Published in -RXUQDORI([SHULPHQWDO=RRORJ\3DUW%0ROHFXODUDQG 'HYHORSPHQWDO(YROXWLRQGRLMH]E which should be cited to refer to this work. 4HE /RIGIN OF 4URTLES ! 0ALEONTOLOGICAL 0ERSPECTIVE 7!,4%2 ' */9#% $EPARTMENT OF 'EOSCIENCE 5NIVERSITY OF &RIBOURG &RIBOURG 3WITZERLAND 4HE ORIGIN OF TURTLES AND THEIR UNUSUAL BODY PLAN HAS FASCINATED SCIENTISTS FOR THE LAST TWO CENTURIES /VER THE COURSE OF THE LAST DECADES A BROAD SAMPLE OF MOLECULAR ANALYSES HAVE FAVORED A SISTER GROUP RELATIONSHIP OF TURTLES WITH ARCHOSAURS BUT RECENT STUDIES REVEAL THAT THIS SIGNAL MAY BE THE RESULT OF SYSTEMATIC BIASES AFFECTING MOLECULAR APPROACHES IN PARTICULAR SAMPLING NON RANDOMLY DISTRIBUTED RATE HETEROGENEITY AMONG TAXA AND THE USE AND THE USE OF CONCATENATED DATA SETS -ORPHOLOGICAL STUDIES BY CONTRAST DISFAVOR ARCHOSAURIAN RELATIONSHIPS FOR TURTLES BUT THE PROPOSED ALTERNATIVE TOPOLOGIES ARE POORLY SUPPORTED AS WELL 4HE RECENTLY REVIVED PALEONTOLOGICAL HYPOTHESIS THAT THE -IDDLE 0ERMIAN %UNOTOSAURUS AFRICANUS IS AN INTERMEDIATE STEM TURTLE IS NOW ROBUSTLY SUPPORTED BY NUMEROUS CHARACTERS THAT WERE PREVIOUSLY THOUGHT TO BE UNIQUE TO TURTLES AND THAT ARE NOW SHOWN TO HAVE ORIGINATED OVER THE COURSE OF TENS OF MILLIONS OF YEARS UNRELATED TO THE ORIGIN OF THE TURTLE SHELL !LTHOUGH % AFRICANUS DOES NOT SOLVE THE PLACEMENT OF TURTLES WITHIN !MNIOTA IT SUCCESSFULLY EXTENDS THE STEM LINEAGE OF TURTLES TO THE 0ERMIAN AND HELPS RESOLVE SOME QUESTIONS ASSOCIATED WITH THE ORIGIN OF TURTLES IN PARTICULAR THE NON COMPOSITE ORIGIN OF THE SHELL THE SLOW ORIGIN OF THE SHELL AND THE TERRESTRIAL SETTING FOR THE ORIGIN OF TURTLES 4HE ORIGIN OF TURTLES AND THEIR UNUSUAL BODY PLAN REMAIN SOME OF GIRDLES AND PERHAPS ALSO THE GASTRALIA WITH THE DERMIS AS HAD THE MOST VEXING QUESTIONS IN VERTEBRATE EVOLUTION 4HE DEBATE IS BEEN PREDICTED FOR YEARS BY DEVELOPMENTAL BIOLOGISTS EG UNUSUALLY COMPLEX AS IT INVOLVES SEVERAL INTERRELATED ISSUES IN :ANGERL f "URKE f 'ILBERT ET AL AND NOT THROUGH THE PARTICULAR THE RELATIONSHIP OF TURTLES RELATIVE TO EXTANT AMNIOTES FUSION OF THESE ELEMENTS WITH OSTEODERMS AS HAD LARGELY BEEN EG :ARDOYA AND -EYER f 4ZIKA ET AL &IELD ET AL FAVORED BY PALEONTOLOGISTS EG #OX f ,EE f *OYCE ET AL http://doc.rero.ch THE CLOSEST FOSSIL RELATIVES OF TURTLES EG ,AURIN AND 2EISZ f 4HE kNDING OF / SEMITESTACEA FURTHERMORE SPAWNED DE"RAGA AND 2IEPPEL f ,EE f #ARROLL THE PLACEMENT RENEWED INTEREST IN THE OLD HYPOTHESIS 7ATSON f THAT TURTLES OF THE SHOULDER GIRDLE .AGASHIMA ET AL ,YSON AND MAY BE RELATED TO THE 0ERMIAN TAXON %UNOTOSAURUS AFRICANUS *OYCE THE ORIGIN OF THE TURTLE SHELL EG "URKE f #ARROLL ,YSON ET AL A (OWEVER WHILE .AGASHIMA ET AL 3CHEYER ET AL *OYCE ET AL THE HYPOTHESIS THAT THE -IDDLE 4RIASSIC / SEMITESTACEA IS A ,YSON ET AL A THE SPEED OF THE ORIGIN OF THE TURTLE SHELL EG DERIVED STEM TURTLE HAS BEEN UNIVERSALLY ACCEPTED EG 2IEPPEL *OYCE ET AL AND THE ECOLOGICAL SETTINGS FOR .AGASHIMA ET AL +URATANI ET AL !NQUETIN THE ORIGIN OF TURTLES EG 2IEPPEL AND 2EISZ f *OYCE AND .AGASHIMA ET AL (IRASAWA ET AL LIKELY 'AUTHIER 3CHEYER AND 3ANDER 4HE RECENT DISCOVERY BECAUSE OF THE PRESENCE OF A FULLY DEVELOPED PLASTRON THE OF THE INTERMEDIATE FOSSIL TAXON /DONTOCHELYS SEMITESTACEA FROM REINTERPRETATION OF THE ,ATE 0ERMIAN % AFRICANUS AS AN THE ,ATE 4RIASSIC OF #HINA ,I ET AL SHEDS MUCH LIGHT ON SOME ASPECTS OF THIS DISCUSSION AS IT CLEARLY IS SITUATED OUTSIDE THE PREVIOUSLY RECOGNIZED TURTLE CLADE 4ESTUDINATA HEREIN DEkNED AS Ã#ORRESPONDENCE TO 7ALTER ' *OYCE $EPARTMENT OF 'EOSCIENCE THE CLADE ORIGINATING FROM THE kRST AMNIOTE WITH A FULLY 5NIVERSITY OF &RIBOURG &RIBOURG 3WITZERLAND DEVELOPED TURTLE SHELL ;SENSU *OYCE ET AL = CONSISTING OF % MAIL WALTERGJOYCE GMAILCOM INTERLOCKING NEURALS COSTALS PERIPHERALS PYGALS AND PLASTRAL ELEMENTS ;'AFFNEY AND -EYLAN f= -OST IMPORTANTLY THIS TAXON REVEALS THAT THE ORIGIN OF THE TURTLE SHELL OCCURRED THROUGH THE NOVEL INTERACTION OF THE DORSAL VERTEBRAE AND RIBS THE SHOULDER 1 INTERMEDIATE STEM TURTLE IS LESS QUICKLY GAINING ACCEPTANCE EG -/,%#5,!2 2%35,43 -!9 "% !&&%#4%$ "9 +URATANI ET AL .AGASHIMA ET AL (IRASAWA 3934%-!4)# ")!3%3 ET AL 4HIS RELUCTANCE LIKELY STEMS FROM A SERIES OF 4HE DISCUSSION REGARDING THE ORIGIN OF TURTLES HAS BEEN DOMINATED MISCONCEPTIONS ABOUT AMNIOTE SYSTEMATICS AND THE FOSSIL RECORD OVER THE COURSE OF THE LAST YEARS BY PHYLOGENETIC HYPOTHESES IN PARTICULAR THE REMAINING AMBIGUITY REGARDING THE PHYLOGE OBTAINED FROM MOLECULAR DATA AND ) HEREIN ONLY INTEND TO PROVIDE NETIC POSITION OF TURTLES 4HE PURPOSE OF THIS CONTRIBUTION IS A BRIEF OVERVIEW 4HE kRST DECADE OF MOLECULAR RESEARCH DID NOT THEREFORE TO CLEAR UP THESE MISCONCEPTIONS AND TO SUMMARIZE THE PROVIDE CONSISTENT RESULTS FOR AMNIOTE PHYLOGENY AND TURTLES WERE MOUNTING EVIDENCE IN FAVOR OF % AFRICANUS AS AN INTERMEDIATE VARIOUSLY PLACED AS SISTER TO !VES 0OLLOCK ET AL #OTTON AND STEM TURTLE 0AGE #ROCODILIA (EDGES AND 0OLING f -ANNEN AND ,I f #AO ET AL $IAPSIDA EG #ASPERS ET AL f 3TRIMMER 4(% 42!$)4)/.!, #,!33)&)#!4)/. /& &/33), 2%04),%3 AND VON (AESELER f ,EPIDOSAURIA (EDGES f 4HECODONTIA 53).' 4%-0/2!, &%.%342!% )3 /54 /& $!4% IE -AMMALIA þ !RCHOSAURIA 'ARDINER f OR !RCHOSAURIA 7ILLISTON f PUBLISHED A FUNDAMENTAL TREATMENT OF THE PHYLOGENY EG 0LATZ AND #ONLON f #AO ET AL f :ARDOYA AND -EYER AND CLASSIkCATION OF AMNIOTES BASED ON /SBORNfS @ WORK ON f +UMAZAWA AND .ISHIDA f 2EST ET AL /VER THE TEMPORAL FENESTRATION THAT WAS HIGHLY INlUENTIAL FOR MANY DECADES COURSE OF THE SECOND DECADE HOWEVER THE VAST MAJORITY OF 4HE BASIS OF THIS CLASSIkCATION WAS THE NUMBER OF OPENINGS IN THE ANALYSES UTILIZING MOLECULAR DATA SUPPORTED A SISTER GROUP TEMPORAL REGION OF THE SKULL !CCORDING TO 7ILLISTONfS CLASSIkCATION RELATIONSHIP OF TURTLES TO ARCHOSAURS USING A BROAD RANGE OF TAXA THAT LACK TEMPORAL FENESTRAE ARE GROUPED AS !NAPSIDA DATA AND ANALYTICAL TECHNIQUES EG )WABE ET AL (UGALL EG TURTLES VARIOUS BASAL REPTILES TAXA WITH A PAIR OF UPPER ET AL 3HEN ET AL #HIARI ET AL #RAWFORD ET AL TEMPORAL FENESTRAE AS 0ARAPSIDA AKA %URYAPSIDA EG ICHTHYO &ONG ET AL !BRAMYAN ET AL 3CHAFFER ET AL SAURS AND SQUAMATES TAXA WITH A PAIR OF LOWER TEMPORAL FENESTRAE 7ANG ET AL ALTHOUGH OCCASIONAL SUPPORT WAS ALSO AS 3YNAPSIDA EG MAMMALS AND TAXA WITH TWO PAIRS OF TEMPORAL FOUND FOR A SISTER GROUP RELATIONSHIP WITH CROCODILIANS EG FENESTRAE ARE GROUPED AS $IAPSIDA EG CROCODILIANS 3PHENODON 3HEDLOCK ET AL 4ZIKA ET AL 4HE ONLY MAJOR MOLECULAR 4HE MOST INlUENTIAL NEW STATEMENT UNDER 7ILLISTONfS MODEL IS THAT STUDY TO ARRIVE AT A TRULY CONlICTING RESULT IN THE LAST YEARS WAS THE ANAPSID CONDITION IS PRIMITIVE AND THAT TURTLES ARE CONSEQUENTLY THE STUDY OF ,YSON ET AL UTILIZING MICRO$.! DATA BUT THE TO BE CONSIDERED THE MOST PRIMITIVE OF LIVING AMNIOTES -OST RECENT EXPANSION AND REANALYSES OF THIS DATA SET BY &IELD ET AL SUBSEQUENT AUTHORS FOLLOWED 7ILLISTONfS MODEL AND PLACED AND 4HOMSON ET AL RETRIEVED ARCHOSAURIAN AFkNITIES gANAPSIDu TETRAPODS FROM THE 0ERMIAN AND 4RIASSIC AS THE gDIRECT AS WELL -OLECULAR ANALYSES ARE THEREFORE CONVERGING UPON A ANCESTORSu TO TURTLES SUCH AS PAREIASAURS 'REGORY f DIADECTIDS TURTLE AND ARCHOSAUR RELATIONSHIP /LSON f OR gCAPTORHINOMORPHSu #ARROLL f 3OME OF THE GREATEST CONCERNS FOR ALL TYPES OF SYSTEMATICS ARE !LTHOUGH THE TEMPORAL REGION PROVIDES IMPORTANT PHYLOGE REFERRED TO AS gSYSTEMATIC BIASESu /NE OF THE kRST SUCH BIASES TO BE NETIC INFORMATION FOR AMNIOTE PHYLOGENY THE LAST DECADES OF DISCOVERED IS ALSO ONE OF THE MOST INTUITIVE TO UNDERSTAND RESEARCH HAVE SHOWN THAT 7ILLISTONfS @ SYSTEM IS FAR TOO &ELSENSTEIN @ NOTED THAT PARSIMONY METHODS WILL RETRIEVE THE http://doc.rero.ch SIMPLISTIC BECAUSE MANY FORMERLY HOMOGENOUS GROUPS WERE WRONG RESULT IN A FOUR TAXON SYSTEM IF TWO UNRELATED BRANCHES SHOWN TO EXHIBIT MULTIPLE CONDITIONS EG $ILKES f 2IEPPEL ARE SIGNIkCANTLY LONGER THAN THE OTHERS BECAUSE RANDOMLY B 4SUJI AND -ÌLLER AND BECAUSE PHYLOGENETIC ACCUMULATED HOMOPLASY IN THE LONG BRANCHES WILL WRONGFULLY ANALYSES HAVE SHOWN THAT THE NUMBER OF TEMPORAL FENESTRAE SERVE AS SYNAPOMORPHIES IE SECONDARY HOMOLOGIES SENSU DE CHANGED MULTIPLE TIMES THROUGHOUT AMNIOTE EVOLUTION EG 0INNA f AN EFFECT REFERRED TO AS LONG BRANCH ATTRACTION -OST -ÌLLER 4HE POSSIBLE PLACEMENT OF ANAPSID TURTLES WITHIN VEXINGLY THE ADDITION OF DATA DOES NOT SOLVE THIS PROBLEM BUT CROWN $IAPSIDA ONLY UNDERLINES THIS POINT AS IT IMPLIES THE RATHER AMPLIkES IT THEREBY PRODUCING GREATER CONkDENCE FOR THE SECONDARY LOSS OF BOTH TEMPORAL FENESTRAE 2IEPPEL AND DE"RAGA WRONG RESULT &ELSENSTEIN f 4AKEN TO THE EXTREME THE USE OF 2IEPPEL A A CONCLUSION ALREADY PROPOSED BY EARLY THE TOTAL GENOMES WILL NOT SOLVE PROBLEMS ASSOCIATED WITH LONG OPPONENTS TO THE 7ILLISTON MODEL "ROOM f 'OODRICH f BRANCH ATTRACTION BUT ONLY COMPOUND THEM DE"EER f AND READILY ACCEPTED BY THOSE FAVORING THIS !LTHOUGH THE CONSISTENT SIGNAL BEING RETRIEVED FROM INCREAS PHYLOGENETIC ARRANGEMENT (OWEVER EVEN IF TURTLES EVOLVED INGLY DIVERSE SETS OF MOLECULAR DATA IS IMPRESSIVE THE PERSISTENT FROM DIAPSID ANCESTORS THERE IS NO REASON TO BELIEVE A PRIORI THAT MORPHOLOGICAL SIGNAL AGAINST THE ARCHOSAURIAN RELATIONSHIPS OF THE LOSS OF BOTH TEMPORAL FENESTRATIONS OCCURS IN SYNCHRONY WITH TURTLES EG 2EISZ AND ,AURIN f DE"RAGA AND 2IEPPEL f ,EE THE ACQUISITION OF THE TURTLE SHELL 4HE EARLY STEM LINEAGE OF TURTLES f -ÌLLER ,YSON ET AL ,EE SEE BELOW IS THEREFORE EXPECTED TO POTENTIALLY BE POPULATED WITH TAXA WITH COMBINED WITH THE COMPLETE LACK OF A MORPHOLOGICAL SIGNAL IN THE DIAPSID CONDITION &ENESTRATION ALONE IS THEREFORE NOT A SUPPORT OF