PALAEOBIOLOGY IIEDITED BY

DEREK E.G. BRIGGSDepartment of Geology & Geophysics

Yale UniversityNew Haven

Connecticut 06511USA

AND

PETER R. CROWTHERKeeper of Geology

National Museums and Galleries of Northern IrelandUlster MuseumBotanic GardensBelfast BT9 5AB

OF THE PALAEONTOLOGICAL ASSOCIATION

To the memory of J.J. Sepkoski Jr

PALAEOBIOLOGY II

The dinosaur Diplodocus as seen in the BBC’s acclaimed series ‘Walking with Dinosaurs’ — the world’s first natural history ofdinosaurs. © BBC Worldwide Ltd, 1999.

PALAEOBIOLOGY IIEDITED BY

DEREK E.G. BRIGGSDepartment of Geology & Geophysics

Yale UniversityNew Haven

Connecticut 06511USA

AND

PETER R. CROWTHERKeeper of Geology

National Museums and Galleries of Northern IrelandUlster MuseumBotanic GardensBelfast BT9 5AB

OF THE PALAEONTOLOGICAL ASSOCIATION

To the memory of J.J. Sepkoski Jr

© 2001, 2003 by Blackwell Science Ltd,a Blackwell Publishing company

350 Main Street, Malden, MA 02148-5018, USA108 Cowley Road, Oxford OX4 1JF, UK550 Swanston Street, Carlton South, Melbourne, Victoria 3053, AustraliaKurfürstendamm 57, 10707 Berlin, Germany

The right of the Authors to be identified as the Authors of the Editorial Material in this Work has been asserted in accordance with the UK Copyright, Designs, andPatents Act 1988.

All rights reserved. No part of this publication may be reproduced, stored in aretrieval system, or transmitted, in any form or by any means, electronic,mechanical, photocopying, recording or otherwise, except as permitted by the UKCopyright, Designs, and Patents Act 1988, without the prior permission of thepublisher.

First published 2001First published in paperback 2003

Library of Congress Cataloging-in-Publication Data

Palaeobiology II / edited by D.E.G. Briggs, P.R. Crowther; foreword by E.N.K. Clarkson.

p. cm.Includes bibliographical references and index.ISBN 0-632-05147-7 (hb : alk. paper)—ISBN 0-632-05149-3 (pb. : alk.

paper)1. Palaeobiology. I. Title: Palaeobiology two. II. Title: Palaeobiology 2.

III. Briggs, D.E.G. IV. Crowther, Peter R.

QE719.8 .P34 2001560 — dc21

00-031211

A catalogue record for this title is available from the British Library.

Set by SNP Best-set Typesetter Ltd., Hong KongPrinted and bound in the United Kingdomby MPG Books Ltd, Bodmin, Cornwall

For futher information onBlackwell Publishing, visit our website:http://www.blackwellpublishing.com

List of Contributors, ix

Foreword, xve.n.k. clarkson

1 Major Events in the History of Life

1.1 Early Life, 31.1.1 Origin of Life, 3

a. lazcano1.1.2 Exploring for a Fossil Record of

Extraterrestrial Life, 8j.d. farmer

1.1.3 Life in the Archaean, 13r. buick

1.1.4 Late Proterozoic Biogeochemical Cycles, 22g.a. logan and r.e. summons

1.2 The Cambrian Radiation, 251.2.1 Metazoan Origins and Early Evolution, 25

d.h. erwin1.2.2 Significance of Early Shells, 31

s. conway morris1.2.3 Cambrian Food Webs, 40

n.j. butterfield1.2.4 The Origin of Vertebrates, 43

m.p. smith and i . j. sansom1.3 Palaeozoic Events, 49

1.3.1 Ordovician Radiation, 49a.i . miller

1.3.2 Rise of Fishes, 52j.a. long

1.3.3 Evolution of Reefs, 57r.a. wood

1.3.4 Early Land Plants, 63d. edwards

1.3.5 Afforestation — the First Forests, 67s.e. scheckler

1.3.6 Terrestrialization of Animals, 71p.a. selden

1.3.7 Origin of Tetrapods, 74m.i. coates

1.3.8 Carboniferous Coal-swamp Forests, 79w.a. dimichele

1.3.9 Rise and Diversification of Insects, 82c.c. labandeira

1.3.10 Origin of Mammals, 88j.a. hopson

1.4 Mesozoic Events, 941.4.1 Mesozoic Marine Revolution, 94

p.h. kelley and t.a. hansen1.4.2 Origin and Radiation of Angiosperms, 97

e.m. friis , k.r. pedersen andp.r. crane

1.4.3 Rise of Birds, 102l.m. chiappe

1.5 Cenozoic Events, 1061.5.1 Evolution of Modern Grasslands and

Grazers, 106t.e. cerling

1.5.2 Radiation of Tertiary Mammals, 109c.m. janis

1.5.3 Rise of Modern Land Plants and Vegetation, 112m.e. collinson

1.5.4 Early Primates, 115k.d. rose

1.5.5 Hominid Evolution, 121b.a. wood

1.5.6 Neandertals, 127l.c. aiello

2 The Evolutionary Process and the Fossil Record

2.1 Species Evolution, 1332.1.1 Speciation and Morphological

Change, 133d.b. lazarus

2.1.2 Evolutionary Stasis vs. Change, 137a.h. cheetham

2.1.3 Rapid Speciation in Species Flocks, 143a.r. mccune

2.2 Evolution of Form, 1472.2.1 Developmental Genes and the Evolution of

Morphology, 147g.a. wray

2.2.2 Constraints on the Evolution of Form, 152p.j. wagner

2.2.3 Occupation of Morphospace, 157a.r.h. swan

Contents

v

2.3 Macroevolution, 1622.3.1 Origin of Evolutionary Novelties, 162

d. jablonski2.3.2 Controls on Rates of Evolution, 166

s.m. stanley2.3.3 Competition in Evolution, 171

j. j. sepkoski jr2.3.4 Biotic Interchange, 176

d.r. lindberg2.3.5 Importance of Heterochrony, 180

k.j. mcnamara2.3.6 Hierarchies in Evolution, 188

t.a. grantham2.3.7 Phylogenetic Tree Shape, 192

p.n. pearson2.3.8 Contingency, 195

s.j. gould2.3.9 Selectivity during Extinctions, 198

m.l. mckinney2.3.10 Biotic Recovery from Mass Extinctions, 202

d.j. bottjer2.3.11 Evolutionary Trends, 206

d.w. mcshea2.4 Patterns of Diversity, 211

2.4.1 Biodiversity through Time, 211m.j. benton

2.4.2 Late Ordovician Extinction, 220p.j. brenchley

2.4.3 Late Devonian Extinction, 223g.r. mcghee jr

2.4.4 End-Permian Extinction, 226p.b. wignall

2.4.5 Impact of K–T Boundary Events on MarineLife, 229r.d. norris

2.4.6 Impact of K–T Boundary Events on Terrestrial Life, 232j.a. wolfe and d.a. russell

2.4.7 Pleistocene Extinctions, 234k. roy

3 Taphonomy

3.1 Fossilized Materials, 2413.1.1 DNA, 241

h.n. poinar and s. pääbo3.1.2 Proteins, 245

m.j. collins and a.m. gernaey3.1.3 Lipids, 247

r.p. evershed and m.j. lockheart3.1.4 Bacteria, 253

k. liebig3.1.5 Resistant Plant Tissues — Cuticles and

Propagules, 256p.f. van bergen

3.1.6 Animal Cuticles, 259b.a. stankiewicz and d.e.g. briggs

3.1.7 Shells, 262k.h. meldahl

3.1.8 Bones, 264c. denys

3.2 Fossilization Processes, 2703.2.1 Decay, 270

p.a. allison3.2.2 Bioerosion, 273

e.n. edinger3.2.3 Preservation by Fire, 277

a.c. scott3.2.4 Role of Microbial Mats, 280

j. -c. gall3.2.5 Bioimmuration, 285

p.d. taylor and j.a. todd3.2.6 Transport and Spatial Fidelity, 289

l.c. anderson3.2.7 Time-averaging, 292

k.w. flessa3.3 Preservation in Different Ecological

Settings, 2973.3.1 Major Biases in the Fossil Record, 297

s.m. kidwell3.3.2 Benthic Marine Communities, 303

w.d. allmon3.3.3 Ancient Reefs, 307

j.m. pandolfi3.3.4 Marine Plankton, 309

r.e. martin3.3.5 Terrestrial Plants, 312

r.a. gastaldo3.3.6 Pollen and Spores, 315

j.m. van mourik3.3.7 Terrestrial Vertebrates, 318

a.k. behrensmeyer3.3.8 Sphagnum-dominated Peat Bogs, 321

t.j. painter3.3.9 Archaeological Remains, 325

v. straker3.4 Lagerstätten, 328

3.4.1 Exceptionally Preserved Fossils, 328d.e.g. briggs

3.4.2 Precambrian Lagerstätten, 332a.h. knoll and shuhai xiao

3.4.3 Chengjiang, 337j. bergström

3.4.4 The Soom Shale, 340r.j. aldridge, s .e . gabbott andj.n. theron

3.4.5 The Rhynie Chert, 342n.h. trewin

3.4.6 Hunsrück Slate, 346r. raiswell, c. bartels andd.e.g. briggs

vi Contents

3.4.7 La Voulte-sur-Rhône, 349p.r. wilby

3.4.8 The Santana Formation, 351d.m. martill

3.4.9 Las Hoyas, 356j.l . sanz, m.a. fregenal-martínez, n. meléndez and f. ortega

3.4.10 The Princeton Chert, 359r.a. stockey

3.4.11 Dominican Amber, 362g.o. poinar jr

4 Palaeoecology

4.1 Fossils as Living Organisms, 3674.1.1 Bringing Fossil Organisms to Life, 367

p.w. skelton4.1.2 Stromatolites, 376

m.r. walter4.1.3 Plant Growth Forms and Biomechanics, 379

t. speck and n.p. rowe4.1.4 Sessile Invertebrates, 384

w.i. ausich and d.j. bottjer4.1.5 Trilobites, 386

b.d.e. chatterton4.1.6 Trackways — Arthropod Locomotion, 389

s.j. braddy4.1.7 Durophagy in Marine Organisms, 393

r.b. aronson4.1.8 Buoyancy, Hydrodynamics, and Structure in

Chambered Cephalopods, 397d.k. jacobs

4.1.9 Feeding in Conodonts and other Early Vertebrates, 401m.a. purnell

4.1.10 Locomotion in Mesozoic Marine Reptiles, 404m.a. taylor

4.1.11 Trackways — Dinosaur Locomotion, 408m.g. lockley

4.1.12 Dinosaur Ethology, 412j.r. horner

4.1.13 Predatory Behaviour in Maniraptoran Theropods, 414a.d. gishlick

4.1.14 Pterosaur Locomotion, 417d.m. unwin

4.1.15 Predation in Sabre-tooth Cats, 420b. van valkenburgh

4.1.16 Plant–Animal Interactions: Herbivory, 424s. ash

4.1.17 Plant–Animal Interactions: Insect Pollination, 426w.l. crepet

4.1.18 Plant–Animal Interactions: Dispersal, 429j. j. hooker and m.e. collinson

4.2 Ancient Communities, 4324.2.1 Ecological Changes through Geological

Time, 432m.l. droser

4.2.2 Do Communities Evolve? 437r.k. bambach

4.2.3 Palaeobiogeography of Marine Communities, 440g.r. shi

4.2.4 Deep-sea Communities, 444t. oji

4.2.5 Ancient Hydrothermal Vent and Cold Seep Faunas, 447c.t.s . little

4.2.6 Zooplankton, 451s. rigby and c.v. milsom

4.2.7 Terrestrial Palaeobiogeography, 454r.s. hill

4.2.8 Epibionts, 460h.l. lescinsky

4.2.9 Fungi in Palaeoecosystems, 464t.n. taylor and e.l. taylor

4.3 Fossils as Environmental Indicators, 4674.3.1 Taphonomic Evidence, 467

m.v.h. wilson4.3.2 Oxygen in the Ocean, 470

w. oschmann4.3.3 Carbon Isotopes in Plants, 473

d.j. beerling4.3.4 Bathymetric Indicators, 475

p.j. orr4.3.5 Atmospheric Carbon Dioxide — Stomata, 479

j.c. mcelwain4.3.6 Climate — Wood and Leaves, 480

d.r. greenwood4.3.7 Climate — Modelling using Fossil Plants, 483

g.r. upchurch jr4.3.8 Climate — Quaternary Vegetation, 485

t. webb

5 Systematics, Phylogeny, and Stratigraphy

5.1 Morphology and Taxonomy, 4895.1.1 Quantifying Morphology, 489

r.e. chapman and d. rasskin-gutman5.1.2 Morphometrics and Intraspecific

Variation, 492n.c. hughes

5.1.3 Disparity vs. Diversity, 495m.a. wills

5.2 Calibrating Diversity, 5005.2.1 Estimating Completeness of the Fossil

Record, 500m. foote

Contents vii

5.2.2 Analysis of Diversity, 504a.b. smith

5.3 Reconstructing Phylogeny, 5095.3.1 Phylogenetic Analysis, 509

m. wilkinson5.3.2 Fossils in the Reconstruction of Phylogeny, 515

p.l. forey and r.a. fortey5.3.3 Stratigraphic Tests of Cladistic

Hypotheses, 519m.a. norell

5.3.4 Molecular Phylogenetic Analysis, 522j.p. huelsenbeck

5.3.5 Molecules and Morphology in Phylogeny —the Radiation of Rodents, 529f.m. catzeflis

5.3.6 Using Molecular Data to Estimate Divergence Times, 532a. cooper, n. grassly and a. rambaut

5.4 Fossils in Stratigraphy, 5355.4.1 Stratigraphic Procedure, 535

p.f. rawson5.4.2 Calibration of the Fossil Record, 539

s.a. bowring and m.w. martin5.4.3 Confidence Limits in Stratigraphy, 542

c.r. marshall5.4.4 High-resolution Biostratigraphy, 545

j. backman5.4.5 Sequence Stratigraphy and Fossils, 548

s.m. holland

Index, 555

viii Contents

L.C. AIELLO Department of Anthropology, UniversityCollege London, Gower Street, London WC1E 6BT, UK.

R.J . ALDRIDGE Department of Geology, University ofLeicester, University Road, Leicester LE1 7RH, UK.

P.A. ALLISON T.H . Huxley School for Environment,Earth Science & Engineering, Imperial College of Science,Technology & Medicine, Prince Consort Road, South Kens-ington, London SW7 5BP, UK.

W.D. ALLMON Paleontological Research Institution,1259 Trumansburg Road, Ithaca, New York 14850, USA.

L.C. ANDERSON Department of Geology & Geophysics,Louisiana State University, Baton Rouge, Louisiana 70803,USA.

R.B. ARONSON Dauphin Island Sea Lab, 101 BienvilleBoulevard, Dauphin Island, Alabama 36528, USA.

S. ASH Department of Earth & Planetary Sciences, Univer-sity of New Mexico, Albuquerque, New Mexico 87131,USA.

W.I. AUSICH Department of Geological Sciences, OhioState University, 155 South Oval Mall, Columbus, Ohio43210-1397, USA.

J . BACKMAN Department of Geology & Geochemistry,Stockholm University, S-106 91 Stockholm, Sweden.

R.K. BAMBACH Department of Geological Sciences, Virginia Polytechnic Institute & State University, 4044Derring Hall, Blacksburg, Virginia 24061-0420, USA.

C. BARTELS Deutsches Bergbau-Museum, Am Bergbau-museum 28, D-44791 Bochum, Germany.

D.J. BEERLING Department of Animal & Plant Sciences,University of Sheffield, Alfred Denny Building, WesternBank, Sheffield S10 2TN, UK.

A.K. BEHRENSMEYER Department of Paleobiology,National Museum of Natural History, Smithsonian Insti-tution, Washington, DC 20560-0121, USA.

M.J. BENTON Department of Earth Sciences, Universityof Bristol, Wills Memorial Building, Queen's Road, BristolBS8 1RJ, UK.

P.F. van BERGEN Shell Global Solutions InternationalBV, PO Box 38000, 1030 BN Amsterdam, The Netherlands.

J . BERGSTRÖM Department of Palaeozoology, SwedishMuseum of Natural History, PO Box 50007, S-104 05Stockholm, Sweden.

D.J. BOTTJER Department of Earth Sciences, Universityof Southern California, Los Angeles, California 90089,USA.

S.A. BOWRING Department of Earth, Atmospheric &Planetary Sciences, Massachusetts Institute of Technology,Cambridge, Massachusetts 02139, USA.

S.J . BRADDY Department of Earth Sciences, University ofBristol, Wills Memorial Building, Queen's Road, BristolBS8 1RJ, UK.

P.J . BRENCHLEY Department of Earth Sciences, Univer-sity of Liverpool, PO Box 147, Liverpool L69 3GP, UK.

D.E.G. BRIGGS Department of Geology & Geophysics,Yale University, New Haven, Connecticut 06511, USA.

R. BUICK Department of Earth & Space Sciences andAstrobiology Program, University of Washington, Seattle,Washington 98195-1310, USA.

N.J. BUTTERFIELD Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK.

F.M. CATZEFLIS Institut des Sciences de l'Evolution,UMR 5554 CNRS & Université Montpellier 2, F-34095Montpellier 05, France.

T.E. CERLING Department of Geology & Geophysics,University of Utah, Salt Lake City, Utah 84103, USA.

R.E. CHAPMAN Applied Morphometrics Laboratory(ADP) & Department of Paleobiology, National Museum ofNatural History, Smithsonian Institution, Washington,DC 20560, USA.

B.D.E. CHATTERTON Department of Earth & Atmos-pheric Sciences, University of Alberta, Edmonton, Alberta,Canada T6G 2E1.

A.H. CHEETHAM Department of Paleobiology, NationalMuseum of Natural History, Smithsonian Institution,Washington, DC 20560, USA.

L.M. CHIAPPE Department of Vertebrate Paleontology,Natural History Museum of Los Angeles County, 900 Ex-position Boulevard, Los Angeles, California, 90007, USA.

List of Contributors

ix

E.N.K. CLARKSON Grant Institute of Geology, Univer-sity of Edinburgh, West Mains Road, Edinburgh EH9 3JW,UK.

M.I . COATES Department of Organismal Biology andAnatomy, University of Chicago, 1027 East 57th Street,Chicago, Illinios 60637, USA.

M.J. COLLINS Postgraduate Institute in Fossil Fuels &Environmental Geochemistry (NRG), Drummond Build-ing, The University, Newcastle upon Tyne NE1 7RU, UK.

M.E. COLLINSON Department of Geology, Royal Holloway University of London, Egham, Surrey TW20 0EX, UK.

S. CONWAY MORRIS Department of Earth Sciences,University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK.

A. COOPER Institute of Biological Anthropology, University of Oxford, 58 Banbury Road, Oxford OX2 6QS, UK.

P.R. CRANE Royal Botanic Gardens, Kew, Richmond,Surrey TW9 3AB, UK.

W.L. CREPET L.H. Bailey Hortorium, Cornell Univer-sity, Mann Lib 462, Ithaca, New York 14853, USA.

P.R. CROWTHER Keeper of Geology, Museums and Galleries of Northern Ireland, Ulster Museum, BotanicGardens, Belfast, BT9 5AB, UK.

C. DENYS Laboratoire Mammifères et Oiseaux, MuséumNational d’Histoire Naturelle, 55 rue Buffon, F-75005Paris, France.

W.A. DIMICHELE Department of Paleobiology,National Museum of Natural History, Smithsonian Insti-tution, Washington, DC 20560, USA.

M.L. DROSER Department of Earth Sciences, Universityof California at Riverside, California 92521, USA.

E.N. EDINGER Departments of Geography & Biology,Memorial University of Newfoundland, St John’s, New-foundland A1B 3X9, Canada.

D. EDWARDS Department of Earth Sciences, Cardiff University, Main Building, PO Box 941, Cardiff CF103YE, UK.

D.H. ERWIN Department of Paleobiology, NationalMuseum of Natural History, Smithsonian Institution,Washington, DC 20560, USA.

R.P. EVERSHED Organic Geochemistry Unit, School ofChemistry, University of Bristol, Cantock's Close, BristolBS8 1TS, UK.

J .D. FARMER Department of Geological Sciences, ArizonaState University, Box 871404, Tempe, Arizona 85254-1404, USA.

K.W. FLESSA Department of Geosciences, University ofArizona, Tucson, Arizona 85721, USA.

M. FOOTE Department of the Geophysical Sciences, Uni-versity of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637, USA.

P.L. FOREY Department of Palaeontology, The NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

R.A. FORTEY Department of Palaeontology, The NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

M.A. FREGENAL-MARTÍNEZ Departamento deEstratigrafía, Facultad de Ciencias Geológicas, UniversidadComplutense, 28040 Madrid, Spain.

E.M. FRIIS Department of Palaeobotany, Swedish Museumof Natural History, Box 50007, S-104 05 Stockholm,Sweden.

S.E. GABBOTT Department of Geology, University ofLeicester, University Road, Leicester LE1 7RH, UK.

J . -C. GALL Institut de Géologie, Université Louis Pasteur,1 rue Blessig, F-67084 Strasbourg, France.

R.A. GASTALDO Department of Geology, Colby College,5820 Mayflower Hill, Waterville, Maine 04901-8858,USA.

A.M. GERNAEYBiosciences Research Institute, Cock-croft Building, University of Salford, Greater ManchesterM5 4WT, UK.

A.D. GISHLICK National Center for Science Education,PO Box 9477, Berkeley, California 94709-0477, USA.

S.J . GOULD (Deceased) Formerly of Museum of Comparative Zoology, Harvard University, Cambridge,Massachusetts 02138, USA.

T.A. GRANTHAM Department of Philosophy, College ofCharleston, 66 George Street, Charleston, South Carolina29424-0001, USA.

N. GRASSLY Infectious Disease Epidemiology, St Mary’sHospital, Norfolk Place, London W2 1PG, UK.

D.R. GREENWOOD School of Life Sciences & Technol-ogy, Victoria University of Technology, PO Box 14428,Melbourne City, Victoria 8001, Australia.

T.A. HANSEN Department of Geology, Western Washington University, Bellingham, Washington 98225,USA.

R.S. HILL Department of Environmental Biology, University of Adelaide, Adelaide, South Australia 5005,Australia.

S.M. HOLLAND Department of Geology, University ofGeorgia, Athens, Georgia 30602-2501, USA.

J . J . HOOKER Department of Palaeontology, The NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

x List of Contributors

J .A. HOPSON Department of Organismal Biology &Anatomy, University of Chicago, 1027 East 57th Street,Chicago, Illinois 60637, USA.

J .R. HORNER Museum of the Rockies, Montana StateUniversity, Bozeman, Montana 59717, USA.

J .P. HUELSENBECK Department of Biology, Universityof Rochester, Rochester, New York 14627, USA.

N.C. HUGHES Department of Earth Sciences, Universityof California at Riverside, California 92521-0423, USA.

D. JABLONSKI Department of Geophysical Sciences,University of Chicago, 5734 South Ellis Avenue, Chicago,Illinois 60637, USA.

D.K. JACOBS Department of Organismic Biology, Ecology& Evolution, University of California at Los Angeles, 621Charles Young Drive South, Box 951606, Los Angeles, California 90095-1606, USA.

C.M. JANIS Department of Ecology & EvolutionaryBiology, Box G-B207, Brown University, Providence,Rhode Island 02912, USA.

P.H. KELLEY Department of Earth Sciences, University ofNorth Carolina at Wilmington, 601 South College Road,Wilmington, North Carolina 28403-3297, USA.

S.M. KIDWELL Department of Geophysical Sciences,University of Chicago, 5734 South Ellis Avenue, Chicago,Illinois 60637, USA.

A.H. KNOLL Botanical Museum, Harvard University, 26Oxford Street, Cambridge, Massachusetts 02138, USA.

C.C. LABANDEIRA Department of Paleobiology,National Museum of Natural History, Smithsonian Insti-tution, Washington, DC 20560, USA.

D.B. LAZARUS Institut für Paläontologie, Museum für Naturkunde, Zentralinstitut der Humboldt-Universitätzu Berlin, Invalidenstrasse 43, D-10115 Berlin, Germany.

A. LAZCANO Facultad de Ciencias, UniversidadNacional Autónoma de México, Apdo. Postal 70-407, Cd.Universitaria, Mexico City, 04510 DF, Mexico.

H.L. LESCINSKY Department of Life & Earth Sciences,Otterbein College, Westerville, Ohio 43081, USA.

K. LIEBIG Fakultät für Biologie, Ruprecht-Karls-Universität Heidelberg, Im Nevenheimer Feld 234, D-69120 Heidelberg, Germany.

D.R. LINDBERG Department of Integrative Biology,University of California at Berkeley, Berkeley, California 94720, USA.

C.T.S. LITTLE School of Earth Sciences, University ofLeeds, Leeds LS2 9JT, UK.

M.J. LOCKHEART Organic Geochemistry Unit, Schoolof Chemistry, University of Bristol, Cantock's Close, BristolBS8 1TS, UK.

M.G. LOCKLEY Department of Geology, University ofColorado at Denver, Campus Box 172, PO Box 173364,Denver, Colorado 80217-3364, USA.

G.A. LOGAN Geoscience Australia, GPO Box 378, Constitution Avenue, Canberra, ACT 2601, Australia.

J .A. LONG Department of Earth & Planetary Sciences,Western Australian Museum, Francis Street, Perth,Western Australia 6000, Australia.

C.R. MARSHALL Departments of Earth & Planetary Sciences, and Organismic & Evolutionary Biology, Har-vard University, Cambridge, Massachusetts 02138, USA.

D.M. MARTILL School of Earth & Environmental Sci-ences, Burnaby Building, University of Portsmouth,Burnaby Road, Portsmouth PO1 3QL, UK.

M.W. MARTIN Shell International Exploration and Production Inc., Woodcreek-Rm-7516, 200 North DairyAshford, Houston, Texas 77001-2121, USA.

R.E. MARTIN Department of Geology, University ofDelaware, Newark, Delaware 19716, USA.

A.R. McCUNE Department of Ecology & EvolutionaryBiology, Corson Hall, Cornell University, Ithaca, New York14853, USA.

J .C. McELWAIN Department of Geology, Field Museumof Natural History, 1400S Lake Shore Drive, Chicago, Illinois 60605-2496, USA.

G.R. McGHEE Department of Geological Sciences,Rutgers University, Wright-Rieman Laboratories, BuschCampus, Piscataway, New Jersey 08854-8066, USA.

M.L. McKINNEY Department of Geological Sciences,University of Tennessee, Knoxville, Tennessee 37996-1410,USA.

K.J . McNAMARA Department of Earth & Planetary Sciences, Western Australian Museum, Francis Street,Perth, Western Australia 6000, Australia.

D.W. McSHEA Department of Biology, Box 90338, DukeUniversity, Durham, North Carolina 27708-0338, USA.

K.H. MELDAHL Physical Sciences Department, MiraCosta College, 1 Barnard Drive, Oceanside, California92056, USA.

N. MELÉNDEZ Departamento de Estratigrafía, Facultadde Ciencias Geológicas, Universidad Complutense, 28040Madrid, Spain.

A.I. MILLER Department of Geology, PO Box 210013,University of Cincinnati, Cincinnati, Ohio 45221-0013,USA.

C.V. MILSOM School of Biological & Earth Sciences, Liv-erpool John Moores University, James Parsons Building,Byrom Street, Liverpool L3 3AF, UK.

List of Contributors xi

M.A. NORELL Department of Vertebrate Paleontology,American Museum of Natural History, Central Park Westat 79th Street, New York, New York 10024-5192, USA.

R.D. NORRIS Scripps Institution of Oceanograpy, University of California, La Jolla, California 92093-0244,USA.

T. OJI Department of Earth & Planetary Science, Universityof Tokyo, Hongo, Tokyo 113-0033, Japan.

P.J . ORR Department of Geology, National University ofIreland, Galway, Ireland.

F. ORTEGA Unidad de Paleontología, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma,Cantoblanco, 28049 Madrid, Spain.

W. OSCHMANN Geologisch-Paläontologisches Institut,Senckenberganlage 32-34, Universität Frankfurt, D-60054Frankfurt-am-Main, Germany.

S. PÄÄBO Max-Planck Institute for Evolutionary Anthro-pology, Inselstrasse 22, D-04103 Leipzig, Germany.

T.J . PAINTER Institute of Biotechnology, Norwegian University of Science & Technology, N-7491 Trondheim,Norway.

J .M. PANDOLFI Department of Paleobiology, NationalMuseum of Natural History, Smithsonian Institution,Washington, DC 20560, USA.

P.N. PEARSON Department of Earth Sciences, Univer-sity of Bristol, Wills Memorial Building, Queen's Road,Bristol BS8 1RJ, UK.

K.R. PEDERSEN Department of Geology, University ofAarhus, DK-8000 Aarhus C, Denmark.

G.O. POINAR Jr Department of Entomology, OregonState University, 2046 Cordley Hall, Corvallis, Oregon97331-2907, USA.

H.N. POINAR Max-Planck Institute for EvolutionaryAnthropology, Inselstrasse 22, D-04103 Leipzig, Germany.

M.A. PURNELL Department of Geology, University ofLeicester, University Road, Leicester LE1 7RH, UK.

R. RAISWELL School of Earth Sciences, University ofLeeds, Leeds LS2 9JT, UK.

A. RAMBAUT Department of Zoology, University ofOxford, Oxford OX1 3PS, UK.

D. RASSKIN-GUTMAN The Salk Institute for Biologi-cal Studies, PO Box 85800, San Diego, California 92186-5800, USA.

P.F. RAWSON Department of Geological Sciences, Uni-versity College London, Gower Street, London WC1E 6BT,UK.

S. RIGBY Grant Institute of Geology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JW, UK.

K.D. ROSE Department of Cell Biology & Anatomy, Schoolof Medicine, The Johns Hopkins University, Baltimore,Maryland 21205, USA.

N.P. ROWE Institut des Sciences de l'Evolution, UMR5554 CNRS & Université Montpellier 2, F-34095 Mont-pellier 05, France.

K. ROY Department of Biology, University of California,San Diego, 9500 Gilman Drive, La Jolla, California 92093-0116, USA.

D.A. RUSSELL North Carolina State Museum of NaturalScience, Raleigh, North Carolina 27695, USA.

I . J . SANSOM School of Earth Sciences, University ofBirmingham, Edgbaston, Birmingham B15 2TT, UK.

J .L. SANZ Unidad de Paleontología, Departamento deBiología, Facultad de Ciencias, Universidad Autónoma,Cantoblanco, 28049 Madrid, Spain.

S.E. SCHECKLER Department of Biology, Virginia Polytechnic Institute & State University, Blacksburg, Virginia 24061-0406, USA.

A.C. SCOTT Department of Geology, Royal Holloway Uni-versity of London, Egham, Surrey TW20 0EX, UK.

P.A. SELDEN Department of Earth Sciences, University ofManchester, Oxford Road, Manchester M13 9PL, UK.

J . J . SEPKOSKI Jr [Deceased] Formerly of Department ofGeophysical Sciences, University of Chicago, 5734 SouthEllis Avenue, Chicago, Illinois 60637, USA.

G.R. SHI School of Ecology & Environment, Deakin University, Rusden Campus, Clayton, Victoria 3168, Australia.

P.W. SKELTON Department of Earth Sciences, Open Uni-versity, Walton Hall, Milton Keynes MK7 6AA, UK.

A.B. SMITH Department of Palaeontology, NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

M.P. SMITH Lapworth Museum, School of Earth Sciences,University of Birmingham, Edgbaston, Birmingham B15 2TT, UK.

T. SPECK Botanischer Garten, Albert-Ludwigs-Universität Freiburg, Schänzlestrasse 1, D-79104Freiburg, Germany.

B.A. STANKIEWICZ Shell International Explorationand Production BV, Volmerlaan 8, Postbus 60, 2280 ABRijswijk, The Netherlands.

S.M. STANLEY Department of Earth & Planetary Sci-ences, The Johns Hopkins University, Baltimore, Maryland21218, USA.

xii List of Contributors

R.A. STOCKEY Department of Biological Sciences, Uni-versity of Alberta, Edmonton, Alberta, Canada T6G 2E9.

V. STRAKER School of Geographical Sciences, Universityof Bristol, University Road, Bristol BS8 1SS, UK.

R.E. SUMMONS Department of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Tech-nology, 77 Massachusetts Avenus E34-246, Cambridge,Massachusetts 02139-4307, USA.

A.R.H. SWAN School of Geological Sciences, KingstonUniversity, Penrhyn Road, Kingston-upon-Thames,Surrey KT1 2EE, UK.

E.L. TAYLOR Department of Ecology & EvolutionaryBiology, University of Kansas, Lawrence, Kansas 66045,USA.

M.A. TAYLOR Department of Geology & Zoology,National Museums of Scotland, Chambers Street, Edinburgh EH1 1JF, UK.

P.D. TAYLOR Department of Palaeontology, The NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

T.N. TAYLOR Department of Ecology & EvolutionaryBiology, University of Kansas, Lawrence, Kansas 66045,USA.

J .N. THERON Department of Geology, University of Stel-lenbosch, Stellenbosch, Republic of South Africa.

J .A. TODD Department of Palaeontology, The NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

N.H. TREWIN Department of Geology & PetroleumGeology, University of Aberdeen, Meston Building, King'sCollege, Aberdeen AB24 3UE, UK.

D.M. UNWIN Institüt für Paläontologie, Museum fürNaturkunde, Zentralinstitut der Humboldt-Universität zuBerlin, Invalidenstrasse 43, D-10115 Berlin, Germany.

G.R. UPCHURCH Jr Department of Biology, SouthwestTexas State University, 601 University Drive, San Marcos,Texas 78666-4616, USA.

J .M. VAN MOURIK Institute for Biodiversity & Ecosys-tem Dynamics, University of Amsterdam, Niewe Achter-gracht 166, 1018-WV Amsterdam, The Netherlands.

B. VAN VALKENBURGH Department of OrganismicBiology, Ecology & Evolution, University of California atLos Angeles, 621 Charles E. Young Drive South, PO Box951606, Los Angeles, California 90095-1606, USA.

P.J . WAGNER Department of Geology, Field Museum ofNatural History, Roosevelt Road at Lake Shore Drive,Chicago, Illinois 60615-2496, USA.

M.R. WALTER Department of Earth & Planetary Sciences, Macquarie University, New South Wales 2109,Australia.

T. WEBB Department of Geology, Brown University, Provi-dence, Rhode Island 02912, USA.

P.B. WIGNALL School of Earth Sciences, University ofLeeds, Leeds LS2 9JT, UK.

P.R. WILBY Kingsley Dunham Centre, British GeologicalSurvey, Keyworth, Nottingham NG12 5GG, UK.

M. WILKINSON Department of Zoology, NaturalHistory Museum, Cromwell Road, London SW7 5BD, UK.

M.A. WILLS Department of Biology & Biochemistry, Uni-versity of Bath, South Building, Claverton Down, BathBA2 7AY, UK.

M.V.H. WILSON Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G2E9.

J .A. WOLFE Department of Geosciences, University ofArizona, Tucson, Arizona 85721-0077, USA.

B.A. WOOD Department of Anthropology, George Wash-ington University, 2110 G Street NW, Washington, DC20052, USA.

R.A. WOOD Schlumberger Cambridge Research, HighCross, Madingley Road, Cambridge CB3 0EL, UK.

G.A. WRAY Department of Biology, Duke University,Durham, North Carolina 27708-0325, USA.

SHUHAI XIAO Department of Geology, Tulane Univer-sity, New Orleans, Louisiana 70118, USA.

List of Contributors xiii

When Palaeobiology — a synthesis appeared in 1990, it wasimmediately recognized as an invaluable compilationwhich no palaeobiologist should be without. Each of thearticles had been commissioned to provide authoritativeand up-to-date information in as concise a form as poss-ible, and only essential references were included. Whilealmost any of these articles could be read by non-experts,their value for advanced students was unquestioned.Where else between two covers could such appropriateand easily mastered source material be found for essaysand presentations?

In the decade since the publication of Palaeobiology — asynthesis, new data have accumulated, new expertise hasarisen, concepts have evolved, and emphases havechanged. It is now time for a new synthesis, and here itis — Palaeobiology II. Readers familiar with the first bookwill recognize the main divisions here, but PalaeobiologyII is by no means a second edition — it is an entirely newbook. The great majority of the 137 articles deal with newtopics (all are new treatments), and over 100 authors arenew. The basic concept that proved so successful in thefirst book has nevertheless been retained: the articleshave been written by recognized authorities in eachfield; the content is concise but informative; and theaccompanying reference lists are brief and up to date.

In all respects this volume is timely, and it will be

widely used. The new generation of articles reflects notonly the vigorous and exciting developments that aretaking place in palaeontology at the opening of thetwenty-first century, but also the many links with otherscientific disciplines. Palaeontologists today must know about developmental genes and fossil proteins,sequence stratigraphy and fossils, and how to test cladistic analyses against the fossil record. All thesetopics, and many more, are to be found here. But the sci-entific themes that have been developed within palaeo-biology are also necessary for other sciences, and thebook will prove of great value outside its own specificarea.

Derek Briggs and Peter Crowther commissioned andedited the articles for Palaeobiology — a synthesis and sawthe whole gigantic project through to completion. Theyhave again been active; Palaeobiology II is a testament totheir vision, to the many hours of labour required torealize it, and to the fruitful partnership that they havedeveloped with Blackwell Science.

On behalf of the Palaeontological Association, I wishPalaeobiology II the success it deserves. It is very wel-come, and the topics covered here cannot fail to interestbiologists and palaeontologists of all kinds. Perhaps inanother ten years there will be a further version, but thisone is unlikely to be quickly superseded.

ForewordEUAN N.K. CLARKSON

President of thePalaeontological Association

1998–2000

ThePalaeontologicalAssociation

xv

1MAJOR EVENTS IN THE

HISTORY OF LIFE

Cranium of Neandertal (Guattari 1) from Monte Circeo, Italy, approximately two-thirds natural size. (Photographcourtesy of R. Macchiarelli, Museo Nazionale Preistorico Etnografico, Rome.)

1.1 Early Life

development of proteins and DNA genomes, duringwhich alternative life forms based on ribozymes existed(Gesteland et al. 1999). This has led many to argue thatthe starting point for the history of life on Earth was thede novo emergence of the RNA world from a nucleotide-rich prebiotic soup. Others are more sceptical andbelieve that it lies in the origin of cryptic and largelyunknown pre-RNA worlds. There is even a third groupthat favours the possibility that life began with theappearance of chemoautotrophic autocatalytic meta-bolic networks, lacking genetic material.

Despite the seemingly insurmountable obstacles sur-rounding the understanding of the origin of life (orperhaps because of them), there has been no shortage of discussion about how it took place. Not surprisingly,several alternative and even opposing suggestions havebeen made regarding how life emerged and what werethe defining characteristics of the first organisms. Whilethe classical version of the hypothesis of chemical evolu-tion and primordial heterotrophy needs to be updated, itstill provides the most useful framework for addressingthe issue of emergence of life.

How can the origin of life be studied?

Of necessity, work on the origin of life should beregarded as enquiring and explanatory rather thandefinitive and conclusive. This does not imply that ourtheories and explanations can be dismissed as pure speculation, but rather that the issue should beaddressed conjecturally, in an attempt to construct acoherent, non-teleological historical narrative (Kam-minga 1991). It is unlikely that the origin of life will everbe described in full detail; at best a sketchy outline, con-sistent with conditions on the prebiotic Earth (such as itsanoxic environment) and the physicochemical proper-ties of the likely molecular precursors of living systems,will be constructed.

The attributes of the first living organisms areunknown. They were probably simpler than any cellnow alive, and may have lacked not only protein-basedcatalysis, but perhaps even the familiar genetic macro-molecules, with their ribose-phosphate backbones. It ispossible that the only property they shared with extantorganisms was the structural complementarity betweenmonomeric subunits of replicative informational poly-mers, e.g. joining together a growing chain of residues in a sequence directed by preformed polymers. How-ever, such ancestral polymers may not have involvednucleotides. Hence caution must be exercised in extrapo-

3

1.1.1 Origin of Life

A. LAZCANO

Introduction

‘All the organic beings which have ever lived on thisEarth’, wrote Charles Darwin in On the Origin of Speciesby Means of Natural Selection, ‘may be descended fromsome one primordial form’. It is not known how this first ancestor came into being nor what its nature was.However, the presence of cyanobacteria-like microfos-sils in the 3.5 billion years old (Ga) Australian Apex sedi-ments (Schopf 1993), deposited only a few million yearsafter the end of the intense bombardment caused by thelate accretion of planetesimals left over from the forma-tion of the Solar System, demonstrates that the emer-gence and early diversification of life on Earth requiredno more than 500 million years. Together with the inclu-sions enriched in light isotopic carbon in 3.86Ga samplesfrom south-west Greenland (Mojzsis et al. 1996), theseresults show that a widespread, complex, and highlydiversified Archaean microbiota was thriving soon afterthe Earth had cooled down and the influx of myriads ofcomets and asteroids had ceased.

It is unlikely that data on how life originated will beprovided by the palaeontological record. There is no geological evidence of the environmental conditions onEarth at the time of the origin of life, nor any fossil reg-ister of the evolutionary processes that preceded theappearance of the first cells. Direct information is lackingnot only on the composition of the terrestrial atmosphereduring the period of the origin of life, but also on thetemperature, ocean pH values, and other general andlocal environmental conditions which may or may nothave been important for the emergence of livingsystems.

The lack of an all-embracing, generally agreeddefinition of life sometimes gives the impression thatwhat is meant by its origin is defined in somewhatimprecise terms, and that several entirely different ques-tions are often confused. For instance, until a few yearsago the origin of the genetic code and of protein synthe-sis were considered synonymous with the appearance oflife itself. This is no longer a dominant point of view; thediscovery and development of the catalytic activity ofRNA molecules has given considerable support to theidea of an ‘RNA world’ — a hypothetical stage, before the

lating deep molecular phylogenies back into primordialtimes. Genome sequencing and analysis is becomingcritical for understanding early cellular evolution, but itcannot be applied to events prior to the evolution ofprotein biosynthesis. Older stages are not yet amenableto this type of analysis, and the organisms at the base ofuniversal phylogenies are cladistically ancient species,not primitive unmodified microbes.

Given the huge gap between the abiotic synthesis ofbiochemical monomers and the DNA/protein-based lastcommon ancestor of all living systems, it is naive toattempt to describe the origin of life on the basis of avail-able phylogenetic trees. Like a mangrove, the roots ofuniversal evolutionary trees may be submerged in themuddy waters of a prebiotic broth — but how the transi-tion from the non-living to the living took place is stillunknown.

Heterotrophic or autotrophic origins of life?

Although the idea of life as an emergent feature of naturehas been widespread since the nineteenth century, amajor methodological breakthrough by A.I. Oparin andJ.B.S. Haldane in the 1920s transformed the origin of lifefrom a purely speculative issue to a workable researchprogramme. This was based on the idea that the first lifeforms were the outcome of a slow, multistep process thatbegan with the abiotic synthesis of organic compoundsand the formation of a ‘primitive soup’. There followedthe formation of colloidal gel-like systems, from whichanaerobic heterotrophs evolved that could take up sur-rounding organic compounds and use them directly forgrowth and reproduction.

Many of Oparin’s original ideas have been super-seded, but his hypothesis provided a conceptual frame-work for the development of this field. His proposalbecame widely accepted, not only because it is simpler toenvision a heterotrophic organism originating fromorganic molecules of abiotic origin rather than from anautotroph, but also because laboratory experiments haveshown how easy it is to produce a number of biochem-ical monomers under reducing conditions.

The first successful synthesis of organic compoundsunder plausible primordial conditions was accom-plished by the action of electrical discharges acting for aweek over a mixture of CH4, NH3, H2, and H2O; racemicmixtures of several proteinic amino acids were pro-duced, as well as hydroxy acids, urea, and other organicmolecules (Miller 1993). This was followed a few yearslater by the demonstration of rapid adenine synthesis bythe aqueous polymerization of HCN. The potential roleof HCN as a precursor in prebiotic chemistry is furthersupported by the discovery that the hydrolytic productsof its polymers include amino acids, purines, and oroticacid (a biosynthetic precursor of uracil). A potential pre-

biotic route for the synthesis of cytosine in high yields is provided by the reaction of cyanoacetylene with urea, especially when the concentration of the latter isincreased by simulating the conditions of an evaporatingpond.

The ease with which amino acids, purines, and pyrimidines can form by reactions in a simple vesselstrongly suggests that these molecules were componentsof the prebiotic broth. They would have been associatedwith many other compounds, such as urea and carb-oxylic acids, sugars formed by the non-enzymatic con-densation of formaldehyde, a wide variety of aliphaticand aromatic hydrocarbons, alcohols, and branched andstraight fatty acids, including some which are mem-brane-forming compounds. The list also includes severalhighly reactive derivatives of HCN, such as cyanamide(H2NCN) and its dimer (H2NC(NH)NH–CN), di-cyanamide (NC–NH–CN), and cyanogen (NC– CN),which are known to catalyse polymerization reactions.Additional aspects of prebiotic chemistry have beenreviewed by Miller (1993), Deamer and Fleischaker(1994), Chyba and McDonald (1995), and Brack (1998).

The synthesis of chemical constituents of contempor-ary organisms by non-enzymatic processes under labor-atory conditions does not necessarily imply that theywere either essential for the origin of life or available inthe primitive environment. However, the significance ofprebiotic simulation experiments is supported by theoccurrence of a large array of protein and non-proteinamino acids, carboxylic acids, purines, pyrimidines,hydrocarbons, and other molecules in the 4.6Ga Murch-ison meteorite (a carbonaceous chondrite which alsoyields evidence of liquid water) (Miller 1993; Chyba andMcDonald 1995). The presence of these compounds inthe meteorite makes it plausible, but does not prove, thata similar synthesis took place on the primitive Earth — oris it simply a coincidence?

The evolutionary framework provided by Oparin’stheory and methodology has allowed further develop-ment and refinement without losing the overall structureand internal coherence of his approach (Kamminga1991). Several competing approaches to the study of theorigin of life coexist today, including proposals for RNAor thioester worlds, for an extraterrestrial origin of theprimitive soup’s components, and for the role of sub-marine hot springs as sites for prebiotic chemistry(Chyba and McDonald 1995; de Duve 1995).All,however,are based on the assumption that abiotic organic com-pounds were a necessary precursor to the appearance of life.

Pyrite formation and the emergence of life

So far, the only serious rival to the heterotrophic theorystems from the work of Wächtershäuser (1988). Accord-

4 1 Major Events in the History of Life

ing to this hypothesis, life began with the appearance of an autocatalytic two-dimensional chemolithotrophicmetabolic system based on the formation of the highlyinsoluble mineral pyrite. Synthesis and polymeriza-tion of organic compounds took place on the surface of FeS and FeS2 in environments that resemble those of deep-sea hydrothermal vents. Replication followed the appearance of non-organismal iron sulphide-basedtwo-dimensional life, in which chemoautotrophiccarbon fixation took place by a reductive citric acid cycle,or reverse Krebs cycle, of the type originally describedfor the photosynthetic green sulphur bacterium Chloro-bium limicola. Molecular phylogenetic trees show thatthis mode of carbon fixation and its modifications (suchas the reductive acetyl-CoA or the reductive malonyl-CoA pathways) are found in anaerobic archaebacteriaand the most deeply divergent eubacteria, which hasbeen interpreted as evidence of its primitive character(Maden 1995). But is the reverse Krebs cycle truly primordial?

The reaction FeS + H2S = FeS2 + H2 is a very favourableone. It has an irreversible, highly exergonic (energy liber-ating) character with a standard free energy change DG° = -9.23 kcal/mol, which corresponds to a reductionpotential E° = -620mV. Thus, the FeS/H2S combinationis a strong reducing agent, and has been shown toprovide an efficient source of electrons for the reductionof organic compounds under mild conditions. Pyrite for-mation can produce molecular hydrogen, and reducenitrate to ammonia, acetylene to ethylene, thioacetic acidto acetic acid, as well as more complex synthesis (Maden1995), including peptide-bonds that result from the activation of amino acids with carbon monoxide and (Ni, Fe)S (Huber and Wächtershäuser 1998). Althoughpyrite-mediated CO2 reduction to organic compoundshas not been achieved, the fixation under plausible pre-biotic conditions of carbon monoxide into activatedacetic acid by a mixture of coprecipitated NiS/FeS hasbeen reported (cf. Huber and Wächtershäuser 1998).However, in these experiments the reactions occur in anaqueous environment to which powdered pyrite hasbeen added; they do not form a dense monolayer of ion-ically bound molecules or take place on the surface ofpyrite.

None of the above experiments itself proves that bothenzymes and nucleic acids are the evolutionary outcomeof surface-bounded metabolism. In fact, the results arealso compatible with a more general, modified model ofthe primitive soup in which pyrite formation is recog-nized as an important source of electrons for the reduc-tion of organic compounds. It is thus possible that undercertain geological conditions the FeS/H2S combinationcould have reduced not only CO but also CO2 releasedfrom molten magma in deep-sea vents, leading to bio-chemical monomers. Peptide synthesis, for instance,

could have taken place in an iron and nickel sulphidesystem (Huber and Wächtershäuser 1998) involvingamino acids formed by electrical discharges via a Miller-type synthesis. If the compounds synthesized by thisprocess do not remain bound to the pyrite surface, butdrift away into the surrounding aqueous environment,then they would become part of the prebiotic soup, notof a two-dimensional organism. Thus, the experimentalresults achieved so far with the FeS/H2S combinationare consistent with a heterotrophic origin of life.

The essential question in deciding between these twodifferent theories is not whether pyrite-mediatedorganic synthesis can occur, but whether direct CO2reduction and synthesis of organic compounds can beachieved by a hypothetical two-dimensional livingsystem that lacks genetic information. Proof of Wächters-häuser’s hypothesis requires the demonstration of notonly the tight coupling of the reactions necessary todrive autocatalytic CO2 assimilitation via a reductivecitric acid cycle, but also the interweaving of a networkof homologous cycles which, it is assumed, led to all theanabolic pathways (Maden 1995).

Many original assumptions of the heterotrophictheory have been challenged by our current understand-ing of genetics, biochemistry, cell biology, and the basicmolecular processes of living organisms. The view advo-cated here assumes that, even if the first living systemswere endowed with minimum synthetic abilities, theirmaintenance and replication depended primarily onprebiotically synthesized organic compounds. Anupdated heterotrophic hypothesis assumes that the rawmaterial for assembling the first self-maintaining,replicative chemical systems was the outcome of abioticsynthesis, while the energy required to drive the chem-ical reactions involved in growth and reproduction mayhave been provided by cyanamide, thioesters, glycinenitrile, or other high energy compounds (de Duve 1995;Lazcano and Miller 1996). This modified version of theclassical theory of chemical evolution and primordialheterotrophy can be examined experimentally, and canbe expected to generate additional lines of research.

Prebiotic chemistry and the ‘primitive soup’

Although it is generally agreed that free oxygen wasabsent from the primitive Earth, there is no agreement onthe composition of the primitive atmosphere; opinionsvary from strongly reducing (CH4 + N2, NH3 + H2O, orCO2 + H2 + N2) to neutral (CO2 + N2 + H2O). In general,non-reducing atmospheric models are favoured byatmospheric chemists, while prebiotic chemists leantowards more reducing conditions, under which theabiotic syntheses of amino acids, purines, pyrimidines,and other compounds are very efficient.

The possibility that the primitive atmosphere was

1.1 Early Life 5

non-reducing does not create insurmountable problems,since the primitive soup could still form. For instance,geological sources of hydrogen, such as pyrite, may havebeen available; in the presence of ferrous iron, a sulphideion (SH-) would have been converted to a disulphide ion(S2-), thereby releasing molecular hydrogen (Maden1995). It is also possible that the impacts of iron-richasteroids enhanced the reducing conditions, and thatcometary collisions created localized environmentsfavouring organic synthesis. Based on what is knownabout prebiotic chemistry and meteorite composition, ifthe primitive Earth was non-reducing, then the organiccompounds required must have been brought in byinterplanetary dust particles, comets, and meteorites.Recent measurements suggest that a significant percent-age of meteoritic amino acids and nucleobases couldsurvive the high temperatures associated with frictionalheating during atmospheric entry, and become part ofthe primitive broth (Glavin and Bada 1999).

This eclectic view, in which the prebiotic soup isformed by contributions from endogenous syntheses,extraterrestrial organic compounds delivered by cometsand meteorites, and pyrite-mediated CO reduction, doesnot contradict the heterotrophic theory. Even if the ulti-mate source of the organic molecules required for theorigin of life turns out to be comets and meteorites,recognition of their extraterrestrial origin is not a rehabilitation of panspermia (the hypothesis that lifeexisted elsewhere in the universe and had been trans-ferred from planet to planet, eventually gaining afoothold on Earth), but an acknowledgement of the role of collisions in shaping the primitive terrestrial environment.

The search for the primordial genetic polymers

There is no evidence of abiotically produced oligopep-tides or oligonucleotides in the Murchison meteorite, butcondensation reactions clearly took place in the primi-tive Earth. Synonymous terms like ‘primitive soup’, ‘pri-mordial broth’, or ‘Darwin’s warm little pond’ have ledin some cases to major misunderstandings, including the simplistic image of a worldwide ocean, rich in self-replicating molecules and accompanied by all sorts ofbiochemical monomers. The term ‘warm little pond’,which has long been used for convenience, refers notnecessarily to the entire ocean, but to parts of the hydro-sphere where the accumulation and interaction of theproducts of prebiotic synthesis may have taken place.These include not only membrane-bound systems, but also oceanic sediments, intertidal zones, shallowponds, freshwater lakes, lagoons undergoing wet-and-dry cycles, and eutectic environments (e.g. glacialponds), where evaporation or other physicochemicalmechanisms (such as the adherence of biochemical

monomers to active surfaces) could have raised localconcentrations and promoted polymerization.

It is difficult to estimate the rate of self-organization ofthese polymers into replicating systems, because thechemical steps are unknown. Whatever the time scalerequired for the appearance of an informationalpolymer, once formed it must have persisted at least longenough to allow its replication. If polymers formed by aslow addition of monomers, this process must have beenrapid compared to rates of hydrolysis, especially if a con-siderable amount of genetic information was containedin the polymer. Self-replicating systems capable ofundergoing Darwinian evolution must have emerged ina period shorter than the destruction rates of their com-ponents; even if the backbone of primitive genetic poly-mers was highly stable, the nitrogen bases themselveswould decompose over long periods of time. In fact, theaccumulation of all components of the primitive soupwill be limited by destructive processes, including thepyrolysis of organic compounds in submarine vents.Large amounts of the entire Earth’s oceans circulatethrough the ridge crests every 10 million years, facingtemperatures of 350°C or more, and placing an upperlimit to the time available for the origin and earlydiversification of life (Lazcano and Miller 1996).

The popular idea of a hot origin of life is foundedlargely on the basal position in molecular phylogenies ofhyperthermophiles, which exhibit optimal growth tem-peratures of 80–110°C. Although this hypothesis is alsoconsistent with the emergence of life on a turbulent, hotprimitive Earth (which may or may not be true), it ismerely an extrapolation of the growth temperature ofextant thermophilic prokaryotes. Since most biochem-icals decompose rather rapidly at temperatures of 100°C,prebiotic chemistry clearly supports a low-temperatureorigin of life. A high-temperature origin, under con-ditions such as those found in deep-sea vents, may be possible, but chemical stability arguments rule outany involvement of the purines, pyrimidines, sugar-phosphate backbone, or even most of the 20 amino acidsused by life today: under such extreme conditions, theirhalf-lives are a few seconds. Any theory arguing other-wise must explain not only how life originated undersuch conditions, but also how the evolutionary trans-ition occurred from the hypothetical high temperature-resistant origin to extant biochemistry.

Bridge(s) to the RNA world

The primitive broth must have been a bewilderingorganic chemical wonderland in which a wide array ofdifferent molecules were constantly synthesized,destroyed, or incorporated into cycles of chemical trans-formations. Regardless of the complexity of the prebioticenvironment, life could not have evolved in the absence

6 1 Major Events in the History of Life

of a genetic replicating mechanism to guarantee themaintenance, stability, and diversification of its basiccomponents under the action of natural selection.

The nature of the system that preceded the ubiquitousDNA-based genetic machinery of extant living systemsis unknown, but it must have been endowed with somecapacity for self-replication. There is experimental evid-ence for self-replication in some chemical systems whichlack the familiar nucleic acid-like structure. Theseinclude replicative micelles and vesicles, and self-complementary molecules which result from the chem-ical reaction between an amino-adenosine derivativeand a complex aromatic ester (cf. Orgel 1992). There are also prions, the infamous infectious agents associatedwith bovine spongiform encephalopathy (BSE, or ‘madcow disease’) and several human neurodegenerativemaladies, which may represent a case of phenotypic in-heritance that propagate by changing the harmless conformation of a normal protein into an infectiousisoform.

Although the above examples suggest that replicationmay be a widespread phenomenon, these systems do notexhibit heritability, i.e. they are considered autocatalyticbut non-informational (Orgel 1992). Hence, they areprobably not related to the origin of life. On the otherhand, although the properties of RNA molecules makethem an extremely attractive model for the origin of life,their existence in the prebiotic environment is unlikely. Itis not clear that phosphate esters could have beeninvolved in the first genetic material, and the self-condensation of formaldehyde (i.e. the formose reaction,which appears to be the only plausible route for the pre-biotic synthesis of sugars) leads to a complex array ofcarbohydrates, of which ribose is a minor unstable com-ponent. Without phosphate and ribose, RNA moleculescould not have formed in the primitive soup. Thus, it ispossible that the RNA world itself was the end productof ancient metabolic pathways that evolved in unknownpre-RNA worlds, in which informational macromolec-ules with different backbones may have been endowedwith catalytic activity, i.e. with phenotype and genotypealso residing in the same molecules, so that the synthesisof neither protein nor related catalysts is necessary(Lazcano and Miller 1996).

The chemical nature of the first genetic polymers andthe catalytic agents that may have formed the pre-RNAworlds are completely unknown and can only be sur-mised. Modified nucleic acid backbones have been syn-thesized, which either incorporate a different version ofribose or lack it altogether. Experiments on nucleic acidwith hexoses instead of pentoses, and on pyranosesinstead of furanose (Eschenmoser 1994), suggest that awide variety of informational polymers is possible, evenwhen restricted to sugar-phosphate backbones.

One possibility that has not been explored is that the

backbone of the original informational macromoleculesmay have been atactic (e.g. disordered) kerogen-likepolymers such as those formed in some prebiotic simula-tions. There are other possible substitutes for ribose,including open chain, flexible molecules that lack asym-metric carbons. One of the most interesting chemicalmodels for a possible precursor to RNA involves the so-called peptide nucleic acids (PNAs), which have aprotein-like backbone of achiral 2-amino-ethyl-glycine,to which nucleic acid bases are attached by an acetic acid(Nielsen 1993). Such molecules form very stable com-plementary duplexes, both with themselves and withnucleic acids. Although they lack ribose, their functionalgroups are basically the same as in RNA, so they mayalso be endowed with catalytic activity.

Although the identification of adenine, guanine, anduracil in the Murchison meteorite supports the idea thatthese bases were present in the primitive environment(Miller 1993; Chyba and McDonald 1995), it is prob-able that other heterocycles capable of forming non-standard hydrogen bonding were also available. The Watson–Crick base-pair geometry permits morethan the four usual nucleobases, and simpler geneticpolymers may not only have lacked the sugar-phosphatebackbones, but may also have depended on alternativenon-standard hydrogen bonding patterns. The searchfor experimental models of pre-RNA polymers will berewarding but difficult; it requires the identification ofpotentially prebiotic components and the demonstrationof their non-enzymatic template-dependent polymeriza-tion, as well as coherent descriptions of how they mayhave catalysed the transition to an RNA world.

Questions for future research

Even though considerable progress has been made inunderstanding the emergence and early evolution of life,major uncertainties remain. The chemistry of some pre-biotic simulations is robust and supported by meteoriteanalyses, but the gap between these rudimentary experi-ments and the simplest extant cell is enormous. There isa range of issues relevant to the origin of life, many ofwhich cut across different scientific fields. The geo-chemical environments under which prebiotic synthesesof biochemical monomers and their polymers couldhave taken place need to be characterized. Experimentalsystems to study polymer replication, sequestration oforganic compounds, the energy sources that may have been employed by the first replicating systems, andthe appearance of metabolic pathways all need to bedeveloped.

The origin of the main features of the genetic code is not understood, but the discovery of the catalyticactivity of RNA molecules and the development of novelRNA enzymes through in vitro evolution has given

1.1 Early Life 7

considerable support to the idea that the primitive translation apparatus may have been shaped, at least inpart, by interactions between amino acids of prebioticorigin and polyribonucleotides (Gesteland et al. 1999).If the current interpretation of the evolutionarysignificance of these and other properties of RNA mol-ecules is correct, then one of the central issues thatorigin-of-life research must confront is the understand-ing of the processes that led from the primitive soup intoRNA-based life forms. The search for simple organicreplicating polymers will play a central role in thisinquiry. Even if the appearance of life remains an elusiveissue, redefining the questions that need to be addressedto understand how it took place is, in itself, an encourag-ing scientific achievement.

References

Brack, A., ed. (1998) The molecular origins of life: assemblingpieces of the puzzle. Cambridge University Press, New York.

Chyba, C.F. and McDonald, G.D. (1995) The origin of life in the Solar System: current issues. Annual Review of Earth andPlanetary Sciences 23, 215–249.

Deamer, D.W. and Fleischaker, G.R., eds. (1994) Origins of life:the central concepts. Jones and Bartlett, Boston.

de Duve, C. (1995) Vital dust: life as a cosmic imperative. BasicBooks, New York.

Eschenmoser, A. (1994) Chemistry of potentially prebiologicalnatural products. Origins of Life and Evolution of the Biosphere24, 389–423.

Gesteland, R.F., Cech, T. and Atkins, J.F., eds. (1999) The RNAWorld II. CSHL Press, Cold Spring Harbor.

Glavin, D.P. and Bada, J.L. (1999) The sublimation and sur-vival of amino acids and nucleobases in the Murchison meteorite during a simulated atmospheric entry heatingevent. In: Abstracts of the 12th International Conference on the Origin of Life (11–16 July 1999), p. 108. San Diego, California.

Huber, C. and Wächtershäuser, G. (1998) Peptides by activationof amino acids with CO on (Ni, Fe) S surfaces and implica-tions for the origin of life. Science 281, 670–672.

Kamminga, H. (1991) The origin of life on Earth: theory, history,and method. Uroboros 1, 95–110.

Lazcano, A. and Miller, S.L. (1996) The origin and early evolu-tion of life: prebiotic chemistry, the pre-RNAworld, and time.Cell 85, 793–798.

Maden, B.E.H. (1995) No soup for starters? Autotrophy andorigins of metabolism. Trends in Biochemical Sciences 20,337–341.

Miller, S.L. (1993) The prebiotic synthesis of organic compounds on the early Earth. In: M.H. Engel and S.A.Macko, eds. Organic geochemistry, pp. 625–637. Plenum Press,New York.

Mojzsis, S.J., Arrhenius, G., McKeegan, K.D., Harrison, T.M.,Nutman, A.P. and Friend, C.R.L. (1996) Evidence for lifebefore 3,800 million years ago. Nature 384, 55–59.

Nielsen, P.E. (1993) Peptide nucleic acid (PNA): a model struc-ture for the primordial genetic material? Origins of Life andEvolution of the Biosphere 23, 323–327.

Orgel, L.E. (1992) Molecular replication. Nature 358, 203–209.Schopf, J.W. (1993) Microfossils of the early Archean Apex

chert: new evidence of the antiquity of life. Science 260,640–646.

Wächtershäuser, G. (1988) Before enzymes and templates:theory of surface metabolism. Microbiological Reviews 52,452–484.

1.1.2 Exploring for a Fossil Record ofExtraterrestrial Life

J .D. FARMER

Introduction

While speculation about the possibility of life elsewherein the Cosmos has been a persistent theme throughoutthe history of humankind, the last decade of the twen-tieth century has witnessed a number of importantadvances in our understanding of the nature and evolu-tion of terrestrial life. These developments have openedup important new possibilities for the existence of livingsystems elsewhere in the Solar System (or beyond) andhave spawned a new interdisciplinary science called‘astrobiology’ — the study of the origin, evolution, distri-bution, and destiny of life in the Cosmos. This new disci-pline embraces the traditional field of exobiology, whichfocuses on the origin of life and early biosphere evolu-tion, along with a newer sister discipline, exopalaeontol-ogy, which seeks evidence for a fossil record of ancientlife or prebiotic chemistry in extraterrestrial materials, orfrom other planets in the Solar System.

An important legacy of the Apollo space missions was the development of a detailed cratering history forthe moon. This led to the view that during early accre-tion, prior to ª4.4Ga, surface conditions on Earth wereunfavourable for the origin of life (Chang 1994). As aconsequence of frequent giant impacts, magma oceanscould have been widespread over the Earth’s surface,and volatile compounds, including water and the bio-genic elements needed for life’s origin, would have been lost to space. Models of early accretion suggest that during the interval 4.4–4.2Ga impact rates andobject sizes declined to a point where the water (andassociated organics) delivered to the Earth by volatile-rich impactors (e.g. comets) was retained. A stableatmosphere and oceans probably developed during this time, providing the first suitable environments forprebiotic chemical evolution and the origin of life.

8 1 Major Events in the History of Life

Models also suggest that early biosphere developmentoverlapped with one or more late, giant impacts thatwere large enough to volatilize the oceans and perhapssterilize surface environments (Sleep et al. 1989). Suchevents would have frustrated the development of theearly biosphere and may have even required that lifeoriginate more than once. The most protected habitatduring this early period would have been the deep subsurface.

Discoveries of ª3.45Ga cellular microfossils fromcherts in volcanic sequences in Western Australia(Schopf 1993), and possible 3.86Ga chemofossils (carbonisotopic signatures) from phosphate-rich metasedimentsin Greenland (Mojzsis et al. 1996) indicate that once theconditions necessary for life’s origin were in place, lifearose very quickly, perhaps in a few hundred millionyears or less. This observation significantly improves thepossibility that life originated on Mars, or elsewhere inthe Solar System where habitable zones of liquid surfacewater were more ephemeral features of early planetaryevolution.

While recent discoveries in Precambrian palaeontol-ogy have pushed back the dates for the oldest fossils,molecular phylogenies have also provided importantclues about the origin and early evolution of life onEarth, based on the historical record preserved in thegenomes of living organisms. Comparisons of geneticsequences in 16S ribosomal RNA indicate that terrestriallife is subdivided into three major domains: the Archaea,the Bacteria, and the Eukarya. It is also apparent that the vast proportion of biodiversity on Earth is microbial.Higher forms of multicellular life appeared quite late in Earth history and make up only a tiny fraction of the total number of species. The deepest branching lineages in the RNA tree are high-temperature forms that utilize reduced inorganic substrates, like sulphur or hydrogen. This suggests that the last common ancestor of life on Earth was a high-temperature (‘ther-mophilic’) chemotroph, a view that is consistent with thehigher rates of heat flow, volcanism, and frequentimpacts that prevailed on the early Earth. However, theRNA tree may reveal little about life’s origin (see Section1.1.1). The thermophilic properties of the most deeplyrooted lineages may simply be a legacy of late giantimpacts that eliminated all but the highest temperaturespecies.

Possible extant life on Mars and Europa

The discovery of an extensive subsurface biosphere onthe Earth opened up exciting new possibilities for theexistence of habitable zones elsewhere in the SolarSystem. On Earth, subsurface habitats harbour manyspecies that are capable of synthesizing organic mol-ecules from simple inorganic substrates. The subsurface

is the most compelling environment for extant Martianlife because of the possibility that a deep subsurfaceground water system may exist at several kilometresdepth (Carr 1996). In addition, results from the Galileomission provide support for the existence of a subsurfaceocean beneath the crust of Europa, one of Jupiter’smoons. It is postulated that heating of the moon’s inter-ior by tidal friction could sustain a subcrustal ocean ofliquid water, and sea floor hydrothermal systems (Beltonet al. 1996). Indeed, the complexly fractured and largelyuncratered surface of Europa (Fig. 1.1.2.1) indicates anactive ice ‘tectonics’ involving the periodic upflow of ice-brines from beneath the Europan crust. It is possible thatwhere water welled up from below, it carried life formsor prebiotic chemistry from the underlying ocean andincorporated these materials into surface ices. Terrestrialmicrobes are known to retain viability at subzero tem-peratures by exploiting thin films of brine on grain surfaces in permafrost soils. Could viable organisms be present within similar ice-brine environments onEuropa? Viability arguments aside, ice could alsoprovide a means for the prolonged cryopreservation oforganic materials, accessible to robotic landers.

Exploring for an ancient Martian biosphere

The Viking lander missions showed the present surfaceenvironment of Mars to be unfavourable for life due tothe absence of liquid water, intense UV radiation, andoxidizing soils. At the same time, images obtained fromMars orbit revealed the early planet to be more Earth-like, with a broad range of surface environments suitablefor life. It is likely that habitable environments disap-peared from the surface ª3.8Ga as Mars began to lose its atmosphere (Farmer and Des Marais 1999). If extantlife exists on Mars today, it is likely to be in deep subsur-face environments that will be inaccessible to roboticplatforms. Deep subsurface drilling will likely require a human presence. However, if life once existed insurface environments, it is likely to have left behind afossil record in ancient sediments now exposed at thesurface. Such deposits could be accessed during therobotic phase of exploration. This simple concept under-lies the basic rationale of the present Mars explorationprogramme.

Studies of the Precambrian fossil record on Earth, andof modern microbial systems that are analogues forthose on the early Earth and Mars, provide a conceptualframework for guiding the search for a fossil record onMars. An understanding of how preservation variesbetween different groups of microorganisms overextremes of the environment, and how postdepositional,diagenetic changes affect the long-term preservation ofmicrobial biosignatures in rocks, is crucial (Farmer andDes Marais 1999). Such studies allow the formulation of

1.1 Early Life 9

‘rules’ of preservation that help optimize strategies toexplore for past life on Mars and other planetary bodies,such as Europa.

As with Earth-based palaeontology, site selection iscrucial for the successful implementation of Mars mis-sions designed to explore for past life. Preservation is a selective process that is strongly dependent upon the biogeological environment. Studies of microbial fossilization reveal that the rapid entombment ofmicroorganisms and their by-products by fine-grained,clay-rich sediments and/or chemical precipitates is of singular importance in enhancing preservation.Favourable geological environments are those wheremicrobial systems coexist with high rates of fine-graineddetrital sedimentation, and/or aqueous mineral pre-cipitation. Examples include rapidly mineralizinghydrothermal systems (below the upper temperaturelimit for life), terminal lake basins (where chemical sediments such as evaporites, fine-grained lacustrinesediments, and sublacustrine cold spring tufas aredeposited), and mineralizing soils (e.g. hard-pans,including calcretes, ferracretes, and silcretes). Even if lifedid not develop on Mars, this exploration strategy is stillimportant because the same sedimentary environmentscould preserve a record of prebiotic chemistry similar tothat which spawned the development of life on Earth.This early prebiotic history has been lost from the terres-trial record.

Mars may preserve the most complete record of early

events of planetary evolution anywhere in the SolarSystem. The 4.56Ga age of Martian meteorite ALH 84001(McKay et al. 1996) indicates that the ancient, heavilycratered highlands of Mars contain a crustal recordextending back to the earliest period of planetary evolu-tion. On Earth, comparably aged crustal sequences havebeen destroyed by tectonic cycling, metamorphism,weathering, and erosion. In contrast, Mars never developed a plate tectonic cycle and extensive water-mediated weathering and erosion was probably limitedto the first billion years or so of the planet’s history. Geomorphic features suggest that surface hydrologicalsystems were active until near the end of heavy bom-bardment (ª3.8Ga), after which time liquid waterquickly disappeared from the surface, presumably as aresult of the loss of the Martian atmosphere (Carr 1996).

The preservation of fossil biosignatures is favouredwhen organisms or their by-products are incorporatedinto low permeability sedimentary deposits (producinga closed chemical system during diagenesis) of stablemineralogy (promoting a prolonged residence time inthe crust). Chemical sediments composed of silica, phos-phate, and carbonate, along with fine-grained, clay-richdetrital sediments and water-deposited volcanic ash, are especially favourable lithologies for long-termpreservation. This is illustrated by the fact that on Earthmost of the Precambrian record is preserved in suchlithologies.

Many potential sites for a fossil record have been

10 1 Major Events in the History of Life

Fig. 1.1.2.1 (a) Galileo orbiter image of the surface of Europa,one of the moons of Jupiter. The surface crust is composed ofwater ice that has been fractured into irregular blocks. Thefracture patterns suggest that the crust was mobilized by alayer of subsurface water which flowed up from below, fillingfractures between blocks as they separated. Such observationssupport the view that Europa once had, and perhaps still has, asubcrustal ocean of liquid water that could sustain life or

prebiotic chemistry. The smallest features visible in this imageare about 20 m across. (b) Close-up of the surface of Europashowing a complex network of ridged fractures originallyformed when plates of ice crust pulled apart. Many ridgesegments were later offset along strike–slip faults. The largeridge in the lower right corner of the image is about 1kmacross. (Photographs by courtesy of NASA.)

identified on Mars using orbital photographs obtainedby Viking (e.g. Fig. 1.1.2.2). However, information aboutthe mineralogical composition of the Martian surface isstill lacking. Mineralogy provides important clues aboutthe palaeoenvironment , information needed to deter-mine the best sites for detailed surface exploration. Animportant exploration goal is to identify aqueousmineral assemblages (of the types that commonlycapture and preserve fossil biosignatures) from orbitusing spectral mapping methods prior to landed mis-sions. In targeting sites for sample return, evaporativelake basins and hydrothermal sites are given a high pri-ority. In terrestrial settings, the deposits formed in theseenvironments frequently provide optimal conditions forpreservation.

Putative signs of life in a Martian meteorite

The report of possible fossil signatures in Martian met-

eorite Allan Hills 84001 (McKay et al. 1996) generated anintense, ongoing debate over the usefulness of a varietyof morphological, mineralogical, and geochemical datafor detecting biosignatures in ancient rocks. Subsequentwork by the broader scientific community indicates thatthe major lines of evidence used to support the biologicalhypothesis for ALH 84001 are more easily explained byinorganic processes.

Polycyclic aromatic hydrocarbons (PAHs), such asthose found in ALH 84001, are not generally regarded asbeing diagnostic of life. In addition, it has been shownthat a major fraction of the organic matter present in themeteorite exhibits radiocarbon activity, indicating that itoriginated through terrestrial contamination after reach-ing the Earth (Jull et al. 1998). Although a small fractionof remaining organic matter could be Martian, it has notyet been characterized.

A key test of the biological hypothesis for ALH 84001is the formation temperature of the carbonates that

1.1 Early Life 11

Fig. 1.1.2.2 (a) Gusev Crater, Mars. A large river canyon to thesouth (Ma’adim Vallis) drained into this ª 150 km diametercrater, depositing a delta where it entered the crater. Geologicalstudies suggest a prolonged hydrological history for thisregion of Mars, with the Gusev Crater being the site of anancient palaeolake system. (b) The slopes of Hadriaca Patera,an ancient Martian volcano, show channels radiatingdownslope, away from the caldera rim (caldera ª 75 kmacross). These small channels are interpreted to be the result of

pyroclastic flows, the channels being subsequently enlarged bysapping flow. The basal slope of Hadriaca Patera was latereroded by outfloods of subsurface water which carved DaoVallis, a large channel located near the bottom of thephotograph (channel ª 45 km wide). The association ofsubsurface water and a heat source (the subsurface magmathat produced the volcano) suggests the potential for sustainedhydrothermal activity in this region. (Photographs by courtesyof NASA.)

contain the putative fossil evidence. Carbon and oxygenisotope measurements obtained for carbonates in theAlan Hills meteorite indicate a wide range of formationtemperatures, the lowest falling within the range for life(<120°C). Because the carbonates experienced multipleshock events, each with highly localized effects, thespread of isotopic values is perhaps not surprising.However, the lowest temperature estimates are likely tobe primary, having been least affected by shock meta-morphism (Treiman and Romanek 1998).

Magnetite grains present in the rims of the ALH 84001carbonates (Fig. 1.1.2.3b) were compared to intracellularmagnetite crystals (‘magnetosomes’) formed by terres-trial magnetotactic bacteria. However, ultrastructuralfeatures (spiral defects) discovered in some of the ALH84001 magnetites suggest that they were formed byvapour deposition at high temperatures. In addition, theALH 84001 magnetites exhibit epitaxial growth relation-ships with the host carbonate, and are therefore unlikelyto have formed within the cells of bacteria (Bradley et al.1998).

Nanometre-scale morphologies having shapes similarto microbes were observed on some fracture surfaces ofcarbonates in the ALH 84001 meteorite (Fig. 1.1.2.3a).These were compared to terrestrial ‘nanobacteria’. Thisis an informal term used to describe small (<0.1mm) rodsand spheroids found in rocks which resemble spores orresting stages of microorganisms (see Kirkland et al.1999). At this observational scale, problems often arise indistinguishing biological structures from inorganic

forms which originate by self-organizing crystal growth,or as artefacts created during the application of crystalline metal coatings used to prepare samples for scanning electron microscopy (SEM). The putativemicrofossils in the ALH 84001 meteorite have subse-quently been explained by a combination of the aboveprocesses. At the nanometre scale, shape is clearly a poor criterion for biogenicity. In the absence of othertypes of compelling evidence, it is probably best to avoidthe use of the term ‘nanobacteria’, and adopt instead anon-genetic descriptive term, like ‘nanostructures’,which does not imply an origin.

The apparent refutation of the biological hypothesisfor the ALH 84001 meteorite leaves the question ofMartian life unresolved. Answering this question islikely to require the careful in situ study of Martiansamples that formed under aqueous conditions thatwere favourable for the rapid capture and long-termpreservation of biosignatures. Given the difficulty of rec-ognizing ancient microbial signatures in rocks, thereturn of samples to the Earth for analysis in specializedlaboratories may be required for an adequate test of thelife hypothesis. The careful re-examination of biologicalevidence for the ALH 84001 meteorite has improved thebasis for interpreting the Precambrian record on Earth byestablishing more rigorous standards for biogenicity inancient materials. The broadly based effort has alsohelped to prepare the scientific community for a series ofMars sample return missions tentatively scheduled tobegin in 2009.

12 1 Major Events in the History of Life

Fig. 1.1.2.3 (a) Scanning electron micrograph ofnanostructures found on fracture surfaces of carbonateminerals in Martian meteorite, ALH 84001. The elongatedstructure in the centre of the image is ª 2 mm long and consistsof a series of smaller segments each ª 0.1 mm wide. (b)Transmission electron micrograph showing small magnetite

grains found within carbonate minerals of ALH 84001. Themagnetite grains average 15–20 nm wide. Magnetitecrystallites in ALH 84001 exhibit epitaxial relationships withthe host carbonate grains and screw dislocations suggestive ofvapour-phase deposition. (Photographs by courtesy of theLunar Planetary Institute.)