your inner fish - weebly

EPILOGUE

Asaparentoftwoyoungchildren,Ifindmyselfspendingalotoftimelatelyinzoos,museums,andaquaria.Beingavisitorisastrangeexperience,becauseI’vebeeninvolvedwiththeseplacesfordecades,workinginmuseumcollectionsandevenhelpingtoprepareexhibitsonoccasion.Duringfamilytrips,I’vecometorealizehowmuchmyvocationcanmakemenumbtothebeautyandsublimecomplexityofourworldandourbodies.Iteachandwriteaboutmillionsofyearsofhistoryandaboutbizarreancientworlds,andusuallymyinterestisdetachedandanalytic.NowI’mexperiencingsciencewithmychildren—inthekindsofplaceswhereIdiscoveredmyloveforitinthefirstplace.Onespecialmomenthappenedrecentlywithmysonat

theMuseumofScienceandIndustryinChicago.We’vegonethereregularlyoverthepastthreeyearsbecauseofhisloveoftrainsandthefactthatthereisahugemodelrailroadsmackinthecenteroftheplace.I’vespentcountlesshoursatthatoneexhibittracingmodellocomotivesontheirlittletrekfromChicagotoSeattle.Afteranumberofweeklyvisits

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tothisshrineforthetrain-obsessed,NathanielandIwalkedtocornersofthemuseumwehadfailedtovisitduringourtrain-watchingventuresoroccasionalforaystothefull-sizetractorsandplanes.Inthebackofthemuseum,intheHenryCrownSpaceCenter,modelplanetshangfromtheceilingandspacesuitslieincasestogetherwithothermemorabiliaofthespaceprogramofthe1960sand1970s.IwasunderthepresumptionthatinthebackofthemuseumIwouldseethetriviathatdidn’tmakeittothemajorexhibitsupfront.Onedisplayconsistedofabatteredspacecapsulethatyoucouldwalkaroundandlookinside.Itdidn’tlooksignificant;itseemedwaytoosmallandjerry-riggedtobeanythingreallyimportant.Theplacardwasstrangelyformal,andIhadtoreaditseveraltimesbeforeitdawnedonme:herewastheoriginalCommandModulefromApollo8,theactualvesselthatcarriedJamesLovell,FrankBorman,andWilliamAndersonhumanity’sfirsttriptothemoonandback.ThiswasthespacecraftwhosepathIfollowedduringChristmasbreakinthirdgrade,andhereIwasthirty-eightyearslaterwithmyownson,lookingattherealthing.Ofcourseitwasbattered.Icouldseethescarsofitsjourneyandsubsequentreturntoearth.Nathanielwascompletelydisinterested,soIgrabbedhimandtriedtoexplainwhatitwas.ButIcouldn’tspeak;myvoicebecamesochokedwithemotionthatIcouldbarelyutterasingleword.Afterafewminutes,Iregainedmycomposureandtoldhimthestoryofman’striptothemoon.ButthestoryIcan’ttellhimuntilheisolderiswhyI

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becamespeechlessandemotional.TherealstoryisthatApollo8isasymbolforthepowerofsciencetoexplainandmakeouruniverseknowable.Peoplecanquibbleovertheextenttowhichthespaceprogramwasaboutscienceorpolitics,butthecentralfactremainsascleartodayasitwasin1968:Apollo8wasaproductoftheessentialoptimismthatfuelsthebestscience.Itexemplifieshowtheunknownshouldnotbeasourceofsuspicion,fear,orretreattosuperstition,butmotivationtocontinueaskingquestionsandseekinganswers.Justasthespaceprogramchangedthewaywelookatthe

moon,paleontologyandgeneticsarechangingthewayweviewourselves.Aswelearnmore,whatonceseemeddistantandunattainablecomeswithinourcomprehensionandourgrasp.Weliveinanageofdiscovery,whenscienceisrevealingtheinnerworkingsofcreaturesasdifferentasjellyfish,worms,andmice.Wearenowseeingtheglimmerofasolutiontooneofthegreatestmysteriesofscience—thegeneticdifferencesthatmakehumansdistinctfromotherlivingcreatures.Couplethesepowerfulnewinsightswiththefactthatsomeofthemostimportantdiscoveriesinpaleontology—newfossilsandnewtoolstoanalyzethem—havecometolightinthepasttwentyyears,andweareseeingthetruthsofourhistorywithever-increasingprecision.Lookingbackthroughbillionsofyearsofchange,everythinginnovativeorapparentlyuniqueinthehistoryoflifeisreallyjustoldstuffthathasbeenrecycled,recombined,repurposed,orotherwisemodifiedfornew

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uses.Thisisthestoryofeverypartofus,fromoursenseorganstoourheads,indeedourentirebodyplan.Whatdobillionsofyearsofhistorymeanforourlives

today?Answerstofundamentalquestionsweface—abouttheinnerworkingsofourorgansandourplaceinnature—willcomefromunderstandinghowourbodiesandmindshaveemergedfrompartscommontootherlivingcreatures.Icanimaginefewthingsmorebeautifulorintellectuallyprofoundthanfindingthebasisforourhumanity,andremediesformanyoftheillswesuffer,nestledinsidesomeofthemosthumblecreaturesthathaveeverlivedonourplanet.

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NOTES,REFERENCES,ANDFURTHERREADING

CHAPTERONEFINDINGANINNERFISH

Ihaveincludedamixofprimaryandsecondarysourcesforthoseinterestedinpursuingthetopicsinthebookfurther.Foraccountsthatuseexploratorypaleontologicalexpeditionsasavehicletodiscussmajorquestionsinbiologyandgeology,seeMikeNovacek’sDinosaursoftheFlamingCliffs(NewYork:Anchor,1997),AndrewKnoll’sLifeonaYoungPlanet(Princeton:PrincetonUniversityPress,2002),andJohnLong’sSwimminginStone(Melbourne:FreemantlePress,2006).Allbalancescientificanalysiswithdescriptionsofdiscoveryinthefield.ThecomparativemethodsthatIdiscuss,includingthe

methodsusedinourwalkthroughthezoo,arethemethodsofcladistics.AsuperboverviewisHenryGee’sInSearchofDeepTime(NewYork:FreePress,1999).Basically,Ipresentaversionofthethree-taxonstatement,thestartingpointforcladisticcomparisons.AgoodtreatmentwithbackgroundsourcesisfoundinRichardForeyetal.,“TheLungfish,theCoelacanthandtheCowRevisited,”inH.-P.

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SchultzeandL.Trueb,eds.,OriginoftheHigherGroupsofTetrapods(Ithaca,N.Y.:CornellUniversityPress,1991).Thecorrelationbetweenthefossilrecordandour“walk

throughthezoo”isdiscussedinseveralpapers.Asampling:Benton,M.J.,andHitchin,R.(1997)Congruencebetweenphylogeneticandstratigraphicdatainthehistoryoflife,ProceedingsoftheRoyalSocietyofLondon,B264:885–890;Norell,M.A.,andNovacek,M.J.(1992)Congruencebetweensuperpositionalandphylogeneticpatterns:Comparingcladisticpatternswithfossilrecords,Cladistics8:319–337;Wagner,P.J.,andSidor,C.(2000)Agerank/claderankmetrics—sampling,taxonomy,andthemeaningof“stratigraphicconsistency,”SystematicBiology49:463–479.Thelayersoftherockcolumnandthefossilscontained

thereinarebeautifullyandcomprehensivelydiscussedinRichardFortey’sLife:ANaturalHistoryoftheFirstFourBillionYearsofLifeonEarth(NewYork:Knopf,1998).ResourcesforvertebratepaleontologyincludeR.Carroll,VertebratePaleontologyandEvolution(SanFrancisco:W.H.Freeman,1987),andM.J.Benton,VertebratePaleontology(London:Blackwell,2004).Fortheoriginoftetrapods:CarlZimmerreviewedthe

stateoftheartinthefieldinhishighlyreadableandwell-researchedAttheWater’sEdge(NewYork:FreePress,1998).JennyClackhaswrittenthedefinitivetextonthewholetransition,GainingGround(Bloomington:IndianaUniversityPress,2002).Thebibleofthistransition,Clack’sbookwillbringanovicetoexpertstatusquickly.

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OuroriginalpapersdescribingTiktaalikappearedintheApril6,2006,issueofNature.Thereferencesare:Daeschleretal.(2006)ADevoniantetrapod-likefishandtheoriginofthetetrapodbodyplan,Nature757:757–763;Shubinetal.(2006)ThepectoralfinofTiktaalikroseaeandtheoriginofthetetrapodlimb,Nature757:764–771.JennyClackandPerAhlberghadaveryreadableandcomprehensivecommentarypieceinthesameissue(Nature757:747–749).Everythingaboutourpastisrelative,eventhestructure

ofthisbook.Icouldhavecalledthisbook“OurInnerHuman”andwrittenitfromafish’spointofview.Thestructureofthatbookwouldhavebeenstrangelysimilar:afocusonthehistoryhumansandfishshareinbodies,brains,andcells.Aswe’veseen,alllifesharesadeeppartofitshistorywithotherspecies,whileanotherpartofitshistoryisunique.

CHAPTERTWOGETTINGAGRIP

Owenwasbynomeansthefirstpersontoseethepatternofonebone–twobones–lotsablobs–digits.Vicq-d’Azyrinthe1600sandGeoffroySt.Hilaire(1812)alsomadethispatternpartoftheirworldviews.WhatdistinguishedOwenwashisconceptofthearchetype.Thiswasatranscendentalorganizationofthebody,reflectingthedesignoftheCreator.St.Hilairewassearchinglessforanarchetypicalpatternhiddeninallstructurethanfor“lawsofform”that

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governtheformationofbodies.AnicetreatmentoftheseissuesisinT.Appel,TheCuvier-GeoffroyDebate:FrenchBiologyintheDecadesBeforeDarwin(NewYork:OxfordUniversityPress,1987),andE.S.Russell,FormandFunction:AContributiontotheHistoryofMorphology(Chicago:UniversityofChicagoPress,1982).ArecentvolumeeditedbyBrianHallisone-stop

shoppingforinformationonlimbdiversityanddevelopmentandcontainsanumberofimportantpapersondifferentkindsoflimbs:BrianK.Hall,ed.,FinsintoLimbs:Evolution,Development,andTransformation(Chicago:UniversityofChicagoPress,2007).UsefulreferencesforexploringtheshiftfromfinsandlimbsinmoredetailincludeShubinetal.(2006)ThepectoralfinofTiktaalikroseaeandtheoriginofthetetrapodlimb,Nature757:764–771;Coates,M.I.,Jeffery,J.E.,andRuta,M.(2002)Finstolimbs:whatthefossilssay,EvolutionandDevelopment4:390–412.

CHAPTERTHREEHANDYGENES

Thedevelopmentalbiologyoflimbdiversityhasseenanumberofreviewsandprimarypapers.ForareviewoftheclassicliteratureseeShubin,N.,andAlberch,P.(1986)Amorphogeneticapproachtotheoriginandbasicorganizationofthetetrapodlimb,EvolutionaryBiology20:319–387;andHinchliffe,J.R.,andGriffiths,P.,“ThePre-chondrogenicPatternsinTetrapodLimbDevelomentand

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TheirPhylogeneticSignificance,”inB.Goodwin,N.Holder,andC.Wylie,eds.,DevelopmentandEvolution(Cambridge,Eng.:CambridgeUniversityPress,1983),pp.99–121.Saunders’sandZwilling’sexperimentsarenowclassic,sosomeofthebestaccountsarenowseeninthemajortextbooksindevelopmentalbiology.TheseincludeS.Gilbert,DevelopmentalBiology,8thed.(Sunderland,Mass.:SinauerAssociates,2006);L.Wolpert,J.Smith,T.Jessell,F.Lawrence,E.Robertson,andE.Meyerowitz,PrinciplesofDevelopment(Oxford,Eng.:OxfordUniversityPress,2006).ForthefirstpaperdescribingSonichedgehog’srolein

limbpatterning,gotoRiddle,R.,Johnson,R.L.,Laufer,E.,Tabin,C.(1993)SonichedgehogmediatesthepolarizingactivityoftheZPA,Cell75:1401–1416.Randy’sworkonSonicsignalinginsharkandskatefinsis

inDahn,R.,Davis,M.,Pappano,W.,Shubin,N.(2007)Sonichedgehogfunctioninchondrichthyanfinsandtheevolutionofappendagepatterning,Nature445:311–314.Subsequentworkfromthelabontheoriginoflimbs,atleastfromageneticperspective,iscontainedinDavis,M.,Dahn,R.,andShubin,N.(2007)Alimbautopodial-likepatternofHoxexpressioninabasalactinopterygianfish,Nature447:473–476.Thestunninggeneticsimilaritiesinthedevelopmentof

flies,chickens,andhumansisdiscussedinShubin,N.,Tabin,C.,Carroll,S.(1997)Fossils,genes,andtheevolutionofanimallimbs,Nature388:639–648;andErwin,D.andDavidson,E.H.(2003)Thelastcommonbilaterian

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ancestor,Development129:3021–3032.

CHAPTERFOURTEETHEVERYWHERE

Theimportanceofteethtoanunderstandingofmammalsisevidentinthemanytreatmentsinthefield.Dentalstructureplaysaparticularlyimportantroleinunderstandingtheearlyrecordofmammals.ExtensivereviewsarefoundinZ.Kielan-Jaworowska,R.L.Cifelli,andZ.Luo,MammalsfromtheAgeofDinosaurs(NewYork:ColumbiaUniversityPress,2004);andJ.A.Lillegraven,Z.Kielan-Jaworowska,andW.Clemens,eds.,MesozoicMammals:TheFirstTwo-ThirdsofMammalianHistory(Berkeley:UniversityofCaliforniaPress,1979),p.311.Farish’smammalfromArizonaisanalyzedinJenkins,F.

A.,Jr.,Crompton,A.W.,Downs,W.R.(1983)MesozoicmammalsfromArizona:Newevidenceonmammalianevolution,Science222:1233–1235.ThetritheledontswefoundinNovaScotiaaredescribed

inShubin,N.,Crompton,A.W.,Sues,H.-D.,andOlsen,P.(1991)Newfossilevidenceonthesister-groupofmammalsandearlyMesozoicfaunaldistributions,Science251:1063–1065.Arecentreviewontheoriginofteeth,bone,andskulls,in

particularthenewevolutiongleanedfromconodontanimals,isfoundinDonoghue,P.,andSansomI.(2002)Originandearlyevolutionofvertebrateskeletonization,MicroscopyResearchandTechnique59:352–372.A

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thoroughreviewoftheevolutionaryrelationshipsamongconodontsandtheirsignificanceisinDonoghue,P.,Forey,P.,andAldridge,R.(2000)Conodontaffinityandchordatephylogeny,BiologicalReviews75:191–251.

CHAPTERFIVEGETTINGAHEAD

Awonderfullycomprehensiveanddetailedtreatmentofthedetailsofskullstructure,development,andevolutionisfoundinathree-volumeset:TheSkull,JamesHankenandBrianHall,eds.(Chicago:UniversityofChicagoPress,1993).Thisisamulti-authorupdateofoneoftheclassicvolumesonheaddevelopmentandstructure:G.R.deBeer,TheDevelopmentoftheVertebrateSkull(Oxford,Eng.:OxfordUniversityPress,1937).Detailsofheaddevelopmentandstructureinhumanscan

befoundintextsonhumananatomyandembryology.Forembryology,seeK.MooreandT.V.N.Persaud,TheDevelopingHuman,7thed.(Philadelphia:Elsevier,2006).ThecompanionanatomytextisK.MooreandA.F.Dalley,ClinicallyOrientedAnatomy(Philadelphia:LippincottWilliams&Wilkins,2006).FrancisMaitlandBalfour’sseminalworkisencapsulated

inBalfour,F.M.(1874)Apreliminaryaccountofthedevelopmentoftheelasmobranchfishes,Q.J.Microsc.Sci.14:323–364;F.M.Balfour,AMonographontheDevelopmentofElasmobranchFishes,4vols.(London:Macmillan&Co.,1878);F.M.Balfour,ATreatiseonComparativeEmbryology,

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2vols.(London:Macmillan&Co.,1880–81);M.FosterandA.Sedgwick,TheWorksofFrancisMaitlandBalfour,withanintroductorybiographicalnoticebyMichaelFoster,4vols.(London:Macmillan&Co.,1885).AsuccessoratOxford,EdwinGoodrich,producedoneoftheclassicsofcomparativeanatomy,StudiesontheStructureandDevelopmentofVertebrates(London:Macmillan,1930).Balfour,Oken,Goethe,Huxley,andotherswere

addressingtheproblemknownasheadsegmentation.Justasthevertebraedifferinaregularprogressionfromfronttoback,sotheheadhasasegmentalpattern.Aselectionofclassicandrecentresources(allwithgoodbibliographies)topursuethisfieldfurther:Olsson,L.,Ericsson,R.,Cerny,R.(2005)Vertebrateheaddevelopment:Segmentation,novelties,andhomology,TheoryinBiosciences124:145–163;Jollie,M.(1977)Segmentationofthevertebratehead,AmericanZoologist17:323–333;Graham,A.(2001)Thedevelopmentandevolutionofthepharyngealarches,JournalofAnatomy199:133–141.Arecentoverviewofthegeneticbasisofgillarch

formationisfoundinKuratani,S.(2004)Evolutionofthevertebratejaw:comparativeembryologyandmoleculardevelopmentalbiologyrevealthefactorsbehindevolutionarynovelty,JournalofAnatomy205:335–347.Examplesoftheexperimentalmanipulationofonegillarchintoanother,usinggenetictechnologies,includeBaltzinger,M.,Ori,M.,Pasqualetti,M.,Nardi,I.,Riji,F.(2005)Hoxa2knockdowninXenopusresultsinhyoidtomandibular

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homeosis,DevelopmentalDynamics234:858–867;Depew,M.,Lufkin,T.,Rubenstein,J.(2002)SpecificationofjawsubdivisionsbyDlxgenes,Science298:381–385.Acomprehensive,well-illustrated,andinformative

resourceforearlyfossilrecordsofskulls,heads,andprimitivefishisreviewedinP.Janvier,EarlyVertebrates(Oxford,Eng.:OxfordUniversityPress,1996).ThepaperdescribingHaikouella,the530-million-year-oldwormwithgills,isChen,J.-Y.,Huang,D.Y.,andLi,C.W.(1999)AnearlyCambriancraniate-likechordate,Nature402:518–522.

CHAPTERSIXTHEBEST-LAID(BODY)PLANS

Theoriginofbodyplanshasbeenthesubjectofanumberofbook-lengthtreatments.Foronewithanexceptionalscopeandbibliography,gotoJ.Valentine,OntheOriginofPhyla(Chicago:UniversityofChicagoPress,2004).TherehavebeenseveralbiographiesofvonBaer.Ashort

oneisJaneOppenheimer,“Baer,KarlErnstvon,”inC.Gillespie,ed.,DictionaryofScientificBiography,vol.1(NewYork:Scribners,1970).Formoredetailedtreatments,seeAutobiographyofDr.KarlErnstvonBaer,ed.JaneOppenheimer(1986;originallypublishedinGerman,2nded.,1886).SeealsoB.E.Raikov,KarlErnstvonBaer,1792–1876,trans.fromRussian(1968),andLudwigStieda,KarlErnstvonBaer,2nded.(1886).Alltheseresourceshavelargebibliographies.SeealsoS.Gould,OntogenyandPhylogeny(Cambridge,Mass.:HarvardUniversityPress,

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1977),foradiscussionofvonBaer’slaws.SpemannandMangold’sexperimentsarediscussedin

embryologytextbooks:S.Gilbert,DevelopmentalBiology,8thed.(Sunderland,Mass.:SinauerAssociates,2006).AmoderngeneticperspectiveontheOrganizeriscontainedinDeRobertis,E.M.(2006)Spemann’sorganizerandselfregulationinamphibianembryos,NatureReviews7:296–302,andDeRobertis,E.M.,andArecheaga,J.TheSpemannOrganizer:75yearson,InternationalJournalofDevelopmentalBiology45(specialissue).ForaccesstothehugeliteratureonHoxgenesand

evolution,thebeststartingreferenceisSeanCarroll’srecentbookEndlessFormsMostBeautiful(NewYork:Norton,2004).ArecentreviewandinterpretationofthewaysthatgenesallowustounderstandthecommonancestorofbilaterallysymmetricalanimalsisinErwin,D.,andDavidson,E.H.(2002)Thelastcommonbilaterianancestor,Development129:3021–3032.Anumberofinvestigatorsarguethatagenetic“flip”

betweenthebodyplanofananthropodandthebodyplanofahumanhappenedsometimeinthedistantpast.ThisideaisdiscussedinDeRobertis,E.,andSasai,Y.(1996)AcommonplanfordorsoventralpatterninginBilateria,Nature380:37–40.HistoricalperspectiveonSt.Hilaire’sviews,aswellasothercontroversiesintheearlyyearsofcomparativeanatomy,arefoundinT.Appel,TheCuvier-GeoffroyDebate:FrenchBiologyintheDecadesBeforeDarwin(NewYork:OxfordUniversityPress,1987).Data

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fromacornwormsdoesnoteasilyfitthismodel,andsuggeststhatinsometaxathemapbetweengeneactivityandaxisspecificationmayhaveevolved.Forthiswork,seeLowe,C.J.,etal.(2006)Dorsoventralpatterninginhemichordates:insightsintoearlychordateevolution,PLoSBiologyonlineaccess:http://dx.doi.org/journal.0040291.Theevolutionofthegenesthatdeterminethebodyaxes

isreviewedinMartindale,M.Q.(2005)Theevolutionofmetazoanaxialproperties,NatureReviewsGenetics6:917–927.Bodyplangenesincnidarians(jellyfish,seaanemones,andtheirrelatives)arediscussedinaseriesofprimarypapers:Martindale,M.Q.,Finnerty,J.R.,Henry,J.(2002)TheRadiataandtheevolutionaryoriginsofthebilaterianbodyplan,MolecularPhylogeneticsandEvolution24:358–365;Matus,D.Q.,Pang,K.,Marlow,H.,Dunn,C.,Thomsen,G.,Martindale,M.(2006)Molecularevidencefordeepevolutionaryrootsofbilateralityinanimaldevelopment,ProceedingsoftheNationalAcademyofSciences103:11195–11200;Chourrout,D.,etal.(2006)MinimalprotohoxclusterinferredfrombilaterianandcnidarianHoxcomplements,Nature442:684–687;Martindale,M.,Pang,K.,Finnerty,J.(2004)Investigatingtheoriginsoftriploblasty:“mesodermal”geneexpressioninadiploblasticanimal,theseaanemoneNemostellavectensis(phylum,Cnidaria;class,Anthozoa),Development131:2463–2474;Finnerty,J.,Pang,K.,Burton,P.,Paulson,D.,Martindale,M.Q.(2004)Deeporiginsforbilateralsymmetry:HoxandDppexpressioninaseaanemone,Science304:1335–1337.

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CHAPTERSEVENADVENTURESINBODYBUILDING

Threekeyarticlesreviewtheoriginsandevolutionofbodiesandofferanintegrativeperspectiveongenetics,geology,andecology:King,N.(2004)Theunicellularancestryofanimaldevelopment,DevelopmentalCell7:313–325;Knoll,A.H.,andCarroll,S.B.(1999)Earlyanimalevolution:Emergingviewsfromcomparativebiologyandgeology,Science284:2129–2137;Brooke,N.M.,andHolland,P.(2003)Theevolutionofmulticellularityandearlyanimalgenomes,CurrentOpinioninGeneticsandDevelopment13:599–603.Allthreepapersarewellreferencedandofferagoodintroductiontothetopicsofthechapter.Forstimulatingtreatmentsoftheconsequencesofthe

originofbodiesandofothernewformsofbiologicalorganization,seeL.W.Buss,TheEvolutionofIndividuality(Princeton:PrincetonUniversityPress,2006),andJ.MaynardSmith,andE.Szathmary,TheMajorTransitionsinEvolution(NewYork:OxfordUniversityPress,1998).ThestorybehindtheEdiacariananimalsiscovered,with

references,inRichardFortey’sLife:ANaturalHistoryoftheFirstFourBillionYearsofLifeonEarth(NewYork:Knopf,1998),andAndrewKnoll’sLifeonaYoungPlanet(Princeton:PrincetonUniversityPress,2002).Theexperimentthatyielded“proto-bodies”from“no-

bodies”isdescribedinBoraas,M.E.,Seale,D.B.,Boxhorn,J.(1998)Phagotrophybyaflagellateselectsforcolonialprey:Apossibleoriginofmulticellularity,EvolutionaryEcology

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12:153–164.

CHAPTEREIGHTMAKINGSCENTS

TheUniversityofUtahhasaneffectivewebsite,Learn.Genetics,thatprovidesawonderfullysimplekitchenprotocolforextractingDNA.TheURLishttp://learn.genetics.utah.edu/units/activities/extraction/.Theevolutionoftheso-calledodorgenesor,more

precisely,olfactoryreceptorgeneshasalargeliterature.BuckandAxel’sseminalpaperisBuck,L.,andAxel,R.(1991)Anovelmultigenefamilymayencodeodorantreceptors:amolecularbasisforodorrecognition,Cell65:175–181.Comparativeaspectsofolfactorygeneevolutionare

treatedinYoung,B.,andTrask,B.J.(2002)Thesenseofsmell:genomicsofvertebrateodorantreceptors,HumanMolecularGenetics11:1153–1160;Mombaerts,P.(1999)Molecularbiologyofodorantreceptorsinvertebrates,AnnualReviewsofNeuroscience22:487–509.Olfactoryreceptorgenesinjawlessfisharediscussedin

Freitag,J.,Beck,A.,Ludwig,G.,vonBuchholtz,L.,Breer,H.(1999)Ontheoriginoftheolfactoryreceptorfamily:receptorgenesofthejawlessfish(Lampetrafluviatilis),Gene226:165–174.ThedistinctionbetweenaquaticandterrestrialolfactoryreceptorgenesisdescribedinFreitag,J.,Ludwig,G.,Andreini,I.,Rossler,P.,Breer,H.(1998)Olfactoryreceptorsinaquaticandterrestrialvertebrates,

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JournalofComparativePhysiologyA183:635–650.Humanolfactoryreceptorevolutionisdiscussedina

numberofpapers.Thisselectionreflectstheissuesdiscussedinthetext:Gilad,Y.,Man,O.,Lancet,D.(2003)Humanspecificlossofolfactoryreceptorgenes,ProceedingsoftheNationalAcademyofSciences100:3324–3327;Gilad,Y.,Man,O.,andGlusman,G.(2005)Acomparisonofthehumanandchimpanzeeolfactoryreceptorgenerepertoires,GenomeResearch15:224–230;Menashe,I.,Man,O.,Lancet,D.,Gilad,Y.(2003)Differentnosesfordifferentpeople,NatureGenetics34:143–144;Gilad,Y.,Wiebe,V.,Przeworski,M.,Lancet,D.,Paabo,S.(2003)Lossofolfactoryreceptorgenescoincideswiththeacquisitionoffulltrichromaticvisioninprimates,PLoSBiologyonlineaccess:http://dx.doi.org/journal.pbio.0020005.Thenotionofgeneduplicationasanimportantsourceof

newgeneticvariationtracestotheseminalworkofOhnoalmostfortyyearsago:S.Ohno,EvolutionbyGeneDuplication(NewYork:Springer-Verlag,1970).ArecentreviewoftheissuethatcontainsadiscussionofbothopsinsandolfactoryreceptorgenesisfoundinTaylor,J.,andRaes,J.(2004)Duplicationanddivergence:theevolutionofnewgenesandoldideas,AnnualReviewsofGenetics38:615–643.

CHAPTERNINEVISION

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Opsingenesintheevolutionofeyeshavebeendescribedinanumberofpapersinrecentyears.ReviewsofthebasicbiologyandtheconsequencesofopsingeneevolutionincludeNathans,J.(1999)Theevolutionandphysiologyofhumancolorvision:insightsfrommoleculargeneticstudiesofvisualpigments,Neuron24:299–312;Dominy,N.,Svenning,J.C.,Li,W.H.(2003)Historicalcontingencyintheevolutionofprimatecolorvision,JournalofHumanEvolution44:25–45;Tan,Y.,Yoder,A.,Yamashita,N.,Li,W.H.(2005)Evidencefromopsingenesrejectsnocturnalityinancestralprimates,ProceedingsoftheNationalAcademyofSciences102:14712–14716;Yokoyama,S.(1996)Molecularevolutionofretinalandnonretinalopsins,GenestoCells1:787–794;Dulai,K.,vonDornum,M.,Mollon,J.,Hunt,D.M.(1999)TheevolutionoftrichromaticcolorvisionbyopsingeneduplicationinNewWorldandOldWorldprimates,Genome9:629–638.DetlevArendtandJoachimWittbrodt’sworkon

photoreceptortissueswasoriginallydescribedinapaperfromtheprimaryliterature:Arendt,D.,Tessmar-Raible,K.,Synman,H.,Dorresteijn,A.,Wittbrodt,J.(2004)Ciliaryphotoreceptorswithavertebrate-typeopsininaninvertebratebrain,Science306:869–871.Anassociatedcommentaryappearedwiththepiece:Pennisi,E.(2004)Worm’slight-sensingproteinssuggesteye’ssingleorigin,Science306:796–797.AnearlierreviewbyArendtprovidesthelargerframeworkthatheusestointerpretthediscovery:Arendt,D.(2003)Theevolutionofeyesand

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photoreceptorcelltypes,InternationalJournalofDevelopmentalBiology47:563–571.FurthercommentarycanbefoundinPlachetzki,D.C.,Serb,J.M.,Oakley,T.H.(2005)Newinsightsintophotoreceptorevolution,TrendsinEcologyandEvolution20:465–467.StillmorecommentaryonArendtandWittbrodt’sworkbyBerndFritzschandJoramPiatigorskyappearedinalaterissueofScience,withacomment-replythatdiscussedthenotionthattheoriginofeyesmaybeextremelyancient,andtracedtoaverydeepbranchofourevolutionarytree.ThistextcanbefoundinScience(2005)308:1113–1114.AreviewofWalterGehring’sworkonPax6andits

consequencesforeyeevolutioniscontainedinapersonalaccount:Gehring,W.(2005)Newperspectivesoneyedevelopmentandtheevolutionofeyesandphotoreceptors,JournalofHeredity96:171–184.Papersthatlookatthedifferentpossiblerelationships

betweenconservedeyeformationgenesandtheevolutionofeyeorgansincludeOakley,T.(2003)Theeyeasareplicatinganddivergingmodulardevelopmentalunit,TrendsinEcologyandEvolution18:623–627,andNilssonD.-E.(2004)Eyeevolution:aquestionofgeneticpromiscuity,CurrentOpinioninNeurobiology14:407–414.Therelationshipbetweenthelensproteinsinoureyes

andthoseoflarvalseasquirtsisdiscussedinShimeld,S.,Purkiss,A.G.,Dirks,R.P.H.,Bateman,O.,Slingsby,C.,Lubsen,N.(2005)Urochordateby-crystallinandtheevolutionaryoriginofthevertebrateeyelens,CurrentBiology15:1684–

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1689.

CHAPTERTENEARS

ThegeneticsofinnerearevolutionisdiscussedinBeisel,K.W.,andFritzsch,B.(2004)Keepingsensorycellsandevolvingneuronstoconnectthemtothebrain:molecularconservationandnoveltiesinvertebrateeardevelopment,BrainBehaviorandEvolution64:182–197.EardevelopmentandthegenesbehinditarediscussedinRepresa,J.,Frenz,D.A.,VandeWater,T.(2000)Geneticpatterningofembryoniceardevelopment,ActaOtolaryngolica120:5–10.Thetransformationofthehyomandibulaintothestapes

isreviewedincomprehensivebook-lengthtreatmentsoftheevolutionofprimitivefishortheoriginofland-livinganimals:J.Clack,GainingGround(Bloomington:IndianaUniversityPress,2002);P.Janvier,EarlyVertebrates(Oxford,Eng.:OxfordUniversityPress,1996).Itisalsodiscussedinrecentresearchpapers,includingClack,J.A.(1989)Discoveryoftheearliestknowntetrapodstapes,Nature342:425–427;Brazeau,M.,andAhlberg,P.(2005)Tetrapod-likemiddleeararchitectureinaDevonianfish,Nature439:318–321.Theoriginofthemammalianmiddleearisdiscussed

fromtheperspectiveofascientifichistorianinP.Bowler,Life’sSpendidJourney(Chicago:UniversityofChicagoPress,1996).Keyprimarysourcesinclude:Reichert,C.(1837)UberdieVisceralbogenderWirbeltiereimallgemeinenund

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derenMetamorphosenbeidenVogelnundSaugetieren,Arch.Anat.Physiol.Wiss.Med.1837:120–222;Gaupp,E.(1911)BeiträgezurKenntnisdesUnterkiefersderWirbeltiereI.DerProcessusanterior(Folii)desHammersderSaugerunddasGonialederNichtsäuger,AnatomischerAnzeiger39:97–135;Gaupp,E.(1911)BeiträgezurKenntnisdesUnterkiefersderWirbeltiereII.DieZusammensetzungdesUnterkiefersderQuadrupeden,AnatomischerAnzeiger,39:433–473;Gaupp,E.(1911)BeiträgezurKenntnisdesUnterkiefersderWirbeltiereIII.DasProblemederEntstehungeines“sekundären”KiefergelenkesbeidenSäugern,AnatomischerAnzeiger,39:609–666;Gregory,W.K.(1913)Critiqueofrecentworkonthemorphologyofthevertebrateskull,especiallyinrelationtotheoriginofmammals,JournalofMorphology24:1–42.Majorliteratureontheoriginofthemammalianjaw,

chewing,andthethree-bonedmiddleearincludesCrompton,A.W.(1963)Theevolutionofthemammalianjaw,Evolution17:431–439;Crompton,A.W.,andParker,P.(1978)Evolutionofthemammalianmasticatoryapparatus,AmericanScientist66:192–201;Hopson,J.(1966)Theoriginofthemammalianmiddleear,AmericanZoologist6:437–450;Allin,E.(1975)Evolutionofthemammalianear,JournalofMorphology147:403–438.TheevolutionaryoriginofPax2andPax6andthe

evolutionarylinkofearsandeyestoboxjellyfishisdiscussedinPiatigorsky,J.,andKozmik,Z.(2004)Cubozoanjellyfish:anevo/devomodelforeyesandothersensory

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systems,InternationalJournalforDevelopmentalBiology48:719–729.Linksofsensoryreceptormoleculestodifferent

moleculesinbacteriaarediscussedinKung,C.(2005)Apossibleunifyingprincipleformechanosensation,Nature436:647–654.

CHAPTERELEVENTHEMEANINGOFITALL

Themethodsofphylogeneticsystematicsarediscussedinanumberofsources.KeyprimaryliteratureincludestheclassicworkofWilliHennig,publishedoriginallyinGerman(GrundzügeeinerTheoriederphylogenetischenSystematik[Berlin:DeutscherZentralverlag,1950])andtranslatedintoEnglishmorethanadecadelater(PhylogeneticSystematics,trans.D.D.DavisandR.Zangerl[Urbana:UniversityofIllinoisPress,1966]).Methodsofphylogeneticreconstruction,whichformthe

basisforthechapter,arediscussedindetailinP.Forey,ed.,Cladistics:APracticalCourseinSystematics(Oxford,Eng.:ClarendonPress,1992);D.Hillis,C.Moritz,andB.Mable,eds.,MolecularSystematics(Sunderland,Mass.:SinauerAssociates,1996);R.DeSalle,G.Girbet,andW.Wheeler,MolecularSystematicsandEvolution:TheoryandPractice(Basel:BirkhauserVerlag,2002).Acomprehensivetreatmentofthephenomenonof

independentevolutionofsimilarfeaturesisinM.SandersonandL.Hufford,Homoplasy:TheRecurrenceof

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SimilarityinEvolution(SanDiego:AcademicPress,1996).Toseethetreeoflifeandthedifferenthypothesesforthe

relationshipsbetweenlivingcreatures,visithttp://tolweb.org/tree/.Thenotionthatourevolutionaryhistoryhasmedical

implicationshasbeenthesubjectofseveralgoodrecentbooks.Forcomprehensiveandwell-referencedtreatments,seeN.Boaz,EvolvingHealth:TheOriginsofIllnessandHowtheModernWorldIsMakingUsSick(NewYork:Wiley,2002);D.Mindell,TheEvolvingWorld:EvolutioninEverydayLife(Cambridge,Mass.:HarvardUniversityPress,2006);R.M.NesseandG.C.Williams,WhyWeGetSick:TheNewScienceofDarwinianMedicine(NewYork:Vintage,1996);W.R.Trevathan,E.O.Smith,andJ.J.McKenna,EvolutionaryMedicine(NewYork:OxfordUniversityPress,1999).TheapneaexampleIderivedfromdiscussionswithNino

Ramirez,chairmanoftheDepartmentofAnatomyattheUniversityofChicago.ThehiccupexampleisderivedfromStraus,C.,etal.(2003)Aphylogenetichypothesisfortheoriginofhiccoughs,Bioessays25:182–188.Thehuman-bacterialgeneswitchusedinthestudyofmitochondrialcardioencephalomyopathywasoriginallydiscussedinLucioli,S.,etal.(2006)IntroducinganovelhumanmtDNAmutationintotheParacoccusdenitriticansCOX1geneexplainsfunctionaldeficitsinapatient,Neurogenetics7:51–57.

ONLINERESOURCES

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Anumberofwebsitesandblogscarryaccurateinformationandareupdatedfrequently.

http://www.ucmp.berkeley.edu/ProducedbytheMuseumofPaleontologyattheUniversityofCalifornia–Berkeley,thisisoneofthebestonlineresourcesonpaleontologyandevolution.Itiscontinuouslyupdatedandrevised.

http://www.scienceblogs.com/loom/ThisisCarlZimmer’sblog,awell-written,timely,andthoughtfulsourceofinformationanddiscussiononevolution.

http://www.scienceblogs.com/pharyngula/P.Z.Myers,aprofessorofdevelopmentalbiology,writesthisaccessible,informative,andcutting-edgeblog.Thisisarichsourceofinformation,wellworthfollowing.

BothZimmer’sandMyers’sblogsareathttp://www.scienceblogs.com,asitethatcontainsanumberofexcellentblogsalsoworthfollowingforinformationandcommentaryonrecentdiscoveries.BlogsrelevanttothethemeofthisbookatthatsiteincludeAfarensis,TetrapodZoology,EvolvingThoughts,andGeneExpression.

http://www.tolweb.org/tree/TheTreeofLifeProjectprovidesaregularlyupdatedandauthoritativetreatmentoftherelationshipsamongallgroupsoflife.LiketheUCMP

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pageatBerkeley,italsoincludesresourcesforlearningabouthowevolutionarytreesaremadeandinterpreted.

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ACKNOWLEDGMENTS

Alltheillustrations,exceptwherenoted,arebyMs.KalliopiMonoyios(www.kalliopimonoyios.com).Kapireaddraftsofthemanuscriptandnotonlyimprovedthetextbutdesignedartthatmatchedit.Ihavebeentrulyfortunatetoworkwithsomeonewithsomanytalents.ScottRawlins(ArcadiaUniversity)generouslygavepermissiontousehiselegantrenderingofSauripterusinChapter2.TedDaeschler(AcademyofNaturalSciencesofPhiladelphia)graciouslyprovidedhissuperbphotosofthegreatTiktaalik“C”specimen.ThanksareduetoPhillipDonoghue(UniversityofBristol)andMarkPurnell(UniversityofLeicester)forpermissiontousetheirrenderingoftheconodonttootharray,McGraw-HillforpermissiontousethetextbookfigurethatstartedthehuntforTiktaalik,andStevenCampanaoftheCanadianSharkResearchLaboratoryforthephotosofsharkorgans.Oneofthegreatestdebtsstudentsofanatomyhaveisto

thepeoplewhodonatetheirbodiessothatwecanlearn.Itisarareprivilegetolearnfromarealbody.Sittingthroughlonghoursinthelab,onefeelsaveryprofoundconnection

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tothedonorswhomaketheexperiencepossible.Ifeltthatconnectionagainwhilewritingthisbook.TheideasIpresentherearerootedinresearchI’vedone

andinclassesI’vetaught.Colleaguesandstudentstoonumeroustoname—undergraduates,medicalstudents,andgraduatestudents—haveplayedaroleinthethinkingthatwentintothesepages.IoweagreatdebttothecolleaguesIhaveworkedwith

overtheyears.TedDaeschler,FarishA.Jenkins,Jr.,FredMullison,PaulOlsen,WilliamAmaral,JasonDowns,andChuckSchaffhaveallbeenpartofthestoriesItellhere.WithoutthesepeopleIwouldhavehadnoreservoirofexperienceonwhichtodraw,norwouldIhavehadasmuchfunalongtheway.MembersofmylaboratoryattheUniversityofChicago—RandallDahn,MarcusDavis,AdamFranssen,AndrewGillis,ChristianKammerer,KalliopiMonoyios,andBeckyShearman—allinfluencedmythinkingandtoleratedmytimeawayfromthebenchasIwrote.Colleagueswhogavetheirtimetoprovideneeded

backgroundorcommentsonthemanuscriptincludeKamlaAhluwalia,SeanCarroll,MichaelCoates,RandallDahn,MarcusDavis,AnnaDiRienzo,AndrewGillis,LanceGrande,ElizabethGrove,NicholasHatsopoulos,RobertHo,BettyKatsaros,MichaelLaBarbera,ChrisLowe,DanielMargoliash,KalliopiMonoyios,JonathanPritchard,VickyPrince,CliffRagsdale,NinoRamirez,CallumRoss,AviStopper,CliffTabin,andJohnZeller.HaythamAbu-Zaydhelpedwithmanyadministrativematters.Myownteachers

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ofanatomyintheHarvard–MITHealthSciencesandTechnologyprogram,FarishA.Jenkins,Jr.,andLeeGehrke,stimulatedaninterestthathaslastedovertwentyyears.Keyadviceattheinceptionoftheproject,andinspiration

throughout,camefromSeanCarrollandCarlZimmer.TheWellfleetPublicLibrary(Wellfleet,Massachusetts)

providedacomfortablehome,andmuch-neededretreat,whereIwrotesignificantpartsofthebook.AbriefstintattheAmericanAcademyinBerlinputmeinanenvironmentthatprovedcriticalwhenIwascompletingthemanuscript.Mytwobosses,Dr.JamesMadara,M.D.(CEO,University

ofChicagoMedicalCenter,VicePresidentforMedicalAffairs,DeanandSaraandHaroldThompsonDistinguishedServiceProfessorintheBiologicalSciencesDivisionandthePritzkerSchoolofMedicine),andJohnMcCarter,Jr.(CEO,TheFieldMuseum),supportedthisprojectandtheresearchbehindit.Ithasbeenatruepleasuretoworkwithsuchinsightfulandcompassionateleaders.IhavebeenfortunatetoteachattheUniversityof

ChicagoandtohavehadtheopportunitytointeractwiththeleadershipofthePritzkerSchoolofMedicinethere.Thedeans,HollyHumphreyandHalinaBruckner,graciouslywelcomedapaleontologisttotheirteam.ThroughinteractingwiththemIcametoappreciatethechallengesandimportanceofbasicmedicaleducation.IthasbeenagreatpleasuretobeassociatedwithThe

FieldMuseuminChicago,whereIhavehadtheopportunitytoworkwithauniquegroupofpeoplededicatedto

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scientificdiscovery,application,andoutreach.ThesecolleaguesincludeElizabethBabcock,JosephBrennan,SheilaCawley,JimCroft,LanceGrande,MelissaHilton,EdHorner,DebraMoskovits,LauraSadler,SeanVanDerziel,andDianeWhite.Iamalsogratefulforthesupport,guidance,andencouragementIhavereceivedfromtheleadersoftheCommitteeonScienceoftheBoardofTrusteesatTheFieldMuseum,JamesL.AlexanderandAdeleS.Simmons.Iamindebtedtomyagent,KatinkaMatson,forhelping

meturnanideaintoaproposalandforadvicethroughouttheprocess.IfeelprivilegedtohaveworkedwithMartyAsher,myeditor.Likeapatientteacher,hegavemeanurturingcombinationofadvice,time,andencouragementtohelpmefindmyway.ZacharyWagmancontributedtothisprojectincountlesswaysbybeingfreewithhistime,keeneditorialeye,andgoodcounsel.DanFrankmadeinsightfulsuggestionsthatstimulatedmetothinkaboutthestoryinnewways.JolantaBenalcopyeditedthetextandimprovedthepresentationimmeasurably.IamverygratefultoEllenFeldman,KristenBearse,andtheproductionteamfortheirhardworkunderatightschedule.Myparents,GloriaandSeymourShubin,alwaysknew

thatIwouldwriteabook,evenbeforeIdid.Withouttheirfaithinme,IdoubtthatIeverwouldhaveputawordonpaper.Mywife,MicheleSeidl,andourchildren,Nathanieland

Hannah,havebeenlivingwithfish—bothTiktaalikandthis

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book—forthebetterpartoftwoyears.MichelereadandcommentedoneverydraftofthistextandsupportedlongweekendabsenceswhileIwrote.Herpatienceandlovemadeitallpossible.

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Copyright©2008byNeilShubin

Allrightsreserved.PublishedintheUnitedStatesby

PantheonBooks,adivisionofRandomHouse,Inc.,NewYork,andinCanadabyRandomHouseofCanadaLimited,

Toronto.PantheonBooksandcolophonareregisteredtrademarksof

RandomHouse,Inc.AllillustrationsbyKalliopiMonoyiosunlessotherwise

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Shubin,Neil.Yourinnerfish:ajourneyintothe3.5-billion-yearhistory

ofthehumanbody/ByNeilShubin.—1sted.p.cm.

Includesbibliographicalreferences.eISBN:978-0-307-37716-6

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