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1 Godefroit, P., Sinitsa, S. M., Dhouailly, D., Bolotsky, Y. L., Sizov, A. V., McNamara, M. E.,... Spagna, P. (2014). Dinosaur evolution. A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science, 345(6195), DOI: /science Early version, also known as pre-print Link to published version (if available): /science Link to publication record in Explore Bristol Research PDF-document This is the author's version of the work. It is posted here by permission of the AAAS for personal use, not for redistribution. The definitive version was published in Vol. 345 no pp , doi: /science University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available:
2 1 EVOLUTION How$birds$became$birds Sustainedsizereductionwasessentialfortheoriginofbirdsandavianflight ByMichaelJ.Benton $ Birdsevolvedfromdinosaurs,buthowlongdidthisevolutionarytransitiontake? Twentyyearsago,itwaswidelyassumedthatthefirstbird Archaeopteryx,which livedinthelatejurassic(seethephoto) evolveditsfeathers,wings,andabilityto flywithinjust10millionyearsorso.sincethen,ithasbecomeclearthatmostofthe 30ormorecharacteristicsthatdistinguishedthesmall,flyingArchaeopteryxfrom groundodwelling,carnivorousdinosaurs(theropods)emergedmuchearlier.on page562ofthisissue,leeetal.(1)provideevidenceforsustainedminiaturization for50millionyearsbeforearchaeopteryxevolved(seethegraph). Thestoryofthisrevolutionbeginsin1994,whenpaleontologistsfromChina broughtphotographsofamazingnewfossilstotheannualmeetingofthesocietyof VertebratePaleontologyinNewYork.Thephotosshowedasmalldinosaurwithout wingsorotherbirdcharacters,butcoveredwithafuzzoffeathers.thiswasthe beginningofafloodofchinesetheropodfossilswithfeathersofallkinds,from simplebristlesthroughbrancheddownfeatherstofullyelaboratedflightotype feathers(2,3).sometheropoddinosaursevenhadextendedforearmsandquillolike feathersarrangedaswings.thedromaeosauridmicroraptoralsohaddistinctwings onitslegs,resurrectingtheold tetrapteryx, asupposedfourowingedprecursorof moderntwoowingedbirds(4).thefossilsshowedthatfromabout170to120 millionyearsago,allthesedinosaurs theparaves wereexperimentingwithflight invariousmodes,includingparachuting,gliding,andleapingfromtreetotree.one clade,representedbyarchaeopteryx,madethecrucialleaptopoweredflight,andso birdswereborn. Feathersaresotypicallyaviantodaythattheyareoftenseenasthekey characterofbirds.however,feathersaroseatleast50millionyearsbefore Archaeopteryx,andperhapsmuchearlier(5).Theypresumablyarosefirstfor insulationanddisplay,aswitnessedbythecolorful,patternedfeathersofdinosaurs (6,7),andwerethencoOoptedinexpandedglidingsurfacesandincreasinglyin substantial,aerodynamicwingstructuresamongparaves(8). So,whatmakesabirdabirdandnotaflyingdinosaur?AsLeeetal.show,the keyseemstobeminiaturization.thetrendtominiaturizationinparaveshad alreadybeennotedinsizecomparisonsacrossalltheropods(9).macroevolutionary analysishasconfirmedthatthissizereductionhappenedatevolutionaryrates150 timesfasterthannormal(10).leeetal.nowshowthatminiaturizationwasalongo termtrendover50millionyears(seethegraph).thestudyisbasedonanalysisof anenormousdatasetandusessophisticatedanalyticaltools.theauthorslookedat 120speciesoftheropoddinosaursandearlybirds,codedfor1549skeletal characters(adatamatrixcomprising185,880cells),andcalculatedthebestofitting phylogenetictreewhilealsoexploringevolutionaryrates. Untilrecently,paleontologistsreliedonqualitativeapproachestoestablish narrativesofchangethroughgeologictime.theyusedcladisticmethodstodiscover
3 2 bestofittingormostlikelyphylogenetictrees;evolutionarychangewasthenmapped looselyoverthetree.now,phylogeneticcomparativemethods(11)makeitpossible tocalculateancestralstatesofanycharacter,andtoestablishpointsofunusually fastorslowratesofchange.such diversificationshifts helpindeterminingthe mostlikelyevolutionarymodelsforatreeorpartofatree. Earlierstudies(9,10)usedthreesteps:buildthetree,datethebranching points,andthenmapthecharacters.leeetal.ranallthreecalculations simultaneously,workingwithphylogeneticinformation,geologicdatesfor branchingpoints,andcharacterstatereconstructionsatthesametime.allmethods arewellestablished,anditisnotclearwhichapproachismostreliable.theyallgive similarresultsinthiscase. Theauthorsfindthattheropodbodysizedecreased12times,fromaninitial meanmassof163kgto0.8kginarchaeopteryx.howcouldsuchalongotermtrend bemaintained?leeetal.notethatminiaturizationbroughtnumerouschanges, becauseitshortenednormaldevelopmentalpatterns.forexample,birdheadscan beseenasdinosaurheadsthatretainjuvenilefeaturesintheadult(pedomorphic) (12),withshortsnouts,largebrains,andlargeeyes(seethefigure).Smallersize mightalsohavebeenfacilitatedbycoooptionoffeathersforinsulation.inaddition, birdshavedecoupledhindlimbsandforelimbs(13),allowingeachlimbsetto functionindependently,unlikeinmostothertetrapods(seethefigure).whatmight havetriggeredthesechanges? Thecrucialdrivermayhavebeenamovetothetrees,perhapstoescapefrom predationortoexploitnewfoodresources.treelivingrequiressmallbodies,and reducedbodysizeenablesothercharacteristicsthatenhancesuccessinthetrees, suchasenlargedeyesforthreeodimensionalvision(soavoidingcollisionswhen leapingfrombranchtobranch);enlargedbrainstocopewithdiversearboreal habitats;insulatingfeatherstoenablenocturnalactivity(manyinsectsarenocturnal toevadecoldobloodedpredators);andelongatedforelimbs,distinctfromthe hindlimbsintheirfunction,andwithexpandedflightsurfacestoenableevermore daringleapsfromtreetotree.thephysicalchangesarereminiscentofthosethat lateroccurredinourownclade,theprimates,alsointerpretedasdrivenbytree living. REFERENCES 1.M.S.Y.Leeetal.,Science345,562(2014). 2.P.Chen,Z.Dong,S.Zhen,Nature391,147(1998). 3.J.Qiangetal.,Nature393,753(1998). 4.X.Xu,Z.Zhou,X.Wang,Nature408,705(2000). 5.P.Godefroitetal.,Science345,451(2014). 6.F.Zhangetal.,Nature463,1075(2010). 7.Q.Lietal.,Science327,1369(2010). 8.J.Clarke,Science340,690(2013). 9.A.H.Turneretal.,Science317,1378(2007). 10.M.N.Putticketal.,Evolution68,1497(2014). 11.J.S.Felsenstein,Am.Nat.125,1(1985). 12.B.OA.S.Bhullaretal.,Nature487,223(2012).
4 3 13.V.Allenetal.,Nature497,104(2013). FIGURECAPTIONS: Early$bird.FossilsofArchaeopteryx,whichlivedaround150millionyearsago, provideimportantcluestohowbirdsevolvedfromtheirtheropodancestors. Making$a$bird$from$a$dinosaur.Keycharacteristicsofbirdsthatdistinguishthem fromtheirtheropodancestorsincludequillolikefeathers,forelimbsthatare decoupledfromhindlimbs,apedomorphicskull,andsmallsize. Getting$smaller.Leeetal.showthatbetween210and160millionyearsago(Ma), theancestorsoftoday sbirdsshrankatarapidevolutionaryrate,ascapturedbythe lengthofthefemur(thighbone).thiswascrucialtoenableflight. SchoolofEarthSciences,UniversityofBristol,BristolBS81RJ,
5 2.8 Coelurosaurs Femur length (log10) Body size miniaturization Maniraptorans Paraves Birds Myr TRIASSIC JURASSIC Geological time Ceratosaurus massive size reduction; feathers; forelimb decoupled from hindlimb Pedomorphic skull (juvenilized features, including large eyes and large brain Elongate forelimb, perhaps for gliding wing Deinonychus Forelimb forms wing for powered flight Archaeopteryx
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