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Assembling the Tree of Life

Joel CracraftMichael J. Donoghue,

Editors

OXFORD UNIVERSITY PRESS

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Assembling the Tree of LifeEDITED BY Joel Cracraft

Michael J. Donoghue

12004

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Library of Congress Cataloging-in-Publication DataAssembling the tree of life / edited by Joel Cracraft, Michael J. Donoghue.p. cm.Proceedings of a symposium held at the American Museum of Natural History in New York, 2002.Includes bibliographical references and index.ISBN 0-19-517234-51. Biology—Classification—Congresses. I. Cracraft, Joel. II. Donoghue, Michael J.QH83.A86 2004578'.01'2—dc22 2003058012

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Contents

Contributors ix

Introduction: Charting the Tree of Life 1Michael J. Donoghue and Joel Cracraft

I The Importance of Knowing the Tree of Life

1 The Importance of the Tree of Life to Society 7Terry L. Yates, Jorge Salazar-Bravo, and Jerry W. Dragoo

2 A Tangled Bank: Reflections on the Tree of Life and Human Health 18Rita R. Colwell

3 The Fruit of the Tree of Life: Insights into Evolution and Ecology 25Douglas J. Futuyma

II The Origin and Radiation of Life on Earth

4 The Tree of Life: An Overview 43S. L. Baldauf, D. Bhattacharya, J. Cockrill, P. Hugenholtz, J. Pawlowski, and A. G. B. Simpson

5 The Early Branches in the Tree of Life 76Norman R. Pace

6 Bacteria and Archaea 86W. Ford Doolittle

7 The Origin and Radiation of Eucaryotes 95Hervé Philippe

8 Viruses and the Tree of Life 107David P. Mindell, Joshua S. Rest, and Luis P. Villarreal

III The Relationships of Green Plants

9 Algal Evolution and the Early Radiation of Green Plants 121Charles F. Delwiche, Robert A. Andersen, Debashish Bhattacharya, Brent D. Mishler,

and Richard M. McCourt

10 The Radiation of Vascular Plants 138Kathleen M. Pryer, Harald Schneider, and Susana Magallón

11 The Diversification of Flowering Plants 154Pamela S. Soltis, Douglas E. Soltis, Mark W. Chase, Peter K. Endress, and Peter R. Crane

IV The Relationships of Fungi

12 The Fungi 171John W. Taylor, Joseph Spatafora, Kerry O’Donnell, François Lutzoni, Timothy James,

David S. Hibbett, David Geiser, Thomas D. Bruns, and Meredith Blackwell

V The Relationships of Animals: Overview

13 The History of Animals 197Douglas J. Eernisse and Kevin J. Peterson

14 Protostomes and Platyhelminthes: The Worm’s Turn 209D. Timothy J. Littlewood, Maximilian J. Telford, and Rodney A. Bray

VI The Relationships of Animals: Lophotrochozoans

15 Toward a Tree of Life for Annelida 237Mark E. Siddall, Elizabeth Borda, and Gregory W. Rouse

16 The Mollusca: Relationships and Patterns from Their First Half-Billion Years 252David R. Lindberg, Winston F. Ponder, and Gerhard Haszprunar

VII The Relationships of Animals: Ecdysozoans

17 Arthropod Systematics: The Comparative Study of Genomic, Anatomical, andPaleontological Information 281Ward C. Wheeler, Gonzalo Giribet, and Gregory D. Edgecombe

18 Arachnida 296Jonathan A. Coddington, Gonzalo Giribet, Mark S. Harvey, Lorenzo Prendini, and David E. Walter

19 Are the Crustaceans Monophyletic? 319Frederick R. Schram and Stefan Koenemann

20 Phylogenetic Relationships and Evolution of Insects 330Rainer Willmann

21 Phylogeny of the Holometabolous Insects: The Most Successful Groupof Terrestrial Organisms 345Michael F. Whiting

VIII The Relationships of Animals: Deuterostomes

22 From Bilateral Symmetry to Pentaradiality: The Phylogeny of Hemichordatesand Echinoderms 365Andrew B. Smith, Kevin J. Peterson, Gregory Wray, and D. T. J. Littlewood

23 Chordate Phylogeny and Development 384Timothy Rowe

vi Contents

24 Gnathostome Fishes 410M. L. J. Stiassny, E. O. Wiley, G. D. Johnson, and M. R. de Carvalho

25 Amphibians: Leading a Life of Slime 430David Cannatella and David M. Hillis

26 Resolving Reptile Relationships: Molecular and Morphological Markers 451Michael S. Y. Lee, Tod W. Reeder, Joseph B. Slowinski, and Robin Lawson

27 Phylogenetic Relationships among Modern Birds (Neornithes): Toward an AvianTree of Life 468Joel Cracraft, F. Keith Barker, Michael Braun, John Harshman, Gareth J. Dyke, Julie Feinstein,

Scott Stanley, Alice Cibois, Peter Schikler, Pamela Beresford, Jaime García-Moreno,

Michael D. Sorenson, Tamaki Yuri, and David P. Mindell

28 Building the Mammalian Sector of the Tree of Life: Combining Different Dataand a Discussion of Divergence Times for Placental Mammals 490Maureen A. O’Leary, Marc Allard, Michael J. Novacek, Jin Meng, and John Gatesy

29 Human Origins: Life at the Top of the Tree 517Bernard Wood and Paul Constantino

IX Perspectives on the Tree of Life

30 The Meaning of Biodiversity and the Tree of Life 539Edward O. Wilson

31 A Tree Grows in Manhattan 543David B. Wake

32 The Tree of Life and the Grand Synthesis of Biology 545David M. Hillis

33 Immeasurable Progress on the Tree of Life 548Michael J. Donoghue

34 Assembling the Tree of Life: Where We Stand at the Beginningof the 21st Century 553Joel Cracraft and Michael J. Donoghue

Index 563

Contents vii

Marc AllardDepartment of Biological ScienceThe George Washington UniversityWashington, DC 20052

Robert A. AndersenBigelow Laboratory for Ocean

SciencesW. Boothbay Harbor, ME 04575

S. L. BaldaufDepartment of BiologyUniversity of YorkP.O. Box 373York YO10 5YWEngland, UK

F. Keith BarkerJames Ford Bell Museum of Natural

HistoryUniversity of Minnesota1987 Upper Buford CircleSt. Paul, MN 55108

Pamela BeresfordPercy FitPatrick InstituteUniversity of Cape TownRondebosch 7701Republic of South Africa

Debashish BhattacharyaDepartment of Biological SciencesUniversity of IowaIowa City, IA 52242–1324

Meredith BlackwellDepartment of Biological SciencesLouisiana State UniversityBaton Rouge, LA 70803

Elizabeth BordaDivision of Invertebrate ZoologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

Michael BraunLaboratory of Analytical BiologyDepartment of Systematic BiologySmithsonian Institution4210 Silver Hill RoadSuitland, MD 20746

Rodney A. BrayParasitic Worms DivisionDepartment of ZoologyThe Natural History MuseumCromwell RoadLondon SW7 5BDEngland, UK

Contributors

Thomas D. BrunsPlant and Microbial BiologyUniversity of CaliforniaBerkeley, CA 94720

David CannatellaDepartment of Integrative BiologyUniversity of TexasAustin, TX 78712

M. R. de CarvalhoDepartamento de Biologia–FFCLRPUniversidade de São PauloRibeirão PretoBrazil

Mark W. ChaseJodrell LaboratoryRoyal Botanic GardensKew, RichmondSurrey TW9 3DSEngland, UK

Alice CiboisDepartment of Mammalogy and

OrnithologyNatural History Museum of GenevaCP 64341211 Geneva 6Switzerland

ix

J. CockrillDepartment of BiologyUniversity of YorkP.O. Box 373York YO10 5YWEngland, UK

Jonathan A. CoddingtonDepartment of Systematic BiologyNational Museum of Natural HistorySmithsonian InstitutionWashington, DC 20560

Rita R. ColwellDirectorNational Science FoundationArlington, VA 22230

Paul ConstantinoDepartment of AnthropologyThe George Washington University2110 G Street NWWashington, DC 20052

Joel CracraftDepartment of OrnithologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

Peter R. CraneRoyal Botanic GardensKew, RichmondSurrey TW9 3ABEngland, UK

Charles F. DelwicheDepartment of Cell Biology and

Molecular GeneticsUniversity of Maryland College ParkCollege Park, MD 20742-5815

Michael J. DonoghueDepartment of Ecology and Evolution-

ary BiologyYale UniversityNew Haven, CT 06520

W. Ford DoolittleCanadian Institute for Advanced

ResearchDepartment of Biochemistry and

Molecular BiologyDalhousie UniversityHalifax, Nova ScotiaCanada B3H 4H7

Jerry W. DragooDepartment of Biology andMuseum of Southwestern BiologyUniversity of New MexicoAlbuquerque, NM 87131

Gareth J. DykeDepartment of ZoologyUniversity College DublinBelfield, Dublin 4Ireland

Gregory D. EdgecombeAustralian Museum6 College StreetSydney, New South Wales 2010Australia

Douglas J. EernisseDepartment of Biological ScienceCalifornia State UniversityFullerton, CA 92834

Peter K. EndressInstitute of Systematic BotanyUniversity of ZurichZurichSwitzerland

Julie FeinsteinDepartment of OrnithologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

Douglas J. FutuymaDepartment of Ecology and

Evolutionary BiologyUniversity of MichiganAnn Arbor, MI 48109-1079

Jaime García-MorenoMax Planck Research Centre for

Ornithology and University ofKonstanz

Schlossalleé 2D-78315 RadolfzellGermany

John GatesyDepartment of BiologyUniversity of California-RiversideRiverside, CA 92521

David GeiserPlant PathologyPennsylvania State UniversityUniversity Park, PA 16804

Gonzalo GiribetDepartment of Organismic and

Evolutionary Biology, and Museumof Comparative Zoology

Harvard University16 Divinity AvenueCambridge, MA 02138

John Harshman4869 Pepperwood WaySan Jose, CA 95124

Mark S. HarveyDepartment of Terrestrial Inverte-

bratesWestern Australian MuseumFrancis StreetPerth, Western Australia 6000Australia

Gerhard HaszprunarZoologischen Staatssammlung

MünchenMünchhausenstrasse 2781247 MunichGermany

David S. HibbettDepartment of BiologyClark UniversityWorcester, MA 01610

David M. HillisSection of Integrative Biology and

Center for Computational Biologyand Bioinformatics

University of TexasAustin, TX 78712

P. HugenholtzComBinE GroupAdvanced Computational Modelling

CentreThe University of QueenslandBrisbane 4072Australia

Timothy JamesDepartment of BiologyDuke UniversityDurham, NC 27708

x Contributors

G. D. JohnsonDivision of FishesNational Museum of Natural HistoryWashington, DC 20560

Stefan KoenemannInstitute for Biodiversity and Ecosys-

tem DynamicsUniversity of AmsterdamMauritskade 611092 AD AmsterdamThe Netherlands

Robin LawsonDepartment of HerpetologyCalifornia Academy of SciencesGolden Gate ParkSan Francisco, CA 94118-4599

Michael S. Y. LeeDepartment of Environmental Biology,

University of AdelaideDepartment of Palaeontology, South

Australian MuseumAdelaide, SA 5000Australia

David R. LindbergMuseum of Paleontology1101 Valley Life Science BuildingUniversity of CaliforniaBerkeley, CA 94720-4780

D. Timothy J. LittlewoodParasitic Worms DivisionDepartment of ZoologyThe Natural History MuseumCromwell RoadLondon SW7 5BDEngland, UK

François LutzoniDepartment of BiologyDuke UniversityDurham, NC 27708

Susana MagallónDepartemento de Botánica, Instituto

de BiologíaUniversidad Nacional Autónoma de

MéxicoCircuito Exterior, Anexo al Jardín

BotánicoAP 70–233México DF 04510

Richard M. McCourtDepartment of BotanyAcademy of Natural SciencesPhiladelphia, PA 19103

Jin MengDivision of PaleontologyAmerican Museum of Natural History79th Street at Central Park WestNew York, NY 10024-5192

David P. MindellDepartment of Ecology and Evolution-

ary Biology and Museum ofZoology

University of MichiganAnn Arbor, MI 48109-1079

Brent D. MishlerDepartment of Integrative BiologyUniversity of California BerkeleyBerkeley, CA 94720

Michael J. NovacekDivision of PaleontologyAmerican Museum of Natural History79th Street at Central Park WestNew York, NY 10024-5192

Kerry O’DonnellNational Center for Agricultural

Utilization ResearchAgriculture Research Service1815 N. University StreetPeoria, IL 61604

Maureen A. O’LearyDepartment of Anatomical SciencesHSC T-8 (040)Stony Brook UniversityStony Brook, NY 11794-8081

Norman R. PaceDepartment of Molecular, Cellular

and Developmental BiologyCampus Box 0347University of ColoradoBoulder, CO 80309-0347

J. PawlowskiDepartment of Zoology and Animal

BiologyUniversity of Geneva1224 Chêne-Bougeries/GenevaSwitzerland

Kevin J. PetersonDepartment of Biological SciencesDartmouth CollegeHanover, NH 03755

Hervé PhilippeDépartement de BiochimieUniversité de MontréalPavillon principal—Bureau F-315C. P. 6128 Succursale Centre-VilleMontréal, QuebecCanada H3C 3J7

Winston F. PonderDivision of Invertebrate ZoologyAustralian MuseumSydney, NSW 2010Australia

Lorenzo PrendiniDivision Invertebrate ZoologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

Kathleen M. PryerDepartment of BiologyDuke UniversityDurham, NC 27708

Tod W. ReederDepartment of BiologySan Diego State UniversitySan Diego, CA 92182-4614

Joshua S. RestDepartment of Ecology and

Evolutionary Biology and Museumof Zoology

University of MichiganAnn Arbor, MI 48109-1079

Gregory W. RouseSouth Australian MuseumAdelaide, SA 5000Australia

Timothy RoweJackson School of Geosciences, C1100The University of Texas at AustinAustin, TX 78712

Contributors xi

Jorge Salazar-BravoDepartment of Biology and Museum

of Southwestern BiologyUniversity of New MexicoAlbuquerque, NM 87131

Peter SchiklerDepartment of OrnithologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

Harald SchneiderAlbrecht-von-Haller-Institut für

PflanzenwissenschaftenAbteilung Systematische BotanikGeorg-August-Universität GöttingenUntere Karspüle 237073 GöttingenGermany

Frederick R. SchramInstitute for Biodiversity and

Ecosystem DynamicsUniversity of AmsterdamMauritskade 611092 AD AmsterdamThe Netherlands

Mark E. SiddallDivision of Invertebrate ZoologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

A. G. B. SimpsonCanadian Institute for Advanced

ResearchDepartment of Biochemistry and

Molecular BiologyDalhousie UniversityHalifax, Nova ScotiaCanada B3H 4H7

Joseph B. Slowinski (deceased)Department of HerpetologyCalifornia Academy of SciencesGolden Gate ParkSan Francisco, CA 94118-4599

Andrew B. SmithDepartment of PalaeontologyThe Natural History MuseumCromwell RoadLondon SW7 5BDEngland, UK

Douglas E. SoltisDepartment of BotanyUniversity of FloridaGainesville, FL 32611

Pamela S. SoltisFlorida Museum of Natural HistoryUniversity of FloridaGainesville, FL 32611

Michael D. SorensonDepartment of BiologyBoston University5 Cummington StreetBoston, MA 02215

Joseph SpataforaBotany and Plant PathologyOregon State UniversityCorvallis, OR 97331

Scott Stanley411 Cary Pines DriveCary, NC 27513

M. L. J. StiassnyDepartment of IchthyologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024

John W. TaylorDepartment of Plant and Microbial

BiologyUniversity of CaliforniaBerkeley, CA 94720-3102

Maximilian J. TelfordUniversity Museum of ZoologyDepartment of ZoologyCambridge UniversityDowning StreetCambridge CB2 3EJEngland, UK

Luis P. VillarrealDepartment of Molecular Biology and

Biochemistry, and Center for VirusResearch

University of California at IrvineIrvine, CA 92697

David B. WakeMuseum of Vertebrate Zoology and

Department of Integrative BiologyUniversity of CaliforniaBerkeley, CA 94720-3160

David E. WalterDepartment of Biological SciencesUniversity of AlbertaEdmonton, ABCanada T6G 2E9

Ward C. WheelerDivision of Invertebrate ZoologyAmerican Museum of Natural HistoryCentral Park West at 79th StreetNew York, NY 10024-5192

Michael F. WhitingDepartment of Integrative BiologyBrigham Young UniversityProvo, UT 84042

E. O. WileyEcology and Evolutionary BiologyUniversity of KansasLawrence, KS 66045

Rainer WillmannZoologisches Institut der UniversitätGeorg-August-Universität GöttingenBerliner Strasse 28D-37073 GöttingenGermany

Edward O. WilsonDepartment of Organismic and

Evolutionary Biology and theMuseum of Comparative Zoology

Harvard University16 Divinity AvenueCambridge, MA 02138

Bernard WoodDepartment of AnthropologyThe George Washington University2110 G Street NWWashington, DC 20052

xii Contributors

Gregory WrayDepartment of BiologyDuke UniversityDurham, NC 27708

Terry L. YatesDepartment of Biology and Museum

of Southwestern BiologyUniversity of New MexicoAlbuquerque, NM 87131

Tamaki YuriLaboratory of Analytical BiologyDepartment of Systematic BiologySmithsonian Institution4210 Silver Hill RoadSuitland, MD 20746

Contributors xiii

1IntroductionCharting the Tree of Life

Michael J. Donoghue

Joel Cracraft

Many, perhaps even most, people today are comfortable withthe image of a tree as a representation of how species arerelated to one another. The Tree of Life has become, we think,one of the central images associated with life and with sci-ence in general, alongside the complementary metaphor ofthe ecological Web of Life. But this was not always the case.Before Darwin, the reigning view was perhaps that life wasorganized like a ladder or “chain of being,” with slimy “primi-tive” creatures at the bottom and people (what else!) at thevery top. Darwin (1859) solidified in our minds the radicallynew image of a tree (fig. I.1), within which humans are butone of many (as we now know, millions) of other speciessituated at the tips of the branches. The tree, it turns out, isthe natural image to convey ancestry and the splitting of lin-eages through time, and therefore is the natural frameworkfor “telling” the genealogical history of life on Earth.

Very soon after Darwin, interest in piecing together theentire Tree of Life began to flourish. Ernest Haeckel’s (1866)trees beautifully symbolize this very active period and also,through their artistry, highlight the comparison between realbotanical trees and branching diagrams representing phylo-genetic relationships (fig. I.2).

However, during this period, and indeed until the 1930s,rather little attention was paid to the logic of inferring howspecies (or the major branches of the Tree of Life) are relatedto one another. In part, the lack of a rigorous methodology(especially compared with the newly developing fields ofgenetics and experimental embryology) was responsible for

a noticeable lull in activity in this area during the first sev-eral decades of the 1900s. But, beginning in the 1930s, withsuch pioneers as the German botanist Walter Zimmermann(1931), we begin to see the emergence of the basic conceptsthat underlie current phylogenetic research. For example, thecentral notion of “phylogenetic relationship” was clearly de-fined in terms of recency of common ancestry—we say thattwo species are more closely related to one another than eitheris to a third species if and only if they share a more recentcommon ancestor (fig. I.3).

This period in the development of phylogenetic theoryculminated in the foundational work of the German ento-mologist Willi Hennig. Many of his central ideas were putforward in German in the 1950s (Hennig 1950), but world-wide attention was drawn to his work after the publicationof Phylogenetic Systematics in English (Hennig 1966). Hennigemphasized, among many other things, the desirability ofrecognizing only monophyletic groups (or clades—singlebranches of the Tree of Life) in classification systems, andthe idea that shared derived characteristics (what he calledsynapomorphies) provided critical evidence for the existenceof clades (fig. I.4).

Around this same time, in other circles, algorithms werebeing developed to try to compute the relatedness of spe-cies. Soon, a variety of computational methods were imple-mented and were applied to real data sets. Invariably, giventhe tools available in those early days, these were what wouldnow be viewed as extremely small problems.

1

2 Introduction

Figure I.1. The only illustration in Darwin’s Origin of Species (1859), which can be taken to bethe beginning of “tree thinking.”

Since that time major developments have occurred alongseveral lines. First, although morphological characters wereat first the sole source of evidence for phylogenetic analyses,molecular data, especially DNA sequences, have becomeavailable at an exponential rate. Today, many phylogeneticanalyses are carried out using molecular data alone. How-ever, morphological evidence is crucial in many cases, butespecially when the object is to include extinct species pre-served as fossils. Ultimately, of course, there are advantagesin analyzing all of the evidence deemed relevant to a particularphylogenetic problem—morphological and molecular. Andmany of our most robust conclusions about phylogeny, high-lighted in this volume, are based on a combination of datafrom a variety of sources.

A second major development has been increasing compu-tational power, and the ease with which we can now manipu-late and analyze extremely large phylogenetic data sets. Initially,such analyses were extremely cumbersome and time-consum-ing. Today, we can deal effectively and simultaneously withvast quantities of data from thousands of species.

Beginning in the 1990s these developments all came to-gether—the image and meaning of a tree, the underlying

conceptual and methodological developments, the ability toassemble massive quantities of data, and the ability to quan-titatively evaluate alternative phylogenetic hypotheses usinga variety of optimality criteria. Not surprisingly, the numberof published phylogenetic analysis skyrocketed (Hillis, ch.32 in this vol.). Although it is difficult to make an accurateassessment, in recent years phylogenetic studies have beenpublished at a rate of nearly 15 a day.

Where has this monumental increase in activity reallygotten us in terms of understanding the Tree of Life? Thatwas the question that motivated the symposium that we or-ganized in 2002 at the American Museum of Natural His-tory in New York, and which yielded the book you have infront of you. Although it may be apparent that there has beena lot of activity, and that a lot can now be written about thephylogeny of all the major lineages of life, it is difficult toconvey a sense of just how rapidly these findings have beenaccumulating. Previously, there was a similar attempt to pro-vide a summary statement across all of life—a Nobel sym-posium in Sweden in 1988, which culminated in a book titledThe Hierarchy of Life (Fernholm et al. 1989). That was anexciting time, and the enthusiasm and potential of this en-

Introduction 3

deavor were expressed in the chapters of that book. But, inlooking back at those pages we are struck by the paucity ofdata and the minuscule size of the analyses that were beingperformed at what was surely the cutting edge of research atthe time.

It is also clear that so much more of the Tree of Life isbeing explored today than only a decade ago. Now we canhonestly present a picture of the relationships among all ofthe major branches of the Tree of Life, and within at leastsome of these major branches we are now able to provide

considerable detail. A decade ago the holes in our knowledgewere ridiculously obvious—we were really just getting startedon the project. There are giant holes today, which will be-come increasingly obvious in the years to come (as we learnmore about species diversity, and database phylogeneticknowledge), but we believe that it is now realistic to conceiveof reconstructing the entire Tree of Life—eventually to in-clude all of the living and extinct species. A decade ago, wecould hardly conjure up such a dream. Today we not onlycan imagine what the results will look like, but we now be-lieve it is attainable.

It also has become increasingly obvious to us just howimportant it is to understand the structure of the Tree ofLife in detail. With the availability of better and better esti-mates of phylogeny, awareness has rapidly grown outsideof systematic biology that phylogenetic knowledge is es-sential for understanding the history of character changeand for interpreting comparative data of all sorts within ahistorical context. At the same time, phylogeny and thealgorithms used to build trees have taken on increasingimportance within applied biology, especially in managingour natural resources and in improving our own healthand well-being. Phylogenetic trees now commonly appearin journals that had not previously devoted much spaceto trees or to “tree thinking,” and many new tools havebeen developed to leverage this new information onrelationships.

Figure I.2. A phylogenetic tree realized by Haeckel (1866),soon after Darwin’s Origin.

Figure I.3. Zimmermann’s (1931) tree, illustrating the conceptof “phylogenetic relationship.”

Figure I.4. The conceptual phylogenetic argumentation schemeof Hennig (1966: 91), with solid boxes representing derived(apomorphic) and open boxes representing primitive(plesiomorphic) characters.

4 Introduction

In this volume we have tried, with the chapters in theopening and closing sections, to highlight the value of the Treeof Life, and then, in a series of chapters by leading experts, tosummarize the current state of affairs in many of its majorbranches. In presenting this information, we appreciate thatmany important groups are not covered in sufficient detail, anda few not at all, and we know that in some areas informationwill already be outdated. This is simply the nature of theprogress we are making—new clades are discovered literallyevery day—and the sign of a healthy discipline. Nevertheless,our sense is that a benchmark of our progress early in the 21stcentury is a worthy exercise, especially if it can help motivatethe vision and mobilize the resources to carry out the mega-science project that the Tree of Life presents. This would surelybe one of the most fundamental of all scientific accomplish-ments, with benefits that are abundantly evident already andsurprises whose impacts we can hardly imagine.

Acknowledgments

The rapidly expanding activity in phylogenetics noted above setthe stage for a consideration and critical evaluation of ourcurrent understanding of the Tree of Life. This juncture intime also coincided with the inception of the InternationalBiodiversity Observation Year (IBOY; available at http://www.nrel.colostate.edu/projects/iboy) by the internationalbiodiversity science program DIVERSITAS (http://www.diversitas-international.org) and its partners. Assembling theTree of Life (ATOL) was accepted as a key project of IBOY, anda symposium and publication were planned. This volume is theoutgrowth of that process.

The ATOL symposium would not have been possiblewithout the participation of many institutions and individuals.Key, of course, was the financial commitment received from thehost institutions, the American Museum of Natural History(AMNH) and Yale University, and from the International Unionof Biological Sciences (IUBS), a lead partner of DIVERSITAS andconvenor of Systematics Agenda 2000 International. Assemblingthe Tree of Life (ATOL) was accepted as a core project of theDIVERSITAS program, International Biodiversity ObservationYear (IBOY). We especially acknowledge the leadership of EllenFutter (president) and Michael Novacek (senior vice presidentand provost) of the AMNH and of Alison Richard (provost) ofYale University for making the symposium possible. In addition,a financial contribution from IUBS facilitated internationalattendance, and we are grateful to Marvalee Wake (president),Talal Younes (executive director), and Diana Wall (director,IBOY) for their support.

The scientific program of the symposium was planned withthe critical input of Michael Novacek and many other col-leagues, and we are grateful for their suggestions. Ultimately, wetried to cover as much of the Tree of Life as possible in threedays and at the same time to include plenary speakers whosecharge was to summarize the importance of phylogenetic

knowledge for science and society. We are well aware of theomissions and imbalances that result from an effort such as thisone and which are manifest in this volume. Our ultimate goalwas to produce a single volume that would broadly cover theTree of Life and that would be useful to the systematicscommunity as well as accessible to a much wider audience. Wechallenged the speakers to involve as many of their colleagues aspossible and to summarize what we know, and what we don’tknow, about the phylogeny of each group, and to write theirchapters for a scientifically literate general audience, but not atthe expense of scientific accuracy. We trust that their efforts willcatalyze future research and greatly enhance communicationabout the Tree of Life.

The symposium itself could not have been undertakenwithout the tireless effort of numerous people. The staff of theAMNH and its outside symposium coordinator, DBK Events,spent countless hours over many months facilitating arrange-ments with the speakers and attendees, and not least, makingthe organizers’ lives much easier. It is not possible to identify allof those who contributed, but we would be remiss if we did notmention the following: Senior Vice President Gary Zarr, andespecially Ann Walle, Anne Canty, Robin Lloyd, Amy Chiu, andRose Ann Fiorenzo of the AMNH Department of Communica-tions; Joanna Dales of Events and Conference Services; MikeBenedetto of IT-Network Systems; Frank Rasor and Larry VanPraag of the Audio-Visual Department; and Jennifer Kunin ofDBK Events.

Finally, many colleagues helped with production of thisvolume. Many referees, both inside and outside of our institu-tions, contributed their time to improve the chapters. MerleOkada and Christine Blake, AMNH Department of Ornithology,helped in many ways with editorial tasks, and Susan Donoghueassisted with the index. Most important, we are grateful to KirkJensen of Oxford University Press for believing in the projectand facilitating its publication, and to Peter Prescott for seeing itthrough.

Literature Cited

Darwin, C. R. 1859. On the origin of species. John Murray,London.

Fernholm, B., K. Bremer, and H. Jörnvall (eds.). 1989. Thehierarchy of life. Nobel Symposium 70. Elsevier, Amsterdam.

Haeckel, E. 1866. Generelle Morphologie der Organismen:allgemeine Grundzüge der organischen Formen-Wissenschaft,mechanisch begründet durch die von Charles Darwinreformirte Descendenz-Theorie. G. Reimer, Berlin.

Hennig, W. 1950. Grundzüge einer Theorie des phylogenetischenSystematik. Deutscher Zentraverlag, Berlin.

Hennig, W. 1966. Phylogenetic systematics. University ofIllinois Press, Urbana.

Zimmermann, W. 1931. Arbeitsweise der botanischenPhylogenetik und anderer Gruppierubgswissenschaften.Pp. 941–1053 in Hanbuch der biologischenArbeitsmethoden (E. Abderhalden, ed.), Abt. 3, 2, Teil 9.Urban & Schwarzenberg, Berlin.

http://www.nrel.colostate.edu/projects/iboyhttp://www.nrel.colostate.edu/projects/iboyhttp://www.diversitas-international.orghttp://www.diversitas-international.org

IThe Importance of Knowing the Tree of Life

1The Importance of the Tree of Life to Society

The affinities of all the beings of the same class havesometimes been represented by a great tree. . . . As buds giverise by growth to fresh buds, and these, if vigorous, branchout and overtop on all sides many a feebler branch, so bygeneration I believe it has been with the great Tree of Life,which fills with its dead and broken branches the crust of theearth, and covers the surface with its ever branching andbeautiful ramifications.—Charles Darwin, On the Origin of Species (1859)

Terry L. Yates

Jorge Salazar-Bravo

Jerry W. Dragoo

Despite Darwin’s vision of the existence of a universal Treeof Life, assembly of the tree with a high degree of accuracyhas proven challenging to say the least. Generations of sys-tematists have worked on the problem and debated (orfought) about how to best approach a solution, or questionedif a solution was even possible. Much of the rest of the bio-logical sciences and medicine either simply accepted deci-sions of systematists without question or discounted thementirely as lacking rigor and accuracy. Attempts at solvingthe problem met with only limited success and were gener-ally limited to similarity comparisons of various kinds untilthe convergence of three important developments: (1) con-ceptual and methodological underpinnings of phylogeneticsystematics, (2) development of genomics, and (3) rapidadvances in information technology.

Convergence of these three areas makes construction ofa robust tree representing genealogical relationships of allknown species possible for the first time. This, coupled withthe fact that the current lack of a universal tree is severelyhampering progress in many areas of science and limiting theability of society to address many important problems andto capitalize on a host of opportunities, demands that weundertake this important project now and with conviction.Although many challenges still stand before us (which them-selves represent additional opportunities), constructing acomplete Tree of Life is now conceptually and technologi-cally possible for the first time. It is relevant to note here thatwe still had hundreds of problems to solve when we decided

to land a man on the moon, and their solution producedhundreds of unexpected by-products. The size of this un-dertaking and the human resources needed, however, requirean international collaboration instead of a competition. As-sembling an accurate universal tree depicting relationshipsof all life on Earth, from microbes to mammals, holds enor-mous potential value for society, and it is imperative that westart now. This chapter, although not meant to be exhaus-tive, aims to provide a number of examples where even ourlimited knowledge of the tree has provided tangible benefitsto society. The actual value that a fully assembled tree wouldhold for society would be limitless.

Enabling Technologies and Challenges

Despite widespread acceptance of phylogenetic systematicsduring the 1980s, it was not until the advent of genomicsand modern computer technology, enabled by more efficientand rapid phylogenetic algorithms in the 1990s, that large-scale tree assembly became possible. The rapid growth ofgenomics, in particular, revolutionized the field of phyloge-netic systematics and provided a new level of power to treeassembly. To reconstruct the evolutionary history of all or-ganisms will require continued advances in computer hard-ware and development of faster and more efficient algorithms.

The mathematics and computer science communities arealready actively engaged in this challenge, and breakthroughs

7

8 The Importance of Knowing the Tree of Life

are occurring almost daily. For example, researchers work-ing on resolving the relationships of 12 species of bluebellsback to a common ancestor have used the 105 genes foundin chloroplast DNA from those species (and an outgroup—tobacco) to reconstruct the phylogeny. The resulting analy-sis examined 14 billion trees. But not only did they recon-struct the phylogeny, they also inferred the gene order of the105 genes found in the chloroplast genome for each ances-tor in the tree, which means 100 billion “genomes” wereanalyzed. The process took 1 hour and 40 minutes using a512-processor supercomputer (Moret et al. 2002).

Although this represents a major advancement, addi-tional advancements will be needed for the relationships ofthe current 1.7 million known species to be reconstructed.Necessary software tools have not been developed to take fulladvantage of existing data and to permit integration withexisting biological databases. The enormous amounts of databeing generated by the enabling technologies associated withmodern genomics, although posing considerable challengesto the computer world, will allow tree construction at a levelof detail far exceeding anything in the past.

Even in groups such as mammals that are well known rela-tive to invertebrates and microbes, the use of genomics in treeconstruction is increasing our knowledge base at a phenom-enal rate and providing important bridges to other fields ofknowledge. Recent work by Dragoo and Honeycutt (1997),for example, has revealed that skunks represent a lineage oftheir own distinct from mustelids (fig. 1.1). Skunks histori-cally have been classified as a subfamily within the Mustelidae(weasels), but genetic data suggest that raccoons are moreclosely related to weasels than are skunks. Additionally, stink

badgers were classified within a different subfamily of muste-lids than skunks. Morphological and genetic data both sup-port inclusion of stink badgers within the skunk clade. Theskunk–weasel–raccoon relationship was based on analyses ofgenes within the mitochondrial genome. However, DNA se-quencing of nuclear genes has provided support for this hy-pothesis as well (Flynn et al. 2000, and K. Koepfli, unpubl.obs.). This discovery is already proving valuable to other fieldssuch as public health and conservation.

These types of advances are producing major discover-ies across the entire tree, but nowhere is it more evident thanin the microbial world. New discoveries using genomics andphylogenetic analysis have led to the discovery of entire newgroups of Archaea (DeLong 1992) that will prove critical toour understanding of the functioning of the world’s ecosys-tems. Others using similar techniques are discovering majorgroups of important microbes living in extreme environments(Fuhrman et al. 1992) that could lead to discovery of impor-tant new classes of compounds. In fact, the number of newspecies of bacteria being discovered with these methods, asnoted by DeLong and Pace (2001), is expanding almost ex-ponentially. It is not only new species that are being discov-ered but also new kingdoms of organisms within the domainsBacteria and Archaea.

Human Health

Ten people died in April through June 1993 as a result of anunknown disease that emerged in the desert Southwest ofthe United States. Approximately 70% of the people who ac-

Figure 1.1. Phylogeneticrelationship of skunks withrelation to weasels as well asother caniform carnivores;modified from Dragoo andHoneycutt (1997). The arrowindicates a sister-grouprelationship between weasels(Mustelidae) and raccoons(Procyonidae) to the exclusionof skunks. Skunks thus wererecognized as a distinct family,Mephitidae.

Mephitidae

Mustelidae

Procyonidae

Pinnipedia

UrsidaeCanidae

Feliformia

Hog-nosed SkunkStriped SkunkSpotted SkunkStink BadgerSmall - clawed OtterRiver OtterSea OtterZorillaMinkLong - tailed WeaselFerretWolverineMartenEuropean BadgerAmerican BadgerRingtailRaccoonKinkajouWalrusSea LionSealBearCoyoteGray FoxOcelotMongoose

The Importance of the Tree of Life to Society 9

quired this disease died from the symptoms. No known cureor drugs was available to treat this disease, nor was it knownif the disease was caused by a virus or bacterium or someother toxin. Later, a previously unknown hantavirus wasdetermined to be the cause and was described as Sin Nombrevirus (SNV; Nichol et al. 1993), and it was discovered thatthe reservoir for this virus was the common deer mouse(Childs et al. 1994).

Phylogenetic analyses of viruses in the genus Hantavirussuggested that this new virus was related to Old World hanta-viruses. However, the virus was different enough in sequencedivergence to suggest that it was not a result of an intro-duction from the Old World, but rather had evolved in theWestern hemisphere. Phylogenetic analyses of both muridrodents and known hantaviruses indicated a high level ofagreement between host and virus trees (fig. 1.2), suggest-ing a long history of coevolution between the two groups(Yates et al. 2002). This information allowed researchers topredict that many of the murid rodent lineages may be asso-ciated with other lineages of hantaviruses as well.

Predictions made from analyses of these phylogenetictrees have been supported with the descriptions of at least25 new hantaviruses in the New World since the discoveryof SNV (fig. 1.3). More than half (14) of these newly rec-ognized viruses have been detected in Central and SouthAmerica. Additionally, many of the viruses are capable ofcausing human disease. It is likely that many more yet un-known hantaviruses will be discovered in other murid hostsnot only in North and South America but also in other coun-tries around the world. The poorly studied regions of suchcountries as African and Asia quite probably contain manysuch undescribed viruses.

Further studies enabled by findings of coevolutionaryrelationships have allowed the development of models thatare able to predict areas and times of increased human risk

to disease far in advance of any outbreaks (Yates et al. 2002,Glass et al. 2002). Knowledge of phylogenetic relationshipsof these organisms has thus proven critical for our under-standing of diversity of these pathogens and how to predictthe risk to humans. An understanding of these relationshipsalso will be critical for us to determine if we are under attackfrom introduced pathogens.

In 1999 several people were diagnosed with or died fromsymptoms of a viral infection similar to that caused by theSt. Louis encephalitis virus (Flaviviridae). The virus was de-termined to be transmitted by mosquitoes and not only af-fected humans but also was killing wild and domestic birds.Phylogenetic analyses using RNA sequencing from this vi-rus as well as other flaviviruses were conducted to determinethat the disease causing agent was actually the West Nile virus(Jia et al. 1999, Lanciotti et al. 1999). This virus was deter-mined from those analyses to be closely related to strainsfound in birds from Israel, East Africa, and Eastern Europe(fig. 1.4; Lanciotti et al. 1999). The information obtainedfrom those studies provided the basic biology needed to al-low health officials to effectively treat this new outbreak ofWest Nile virus as well as make predictions about the spreadof the virus using the known potential avian hosts. Advanceknowledge of where it might spread next was critical in pre-venting human and animal infection. West Nile virus hascurrently spread as far west in the United States as Califor-nia and has resulted in numerous human and animal deaths.

Conservation

Conservation biology is quite likely the area of science mostheavily affected (and will continue to be so) by a better knowl-edge of the Tree of Life. A more complete Tree of Life willmean that more species are identified. Currently, one of the

Figure 1.2. Coevolution of New Worldmurid rodents (solid lines) andhantaviruses (dotted lines) based oncomparison of each independentphylogeny; modified from Yates et al.(2002).

Rattus norvegicusMicrotus pennsylvanicusPeromyscus maniculatus(grass)Peromyscus maniculatus (forest)Peromyscus leucopus(NE)Peromyscus leucopus(NW)Peromyscus leucopus(SW)Reithrodontomys megalotisReithrodontomys mexicanusSigmodon hispidustexensisSigmodon hispidusSigmodon alstoniOryzomys palustris Oligoryzomys flavescensOligoryzomys chacoensisOligoryzomys longicaudatus(N)Oligoryzomys longicaudatus(S)Oligoryzomys microtisCalomys lauchaAkodon azaraeBolomys obscurus

SeoulProspect HillSinNombreMonongahelaNew YorkBlue River (IN)Blue River (OK)El Moro CanyonRio SegundoMuleshoeBlack Creek CanalCaño DelgaditoBayouLechiguanasBermejoOranAndesRio MamoreLaguna Negra PergaminoMaciel


most important issues in conservation biology is the ques-tion of how many species are out there (Wheeler 1995).Although no single value can be used with any level of con-fidence, a figure often cited is 12.5–13 million species (e.g.,Singh 2002); Cracraft (2002) estimated (admittedly roughly)that only a very small fraction—in the order of 0.4%—of thisfigure [or some 50–60 (103 taxa)] are included in any sort ofphylogenetic analysis. A more developed, inclusive Treeof Life would help identify, catalog, and database elementsof biodiversity that may not have been included until now.

A more developed Tree of Life would help incorporatean evolutionary framework with which to base conservationstrategies. Two major questions in conservation biology arehow variation is distributed in the landscape, and how it cameabout. Conservation planners, too, need to highlight thesespatial components for conservation action. Erwin (1991)convincingly argued for the need to incorporate phylogeniesand evolutionary considerations in conservation efforts.Desmet et al. (2002), Barker (2002), and Moritz (2002) haveproposed methodological and practical applications for thisstrategy. For example, Barker (2002) reviewed and expandedon some of the properties of phylogenetic diversity measuresto enable capturing both the phylogenetic relatedness ofspecies and their abundances. This measure estimates therelative diversity feature of any nominated set of species bythe sum of the lengths of all those branches spanned by theset. These branch lengths reflect patristic or path-length dis-tances of character change. He then used this method toaddress a number of conservation and management issues(from setting priorities for threatened species management

to monitoring biotic response to management) related tobirds at three different levels of analyses: global, New Zealandonly, and Waikato specifically.

An improved Tree of Life would allow for rigorous testingof old premises in evolutionary theory. For more than 40 years,the premise that shrinking and expanding of tropical forestsin the neotropics and elsewhere has become a paradigmaticforce invoked to explain the diversity of species in thesebiodiverse areas of the world (but see Colinvaux et al. 2001).Research centered on the phylogenies and phylogeographicpatterns of various taxa in several tropical areas of the worldhas now made it clear that the refuge hypothesis (see Haffer1997, Haffer and Prance 2001) of Amazonian speciation doesnot explain the patterns of distribution of many taxa. In fact,

Figure 1.3. Newly discoveredhantaviruses since 1993;modified from Centers forDisease Control and Prevention(2003). Viruses prefixed by anasterisk represent strains knownto be pathogenic to humans.

Figure 1.4. Phylogenetic relationship of New York (*) strain ofthe West Nile virus compared with other strains worldwide;modified from Lanciotti et al. (1999).

CañoDelgadito

*Sin Nombre

RíoSegundo

El Moro Canyon

*Andes

*Bayou*Black Creek Canal

RíoMamoré

*Laguna Negra

Muleshoe

*New York

* Orán

Pergamino

Maciel

*HU39694

*Lechiguanas

IslaVistaBloodland Lake

Prospect Hill

Bermejo

*Juquitiba

*MonongahelaBlue River

*ChocloCalabaso

Romania 1996Israel 1952South AfricaEgypt 1951Senegal 1979Italy 1998Romania 1996Kenya 1998New York 1999*Israel 1998Central African Republic 1967Ivory Coast 1981Kunjin1966-91India 1955- 80


Glor et al. (2001), Moritz et al. (2000), and Richardson et al.(2001) have demonstrated that some of the most specioustropical groups have patterns of diversification that resultedduring or after the unstable period of the Pleistocene, suggest-ing a more recent evolutionary history. Phylogenetic patternsindicate that heterogeneous habitats account for more bio-diversity than does the accumulation of species through timein an unperturbed environment.

These studies and others (e.g., Moritz 2002) have shownthat it is possible to incorporate the knowledge obtained byphylogenetic analyses (i.e., applied phylogenetics of Cracraft2002) and the distribution of genetic diversity into conser-vation planning and priority setting for populations withinspecies and for biogeographic areas within regions. Moritz(2002) suggests that the separation of genetic diversity intotwo dimensions, one concerned with adaptive variation andthe other with neutral divergence caused by isolation, high-lights different evolutionary processes and suggests alterna-tive strategies for conservation that need to be addressed inconservation planning.

The main tenet in conservation biology is that the “valueof biodiversity lies in its option value for the future, thegreater the complement of contemporary biodiversityconserved today, the greater the possibilities for futurebiodiversity because of the diverse genetic resource neededto ensure continued evolution in a changing and uncertainworld” (Barker 2002:165). We cannot conserve what we donot know.

Agriculture

The potential value to agriculture of a fully assembled Treeof Life is enormous. The existence of an accurate phyloge-netic infrastructure will enable directed searches for usefulgenes in ancestors of modern-day crop plans, as opposedto the random explorations of the past. Being able to fol-low individual genes through time armed with knowledgeof their ancestral forms will allow a determination of howthe function of these genes has changed through time. Thisknowledge will, in turn, allow selective modification of newgenerations of plants and animals in a much more preciseway than selective breeding alone. For example, a group ofresearchers working on the Tree of Life for green plants(Oliver et al. 2000) has identified and traced the genes re-sponsible for desiccation tolerance from ancient liverwortsto modern angiosperms (fig. 1.5). Given the rate of desertifi-cation occurring globally and the rapid increases in humanpopulations, these data may prove invaluable in helping tosustain our global agriculture.

However, our knowledge of the relationships of wildrelatives to many important agricultural crops still is limited.Understanding the origins and relationships should help withfurther improvement of many of the world’s crop plants.Recently, however, research on major grain crops such as

wheat, rice, and corn and such other crops as tomatoes andManihot (a major source of starch in South America) has pro-vided insight into the origins of these economically impor-tant agricultural products. But, relationships of many otherimportant food and fiber plants, which large parts of ourpopulations worldwide depend on, still remain virtuallyunknown. These relationships must be understood if wehope to make future genetic improvements, especially be-cause many of the wild progenitors are at risk of extinctionand we have yet to study them.

One good example of how phylogenetic relationshipsmay help us to generate an improved crop is seen in corn(Zea mays mays). This is a crop of enormous economic im-portance, and if it is to be used to assist in sustaining humanpopulations, it is imperative that we be able to make contin-ued improvements in disease and/or drought resistance. Cornis a grass with a unique fruiting body commonly referred toas the “corn cob.” This is not typically seen in wild grasses,so there have been assorted hypotheses regarding the rela-tionships of corn to other species. Potential relatives to cornare the grasses from Mexico and Guatemala known as teosin-tes. Recently, Wang et al. (2001) used molecular techniquesto conclude that two annual teosinte lineages may actuallybe the closest relative to corn (fig. 1.6).

These researchers have demonstrated that the origin ofthis agricultural product probably occurred 9000 years agoin the highlands of Mexico. Additionally, it was determinedthat the allele responsible for the cob was a result of selec-tion on a regulatory gene rather than a protein-coding gene(Wang et al. 2001). Modern cultivated corn has the poten-

Figure 1.5. Phylogeny of major groups of land plants; modifiedfrom Oliver et al. (2000). Asterisks indicate clades that containdesiccation-tolerant species. Oliver et al. (2000) suggest thatdesiccation tolerance is a primitive state in early land plants thatwas lost before the evolution of Tracheophytes and thenreappeared in at least three major lineages. Additionally, thegenes reevolved independently within eight clades found inangiosperms.

Angiosperms*GnetophytesConifersCycadsGingkoFerns*EquisetumSelaginella*IsoetesLycopodiumMosses*Hornworts*Liverworts*

Land Plants

Tracheophytes

Seed Plants


tial to interbreed with several teosinte grasses, so it may bepossible to incorporate new traits from these species to im-prove existing strains of corn crops. These studies illustratehow important it is to protect not only wild species and lin-eages of teosinte grass but also the habitats in Mexico wherethey are found.

Invasive Species

Invasive species have become an enormous problem world-wide and cause billions of dollars in damage each year whiledoing irreparable harm to many native species and ecosys-tems. Phylogenetic analysis is an important tool in the battlefor identifying invasive species and for determining theirgeographic origin. Recent examples include the West Nilevirus example described above and an invasive alga in Cali-fornia. In the latter example, scientists were able to use phy-logenetic analysis of DNA sequences to identify the Australianalga species Caulerpa taxiflora in California waters. This find-ing led to an immediate eradication program that, if success-ful, may save the United States billions of dollars.

In addition, understanding the evolutionary associationsof invasive species in the context of closely affiliated groupsof species such as host plants or animals is critical for pre-dicting their spread and implementing successful controlmeasures. Wang et al. (1999) performed a phylogeneticanalysis to examine relationships of potential pest species oflonghorn beetles (Cerambycidae) and found that beetles incertain clades were not likely to become pests, whereas beetlesin two other clades could become pests outside of their na-tive Australia. Another clade in this group, the Asian long-horn beetle (Anoplophora gladripennis), has been recentlyintroduced into the United States in hardwood packingmaterials and has already spread from points of introductionto many new areas, killing native hardwood trees as it invades(Meyer 1998). Knowledge of the phylogenetic relationshipsof trees that this beetle attacks in its native range could provevaluable in predicting the North American trees most likelyat risk and could help model its future spread. Likewise, anunderstanding of the phylogenetic affinities of natural en-

emies of longhorn beetles in Asia will be critical if biologicalcontrols for this pest are to be considered in North America.

Invasive ant species have become enormous problemsworldwide. The ant Linepithema humile has been particularlyproblematic and has been particularly damaging to nativespecies in Hawaii. Tsutsui et al. (2001) used phylogeneticanalyses to trace the origin of this pest to Argentina. Anotherinvasive ant, the fire ant (Solenopsis invicta), has caused bil-lions of dollars of damage in the southern United States andhas even caused human and animal deaths. Like other eusocialinsects, such as Asian termites, fire ants are extremely diffi-cult to control using chemical and other standard methods.Efforts to date in the latter case have been largely ineffectiveand have led several authors (Morrison and Gilbert 1999,Porter and Briano 2000) to suggest the need for the introduc-tion of biological control agents from the original range of theseants in South America. In particular, these authors have sug-gested the possible use of host-specific ant-decapitating fliesthat lay their eggs in the heads of these ants, where the de-veloping larvae eventually kill the ants. Such introductionsare always risky but would be extremely so without detailedknowledge of the Tree of Life for the groups in question.According to Rosen (1986), “Reliable taxonomy is the basisfor any meaningful research in biology.” It is essential alsoto understand the evolutionary histories of both target pestand natural enemy to predict the possible effects of using oneto “control” the other.

Human Land Use

A well-resolved Tree of Life has important implications fordisciplines as apparently disparate from biology as the studyof human land use patterns, especially when they integratewith other disciplines. For example, phylogenetic analysiswas used to discover that two closely related species ofrodents in the genus Calomys exist in eastern Bolivia (Salazar-Bravo et al. 2002, Dragoo et al. 2003), each harboring a spe-cific arenavirus (fig. 1.7). In the Beni Department of Bolivia,Calomys species harbor the Machupo virus (MACV), the etio-logical agent of Bolivian hemorrhagic fever (BHF), whereasin the Santa Cruz Department, Calomys callosus harbors thenonpathogenic Latino virus (LAT). MACV occurs in theAmazon drainage, whereas LAT is found along the drainageof the Parana River. Additionally, it has been found thatCalomys from each region, despite their genetically basedspecies specificity, will hybridize in the laboratory and cre-ate fertile hybrids. It follows that there exists not only therisk of species invasion into a previously isolated ecologicalzone, but also the risk of hybrids carrying the pathogenicvirus into the new region, the possibility of dual arenavirusinfection in such rodents, and the chance that virus recom-bination with unknown consequences might occur.

In the early 1960s MACV produced several outbreaks innortheastern Bolivia, with infection rates of 25% in some towns

Figure 1.6. Phylogenetic relationship of corn to otherteosintes; modified from Wang et al. (2001). This relationshiphelps explain the morphological variation seen in domesticcorncob.

Zea perennis

Zea diploperennis

Zea maysmexicana

Zea mays parviglumis

Zea maysmays(domestic corn)

Teosintes


and mortality rates approaching 45%. Johnson et al. (1972)noted two distinct phenotypic reactions to infection withMACV and suggested that there may be a genetic component.A Calomys species has been reported to express two differentimmune responses when infected with MACV but not withLAT (Webb et al. 1975). Some individuals become chronicallyinfected, do not produce antibodies, shed large amounts ofvirus in urine, become infertile, and are the principal vectorsof BHF. Others produce an antibody response and all but clearthe virus. Although these individuals remain chronically in-fected, they can reproduce (Justines and Johnson 1969).

There is growing concern in the Bolivian health commu-nity about the unintended consequences of an all-weather roadconnecting Trinidad and Santa Cruz, the capital cities of theBeni and Santa Cruz Departments, respectively, that has beenin service for several years. This road breaches a forested natural

barrier between biomes of the respective rodents and viruses.That barrier contains the north–south continental divide ofSouth America (Salazar-Bravo et al. 2002). The new road link-ing the two home ranges of the virus–rodent pairs is bringinghuman development to the fringes of both areas along itscourse. Human populations in both departments are boom-ing. Thirty-five years ago Trinidad and Santa Cruz had about6000 and 60,000 persons, respectively. Today those numbershave increased 10-fold. Agricultural development has keptpace, especially in the Santa Cruz Department. Therefore, amajor concern is whether the rodent and its virus from thenorth may be now moving, abetted by human commerce, intothe southern department. The potential public health riskposed by construction of new roads and new development inthe Beni and Santa Cruz Departments makes monitoring thissituation essential.

To make predictions about the evolution and spread ofarenaviruses, we need to understand the evolutionary historyof the rodent reservoirs. The significance of understanding ingreater detail evolutionary histories at the population level aswell as at the subfamily level goes beyond the importance ofprevention and treatment of BHF. The observed patterns ofinfection and distribution of MACV exhibit a striking num-ber of similarities with not only other arenaviruses but withhantaviruses as well. In addition to the apparent connectionto rodent population density and human ecology, these viruseswith few exceptions share a common host family of rodents,suggesting a long common evolutionary history.

Economics

Many of the examples presented above will have economicbenefits for society. Understanding the Tree of Life also canlead to discovery of new products that can be derived fromclosely related taxa. These products can be used to affect otherareas such as biological control of pest organisms, agricul-tural productivity, and medicinal necessities. For example,in 1969 a new genus and species of bacterium, Thermusaquaticus, was described (Brock and Freeze 1969), which laterrevolutionized much of the way molecular biology is con-ducted when the DNA polymerase from this organism wasused for the polymerase chain reaction (PCR; Saiki et al.1988). PCR is a multimillion dollar a year industry thatshould top $1 billion by the year 2005. This technology hasgreatly benefited not only systematics and taxonomy but alsomany other biological sciences, including health and foren-sics. Discovery of T. aquaticus and use of the Taq DNA poly-merase has spawned many additional technologies. A cursoryview of any molecular supply catalog will show numerouschemicals and kits designed for use with PCR technology.Furthermore, such hardware as DNA thermocyclers andautomated sequencers also has been developed.

Additionally, DNA polymerases from other closely re-lated thermally stable organisms have been isolated with

Figure 1.7. Summary cladogram of four closely related taxa ofvesper mice (Calomys); modified from Salazar-Bravo et al.(2002). Cb, Calomys species from the Beni Department ofBolivia; Cf, C. fecundus; Cv, C. venustus; Cc, C. callosus. Thewhite arrow points to the forested area that separates the Llanosde Moxos from the Chaco region. Vegetation is as follows: LM;Llanos de Moxos, SEC; Southeast Coordillera, CH; Chaco, EPEspinal.

LM

SEC

CH

EP

Cb

Cc

Cv

Cf


varying properties such as increased half-life at higher tem-peratures, decreased activity at lower temperatures, and3'-5' exonuclease activity. As a result of PCR and the searchfor new DNA polymerases, many new life forms have beendiscovered. For example, the thermally stable microbesfrom which Taq was recovered were thought to comprise atight cluster of a few genera that metabolized sulfur com-pounds (Woese 1987, Woese et al. 1990). Most of these or-ganisms had to be cultured in the lab in order to be studied(DeLong 1992, Barns et al. 1994). However, PCR technol-ogy has allowed for a more in-depth study of these Archaeaby using in situ amplification of uncultivated organisms thatoccur naturally in hot springs found in Yellowstone NationalPark. We now know that the Crenarchaeota display a widevariety of phenotypic and physiological properties in envi-ronments ranging from low temperatures in temperate andAntarctic waters to high-temperature hot springs (Barnset al. 1996, and citations therein). In fact, PCR coupled withphylogenetic analysis has allowed the discovery of not onlynew life forms within the kingdom Crenarchaeota but alsonew kingdoms within the domain Archaea (fig. 1.8; Barnset al. 1996).

Many new DNA polymerases have been discovered andpatented and are now commercially available as a resultof some of these discoveries. According to Bader et al.(2001:160), “Simple identification via phylogenetic classifi-cation of organisms has, to date, yielded more patent filingsthan any other use of phylogeny in industry.” Patents alsohave been filed for vaccines associated with various viruses,such as porcine reproductive and respiratory syndrome vi-rus and human immunodeficiency virus, that can target spe-

cific closely related virus populations based on phylogeneticanalyses (citations within Bader et al. 2001).

Other economically important uses of a well-defined Treeof Life include discovery of biological control organisms aswell as chemicals that target specific metabolic pathways ofrelated taxa. Phylogenetic analyses of root-colonizing fungirevealed a group of nonpathogenic fungi that could serve asa biological control against pathogenic fungi (Ulrich et al.2000). Phylogenetic studies are being conducted on numer-ous organisms for biological control, including nematodesand associated symbiotic bacteria and target moth, fly, andbeetle pests (Burnell and Stock 2000); intracellular bacteriaWolbachia, parasitic wasps, and flies (Werren and Bartos2001); and insect controls of thistles (Briese et al. 2002). Infact, Briese et al. (2002:149) state, “[G]iven the improved stateof knowledge of plant phylogenies and the evolution of hostuse, it is time to base testing procedure purely on phylo-genetic grounds, without the need to include less related testspecies solely because of economic or conservation reasons.”

Other forms of control include using chemicals to attackspecific metabolic pathways found in one clade of organismsbut not in another. Two such pathways that occur in microbesand/or plants but not mammals are the shikimate pathway andthe menevalonant pathway. The chemical glyphosate has beenused commercially as an herbicide/pesticide for its ability todisrupt the shikimate pathway in algae, higher plants, bacte-ria, and fungi but theoretically does not have harmful effectson mammals (Roberts et al. 1998). Another pathway for con-sideration for an antimicrobial target is the mevalonate path-way. This is one of two pathways that convert isopentenyldiphosphate to isoprenoid found in higher organisms but isthe only pathway found in many low-G+C (guanine + cytosine)gram-positive cocci. Phylogenetic analyses indicate that thegenes found in these bacteria are more closely related to highereukaryotic organisms and are likely a result of a very early hori-zontal gene transfer between eukaryotes and bacteria beforethe divergence of plants, animals, and fungi (Wilding et al.2000). This pathway therefore represents a means for controlof the gram-positive bacteria.

Another economic value to society may lie in DNA/RNAvaccines. Knowing the phylogenetic relationships of targetorganisms may allow for the development of broad-scale vac-cines or “species”-specific vaccines. DNA vaccines are relativelyeasy to make and can be produced much quicker than con-ventional vaccines (Dunham 2002). Although there still areseveral safety issues to address before wide-scale use of nucleicacid vaccines (Gurunahan et al. 2000), this technology can beused to treat several wildlife diseases (Dunham 2002) and canbe used potentially as a defense against a bioterrorist attack.

Conclusions

Assembling the Tree of Life will be a monumental task andpossibly one of the greatest missions we as a society could

Figure 1.8. Newly discovered organisms of Archaea; modified(reduced tree) from Barns et al. (1996). Taxa labeled “pJP”represent new life forms discovered using ribosomal RNAsequences amplification from uncultured organisms. New taxawere found within two kingdoms representing Crenarchaeotaand Euryarchaeota as well as the new kingdom Korarchaeota(pJP78 and other similar rDNA sequences).

Desufurococcus mobilispJP74Sulfolobus aciducaldariuspJP7Pyrodictium occultumpJP8Pyrobaculum islandicumPyrobaculum aerophilumThermoproteus tenaxpJP6Thermofilum pendenspJP81pJP33Methanopyrus kandleriTheromococcus celerArchaeoglobus fulgiduspJP9pJP78

Crenarchaeota

Euryarchaeota

Korarchaeota


hope to achieve. It will require numerous collaborations ofmultiple disciplines within the scientific community. TheTree of Life has already provided many benefits, not only toscience but to humanity as well. These benefits are but a smallfraction of what a fully assembled tree would have to offer.In many respects, the power of a complete Tree of Life com-pared with the partial one we have now is analogous to thebreakthroughs made possible by a complete periodic tablecompared with a partial one. Imagine chemists trying to pre-dict the structure and function of new compounds armedwith the knowledge of only 10% of the periodic table. TheTree of Life will form the critical infrastructure on which allcomparative biology will rest. Once completed, this infra-structure will fuel scientific breakthroughs across all of thelife sciences and many other fields of science and engineer-ing and will foster enormous economic development.

Constructing the Tree of Life will create extraordinaryopportunities to promote research across interdisciplinaryfields as diverse as genomics, computer science and engineer-ing, informatics, mathematics, earth sciences, developmen-tal biology, and environmental biology. The scientific andengineering problem of building the Tree of Life is complexand presents many challenges, but these challenges can beaccomplished in our lifetime. Already, the internationalgenomics databases [GenBank (http://www.ncbi.nih.gov/Genbank/index.html), EMBL (http://www.ebi.ac.uk/embl/),and DDBJ (http://www.ddbj.nig.ac.jp/)] grow at an exponen-tial rate, with the number of nucleotide bases doubling ap-proximately every 14 months. Currently, there are more than17 billion bases from more than 100,000 species listed bythe National Center for Biotechnology Information (availableat http://www.ncbi.nlm.nih.gov/). Data from nongenomicsources, such as anatomy, behavior, biochemistry, or physiol-ogy, also have been collected on thousands of species, andmany thousands of phylogenies have been published forgroups widely distributed across the tree. To truly benefitindustry, agriculture, and health and environmental sciences,the overwhelming amount of data required to construct theTree of Life must be appropriately organized and madereadily available.

Cracraft (2002) considered the question “What is theTree of Life?” to be one of seven great questions of system-atic biology. In many respects, the answer to that questionis fundamental to all the others and will enable their resolu-tion. Even fundamental questions such as what a species isand how many there are will be facilitated by assembling thetree. It should be noted that addressing the latter questionand assembling the Tree of Life go hand-in-hand and form apositive feedback loop. Discovery of new species will pro-vide new information that will enhance tree assembly, andat the same time tree assembly will provide the informationnecessary for the discovery of new species.

The other great questions listed by Cracraft (2002) actu-ally require a tree for their resolution. As addressed in thischapter, however, great questions from other disciplines also

require a highly resolved tree for their solution. In fact, theanswer to few scientific questions offers the potential to fuelas many major discoveries in other disciplines as does reso-lution of the Tree of Life. Fields such as evolution and de-velopment, medicine, and bioengineering will immediatelybe able to rapidly address questions not before possiblewithout the phylogenetic infrastructure provided by thetree. These discoveries will in turn fuel economic develop-ment, inform land management decisions, and protect theenvironment.

Assembly of the Tree of Life on this scale, however, willrequire the development of innovative database structures(both hardware and software) that support relational au-thority files with annotation of both genetic and nongeneticinformation. Unprecedented levels and methods of com-putational capabilities will need to be developed as genomicinformation from the “wet” studies in the laboratory and fieldis analyzed in the “dry” environments of computers. Alreadya new field of phyloinformatics and computational phylo-genetics is emerging from these efforts that promise to har-ness phylogenetic knowledge to integrate and transform dataheld in isolated databases, allowing the invention of newinformation and knowledge.

What is needed is an international effort to coordinatetree construction, facilitate hardware and software design,promote collaboration among researchers, and facilitate da-tabase design and maintenance and the creation of a centerto help coordinate and facilitate these activities. Owing tofundamental theoretical advances in manipulating genomicand other kinds of data, to the availability of major newsources of data, and the development of powerful analyticalcomputational tools, we now have the potential (given suf-ficient resources and coordination) to assemble much of theentire Tree of Life within the next few decades, at least forcurrently known species. The potential of building a Treeof Life extends far beyond the basic and applied biologicalsciences and promises to provide much value to society.Building an accurate, complete Tree of Life depicting therelationships of all life on Earth will call for major innova-tion in many fields of science and engineering similar to thosederived from sending a man to the moon or sequencing theentire human genome. The benefits to society from such anundertaking are enormous and may well extend beyond themany provided by these two successful efforts.

Acknowledgments

We thank the Centers for Disease Control and Prevention, theU.S. National Science Foundation, and the National Institutes ofHealth for previous financial support for many of the discoveriesreported here. We especially thank the National ScienceFoundation for providing the leadership for the initiation of thiscritical effort. We also thank the Museum of SouthwesternBiology of the University of New Mexico (UNM) and theDepartment of Biology (UNM) for their support.

http://www.ncbi.nih.gov/Genbank/index.htmlhttp://www.ncbi.nih.gov/Genbank/index.htmlhttp://www.ebi.ac.uk/embl/http://www.ddbj.nig.ac.jp/http://www.ncbi.nlm.nih.gov/


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2A Tangled BankReflections on the Tree of Life and Human Health

Rita R. Colwell

Writing almost 150 years ago, Charles Darwin coined thename “tree of life” to describe the evolutionary patterns thatlink all life on Earth. His work set a grand challenge for thebiological sciences—assembling the Tree of Life—that re-mains incomplete today. In the intervening years, we havecome to understand better the significance of this challengefor our own species. As human activity alters the planet, wedepend more and more on our knowledge of Earth’s otherinhabitants, from microorganisms to mega fauna and flora,to anticipate our own fate. Aldo Leopold, the great natural-ist and writer, wrote, “To keep every cog and wheel is thefirst precaution of intelligent tinkering” (1993:145–146).However, the simple fact is that we do not yet know “what’sout there,” and we are often unaware of what we have alreadylost. The total number of species may number between 10and 100 million, of which approximately 1.7 million areknown and only 50,000 described in any detail.

Today, we are in a better position to carry forwardDarwin’s program. Museums, universities, colleges, and re-search institutions are invaluable repositories for data pains-takingly collected, conserved, and studied over the years. Adda flood of new information from genome sequencing, geo-graphical information systems, sensors, and satellites, and wehave the raw material for realizing Darwin’s vision.

One of the great challenges we face in assembling the Treeof Life is assembling the talent—bringing together the system-atists, molecular biologists, computer scientists, and mathema-ticians—to design and deploy new computational tools for

phylogenetic analysis. Systematists are as scarce as hen’s teeththese days. They may be our most endangered species.

The National Science Foundation (NSF) has a long his-tory of supporting the basic scientific research, across alldisciplines, that has placed us within reach of achieving thisobjective. Now, the NSF has begun a new program to helpsystematists and their colleagues articulate the genealogicalTree of Life. We expect that this tree will do for biology whatthe periodic table did for chemistry and physics—providean organizing framework. But advancing scientific under-standing is not the sole objective. New knowledge is im-portant for our continued prosperity and well being on theplanet. My aim is to explore some of the common groundshared by the Tree of Life project and one important focusof social concern—human health.

My title, “A Tangled Bank,

assembling the tree of lifeagrifs.ir/sites/default/files/assembling the tree of life... · 2018. 5....

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