralized peat) deposits from Antarctica represent a particularly interesting setting for the study of plants and fungi because they preserve remains of distinctive high-latitude ecosystems with polar light regimens that underwent a profound climatic change from icehouse to greenhouse conditions. Two of the conributions in this section focus on plants from these cherts that were also studied by Tom. The first report assesses developmental biology in glossopteridalean roots named Vertebraria (by Decombeix et al.). Two additional reports in this section deal with periods of geological time that were not the primary focus of Tom's work but that also have yielded numerous and valuable fossils from Antarctica. Bomfleur et al. provide evidence of the function of polar regions of the Mesozoic to Paleogene greenhouse world as refugia for relict plant groups, including lycopsids, various seed ferns, Bennettitales, and cheirolepid conifers, while Cantrill surveys the Cretaceous to Paleogene vegetation transition in Antarctica. Finally, Schwendemann investigates leaf venation density and calculated physiological characteristics of fossil leaves from the Permian of Gondwana.

Paleobotany today is a highly integrated interdisciplinary endeavor. A paleobotanist 50  years ago needed only geology and plant biology to study fossil plants. However, we now realize that research areas such as geochemistry, molecular biology, microbiology, biomechanics, phylogeny, etc. are transforming our approaches to, and perception of, the analysis of fossil plants and ecosystems, and some of these once-so-remote research areas are becoming increasingly important for, and integral parts of, paleobotanical research. The present volume exemplifies the potential of utilizing interdisciplinary research in the advancement of paleobiological inquiry. As such, the volume represents a blueprint for paleobotany of the 21st century.

Acknowledgments

We are deeply indebted to all who, by contributing their research, have filled this volume with life and provided a worthy frame for the commemoration of Tom's life and legacy. We thank all chapter referees for their help and our colleagues, families, and friends for their unconditional support and loyalty.

S.R. Ash • B.A. Atkinson • B.J. Axsmith • D.J. Batten • J.-F. Barczi • F. Baron • J. Bechteler • C.B. Beck • M. Bergen • H.K. Bergeman • C.M. Berry • A.C. Bippus • B. Bomfleur • C.K. Boyce • P. Blomenkemper • L. Brindisi • M.C. Brundrett • D.J. Cantrill • D.S. Chaney • X. Chang • X. Chen • M.E. Collinson • P.R. Crane • D.J. Crawford • W.L. Crepet • C.P. Daghlian • A. Dambreville • V. Daviero-Gomez • J.R. Davis • F. De Benedetti • A.-L. Decombeix • T. Delevoryas • M.L. DeVore • J. Dighton • W.A. DiMichele • N. Dotzler • A.N. Drinnan • J.G. Duckett • D. Edwards • I.H. Escapa • K. Feldberg • M.J. Foster • E.-M. Friis • J. Galtier • M.A. Gandolfo • J. García Massini • P.G. Gensel • P. Gerrienne • L. Grega • S. Griffon • C. Gröhn • H. Hass • B.C. Harper • D.B. Harper • C.H. Haufler • D.L. Hawksworth • J. Heinrichs • T.J. Hieger • C.C. Hofmann • R.W. Hook • C.L. Hotton • M.S. Ignatov • B. Ilsemann • J.L. Isbell • D. Johanning • J.R. Keeler • H. Kerp • K. Kingsley • P.C. Klahs • A.H. Knoll • E. Kustatscher • A.B. Leslie • C.V. Looy • R. Lücking • H. Martin • T. Masselter • S. McLoughlin • B. Meyer-Berthaud • A. Micci • M.A. Millay • J. Morris • P. Müller • S. Naugolnykh • M.P. Nelson • K. Niklas • H. Nishida • A. Novotny • J.M. Osborn • K.R. Pedersen • K.B. Pigg • M.S. Pole • C. Pott • C. Prestianni • R. Prevec • L. Regalado • M. Reich • M.I. Remshardt • M.A.M. Renner • H. Rey • J.B. Richardson • J. Rikkinen • R. Rößler • N.P. Rowe • P.E. Ryberg • M.A. Savoretti • A. Schäfer-Verwimp • A.R. Schmidt • H. Schneider • A.B. Schwendemann • J. Skog • R. Sonnhof • S. Sónyi • T. Speck • C. Stabile • W.E. Stein • D.W. Stevenson • R.A. Stockey • P.K. Strother • Tassel Loafers • M.L. Taylor • W.A. Taylor • A.M.F. Tomescu • N.M. Varela-Gastelum • S.K. Verma • H. Vöcks • C. Walker • S.A. Walker • C.H. Wellman • J.F. White Jr. • P. Wilf • E. Wimmer • M. del C. Zamaloa • If we missed or accidently overlooked anyone, we sincerely apologize.

There are several people who were especially close to Tom. We would like to extend very special appreciation and thank you to:

Edith L. Taylor is an esteemed colleague and friend and Tom’s wife. Edie is a prolific and renowned paleobotanist and has written more than 200 publications and nine books or edited volumes. Together with Tom, the Taylors brought paleobotany to the University of Kansas (KU) in 1995 from The Ohio State University and established one of the largest paleobotanical collections in the United States. She was instrumental in securing the continuous National Science Foundation (NSF) Polar Program grants to support the Taylors' legacy in Antarctic fieldwork and research on fossil plants in Antarctica. Due to their continuous perseverance, KU today is home to the NSF National Repository of Antarctic Plant Fossils. Together, Tom and Edie have had a lifetime of traveling around the world conducting paleobotany research and bringing together many international collaborators, colleagues, postdoctorals, and graduate students, many of whom have contributed to this volume. Tom and Edie had unconditional support for one another through life and career endeavors; the Taylors had a profoundly positive and transformative impact on the science of paleobotany. Thank you, Edie, for being a role model as a person, scientist, and friend to us all and for your support in this project. With all our love and sincerest gratitude.

Jeannie M. Houts began working at the KU Department of Ecology and Evolutionary Biology in the administrative office as a graduate coordinator, while Tom was the department chair. Tom took notice of Jeannie's superior organizational skills and meticulous eye for detail and hired her as his executive administrative assistant when he was appointed to the U.S. National Science Board in 2006. Since that time, Jeannie has been invaluable not only to Tom and Edie but also to the success and productivity of the paleobotany program at KU. She helped the Taylors with all administrative duties and coordination of multiple textbooks (including the tedious task of adding several thousand references), manuscripts, all travel-related items (domestic and international), the laborious task of coordinating numerous field expeditions to Antarctica, and much more. Tom had a saying that Jeannie knew where all the bodies were buried because she had a hand in virtually every part of the paleobotany lab. She has been behind the scenes for longer than 12  years, allowing the program to run smoothly and grow, and set the standard for going above and beyond, as well as putting a system in place for the program to thrive for years to come. Jeannie was instrumental in the coordination of many of the visits and success of collaborators working at the KU paleobotany lab, many of whom are represented in this book. We are all indebted to you, Jeannie. Thank you for all that you have done.

Rudolph Serbet has been an integral part of the Division of Paleobotany, Biodiversity Institute, at KU since he started working with the Taylors as collections manager in 1997. When the Taylors moved the James M. Schopf collection from the Byrd Polar Institute, Ohio State University, to KU, he had the arduous task of physically moving and organizing the entire collection. As a result, Rudy set forth a meticulous system that has kept the KU collections going strong and in keeping with the vision that the collections should continuously grow and support research. Rudy created a database of the collections and provided the data online long before any other large collection in the United States had done so. Tom was a strong advocate for always providing a home for orphaned paleobotanical collections and, over the years, Rudy helped to integrate many such collections at KU. Rudy was instrumental in completing one of the Taylor's longstanding missions of further expanding the housing of the KU collections with a new state-of-the-art annex facility on West Campus at KU. Rudy manages the largest collection of Antarctic paleobotanical specimens in the world. Antarctica was one of Tom and Edie's true passions, and Rudy was fortunate enough to go to the ice with Tom during his last field season in 2010–2011. Since then, Rudy has maintained this tradition of Antarctic collection and exploration and has led four subsequent expeditions. In addition, to his services as a collections manager, he still finds time with various outreach and museum activities to vigorously promote paleobotany to the public each year. Rudy has helped immensely in multiple projects and areas of paleobotany, including directly helping many of the contributors and projects in this book.

Taking an edited volume from concept phase to production is a tremendous challenge and would not be possible without the dedication of many people. We acknowledge the assistance provided by Academic Press and Elsevier for support of this project from the beginning. We are especially thankful to Kristi Gomez, who helped us immensely in the early phases of this project, and to the helpful insight and comments from the anonymous reviewers of our book proposal. A special acknowledgment and emphatic gratitude go to Pat Gonzales, editorial project manager. Pat has, again, set the gold standard for book project management and consistently went above and beyond for all contributors to this volume. Pat, thank you for your patience and understanding, attention to detail, answering every email promptly and our questions with poise, as well as your guidance and instrumental help throughout this project. We could not have completed this volume without you.

Section I

Early Land Plants: Innovations and Adaptations

Outline

Chapter 1. The Evolutionary Origin of the Plant Spore in Relation to the Antithetic Origin of the Plant Sporophyte

Chapter 2. Early Devonian Woody Plants and Implications for the Early Evolution of Vascular Cambia

Chapter 3. Using Architecture Modeling of the Devonian Tree Pseudosporochnus to Compute Its Biomass

Chapter 4. The Advantages and Frustrations of a Plant Lagerstätte as Illustrated by a New Taxon From the Lower Devonian of the Welsh Borderland, UK

Chapter 5. Early Tracheophyte Phylogeny: A Preliminary Assessment of Homologies

Chapter 1

The Evolutionary Origin of the Plant Spore in Relation to the Antithetic Origin of the Plant Sporophyte

Paul K. Strother¹, and Wilson A. Taylor²     ¹Weston Observatory of Boston College, Weston, MA, United States     ²University of Wisconsin Eau Claire, Eau Claire, WI, United States

Abstract

The antithetic (interpolational) hypothesis for the origin of the plant sporophyte from algal ancestors calls for the evolution of the embryophytic spore in advance of the vegetative sporophyte. Here we view the fossil record of cryptospores from lower Paleozoic strata in light of this spores before sporophytes paradigm. Cryptospores show marked changes between pre-Darriwilian and post-Darriwilian assemblages. These include shifts from smaller to larger spore diameters, topological changes from irregular to isometric spore-body attachment configurations, and the de novo origin of homogeneous sporoderm. These changes in spore morphology and topology appear to reflect the canalization of meiosis in the sporocyte, as karyokinesis and cytokinesis became tightly coupled and meiosis resulted in only four (meio)spores. Indirect evidence of embryophytic sporangia is first found in Darriwilian rocks in the form of homogeneous sporoderm, which is considered to be tapetal in origin. Thus, the fossil record appears to support the progressive acquisition of evolving sporophyte characters with respect to spore formation. If embryophytic sporogenesis first evolved during the Darriwilian, the antithetic hypothesis would predict that the full suite of vegetative characters that defined the first sporophyte must have evolved later. This scenario is consistent with the Homerian origin of land plants as seen in the (mega)fossil record, but it implies that the origin of lands plants, per se, was not a singularity in geologic time but rather required a long period of adaptive selection in subaerial habitats throughout the early Paleozoic.

Keywords

Antithetic hypothesis; Cryptospores; Origin of plants; Sporogenesis; Successive meiosis

… the fossil record has so far been mute regarding the algae–land plant transition.

Graham (1996)

1. Introduction

The origin of land plants from their algal ancestors involved an evolutionary transition from aquatic algae of relatively simple morphology to subaerial plants whose complex multicellular morphology was expressed, at least in part, through the development of a diploid embryo. For some authors, this transition represents one of a handful of fundamental evolutionary transitions in biology (Margulis and Schwartz, 1982; Smith and Szathmáry, 1995; Knoll, 2011); for others, the origin of embryophytes is represented as a bifurcation in a phylogeny (e.g., Kenrick and Crane, 1997a). But in all cases, the evolutionary origin of land plants most likely required the serial acquisition of a suite of novel characters, including the regulatory genome required for their assembly into a true land plant. The scarcity of any plant (mega)fossil record before the late Silurian traditionally led to the use of trilete spores as a proxy for the embryophytes (Chaloner, 1967), because trilete spores with sporopollenin-containing walls are not found in any green algal group, extant or fossil. The general acceptance that fossilized tetrahedral tetrads of tightly bound spores, such as Tetrahedraletes (Strother and Traverse, 1979) or Cryptotetras (Strother et al., 2015), also represent a good embryophyte proxy (Wellman and Gray, 2000; Edwards et al., 2014) has pushed the putative age of land plant origins to the Darriwilian (Strother et al., 1996, 2015). It is important to note, however, that with respect to the fossil record of the embryophyte plant body, we have no evidence of bone fide embryophytes earlier than the reported Cooksonia axis from the Homerian of Ireland (Edwards et al., 1983).

Bower (1908) developed the antithetic, or interpolational, hypothesis of the origin of the plant sporophyte as an explanation of how the land plants evolved from aquatic algal ancestors. The antithetic hypothesis of sporophyte origins has historically been contrasted with the homologous theory, or sporophyte origins from an isomorphic alternation of generations. The homologous theory remains of interest with regard to early vascular plants that display nearly isomorphic alternation of generations (Kenrick, 1994; Gerrienne and Gonez, 2011). But recent reviews (Blackwell, 2003; Haig, 2015) all favor Bower's hypothesis, along with the supposition that the embryophytes evolved from a charophyte with a haplobiontic life cycle, in which individual zygotes were the only diploid (2n) cells. Bower's key insights were that the embryophyte spore must have evolved first, with vegetative (somatic) sporophyte tissues evolving later in time, and that the entire sporophyte phase evolved in response to natural selection in subaerial settings.

The land plant spore, then, represents a fundamental adaptation to the subaerial habitat in the application of heteropolymers to form a resistant wall surrounding the spore protoplast (Graham, 1996). That same feature, the evolution of a sporopollenin-containing wall, resulted in resistant walled spores, which, in turn, allowed for a fossil record of spore evolution in subaerial settings. In cases of exceptional preservation, both algal and plant vegetative tissues can be preserved as organic compressions or as petrifactions, but these are quite rare in comparison to the fossil record of dispersed spores, acting as organic sedimentary particles that are readily incorporated into the sedimentary rock record (Traverse, 1994). In this report, we review the palynological record of dispersed spores and spore-like microfossils leading up to the origin of the first plant sporophytes preserved in the fossil record. In this way, we hope to document evolutionary changes in spores that occurred during a time of transition from algal ancestors to bone fide embryophytes (land plants). But, more importantly, we hope to tie the morphological changes observed in the spore record into a larger, more general picture of the evolution of the plant sporophyte.

2. The Antithetic Theory as a Scaffold for Interpreting the Fossil Record of the Algal–Plant Transition

The antithetic theory of Bower (1908, 1935) was presaged in the work of Čelakovsky (1874), who recognized that the sporophyte generation in plants was functionally and evolutionary distinct from the gametophyte—hence, antithetic to the gametophytic generation (Qiu et al., 2012). Bower postulated that the ancestral sporophyte derived from zygotes that first delayed meiosis and divided mitotically to produce a multicellular set of (diploid) sporocytes, or sporogenous cells, each of which initially retained the ability to undergo meiosis to produce spores. Subsequently, some of these sporogenous cells underwent sterilization to become vegetative and, under the selective pressure associated with a subaerial existence, gradually evolved into the tissues and organs of a sporophyte plant body. The consequence of this idea is that spores (and sporangia) literally preceded sporophytes in evolutionary time, and that … each fertile tract is a residuum left by advancing sterilization (Bower, 1908, p. 248). Bower also suggested that the initial function of the earliest somatic (vegetative) cells would have been to both protect and nourish the sporogenous cells. Thus, the sporophyte would have evolved de novo through the ontogenetic interpolation of the vegetative plant body into the life cycle before meiotic spore production (sporogenesis).

In contrast to the antithetic theory, the homologous theory, which posits an ancestral alga with isomorphic (or nearly so) alternation of free-living generations, is now considered important only in the context of the origin of the polysporangiates, not the embryophytes per se (Kenrick, 1994). The homologous theory, based, in part, on the isomorphic alternation of generations seen in some macroscopic marine algae such as Dictyota and Ulva, appears to be somewhat of an historical footnote. It played heavily in the transmigration hypothesis of Church (1919), who considered the aquatic-to-terrestrial transmigration of plants to be evolutionarily parallel to that of animals. As the highest type of marine animal (the vertebrate fish) led on to the higher animal organisms of the land, so land-flora has been undoubtedly produced from the highest plant-organism attained in the sea (Church, 1919, p. 9).

However, the fish–tetrapod and charophyte–embryophyte transitions are not evolutionarily equivalent events, despite the fact that they both produced higher organisms that were capable of living on land. In the fish–tetrapod transition, morphologically differentiated species possessed exaptations that were modified later and assisted in survival on land (Janvier, 2010). In contrast, during the algal–plant transition, undifferentiated streptophyte algal species evolved complex multicellularity de novo as a solution to living in a subaerial setting. For animals, the evolution of complex multicellularity from unicellular protist ancestors probably took place entirely within the aquatic realm (Nielsen, 2008). But in plant evolution, the origin of complex multicellularity (and developmental patterning) took place during the transition itself. So the study of the origins of animal terrestrialization shows little or no parallel to that of the streptophyte terrestrialization. From a paleontological perspective, this is the legacy of Bower's theory—while the origins of animals are shrouded in the deep time of the Precambrian, paleobotanists have the opportunity to sample the fossil record as a direct and tangible history of the evolution of complex multicellularity in the streptophyte lineage leading to the embryophytes. Conceptually, then, it should be possible to map out Bower's interpolational scenario as a series of added character states and then compare that series with the tangible fossil record of cryptospores and phytodebris (sensu Gensel et al., 1990). This scaffolding technique allows for the interpretation of the fossil record as a proxy of sporophyte evolution.

That tangible history begins with the origin of resistant walled spores from ancestral streptophyte algae. Intriguingly, the Cambrian cryptospore record has preserved a diverse range of spore wall ultrastructures and spore topologies, many of which may be interpreted as evolutionary responses to adaptations to subaerial lifestyles.

The initial transformation, from charophytic, flagellated zoöspores to resistant walled meiospores, has been tied to a sporopollenin-transfer hypothesis (SPTH) (Graham, 1984, 1993, 1996; Hemsley, 1994). Sporopollenin, or sporopollenin-like substances, are known to occur in the zygote walls of extant Coleochaete (Delwiche et al., 1989). If the deposition of sporopollenin were to be developmentally delayed until after meiosis, this would effectively transfer an overwintering function of the zygote to the meiospores. Although this idea may seem speculative from the standpoint of interpreting the fossil record, there is direct evidence of heterochrony, with respect to the deposition of sporopollenin, during the evolution of spore development in extant bryophytes (Brown and Lemmon, 2011). In essence, both the antithetic theory and the SPTH are well supported by the recognition of heterochrony in bryophyte sporogenesis (Brown and Lemmon, 2011).

The antithetic theory, then, requires a sequence of added evolutionary novelties, which could occur de novo, be co-opted from a prior gametophytic genome, or some combination of both. To the extent that the sequence itself can be constrained, the order in which sporophytic characters evolved, regardless of their ultimate source, would present themselves in the same order of appearance in the fossil record. An attempt to construct such a sequence is presented in Table 1.1.

For each proposed step in the evolutionary acquisition of sporophyte characters, as an extension of Bower's hypothesis, the corresponding biological equivalent and potential fossil structures are presented.

Thus, the first evidence of a transitional sequence might be seen as spore wall formation in streptophytic algae but one in which sporopollenin was retained in the wall of the resting zygote. The biological manifestation of this initial stage might be seen in the fossil record of resistant walls that surrounded either meiospores or multicellular sporogenous masses. And, indeed, the retention of a membrane surrounding fossil cryptospore dyads and tetrads has been cited as possible retention of either a resistant zygote wall (Taylor and Strother, 2008, 2009) or the resistant wall of a spore mother cell (SMC) (Strother and Traverse, 1979; Taylor and Strother, 2008). Taylor and Strother (2009) refer to preserved resistant walls that surround the earliest cryptospores as synoecosporal walls, a term reflecting the enclosed and endosporic nature of the dispersed, late Cambrian cryptospore Agamachates.

After sporopollenin transfer, theoretically there should be a true spore record of dispersed, resistant walled spores, and, in fact, there is such a record—the record of cryptospores. Bower did not anticipate the occurrence of spore dyads and tetrads but, as discussed next, aspects of cryptospore topology provide clues that support their inclusion in the interpolational hypothesis. In addition, cryptospores provide an important record of evolutionary change during the course of sporophyte evolution. For example, dispersed cryptospores provide our only evidence of sporocyte duplication (Strother et al., 2017), Bower's next stage in which he proposed mitotic copies of fertilized zygotes as a means to increase the efficacy of rare fertilization events (Haig, 2008, 2015).

Cryptospores from Cambrian and lower Ordovician strata show morphologies and topologies that appear more relevant to evolving streptophyte algal lineages than they do to living embryophytic spores. Ultimately, these differences can be traced to variations in ploidy levels that persist throughout their lifecycles as seen in charophytic algae today. Haig (2010) has pointed out that many charophyte lifecycles do not show a clear alternation between diploid and haploid phases. His observations, coupled with the documentation of DNA endoreduplication in Coleochaete (Hopkins and McBride, 1976), support the arguments of Taylor and Strother (2009) and Strother (2016), who have shown that cryptospore topologies of Cambrian taxa are consistent with spore-producing reduction divisions in which karyokinesis and cytokinesis are temporally decoupled. The canalization of meiosis, resulting in what is essentially a modern form of bryophytic sporogenesis, is seen clearly in the fossil record with the arrival of Tetrahedraletes grayae and Cryptotetras in the Darriwilian of Saudi Arabia (Strother et al., 2015). In terms of the interpolational hypothesis, the pre-Darriwilian fossil record represents a time during which the plant spore itself evolved from streptophyte algal ancestors. This can also be viewed in terms of the SPTH as a time during which the plant spore wall evolved.

The fossil record does not provide very good direct evidence of Bower's next phase, which is the existence of a sporangium, or at least a sporocyte mass, which was surrounded by vegetative tissue. The homogeneous wall type seen in Cryptotetras erugata is consistent with a spore wall that was produced by tapetal secretion (Taylor et al., 2017). If this is true, it means that the earliest plant-like spores were produced in unilocular sporangia. Wellman et al. (2003) identified cryptospore masses from the Katian of Oman that were partially covered by acellular sheets, which they inferred to represent embryophytic sporangia. Intriguingly, some of these Late Ordovician spore masses were composed of dyads whose wall ultrastructure consisted of parallel laminae, this representing a second ultrastructural wall type found in association with Ordovician embryophytic sporangia.

Table 1.1

The next stages in Bower's hypothesis have not really been explored in a paleobotanical context. The expectation is, of course, that the fossil record should contain a record of plant structures or tissues that evolved serially in association with the evolution of the sporophyte. This would necessarily have involved the evolution of vegetative tissues, such as mesophyll and cortical tissues, whose cells would have possessed cellulosic walls, which may not have been generally susceptible to preservation in the fossil record. There are some possible exceptions to this generalization, however, which include water-conducting cells, suberin-impregnated cell walls (such as endodermis), and impregnated (or coated) epidermal cells or cuticles. So, logically, we should look to later Ordovician and Silurian deposits to find this kind of plant-like cellular debris. This section of the column does contain such remains, but they have, for the most part, been thought of as belonging to the Nematophytales, and, with the caveat that the nematophytes are generally thought of as having a fungal (or lichen) affinity, their relevance to the origin of land plants, or embryophytes in general, has remained largely unexplored. Nevertheless, the recovery of any plant-like tissues in the Darriwilian–Wenlock interval could be viewed in terms of the Bower model and, if so, potentially help to outline both the sequence and pathway taken during the evolution of the interpolational phases of sporophyte origins.

3. Early Cryptospore Morphology

3.1. Sporogenesis and Cryptospore Morphology

Miospore formation in spore-producing embryophytes has been well characterized in extant cryptogams. This includes, in addition to miospores that are shed as haploid spores (monads), spore tetrads in some hornworts and liverworts (Renzaglia et al., 2014) and, more recently, spore dyads in Haplomitrium (Renzaglia et al., 2015). The normal occurrence of meiosis in bryophytes and vascular cryptogams results in four more-or-less morphologically identical miospores, whose derivation from a diploid sporocyte is often retained in the morphological details of the proximal face—especially, the trilete mark. Fossilized cryptospores, as permanent dyads or tetrads, typically do not reveal such haptotypic features, but their derivation from a diploid sporocyte is revealed, in tetrahedral tetrads at least, by their common morphology and tetrahedral arrangement. The individual miospores in a cryptospore tetrad may be subtriangular in outline, as in Tetrahedraletes, or they may be more rounded, as is typically seen in Rimosotetras, which consist of more loosely arranged spores. But, in most cases, a combination of spore shape and position in a tetrad corroborates their meiotic derivation.

As we discuss later, however, cryptospores from pre-Darriwilian strata do not generally show such morphological uniformity. Cambrian cryptospores do not occur exclusively in sets of four, so the normal relation between a single diploid sporocyte and four meiotically derived haploid spores as seen in all land plants today does not pertain to these more ancient forms. Neither do all Cambrian cryptospores possess rigid, uniform spore walls—many have undulating and somewhat irregularly shaped outlines. Fig. 1.1 represents an attempt to show some of these general differences in a graphic way by plotting images of key cryptospore taxa against a lower Paleozoic timeline. The images are plotted roughly in their correct stratigraphic position and are all to the same scale. What is immediately apparent is the general size difference between pre- and post-Darriwilian forms; as a general rule, Cambrian cryptospores are smaller. But the more irregular shapes and clustered habits of the pre-Darriwilian forms are also apparent.

Because of such apparent differences between pre- and post-Darriwilian cryptospores, these more ancient forms have not been included in prior reviews of early land plant spores (e.g., Edwards et al., 2014), as they have been perceived as being of algal rather than plant origin (Wellman and Gray, 2000; Edwards and Wellman, 2001; Wellman, 2003). Strother (2016) has argued more recently that many of the morphological features seen in Cambrian cryptospores can be inferred to have evolved in response to natural selection in subaerial settings and that they are likely the remains of streptophytic, rather than chlorophytic, algae. These fossils may not be the remains of the direct ancestors of the embryophytes, but they probably do represent the remains of an evolving streptophyte algal complex that eventually did give rise to the earliest embryophytes.

To process why pre-Darriwilian cryptospores are so different from embryophytic spores, we need to combine an accurate description of fossil morphology, topology, and wall ultrastructure, with an understanding of spore formation in living representatives of the streptophyte algae. While we cannot guarantee that living representatives of the streptophyte algae possessed the same biology as their ancestors, spore formation in charophytes and, in particular, Coleochaete provides a starting point from which to interpret fossil sporogenesis. This uniformitarian approach has led to some key interpretations that have helped to clarify the seemingly messy morphology of these early cryptospores. In combination with a series of transmission electron microscope (TEM) studies (Strother et al., 2004; Taylor and Strother, 2008, 2009), we now possess a nascent understanding of how these spores formed, enough so, at least, to provide reasonable working hypotheses of sporogenesis in these transitional streptophytes.

Figure 1.1  Diagram showing the general character of pre- and post- Darriwilian cryptospores aligned roughly in stratigraphic order. All specimens are to the same scale, indicated by the 10   μm scale bars. (a) Ambitisporites avitus . (b) Ambitisporites avitus . (c) Rugosphaera sp. (d) Dyadospora murusdensa . (e) Rimosotetras sp. (f) Tetrahedraletes medinensis (holotype). (g) T. medinensis . (h) Velatitetras sp. (i) Tetrahedraletes grayae . (j) Tetrahedraletes sp. (k)  Tetrahedraletes sp. (l) Didymospora luna . (m) Dyadospora cf. D. murusdensa . (n) Cryptotetras erugata . (o) C. erugata . (p) Tetrahedraletes grayae . (q) T. grayae . (r) cryptospore cluster. (s) planar cryptospore dyad pair. (t) small cryptospore planar tetrad. (u) Grododowon orthagonalis . (v) Agamachates casearius (holotype). (w) A. casearius . (x) small Rimosotetras sp. (y) Adinosporus geminus . (z) Adinosporus bullatus . (aa) Adinosporus voluminosus . (ab)  Spissuspora laevigata . (ac) Adinosporus sp. (ad) Sphaerasaccus sp. (ae) Vidalgea maculata . (af) Vidalgea sp. (ag) cryptospore cluster. (ah)  Adinosporus cf. A. voluminosus . (ai) Adinosporus cf. A. voluminosus .

A key feature in the meiotic production of zoöspores in living Coleochaete is the recognition that karyokinesis and cytokinesis are temporally decoupled from each other. To be more precise, multiple rounds of DNA duplication, or endoreduplication, occur within the zygote before nucleation and cytokinesis. This was clarified by Hopkins and McBride (1976) who demonstrated that the nuclei in zygotes of C. scutata may contain up to eight copies (8C) of the haploid (1C) amount of DNA before perennation. After germination, Coleochaete zygotes produce up to 32 haploid (1n) zoöspores per original diploid (2n) zygote. Graham (1993) describes this form of sporogenesis as meiosis I, followed by multiple rounds of meiosis II. However, in a review of cell division in charophytes at large, Haig (2010) considers it unclear as to the nature of chromosomal pairing and karyokinesis in Coleochaete, leaving open the possibility that DNA replication occurred before the sorting of chromosomes into discrete nuclei. Haig (2015) points out that reduction division in Coleochaete does not correspond to either meiosis or mitosis, as seen in plants today. We will return to the nature of reduction division in Coleochaete later in the discussion in the canalization of meiosis, but for now, it is important to realize that many of the charophytes today, and Coleochaete in particular, do not possess a regularized version of reduction division, and, therefore, there is no reason to think that the Cambrian ancestors of these streptophyte algae did either.

Cambrian cryptospore morphology can be characterized by two general features: (1) the close association of two or more spore-like bodies that do not retain regular geometric attachments and (2) the occurrence of multiple wall layers, including synoecosporal walls (Taylor and Strother, 2008), which enclose tightly clustered spores to form packets. Both of these features can be viewed in relation to the haphazard nature of spore development as characterized by zygotic germination in living charophytes (Haig, 2010). In addition, the persistence of multiple resistant walls, surrounding varying numbers of enclosed spore bodies, can be viewed as evidence of an on-going process of sporopollenin transfer, during which sporopollenin deposition shifted from the zygote wall to the walls of the meiospores (Blackmore and Barnes, 1987; Graham, 1993; Hemsley, 1994).

3.2. Early Cryptospore Topology

We use the term topology to refer to the geometric arrangement of spore bodies in combination with the pattern of enclosing walls. The topology of a cryptospore packet can be deconstructed as a combination of cell divisions (produced by cytokinesis) and wall constructions (produced by either centripetal or centrifugal deposition of wall material). The deconstruction methodology was originally applied to Agamachates casearius (Taylor and Strother, 2009), where we were able to demonstrate differences in the number of cell divisions that occurred during spore formation. Ultimately, these late Cambrian cryptospore packets were resolved down to sets of spore pairs, each of which corresponded to mitotic cytokinesis.

The middle Cambrian sample at a depth of 1581  ft (482  m) in the JOY-2 core from Oak Ridge, Tennessee (Strother, 2016), contains a well-preserved cryptospore population that includes examples of spore dyads and tetrads enclosed within a common wall (Fig. 1.2). This structure was interpreted by Strother (2016) as an SMC, whose cell wall was preserved, and which had undergone endosporogenesis resulting in a spore tetrad (T) and a spore dyad (D)—both of which were retained within the original SMC wall. If that is the case, then some form of successive meiosis must have occurred. Ignoring the question of ploidy level, it is possible to view the resultant topology as a series of nuclear division