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Submitted 9March2018 Accepted 27August2018 Published 21September2018 Correspondingauthors JonathanCramb, jonathan.cramb@qm.qld.gov.au GilbertJ.Price,g.price1@uq.edu.au Academiceditor LauraWilson AdditionalInformationand Declarationscanbefoundon page22 DOI 10.7717/peerj.5639 Copyright 2018Crambetal. Distributedunder CreativeCommonsCC-BY4.0 OPENACCESS Short-tailedmicewithalongfossil record:thegenus Leggadina Rodentia: MuridaefromtheQuaternaryof Queensland,Australia JonathanCramb 1 ,GilbertJ.Price 1 andScottA.Hocknull 2 1 SchoolofEarthandEnvironmentalSciences,UniversityofQueensland,Brisbane,Queensland,Australia 2 Geosciences,QueenslandMuseum,Brisbane,Queensland,Australia ABSTRACT Thegenus Leggadina colloquiallyknownas`short-tailedmice'isacommon componentofQuaternaryfaunasofnortheasternAustralia.Theyrepresentamember oftheAustralianoldendemicmuridradiationthatarrivedonthecontinentsometime duringthelateCenozoic.Herewedescribetwonewspeciesofextinct Leggadina fromQuaternarycavedepositsaswellasadditionalmaterialoftheextinct Leggadina macrodonta . Leggadinairvini sp.nov.recoveredfromMiddle-UpperlatePleistocene cavedepositsnearChillagoe,northeasternQueensland,isthebiggestmemberof thegenus,beingsubstantiallylargerthananyotherspeciessofardescribed. Leggadinawebbi sp.nov.fromMiddlePleistocenecavedepositsatMountEtna,central easternQueensland,sharesfeatureswiththeoldestspeciesofthegenus,theEarly Pleistocene L.gregoriensis .Basedonthecurrentpalaeoecologicalinterpretationof thetypelocality, L.webbi ,representstheonlymemberofthegenusthatinhabited rainforest.Thesuccessionof Leggadina speciesthroughthelateQuaternarysuggestsan ecologicalreplacementoftheextinctlarge-bodied L.irvini withtheextant,small-bodied L.lakedownesis atChillagoe.AtMt.Etna,theextinctrainforestspecies L.webbi is replacedwiththeextantxeric-adapted L.forresti duringthelatestMiddlePleistocene. Thisreplacementisassociatedwithamid-Pleistoceneshifttowardsprogressive intensifyingseasonalandaridclimates.OurstudyaddstothegrowinglistofsmallbodiedfaunalextinctionsduringthelateQuaternaryofnorthernAustralia. Subjects Paleontology,Zoology Keywords Leggadina ,Muridae,Quaternary,Pleistocene,Rodents,Palaeoecology,Extinction, Climatechange INTRODUCTION Short-tailedmice Leggadina spp.aresmall-bodiedmurinesthatformpartofthe `AustralianOldEndemicRadiation' Aplin,2006 ; Watts&Aslin,1981 ,nowreferred tothetribeHydromyini Lecompteetal.,2008 .Thegenushasacomplextaxonomic history. Thomas wasthefirsttodescribeaspeciesof Leggadina ,butplaceditin thegenus Mus .Thomaslaterproposedthename Leggadina asasubgenusof Pseudomys Thomas,1910 . Iredale&Troughton elevated Leggadina tofullgenericstatus,a movesupportedby Ellerman and Tate .Severalearlyworkers Thomas, Howtocitethisarticle Crambetal.,Short-tailedmicewithalongfossilrecord:thegenus Leggadina Rodentia:Muridaefrom theQuaternaryofQueensland,Australia. PeerJ6:e5639;DOI10.7717/peerj.5639
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1910 ; Ellerman,1941 ; Tate,1951 placedanyverysmallAustralianrodentspecieswithan accessorycusponM 1 in Leggadina ,butsomeauthors Ellerman,1941 ; Tate,1951 noted thatseveralspeciesnowsynonymisedinto L.forresti weredistinctfromallothers. Ride synonymised Leggadina backinto Pseudomys ,onlytohaveitresurrectedagainby Mahoney&Posamentier . Covacevich&Easton consideredthattheCentralShort-tailedMouse, L.forresti listedas Pseudomysforresti ,waswidespreadacrossQueensland.However,individuals fromthenortheastofQueenslandwerelatershowntobedistinctby Watts and Baverstocketal. ,andsubsequentlynamed Leggadinalakedownensis .Laterauthors consideredthatall Leggadina innorthernAustraliawereconspecificwith L.lakedownensis Moroetal.,1998 ,with L.forresti restrictedtothecontinent'sinterior.Noadditional extantspeciesof Leggadina havebeendescribedsincethattime,althoughregionalvariants havebeenrecognised Cooperetal.,2003 . Leggadina istraditionallyincludedinthe` Pseudomys division'`Conilurini',which alsoincludes Conilurus , Mesembriomys , Leporillus , Notomys , Zyzomys , Mastacomys and Pseudomys itself Musser&Carleton,2005 .However,molecularphylogeniesindicatethat Conilurus , Mesembriomys and Leporillus areactuallythesistergroupofthe` Uromys division' Uromys , Melomys ,andrelatedgenera,makingthe` Pseudomys division'paraphyletic Rowe etal.,2008 ; Steppanetal.,2005 .Regardless,thepositionof Leggadina asacloserelativeof Zyzomys anda Pseudomys / Notomys / Mastacomys cladeiswell-supported Ford,2006 ; Rowe etal.,2008 .Mostrecentlyananalysisby Smissen&Rowe found Leggadina tobe thesistercladeof Zyzomys . Leggadina hasarelativelylongfossilrecordforanAustralianmurinegenusspanning muchoftheQuaternary.TheearliestrecordscomefromtheEarlyPleistoceneRiversleigh WorldHeritageArea,northwesternQueensland Klinkhamer&Godthelp,2015 and Fisherman'sClifffossildepositsinsouthernNewSouthWales Crabb,1977 ; Breed&Ford, 2007 .MiddlePleistocenereportsinclude Hocknull 2005 ; 2009 and Hocknulletal. fromcavedepositsatMt.Etna,centralQueensland.Recentowlroostdepositsincentral Australiacommonlycontaintheskeletalanddentalremainsof L.forresti e.g. Baynes& Johnson,1996 ,whilst L.lakedownensis hasbeenrecordedfromcavedepositsinnorthern WesternAustralia Startetal.,2012 . Inlightofnewmaterialnowavailableforanalysis,weherereviewthefossilrecordof Leggadina innortheasternAustralia,erecttwonewspeciesfromfossilsofPleistoceneage, anddescribeadditionalmaterialreferrabletotheextinct L.macrodonta .Theevolutionand palaeoecologyofspeciesof Leggadina arediscussed,withimplicationsforourunderstanding ofthewiderAustralianmurinefauna. MATERIALANDMETHODS SpecimenswereobtainedaspartofongoingpalaeontologicalinvestigationsofPleistocene depositsinQueensland.Theseincludethefossil-richcavedepositsoftheMountEtna centraleasternQueenslandandChillagoenortheasternQueenslandareas,andopen fluvialdepositsatFloravillenorthwesternQueenslandFig.1.Thefossilmaterial Crambetal., PeerJ ,DOI10.7717/peerj.5639 2/27
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Figure1MapofQueensland,Australia,showingthestudylocalities. Full-size DOI:10.7717/peerj.5639/fig-1 comprisesmaxillae,dentariesandisolatedteeth.Allfossilsdescribedinthispaperare accessionedintothecollectionsoftheQueenslandMuseum,Brisbane,Australia. ImageswereobtainedusingaVisionaryDigital`passportstorm'camerasystemand aHitachiTM-1000environmentalscanningelectronmicroscopeattheQueensland Museum.MeasurementsweretakenusingMitutoyodigitalcallipers.Dentalterminology followsFig.2. TheelectronicversionofthisarticleinPortableDocumentFormatPDFwillrepresent apublishedworkaccordingtotheInternationalCommissiononZoologicalNomenclature ICZN,andhencethenewnamescontainedintheelectronicversionareeffectively publishedunderthatCodefromtheelectroniceditionalone.Thispublishedwork andthenomenclaturalactsitcontainshavebeenregisteredinZooBank,theonline registrationsystemfortheICZN.TheZooBankLSIDsLifeScienceIdentifierscanbe Crambetal., PeerJ ,DOI10.7717/peerj.5639 3/27
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Figure2Molarcuspterminologyforspeciesof Leggadina . AUppermolars.BLowersmolars.Terminologyismodifiedfrom Musser and Aplin&Helgen .Abbreviations:acc,accessorycusp; T1acc,T1accessorycusp;T1sup,T1supplementarycusp;a-lin,antero-lingualcuspid;a-buc,anterobuccalcuspid;amr,anteriormedialridge;md,metaconid;pd,protoconid;ed,entoconid;hd,hypoconid; bc,buccalcingulid;pc,posteriorcingulid;pcc,posteriorcingulidcuspid;pl,posteriorloph.Theterm `complex'isusedwhereindividualcuspscannotbedistinguished. Full-size DOI:10.7717/peerj.5639/fig-2 resolvedandtheassociatedinformationviewedthroughanystandardwebbrowserby appendingtheLSIDtotheprefixhttp://zoobank.org/.TheLSIDforthispublicationis: urn:lsid:zoobank.org:pub:3C34C73B-4800-4256-BC9E-0E7B50689024.Theonlineversion ofthisworkisarchivedandavailablefromthefollowingdigitalrepositories:PeerJ,PubMed CentralandCLOCKSS. Geographicandgeologicalsettings Floraville Numerousvertebrate-bearingfossildepositsoccurinthevicinityofFloravilleDowns Stationinnorth-westernQueenslandFig.1.Thedepositsarepredominantlyfluviatile, occurringadjacenttothewesternbanksoftheLeichhardtRiverandassociatedtributaries. Thefossil-bearingsedimentsconsistofsilts,clays,sands,andgravels,includingsomewith extensive insitu carbonates. Fossilcollectingonthestationhasbeensporadicsincethe1970s,withnosingle depositsubjectedtoextensiveanddetailedexcavation.Themajorityoffindshavebeen ofsurfacespecimensandincludemostlymegafaunaltaxai.e.,large-bodiedextinct Quaternaryvertebratesincludinggiantmarsupialsandcrocodiles.Wherefossilcollecting hasadoptedtechniquesconducivetotherecoveryofsmall-bodiedspeciese.g.,sievingof sedimentsandfossilsusingfine-meshsievesfromselecteddeposits,significantand Crambetal., PeerJ ,DOI10.7717/peerj.5639 4/27
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diversevertebrate-richassemblageshavebeenrecovered Rich,1991 .Thedeposits havepreviouslybeenconsideredtobePlio-Pleistocene Godthelp,1999 ; Tyler,Archer& Godthelp,1994 ,however,recentradiometricdatingstronglysuggeststhatthedepositsare MiddlePleistocene Price,2013 .Moreover,thefossilassemblageslacktypicalPliocenetaxa suchasthelarge-bodiedwombat-likemarsupial Euryzygoma ,buthaveyieldednumerous specimensofthecloselyrelated Diprotodon ,aspeciesfoundexclusivelyinPleistocene deposits Priceetal.,2009 . Chillagoe FossilassemblagesfromtheChillagoearea,north-easternQueenslandFig.1havebeen recoveredfromcavernousandfissure-filldepositswithinoutcropsofDevoniankarst limestone Price,2013 ; Priceetal.,2013 .Thenewrecordsof Leggadina fromChillagoeare derivedfromtwocavesystems,MacropedesWaterholeCaveandFernCave. TheMacropedesWaterholeCavedepositiscurrentlyundated,butcontainsbothextant speciesandmultipleextincttaxa,includinghithertoundescribedmurinerodents Cramb, 2012 .Thefossilassemblagealsocontainsspecimensassignableto Rattus Cramb,2012 , agenusthatispurportedtohavearrivedinAustraliaaround0.85.28Ma Roweetal., 2011 ,thuspotentiallyconstraininganupperagelimitforthedepositasEarlyPleistocene. Thebrecciateddepositisdominatedbyclayswithoccasionalboneclasts.Thesediments withinthedepositclearlyhavealonggeologicalhistoryhavingaccumulatedwithinthe cave,lithified,andthensubsequentlyeroded.We,therefore,hypothesisethatthedeposit isMiddletoLatePleistoceneinage. In2009duringanexploratorysearchofthecaveforfossils,asmall 125gsamplewas collectedfromahollowinthebreccia,whereerodedfossilshadaccumulated.Afterthe significanceofthesamplewasascertaineditwashopedthatadditionalfieldworkwould recoveradditionalsamples.Unfortunatelythecavewasfloodedatthetimeofasubsequent fieldtrip,makingthedepositinaccessible. PreviousinvestigationsatFernCavehavetargetedexcavationofanarchaeological depositwithinite.g., Goodalletal.,2009 .However, Leggadina specimensexaminedinthis paperwerederivedfromanactiveowl-roostpositionedonaledgehighabovethedeposit. Thespecimenswerecollectedatthetimeoftheoriginalarchaeologicalinvestigationsca. 1985AD,buthaveremainedunpublisheduntilnow.Thesedimentsareunconsolidated, andwereexcavatedinfivecmspits.Theowlroosthasnotbeendated,butatleastsomeof theskeletalmaterialwithinitisclearlyRecent.Basedonthesizeofthedepositwesuspect thefaunaareHolocenetorecentinage. Mt.Etnaregion Fossilspecimensof Leggadina collectedfromtheMt.Etnaregionhavecomefromnumerous limestonecavedeposits,locatedonMt.Etna,theadjacentLimestoneRidgeandnearby Olsen'sCave Hocknull,2005 ; Hocknulletal.,2007 ; Hocknull,2009 ; Price&Piper,2009 ; Cramb,Hocknull&Webb,2009 ; Cramb&Hocknull,2010a ; Priceetal.,2015 .Themajority ofthefossil-richdepositsatMt.Etnawereinitiallyexposedasaresultoflimestonemining activitiesonthewesternsideofMt.Etna,whilefossildepositsatLimestoneRidgeand Olsen'sCavearederivedfromnaturallyexposeddepositsordepositsexposedthrough Crambetal., PeerJ ,DOI10.7717/peerj.5639 5/27
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guanomining.Thefossildepositsarevariableintheirlithology,rangingfromphreaticallyderivedbrecciated,redclay-dominatedsedimentsthroughvadose-derived,speleothemrichyellowclay-richsedimentstoguano-derived,chocolate-brownorganic-richsediments Hocknull,2009 .Alldepositsarevariablycementedwithcarbonate;well-cementedsamples werecollectedasblocksanddigestedinaceticacidbaths.Lessconsolidateddepositswere excavatedinfivecmspitswherepossible.OneimportantsiteQML1312Elephanthole Cavewasdestroyedin1988,beforesystematicsamplingcouldbeundertaken.Itis neverthelesswellrepresentedbyasamplecollectedbycaverspriortothecaves'destruction Hocknull,2005 . Uranium-thoriumdatingplacesthemajorityofdepositsintheareawithinthelast 500ka,withsomee.g.,Olsen'sCaveasrecentasthelateHolocene Hocknulletal.,2007 ; Priceetal.,2015 .Theolderdepositsinthearea>500kaBPcontainnumerous speciesinterpretedasindicativeofaclosedrainforestpalaeoenvironment,whiledeposits datedto<250kaBPmostlycontaintaxathataremoreindicativeofopen,xerichabitats Hocknull,2005 ; Hocknulletal.,2007 . RESULTS Systematicpalaeontology ClassMammaliaLinnaeus,1758 SubclassTheriaParkerandHaswell,1897 SupercohortPlacentaliaBonaparte,1838 OrderRodentiaBowdich,1821 FamilyMuridae Illiger,1811 LeggadinaThomas,1910 Typespecies: MusforrestiThomas,1906 Otherspecies: L.lakedownensisWatts,1976 L.gregoriensisKlinkhamer&Godthelp,2015 L.macrodontaKlinkhamer&Godthelp,2015 Genericdiagnosis.Speciesof Leggadina aredistinguishedfromallothermuridsbyaunique combinationofcharactersincludingthepossessionof:largeaccessorycusponM 1 ;large, lingualcuspsonM 1 )]TJ/F75 7.9701 Tf 6.217 0 Td [(2 postero-lingualofassociatedlophs;commonlydiamond-shapedT1 onM 1 ;T1supplementarycuspcommonlypresentonM 1 ,althoughvariablyexpressed; uppermolarcuspsslopedposteriorly;M 1 / 1 enlarged;M 3 / 3 reduced,suchthatM 1 / 1 is longerthanM 2 )]TJ/F75 7.9701 Tf 6.217 0 Td [(3 = 2 )]TJ/F75 7.9701 Tf 6.216 0 Td [(3 combined;largeposteriorpalatalforamen;broadposteriorcingulid cuspidonM 1 ;lowermolarcuspsslopedanteriorly;apexofeachlowermolarcuspdrawn infrommarginsofbase. Genericremarks. Leggadina canbeseparatedfromallotherAustralo-Papuanmurinesbythelargeaccessory cusponM 1 ,largeposteriorpalatalforamen,enlargementofM 1 / 1 withassociatedreduction ofM 3 / 3 sothatM 1 / 1 ismorethanhalfthelengthofthemolarrow.Smallspeciesof Pseudomys e.g., P.delicatulus sharesomesimilaritieswith Leggadina ,butdifferbyhaving Crambetal., PeerJ ,DOI10.7717/peerj.5639 6/27
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Figure3Fossilsof L.lakedownensis and L.forresti fromcavedepositsatChillagoeandMountEtna. ADUpperdentions:AQMF55619 L.lakedownensis rightmaxilla;B L.lakedownensis QMF55618 leftmaxilla;CQMF58982 L.forresti rightmaxilla;DQMF58983 L.forresti leftmaxilla.EGLower dentitions:EQMF55621 L.lakedownensis rightmandible;FQMF55620 L.lakedownensis right mandible;GQMF58981 L.forresti leftmandible.Scalebar D 1mm.APF,anteriorpalatalforamen.The buccaledgeoftheAPFiscurvedin L.lakedownensis ,butstraighterin L.forresti . Full-size DOI:10.7717/peerj.5639/fig-3 asmalleraccessorycusponM 1 ,lessdevelopmentoftheT1supplementarycusponM 1 , smallerposteriorpalatalforamen,proportionallysmallerM 1 / 1 andlargerM 3 / 3 M 1 / 1 commonlyhalfthelengthofthemolarrow,andasmallerposteriorcingulidcusponM 1 . Morphologicaldifferencesbetweenthetwoextantspeciesof Leggadina see Watts,1976 ; Cooperetal.,2003 ; VanDyck,Gynther&Baker,2013 arepartiallybasedonintactskulls. However,mostfossilsarerepresentedbyfragmentaryremains,suchthatonlyasubsetof featurescanbeusedtodiagnosefossilspecieswithin Leggadina .Thosecharactersinclude: thelengthandwidthofM 1 ;lengthofaccessorycusponM 1 ;relativelengthofM 2 compared toM 1 ;relativereductionofM 3 ;lengthofM 1 ;andtheshapeoftheposteriorendofthe anteriorpalatalforamen. Leggadinaforresti Thomas,1906 Fig.3 Crambetal., PeerJ ,DOI10.7717/peerj.5639 7/27
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Diagnosis:See Thomas ,towhichwecanaddthefollowingfeaturesthathaveproved usefulwhenidentifyingfossilspecimens: Leggadinaforresti isasmallspecieswithinthe genusandpossessesthefollowinguniquecombinationofcharacters:enlargedM 1 / 1 ,heavily reducedM 3 / 3 ,stronglydevelopedaccessorycusponM 1 variablydivided,moderatelyto well-developedT1supplementarycusponM 1 ,andananteriorpalatalforamenthathasa straightbuccaledgeonthemaxillaandtaperstoapointposteriorly. Material.QML1312;ElephantHoleCaveSystem,MountEtna:QMF55341leftmaxilla, QMF55646leftmaxilla,QMF55647rightmandible,QMF55648leftM 1 ;QML1313A; SpeakingTubeCaveSystemsubsampleA,MountEtna:QMF55649leftmaxillafragment withM 1 ,QMF55649leftmaxillafragmentwithM 1 ;QML1456;ColosseumChamber, CapricornCaves:QMF55148leftmaxilla,QMF55149rightmaxilla,QMF55150right maxilla,QMF55151rightmaxilla,QMF55152leftmandible,QMF55153rightmandible, QMF55767rightmaxilla,QMF58981leftmandible;QML1466HoneymoonSuite, CapricornCaves:QMF58982rightmaxilla,QMF58983leftmaxilla. Remarks. L.forresti isidentifiedherebyitslargeaccessorycusplargerthanthoseof L.gregoriensis and L.webbi ,relativelysmallsizedentitionsmallerthan L.macrodonta and L.irvini sp.nov.,andrelativelystraightbuccalmarginoftheanteriorpalatalforamena,which alsotaperstoapointposteriorlyunlikethecurvedbuccaledgeandcommonlyrounded posteriorterminationoftheanteriorpalatalforamenain L.lakedownensis . L.forresti occursinseveralMiddlePleistocenetoHolocenecavedepositsintheMountEtnaregion, withtheoldestrecordfromasubsampleofSpeakingTubeCavedesignatedQML1313A withaminimumageof280ka.Interestingly,whilethemainQML1313assemblageis dominatedbyhydric-adaptedfaunainterpretedasarainforestpalaeoecologyatthetimeof deposition Hocknull,2005 ; Hocknull,2009 ; Hocknulletal.,2007 ,theQML1313Asample containsapeculiarmixtureofhydricandxeric-adaptedtaxa.Thisisinstarkcontrasttothe knownhabitatofextant L.forresti ,aspeciesfoundingrasslands,shrublandsandsparsely vegetatedplainsofinlandAustralia Reid,2008 . Leggadinalakedownensis Watts,1976 Fig.3 Diagnosis:See Watts . Material:QML1466;FernCave-owlroostdeposit:QMF55269partialskull,QMF55353 rightmaxilla,QMF55354leftmaxilla,QMF55355rightmaxilla,QMF55356leftM 1 , QMF55618leftmaxilla,QMF55619rightmaxilla,QMF55620rightmandible,QMF55621 rightmandible. Remarks. Theabovespecimensarereferredto L.lakedownensis becausetheypossessanenlargedM 1 / 1 , heavilyreducedM 3 / 3 ,stronglydevelopedaccessorycusponM 1 commonlydivided, prominentT1supplementarycusp,andananteriorpalatalforamenthatiscommonly roundedposteriorly.Ofthesecharacters,theshapeoftheanteriorpalatalforaminaseems tobethemostusefulcharacterfordistinguishingspecimensof L.lakedownensis from L. forresti inQueensland,although Cooperetal. foundittobevariableandtherefore Crambetal., PeerJ ,DOI10.7717/peerj.5639 8/27
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Figure4 Leggadina.irvini sp.nov. QMF55326rightmaxillafragmentwithM 1 fromQML1507MacropediesWaterholebreccia.Scalebar D 1mm. Full-size DOI:10.7717/peerj.5639/fig-4 lessusefulinspecimensfromWesternAustralia. Watts statedthattheposteriorend oftheanteriorpalatalforamenisroundedin L.lakedownensis .Thisiscertainlythecase intheholotypeandtwooftheparatypes,butoneparatypeQMJM1293hasitpointed instead.Wesuggestthatamoreusefulcharacterisationofthisfeatureisthatthebuccal marginoftheanteriorpalatalforamenof L.lakedownensis iscurved,whilethatof L.forresti isrelativelystraight. Specimensof L.lakedownensis havethusfarbeenrecordedonlywithintheRecent owlroostofFernCaveintheChillagoearea,butdonotoccurwithintheolderfossil breccias. Leggadinairvini sp.nov. Figs.45 Holotype.QMF55326rightmaxillafragmentwithM 1 . Typelocality.QML1507;MacropediesWaterholeCavebreccia,Chillagoe,north-eastern Queensland.Amassivebrecciathatoncefilledmuchofthechamber,sinceerodedto relativelysmallblocksthatarestill insitu .Theageofthebrecciaisuncertain,butislikely MiddleorLatePleistocene. Etymology:ThisspeciesisnamedforMr.DouglasIrvininhonourofhiscontributionsto, andsupportof,palaeontologicalworkincavesofeasternAustralia. Crambetal., PeerJ ,DOI10.7717/peerj.5639 9/27
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Figure5ComparisonofrightM 1 of L.irvini with L.macrodonta . AQMF55326 L.irvini .B QMF55624 L.macrodonta rightM 1 .Scalebar D 1mm. Full-size DOI:10.7717/peerj.5639/fig-5 Diagnosis.Aspeciesof Leggadina thatdiffersfromallothermembersofthegenusbybeing substantiallylargerthananyothercurrentlyknownspeciesFig.6.Additionally,theM 1 possessesawell-developedaccessorycuspdividedinholotypeandonlyknownspecimen, andlargediamond-shapedT1inocclusaloutline. Description. Maxilla.QMF55326preservestheportionofthemaxillasurroundingM 1 andpartofthe zygomaticarch;brokenedgesofmaxillaslightlyroundedandpolishedduetoerosion frombreccia;shapeandpositionoftheanteriorpalatalforamencannotbediscernedwith certainty;portionofanteriormarginofposteriorpalatalforamenmaybepreserved,but damageandroundingofspecimenmakesthisuncertain. M 1 .Crownelongate,oval-shapedinocclusaloutlinewithamarkedantero-lingualindent; Cuspsmoderatelyworn,butappeartoberelativelylow-crowned;accessorycuspvery large,dividedintotwosmaller,oval-shapedanteriorcusplet;largercrescent-shaped lingualcusplet;T1shapedlikeadiamondinocclusaloutline;T1large,robust,slightly smallerthanT2-3complex;T1postero-lingualofT2;T3in-linewithT2;T2posterior edgeformsa116degreeanglewithT1;T3heavilyreducedtoasmall,buccalprojectionof T2;T4-6lophmorewornthanT1-3;T4similarinsizetoT1butsemicircular-shapedin occlusaloutline;T5antero-buccalofT4andantero-lingualofT6;T6muchlargerthanT3, possiblymoredistinctwhenunworn;T4joinedtoT8-9complexbyashort,narrowridge; T8directlyposteriorofT5;T9aroundedbuccalprojectionofT8,distinguishedbyashallow Crambetal., PeerJ ,DOI10.7717/peerj.5639 10/27
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Figure6PlotofM 1 dimensionsforspeciesof Leggadina fromQuaternaryfossildepositsin Queensland. Blueopensquare= Leggadinagregoriensis Rackham'sRoost;greenX= Leggadina webbi QML1311H,1311J,1313;darkblueasterisk, Leggadinaforresti QML1312,1456,1457;purple filledsquare, Leggadinalakedownensis QML1466;red C , Leggadinamacrodonta Floraville5C;black dot, Leggadinairvini QML1507.Measurementsinmillimetres. Full-size DOI:10.7717/peerj.5639/fig-6 cleftontheanteriorslopeoftheloph;anteriorcingulumweaklypresentonT1,continuing topoorlydefinedlingualcingulumbetweenbasesofT1andT4;buccalcingulumweakly expressedandappearstobepresentbetweenthebasesofT3andT6;posteriorcingulum appearsabsent,butmayhavebeenobliteratedbyinterstitialmasticatorywear;M 1 has threerootslargeanterior,elongatelingual,andpostero-buccal. Remarks. Theholotypeisreferredto Leggadina basedontheextremedevelopmentoftheaccessory cusp,diamond-shapedT1withsupplementarycusp,andposteriorly-displacedT1and T4.ThesizeofthisspeciesM 1 dimensions:3.52 1.86mmisenoughtoeasily distinguishitfromallotherspeciesof Leggadina Fig.6.Incomparison, L.macrodonta hasalargest-recordedM 1 lengthof3.22mmandM 1 widthof1.75mmQMF57276 andQMF57267,respectively.Measurementsfrom Klinkhamer&Godthelp .The holotypeandonlyspecimenof L.irvini isworn,sothefulllengthoftheM 1 islikelygreater thanmeasuredinFig.6.Relianceonsizedifferencesalonetoinformtaxonomicdecisionsis sometimesproblematice.g. Price,2008b ,butherewenoteadditionalmorphologiesthat allowseparationof L.irvini fromthelargestpreviouslyknownspecieswithinthegenus, L.macrodonta .Inadditiontooverallsize,theholotypeof L.irvini isfurtherdistinguished fromallknownspecimensof L.macrodonta byhavingamorerobustaccessorycuspand T1onM 1 .Somespeciesof Leggadina displayminorvariationinthesecusps,however,the Crambetal., PeerJ ,DOI10.7717/peerj.5639 11/27
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degreeofexpressionofthesefeaturesin L.irvini canonlybeassessedfurtherfollowing recoveryofadditionalspecimens. L.irvini isfurtherdistinguishedfrom Leggadinawebbi sp.novseebelowand L. gregoriensis byitslargeraccessorycusp. Leggadinawebbi sp.nov.Fig.7,AppendixS1 Holotype.QMF55628leftmaxillawithM 1 )]TJ/F75 7.9701 Tf 6.216 0 Td [(3 . Typelocality.QML1313;SpeakingTubeCaveSystem,MountEtna,easterncentral Queensland. Othermaterial.QML1313;SpeakingTubeCaveSystem,MountEtna:QMF55629left maxilla,QMF55630leftM 1 ,QMF55631rightmandiblefragmentwithM 1 ,QMF55632 rightmandible,QMF55633leftmandible,QMF55634leftmandible.QML1311H;Speaking TubeCaveSystem,MountEtna,QMF55642leftM 1 ,QMF55634leftM 1 ,QMF55644left M 1 ,QMF55645rightmandible;QML1311J;SpeakingTubeCaveSystem,MountEtna: QMF55635leftmaxillafragmentwithM 1 ,QMF55636leftM 2 ,QMF55637leftmandible, QMF55638leftmandible,QMF55639leftM 2 ,QMF55640rightmandiblefragmentwith I 1 andM 1 ,QMF55641rightmandible; Etymology.ThisspeciesisnamedforGregoryWebbinrecognitionofhissupportforstudies ofcavefossilsinQueensland,andhisbroadercontributionstoAustralianpalaeontology. Diagnosis.Aspeciesof Leggadina thatcontainsthefollowinguniquecombinationof characters:M 1 / 1 slightlylongerthanhalfofmolarrowAppendixS1;M 3 / 3 moderately reducedinsizeproportionallysmallerthanthatof Pseudomys spp.,butless-reducedthan L.forresti and L.lakedownensis ;accessorycusponM 1 relativelysmallsmallerthanthatof L. forresti and L.lakedownensis ;T1onM 1 notgreatlyenlarged;uppermolarsmoderately overlapping;anteriorpalatalforaminaposteriorlynarrow. Description. Maxilla.Nocompletemaxillaeareknown.Theanteriorpalatalforaminaareposteriorly narrow. M 1 .Crownelongateandoval-shapedinocclusaloutline,withmarkedindentonanterolingualedge;mostspecimenshavearelativelysmallforaspeciesof Leggadina accessory cusp;accessorycuspcommonlyconfinedtolingualmarginonbaseofT2onespecimen, QMF55635,hasitwrappingaroundtheanteriorofT2;T1accessorycuspabsent;T1oval ordiamond-shapedinocclusaloutline;T1postero-lingualofT2,joiningaftermasticationrelatedweartoT1bis;T1bisvariablydeveloped,positionedimmediatelylingualofT2;T2 similarinsizetoT1;T3reducedinsize;T4directlyposteriorofT1;T5directlyposterior ofT2andantero-buccalofT4;T4crescent-shapedinocclusaloutline,joinedtoT5bya narrowridge;T4joinedtoT8byalowridge,moreevidentaftermoderatetoheavywear; T5triangularinocclusaloutline,slightlylargerthanT4;T6ovaltosub-circularinshape, directlybuccalofT5whenunworn,reducedbutlesssothanT3;T7absent;T8rounded, slopingposteriorly;T9reducedandfusedtoT8,stilldistinctwhenunworn;M 1 hasthree rootslargeanterior,elongatelingual,andsmallpostero-buccal. Crambetal., PeerJ ,DOI10.7717/peerj.5639 12/27
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Figure7 Leggadinawebbi sp.nov. AQMF55629leftmaxilla;BQMF55628leftmaxilla; CQMF55635leftmaxillafragmentwithM 1 ;DQMF55636leftM 2 ;EQMF55631rightmandible fragmentwithM 1 ;FQMF55640rightmandiblefragmentwithI 1 andM 1 ;GQMF55641right mandiblewithM 1 )]TJ/F75 5.9776 Tf 4.663 0 Td [(2 ;HQMF55638leftmandible;IQMF55645rightM 3 ,removedfrommandible; JQMF55639leftM 2 .Scalebar D 1mm. Full-size DOI:10.7717/peerj.5639/fig-7 Crambetal., PeerJ ,DOI10.7717/peerj.5639 13/27
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M 2 .T1well-developed,ovaltosemicircular-shapedinocclusaloutline;T2absent;T3 variablyexpressed,smallifpresente.g.,QMF55628,55635;T1incontactwithposterolingualmarginofT8ofM 1 ;T1directlyanteriortoT4;T4tear-shaped,semicircularin occlusaloutlineafterwear;T4postero-lingualofT5,joinedbynarrowridge;T5triangular inocclusaloutline,pointinganteriorly;T6notheavilyreduced,fusedtobuccalcorner ofT5;T4joinedatbasetoT8bylowridge;T8triangularinocclusaloutline;T9heavily reduced,notdiscernibleonsomespecimens;M 2 hasthreerootsantero-buccal,lingual, andpostero-buccal. M 3 .Reduced,butnohyper-reducedspecimensknown;crowntapersposteriorlyto approximatelyhalftotalwidthinocclusaloutline;T1incontactwithpostero-lingual marginofT8ofM 2 ;T1sub-circulartosemicircularinocclusaloutline;T1directlyanterior ofT4andantero-lingualofT5-6complex;T4small,tear-shaped,joinedtoT5-6complex bynarrowridge;T5-6complexrounded,taperingtojunctionwithT4;T6indistinguishable fromT5,possiblyabsent;T8-9complexreduced,narrowerthanT4-6loph;M 3 hasone majorrootthatisbifurcated. M 1 .Crownelongatewithrelativelylargegapsbetweenlophs;anteriorlophcommonly relativelynarrowincomparisontootherspeciesof Leggadina ,boomerangorsemicircularshapedinocclusaloutlinedependingondegreeofwear;antero-lingualandantero-buccal cuspsfused;antero-lingualcuspslopestobaseofmetaconid;antero-lingualcusphas second,smallerridgeslopingtobuccalmarginofbaseofmetaconid;antero-buccalcusp slopestobaseofprotoconid;protoconiddirectlyposteriorofantero-buccalcuspand immediatelybuccalofmetaconid;protoconidandmetaconidsubequalinsize,both tear-shaped,pointedtowardsjunctionatmidpointofanteriormarginofsecondloph; protoconidandmetaconidmergeafterheavywear,butstilldistinguishablebyindents atmidpointofanteriorandposteriormarginsofloph;hypoconiddirectlyposteriorof protoconidandimmediatelybuccalofentoconid;hypoconidjoinedtoprotoconidbya lowridgeonthebuccalmarginofthecrown,almostformingabuccalcingulid;entoconid slightlylargerthanhypoconid;hypoconidandentoconidtear-shapedinocclusaloutline, taperingtopointslightlyanteriorofanteriormarginsofbothcusps;shortandbroad posteriorcingulidcusponwell-developedposteriorcingulid;posteriorcingulidcommonly wrapsaroundbaseofhypoconid,continuingtobaseofprotoconid;M 1 hastworoots anteriorandposterior. M 2 .Roughlysquare-shapedinocclusaloutline;twolophscomprisingtheprotoconidmetaconidandhypoconid-entoconid;protoconid-metaconidlophbroaderthan hypoconid-entoconidloph,andmorerobustatbase;allmajorcuspstear-shapedin occlusaloutline;protoconidtapersantero-linguallytomeettaperingpointofmetaconid atmidpointofanteriormarginofanteriorloph;hypoconidjoinsentoconidinlikewise fashion;lowshelforvariablysmallposteriorcingulidcusponposteriormarginofcrown betweenbasesofhypoconidandentoconid;M 2 hastworootsanteriorandposterior. M 3 .Verysmall;allknownspecimenshavetwolophs;protoconidandmetaconidelliptical inocclusaloutline,alignedwithlophsofothermolars;posteriorlophapproximatelysame sizeandshapeasprotoconid;M 3 hasoneroot,bifurcatedintoanteriorandposterior. Crambetal., PeerJ ,DOI10.7717/peerj.5639 14/27
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Figure8 L.macrodonta. AQMF55622rightmaxillafragmentwithM 1 ;BQMF55623leftmaxilla fragmentwithM 1 ;CQMF55626partialrightmandible;DQMF55627leftmandible;EQMF55625 leftmandible.Scalebars D 1mm. Full-size DOI:10.7717/peerj.5639/fig-8 Remarks.Theupperdentitionof L.webbi issimilartothatofsomeoftheverysmall speciesof Pseudomys .However,weassignsuchmaterialto Leggadina onthebasisofits largeposteriorpalatalforaminaandbroadposteriorcingulidcuspidonM 1 .Additionally, L.webbi differsfrom L.forresti byhavinglessoverlapbetweentheuppermolarsand havingaproportionallysmallerT1andaccessorycusponM 1 . L.webbi differsfrom L.lakedownensis byhavinglessoverlapbetweentheuppermolars;havingaproportionally smallerM 1 / 1 andlargerM 3 / 3 ,proportionallysmallerT1andaccessorycusponM 1 ,and havingposteriorlynarrowanteriorpalatalforamina. L.webbi differsfrom L.macrodonta bybeingsmaller,lackingaT1supplementarycuspcommonlypresenton L.macrodonta , havingamoredevelopedanteriormedialridgeandmoredevelopedbuccalcingulid ontheM 1 . L.webbi sharesseveralfeatureswith L.gregoriensis includingsize,possessionofa relativelysmallaccessorycusponM 1 ,andarelativelysmallT1ontheM 1 .Itdiffersby lackingadefinedT7onM 1 . Leggadinamacrodonta Klinkhamer&Godthelp Figs.5and8 Locality:Allspecimensarefromthesite5CandadjacentWoodbineCreek,bothonthe westernbankoftheLeichardtRiver,FloravilleStation,northwestQueensland. Diagnosis:See Klinkhamer&Godthelp forsomediagnosticcharactersforthemaxilla andassociationdentition.Hereweaddthefollowingcharacters:amoderatelylarge-toothed Fig.6,Table1speciesof Leggadina withaposteriorlyroundedanteriorpalatalforamen, andarelativelynarrowanteriorlophonM 1 . Crambetal., PeerJ ,DOI10.7717/peerj.5639 15/27
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Table1Dentaldimensionsofadditionalspecimensof L.macrodonta . Allmeasurementsinmillimetres. N meansdminmax M 1 length32.920.032.862.96 M 1 width31.610.021.581.65 M 1 length32.310.032.262.34 M 1 width31.470.011.451.48 M 2 length31.390.041.321.47 M 2 width21.390.081.311.46 M 3 length10.73nanana M 3 width10.78nanana M 1 )]TJ/F75 8.3287 Tf 6.496 0 Td [(3 length14.42nanana Referredspecimens:QMF55622partialrightmaxillawithM 1 ;QMF55623partialleft maxillawithM 1 ;QMF55624rightmaxillafragmentwithM 1 ;QMF55625leftmandible withI 1 ,M 1 )]TJ/F75 7.9701 Tf 6.217 0 Td [(3 ;QMF55626partialrightmandiblewithM 1 )]TJ/F75 7.9701 Tf 6.217 0 Td [(2 ;QMF55627leftmandible withM 1 )]TJ/F75 7.9701 Tf 6.217 0 Td [(2 . Description. Additionalfeaturesofthemaxilla:Theanteriorpalatalforamenendsinlinewiththe anteriormarginofthelingualrootofM 1 ;buccalmarginofanteriorpalatalforamenat leastpartiallycurved,butallspecimensaretoodamagedtodeterminetheshapeofthe posteriorendoftheforamen. Dentary.Allknownlowermolarsexhibitmoderatetoheavywear.Onespecimen QMF55625preservestheI 1 ,butnospecimenshaveanintactcoronoidprocess,articular facetorangularprocess. M 1 .Roughlyovoidinocclusaloutline,butwithmorerectangularposteriorend;first lophnarrowerthansecondorthirdlophs;firstlophrounded,kidney-shapedinocclusal outline;antero-buccalandantero-lingualcuspidscannotbedistinguishedonanyavailable specimensduetoheavywear;weakbuccalridgeslopingfromantero-buccalcuspidtobase ofprotoconid,butlackingonantero-lingualcuspid;antero-lingualcuspwithverysmall ridgeslopingtobuccalmarginofbaseofmetaconid;protoconidposteriorandslightly buccalofantero-buccalcuspid;metaconiddirectlylingualofprotoconid;protoconidand metaconidsubequalinsize,eachtaperingtowardstheother,joinedbytallridge;hypoconid directlyposteriorofprotoconidanddirectlybuccalofentoconid;hypoconidandentoconid subequalinsize,slightlysmallerthanprotoconidandmetaconid;hypoconidandentoconid bothtear-shaped,eachtaperingtowardstheother,meetingatanteriormarginofloph; lowridgeconnectsbaseofprotoconidtobaseofhypoconid,butdoesnotcontinueinto abuccalcingulidonpostero-buccalcornerofhypoconid;posteriorcingulidcuspidwell developed,lenticularinocclusaloutline,taperingbuccallyalongbaseofposteriorfaceof hypoconid;tworootspresentanteriorandposterior. M 2 .Almostsquare-shapedinocclusaloutline;protoconid-metaconidlophformsbroadest partofcrown;protoconidlargerthanmetaconid,becominglessobviousafterheavywear; protoconidandmetaconidbothtear-shaped,althoughprotoconidislonger;protoconid Crambetal., PeerJ ,DOI10.7717/peerj.5639 16/27
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andmetaconidmeetonanteriormarginoflophandcrownatmidlineofmolarrow; hypoconid-entoconidlophslightlynarrowerthanprotoconid-metaconidloph;hypoconid posteriorandslightlylingualofprotoconid;entoconidlingualandslightlyanteriorof hypoconid;hypoconidandentoconidbothtear-shaped,eachtaperingtowardtheotherto meetatthemidpointbetweenthem;smallposteriorcingulidcuspidnestledimmediately posteriorofjunctionbetweenhypoconidandentoconid;tworootspresentanteriorand posterior. M 3 .OnlyonespecimenQMF55625preservestheM 3 ;crownsub-circularinocclusal outline;protoconidandmetaconidfused,occlusalsurfacepeanut-shaped;posteriorloph small,directlyposteriorofmetaconid;appearstohaveonlyoneroot,butmaybifurcate withinthedentary. Remarks. Klinkhamer&Godthelp didnotdescribethelowerdentitionof L.macrodonta statingthatnospecimensfromthetypelocalitycouldbedefinitivelyassignedtothe species.However,fromourassessmentoftheavailable,andsomenew,fossilspecimens ofmandiblesandlowermolarsfromthetypelocality,weconsiderthatsuchmaterialis unequivocally Leggadina .Furthermore,consideringthatthisspeciesismorphologically distinctfromallknownspeciesof Leggadina ,andonlyasinglemorphospeciesof Leggadina hasbeenidentifiedinthedeposit,wereferthenewandpreviouslyundescribedlower dentitionto L.macrodonta .Additionalspecimenshavealsobeenrecoveredfromanother depositWoodbineCreekashortdistancefromthetypelocality.Although L.macrodonta wasnamedforitsbulkyM 1 andwasconsideredtobethelargest-knownmemberof thegenusatthetimeofpublication Klinkhamer&Godthelp,2015 , L.irvini sp.nov.is substantiallylargerFigs.5and6. DISCUSSION Dentalandfunctionalmorphologyin Leggadina TheenlargedaccessorycuspontheM 1 isprobablythemoststrikingfeatureofthe dentitioninmostspeciesof Leggadina .Itismuchless-developedintheoldest-known species L.gregoriensis ,suggestingthatitslargersizeinmostotherspeciesof Leggadina maybeaderivedtrait.Thedegreeofwearonmanyspecimenssuggeststhattheaccessory cuspishighlyfunctional,effectivelyformingananterior-mostfourthlophontheM 1 . Thetwoextantspecies, L.forresti and L.lakedownensis ,commonlyexhibitamedian constrictionoftheaccessorycusp,effectivelydividingitintwo.Thisfeatureisalso observedin L.macrodonta and L.irvini. Althoughitsfunctionisunclearitmaybethatthe constrictioncreatesanarrowercuttingedge,ausefultoolforprocessinginvertebrateprey. Phylogeneticrelationships Determiningtheprecisephylogeneticpositionofspecieswithin Leggadina isdifficultdue tothefragmentarynatureoftheknownfossilrecordofskeletalanddentalmaterial.Itis alsohamperedbyapoorunderstandingofmorphologicaldiversityincranialanddental charactersamongAustralianmuridsgenerally.However,weassumethattheoldestknown species, L.gregoriensis fromtheearlyPleistocene,islikelytopossessmoreancestraltraits Crambetal., PeerJ ,DOI10.7717/peerj.5639 17/27
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thanspeciesfoundingeologicallyyoungerdeposits.Threedistinctivefeaturesof Leggadina areless-developedin L.gregoriensis thanotherspecieswithinthegenus:thedevelopment oftheaccessorycusponM 1 ;theenlargementofM 1 relativetoM 3 ,andthedevelopment oftheT1supplementarycusponM 1 .Weinterprettheconditionofthesefeaturesin L.gregoriensis astheplesiomorphicstateforthegenus. L.webbi retainsseveralcharactersthatappeartobeplesiomorphicwithinthegenus. TheseincludetheenlargementoftheaccessorycuspandT1onM 1 ,andthereduction ofM 3 / 3 .Thisassociationofcharactersmayrepresentanevolutionarygrade,astheyare alsoseenintheoldestknownspecies, L.gregoriensis .While L.gregoriensis ,astheoldest knownspeciesofthegenus,isunsurprisinglyplesiomorphic, L.webbi ismuchyoungerand waslikelycontemporaneouswithspeciesthatarestillextanttoday.Wethereforesuggest that L.webbi representsaplesiomorphicspeciesof Leggadina andbasedonitsinterpreted palaeoecologylikelyrepresentsa`relic'lineagefromtheearlierdiversificationofthe genus.`Relic'or`Ghost'lineagesareknownfromtheMiddlePleistoceneMt.Etnafauna includingplesiomorphicbandicoots,possums,koalas,andmarsupial`lions' Hocknull, 2005 ; Hocknull,2009 ; Hocknulletal.,2007 ; Price&Hocknull,2011 .Wehypothesisethat therodentfaunareflectsanearlyradiationofmuridsintoclosedrainforestenvironments andsubsequentextinctionintheseenvironmentsduringthelateMiddlePleistoceneand LatePleistocene.Similardiversificationandbiasedmesicextinctionhasbeensuggested withinthedasyuridmarsupialsfromMt.Etnaalso Cramb,Hocknull&Webb,2009 ; Cramb &Hocknull,2010b . Isitpossiblethat L.webbi representssomethingclosetotheactualancestorofthe genus? Klinkhamer&Godthelp suggestedthat Leggadina evolvedfromarainforestinhabitingancestor,andindeedthemostbasalextanttaxaintheAustralo-Papuanmurine radiationoccurinNewGuineanrainforests Roweetal.,2008 .However,basedon molecularevidencethegenus Leggadina isnestedwithinacladewhoseextantmembers Pseudomys , Notomys , Mastacomys ,and Zyzomys arenotcurrentlyfoundintropical rainforesthabitats Roweetal.,2008 .If,then, L.webbi representstheancestralcondition of Leggadina bothmorphologicallyandecologicallyitsuggeststhat Leggadina diversified withinmesicrainforesthabitatsfirst,withsubsequentsecondaryxeric-adaptationofits derivedendmemberspeciesandsubsequentextinctionofthemesic-adaptedplesiomorphic forms. Alternatively,itmayindicatethatthepredominatelyxeric-adaptedAustralianmurid cladeshaveallexperiencedmesicradiationssometimeinthepastandtheselineagesarenow missingduetotheoverridingextinctionbiasofthesehabitatsthroughouttheQuaternary duetointensifyingariditye.g., Hocknulletal.,2007 ; Price,2012b . L.irvini istheleast-knownspeciesofthegenusduetoalackoffossilspecimens. Onthebasisofgrossmorphology,therelativelylargeaccessorycuspandT1onthe M 1 appeartobederived,indicatingthatitisprobablyclosertothecrownspeciesof Leggadina thanto L.gregoriensis .Theoveralllargesizeof L.irvini couldpossiblyindicate amorphoclinederivedfromthesmallestspeciesthrough L.macrodonta to L.irvini .Apart from L.gregoriensis and L.webbi ,theremainingmembersofthegenusallshareasimilar levelofdevelopmentofcharacterssuchastheenlargementoftheaccessorycuspandT1on Crambetal., PeerJ ,DOI10.7717/peerj.5639 18/27
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Figure9Temporaldistributionofspeciesof Leggadina . Full-size DOI:10.7717/peerj.5639/fig-9 M 1 ,andthepresenceofaT1supplementarycusponM 1 .Thisprecludestheconstruction ofaclearerevolutionarynarrativefortheendmembersofthisgenus. Spatialandtemporaloccurrence Leggadina hasalonghistoryinnorthernAustraliawiththeoldestdescribedspeciesof thegenus, L.gregoriensis ,occurringindepositsdatingtotheEarlyPleistoceneFig.9; Klinkhamer&Godthelp,2015 .Alackofwell-datedfossildepositsbetween1.8.5Ma limitsourunderstandingoftheradiationwithinthegenus.BytheMiddlePleistocene,at leastthreespeciesof Leggadina occur,namely L.webbi and L.forresti fromtheMt.Etna region,and L.macrodonta fromFloraville.Anadditionalspecies, L.irvini fromChillagoe, isinterpretedasprobablybeingofmiddlePleistoceneage.Thefateof L.macrodonta is unclearasitissofarknownfromonlytwodeposits,however, L.webbi appearstohave persisteduntilca.280ka. Apaucityofradiometricdatinglimitsourunderstandingofthetimingoftheorigin ofspeciessuchas L.lakedownensis and L.irvini .Bothtaxalackfirmgeochronological control,butwerepresentbytheMiddle-LatePleistocene.Thepresenceof L.lakedownensis withinfossildepositsoftheChillagoeregionisnotsurprising,asthetypelocalityofthe speciesLakelandDownsisrelativelyclose<150kmtotheNorth-Eastandextant populationsoccurintheregiontoday Moro&Kutt,2008 .Interestinglythough,the absenceof L.lakedownensis fromolderMiddleLatePleistocenedepositsintheChillagoe areamayindicatethatitisageologicallyrecentarrivalinthearea. L.irvini issomethingof apuzzle.Onlyasinglespecimenisknownfromasiteofuncertainage.Whyitwasreplaced bythesmaller L.lakedownensis intheChillagoeareacannotbeascertainedwithoutbetter understandingofitsageandcontemporaryfaunas. Leggadinawebbi isacommonelementoffossilassemblagesfromtheMt.Etnaregion thataredominatedbyrainforest-adaptedtaxa Hocknull,2005 ; Hocknulletal.,2007 . Itslossfromtheregionislikelyassociatedwithintensifyingariditythatbeganduring themid-BruhnesclimaticeventthatsawamajorfaunalturnoveratMt.Etnawhereby Crambetal., PeerJ ,DOI10.7717/peerj.5639 19/27
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rainforest-adaptedfaunawerereplacedbyextantspeciesthatpresentlyliveinxeric habitats Hocknulletal.,2007 ; Price,2012b .Significantlythough,thisfaunalturnover eventbrought L.forresti tothearea.Indeed,fossilsfromMt.Etnaitselfaretheoldest recordca.280kaforthisspeciesandcanthereforebeutilisedasacalibrationpointin futurephylogeneticassessmentsusingmolecularclocks. L.forresti survivedlocallyuntil atleastthelateHolocene,beingrecordedfromdepositssuchasthePleisto-Holocene ColosseumChamber Priceetal.,2015 .Wearecurrentlyunawareofanyextantrecords of L.forresti intheMt.Etnaregion,butthelocalsmall-bodiedextantmammalfaunais likelytobeincompletelyknownwithadditionalrecordsofrodentsthatmayeitherstillbe presentintheregionorveryrecentlyextinct Cramb&Hocknull,2010a .Forexample,the mostcommonsmall-bodieddasyuridmarsupialfoundwithintheColosseumChamber depositistheStripe-facedDunnart, Sminthopsismacroura Cramb,Hocknull&Webb, 2009 ,aspeciesthatwasonlyfoundextantintheareaasrecentlyas2007representedby specimenQMJM18420.Itisthuspossiblethatextantpopulationsof L.forresti mayyetbe discoveredinthearea. Acautionarynoteregardingpalaeoecology Extantspeciesof Leggadina areomnivoresthatdigsimpleburrows Moro&Kutt,2008 ; Reid,2008 .Theyarefoundinavarietyofhabitatsrangingfromdesertstotropical woodlands Kutt&Kemp,2005 .Thediscoveryof L.webbi infossildepositsinterpreted asrepresentingclosedrainforestpalaeoenvironmentsindicates Leggadina hadaneven broaderhabitatrangeinthepast.Thismaybetakenasacautionarynoteforany researcherattemptingtoreconstructpastenvironmentsonthebasisofthepresumedhabitat preferencesofsinglefossiltaxausingonlyextantrelatives.Palaeoecologicalreconstructions shouldideallybebasedonmultipletaxawithcongruenthabitatpreferences,with considerationofanatomicalspecialisations,ecologicalguildsandrelevantpalaeoclimatic data. Forexample,extantTreeKangaroos Dendrolagus spp.arecommonlyassociatedwith rainforesthabitats,yetfossilTreeKangaroos Bohra spp.evidentlyhadbroaderecological tolerances,beingfoundinassemblagesinterpretedaswoodlands Dawson,2004 ; Prideaux &Warburton,2009 aswellasrainforests Hocknull,2005 .Similarly,recentlyextantBilbies Macrotis spp.areexclusivelyfoundinxerichabitats,yetfossilBilbies Liyamayidayi inhabitedrainforests Travouillonetal.,2014 . Itmustberememberedthatthelongspanofgeologicaltimewillincludemanyhabitats hostinglineageassociationsthathavenoanaloguetoday LundeliusJr,1989 . Interestingly, Leggadina ispartofthe` Pseudomys division'ofhydrominerodents,a groupwhichisnotablyabsentfromextantrainforestcommunities.Incontrast,middle PleistocenedepositsatMountEtnae.g.,QML1311Hcontainsixspeciesof Pseudomys divisionmurines.Atleastfiveoftheseappeartohavebeenendemictorainforesthabitats, astheyareonlyfoundindepositswithothermoretypicalrainforest-inhabitingtaxa.This suggeststhatmodernassemblagesofrainforestmurinesarenotagoodanalogueforthose ofthemiddlePleistocene. Crambetal., PeerJ ,DOI10.7717/peerj.5639 20/27
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CONCLUSIONS Thetwonewspeciesof Leggadina describedinthispaper, L.irvini and L.webbi ,demonstrate thatthegenusoncedisplayedgreaterdiversityofmorphologyandecology.Moreover,with sixspeciesof Leggadina nowrecognisedfourextinctandtwoextantitisclearthatspecies diversitywithinthegenuswasgreaterinthepast.Whiletheextinctionof L.webbi appearsto betiedtoclimate-changedrivenhabitatloss,thecausesforthewiderdeclineofthegenusin recenttimesisunclear.Itis,however,apatternalsoapparentinotherAustralianmammal groupssuchaskoalas Price,2008a ; Blacketal.,2014 ; Price,2012a .Thispresentstudy addstothegrowinglistofsmall-bodiedmammalextinctionsthatoccurredinAustralia, alongsidetheextinctionofthemegafauna,throughoutthelateQuaternary.Itdemonstrates thattheQuaternaryextinctionsincludedrepresentativesfrommanyofthemostsuccessful extantlineages,suchasmurids,peramelids,dasyuridsandphascolarctids.Wecontend thatdeterminingthechronological,palaeoecologicalandpalaeoclimaticcontextforthe extinctionofthesesmall-bodiedfaunaisofequalimportancetothatofthemegafauna extinctiondebate. ThefossilrecordofAustralasianrodentshasreceivedrelativelylittleresearchattention, butrecentworkby Klinkhamer&Godthelp ,coupledwiththisstudy,hasgreatly enlargedourunderstandingofatleastonegenus.Thetaskmustnowbetoextendthis worktothe35othermurinegeneraknownfromAustralo-Papua. Institutionalabbreviations QMF QueenslandMuseumfossilspecimen QMJM QueenslandMuseummodernspecimen QML QueenslandMuseumfossillocality ACKNOWLEDGEMENTS WearegreatlyindebtedtothesupportofDouglasandMaryAnnIrvin,GregoryWebb,the ChillagoeCavingClub,ErnieandKylieCampandfamily,MichaelArcher,SueHand,Noel Sandsandfamily,CliveCavannahandmembersoftheCentralQueenslandSpeleological Society,AnnAugustynandAmandaJenningsHintonaswellasthestaffofCapricornCaves, JohnAugustynoftheQueenslandNationalParksandWildlifeService,PaulTierney,Shona Marks,MathewNg,RochelleLawrence,JoanneWilkinson,KristenSpring,Jian-xinZhao andYue-xingFeng.WealsoextendourappreciationtothestaffandvolunteersofThe UniversityofQueenslandandQueenslandMuseumfortheirkindassistanceinpreparing fossils.ThanksalsotoHenkGodthelpandFredFordfordiscussionsaboutthetaxonomy of Leggadina .WethankMattMcDowell,KevinRowe,andananonymousreviewerfor helpfulcommentsthatimprovedthemanuscript. Crambetal., PeerJ ,DOI10.7717/peerj.5639 21/27
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ADDITIONALINFORMATIONANDDECLARATIONS Funding ThisresearchwasfundedbyAustralianResearchCouncilgrantsLP0453664,LP0989969, DP120101752,andDE120101533andagrantfromtheIanPotterFoundation.Thefunders hadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparation ofthemanuscript. GrantDisclosures Thefollowinggrantinformationwasdisclosedbytheauthors: AustralianResearchCouncil:LP0453664,LP0989969,DP120101752,DE120101533. IanPotterFoundation. CompetingInterests Theauthorsdeclaretherearenocompetinginterests. AuthorContributions JonathanCrambconceivedanddesignedtheexperiments,performedtheexperiments, analyzedthedata,contributedreagents/materials/analysistools,preparedfiguresand/or tables,authoredorrevieweddraftsofthepaper,approvedthefinaldraft. GilbertJPriceconceivedanddesignedtheexperiments,analyzedthedata,contributed reagents/materials/analysistools,preparedfiguresand/ortables,authoredorreviewed draftsofthepaper,approvedthefinaldraft. ScottAHocknullconceivedanddesignedtheexperiments,analyzedthedata,contributed reagents/materials/analysistools,authoredorrevieweddraftsofthepaper,approvedthe finaldraft. DataAvailability Thefollowinginformationwassuppliedregardingdataavailability: ThemolarmeasurementsofLeggadinawebbisp.novareprovidedinAppendixS1. NewSpeciesRegistration Thefollowinginformationwassuppliedregardingtheregistrationofanewlydescribed species: PublicationLSID: urn:lsid:zoobank.org:pub:3C34C73B-4800-4256-BC9E-0E7B50689024 LeggadinairviniLSID: urn:lsid:zoobank.org:act:06906882-7329-45DD-BCC8C3474DC925BE, LeggadinawebbiLSID: urn:lsid:zoobank.org:act:E420DF0C-C7BD-421A-B7A27E3EDC598588. SupplementalInformation Supplementalinformationforthisarticlecanbefoundonlineathttp://dx.doi.org/10.7717/ peerj.5639#supplemental-information. Crambetal., PeerJ ,DOI10.7717/peerj.5639 22/27
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REFERENCES AplinKP.2006. TenmillionyearsofrodentevolutioninAustralasia:phylogenetic evidenceandaspeculativehistoricalbiogeography.In:MerrickJR,ArcherM,Hickey GM,LeeMSY,eds. EvolutionandbiogeographyofAustralasianvertebrates .Oatlands: AuscipubPtyLtd.,707. AplinKP,HelgenKM.2010. QuaternarymuridrodentsofTimorpartI:newmaterialof Coryphomysbuehleri Schaub,1937,anddescriptionofasecondspeciesofthegenus. BulletinoftheAmericanMuseumofNaturalHistory 341 :1DOI10.1206/692.1. BaverstockPR,HogarthJT,ColeS,CovacevichJ.1976. Biochemicalandkaryotypic evidenceforthespecificstatusoftherodent Leggadinalakedownensis Watts. TransactionsoftheRoyalSocietyofSouthAustralia 100 :109. BaynesA,JohnsonKA.1996. ThecontributionsoftheHornExpeditionandcave depositstoknowledgeoftheoriginalmammalfaunaofcentralAustralia.In:Morton SR,MulvaneyDJ,eds. ExploringcentralAustralia:society,theenvironmentandthe 1894HornExpedition .Sydney:SurreyBeatty&Sons,168. BlackKH,PriceGJ,ArcherM,HandSJ.2014. Bearingupwell?Understandingthe past,presentandfutureofAustralia'skoalas. GondwanaResearch 25 :1186 DOI10.1016/j.gr.2013.12.008. BreedWG,FordF.2007. Nativemiceandrats .Collingwood:CSIROPublishing. CooperNK,AdamsM,AnthonyC,SchmittLH.2003. Morphologicalandgenetic variationin Leggadina Thomas,1910withspecialreferencetoWesternAustralianpopulations. RecordsoftheWesternAustralianMuseum 21 :333 DOI10.18195/issn.0312-3162.21.2003.333-351. CovacevichJ,EastonA.1974. RatsandmiceinQueensland .Brisbane:Queensland Museum. CrabbPL.1977. FossilmammalsofthelowerPleistoceneMoornaSands,south-west NewSouthWales,Australia,withananalysisoftheAustralianpseudomyinemurid molars.PhD,MonashUniversity,Melbourne. CrambJ.2012. Taxonomyandpalaeoecologyofquaternaryfaunasfromcavesineastern tropicalQueensland:arecordofbroad-scaleenvironmentalchange.D.Phil.Thesis, QueenslandUniversityofTechnology. CrambJ,HocknullSA.2010a. Newquaternaryrecordsof Conilurus Rodentia:Muridae fromeasternandnorthernAustraliawiththedescriptionofanewspecies. Zootaxa 2615 :47. CrambJ,HocknullS.2010b. Twonewspeciesof Antechinus MacleayDasyuridae:Marsupialiafrommid-PleistocenecavedepositsineasterncentralQueensland. AustralianMammalogy 32 :127DOI10.1071/AM09025. CrambJ,HocknullS,WebbGE.2009. HighdiversityPleistocenerainforestdasyurid assemblageswithimplicationsfortheradiationofthedasyuridae. AustralEcology 34 :663DOI10.1111/j.1442-9993.2009.01972.x. Crambetal., PeerJ ,DOI10.7717/peerj.5639 23/27
PAGE 24
DawsonL.2004. AnewspeciesoftreekangarooMarsupialia,Macropodinaefromthe PlioceneChinchillaLocalFauna. Alcheringa 28 :267 DOI10.1080/03115510408619284. EllermanJR.1941. Thefamiliesandgeneraoflivingrodents.Withalistofnamedforms byRoyalW.HaymanandG.W.C.Holt,VolI.I.FamilyMuridae . London:BritishMuseumofNaturalHistory. FordF.2006. Asplittingheadache:relationshipsandgenericboundariesamong Australianmurids. BiologicalJournaloftheLinneanSociety 89 :117 DOI10.1111/j.1095-8312.2006.00663.x. GodthelpH.1999. TheAustralianrodentfauna,flotilla's,flotsamorjustfleetfooted?In: MetcalfI,ed. Whereworldscollide:faunalandfloralmigrationsandevolutioninSE Asia-Australasia .Armidale:UniversityofNewEngland,Australia,319. GoodallRA,DavidB,KershawP,FredericksPM.2009. PrehistorichandstencilsatFern Cave,NorthQueenslandAustralia:environmentalandchronologicalimplications ofRamanspectroscopyandFT-IRimagingresults. JournalofArchaeologicalScience 36 :2617DOI10.1016/j.jas.2009.07.007. HocknullSA.2005. EcologicalsuccessionduringthelateCainozoicofcentraleastern Queensland:extinctionofadiverserainforestcommunity. MemoirsoftheQueenslandMuseum 51 :39. HocknullSA.2009. LateCainozoicrainforestvertebratesfromAustralopapua:evolution, biogeographyandextinction.D.Phil.Thesis,UniversityofNewSouthWales. HocknullSA,ZhaoJ-X,FengY-X,WebbGE.2007. ResponsesofQuaternaryrainforest vertebratestoclimatechangeinAustralia. EarthandPlanetaryScienceLetters 264 :317DOI10.1016/j.epsl.2007.10.004. IlligerC.1811. Prodromussystematismammaliumetaviumadditisterminiszoographicis utriusqueclassis,eorumqueversionegermanica .Berlin:CSalfeld. IredaleT,TroughtonEleG.1934. Acheck-listofthemammalsrecordedfromAustralia. MemoirsoftheAustralianMuseum 6ixii :1 DOI10.3853/j.0067-1967.6.1934.516. KlinkhamerAJ,GodthelpH.2015. Twonewspeciesoffossil Leggadina Rodentia: MuridaefromNorthwesternQueensland. PeerJ 3 :e1088DOI10.7717/peerj.1088. KuttAS,KempJE.2005. Distribution,habitatandconservationstatusof Leggadina lakedownensis Rodentia:MuridaeinQueensland. AustralianZoologist 33 :258 DOI10.7882/AZ.2005.023. LecompteE,AplinK,DenysC,CatzeflisF,ChadesM,ChevretP.2008. Phylogeny andbiogeographyofAfricanMurinaebasedonmitochondrialandnucleargene sequences,withanewtribalclassificationofthesubfamily. BMCEvolutionaryBiology 8 :199DOI10.1186/1471-2148-8-199. LundeliusJrEL.1989. TheimplicationsofdisharmoniousassemblagesforPleistocene extinctions. JournalofArchaeologicalScience 16 :407 DOI10.1016/0305-4403-0. Crambetal., PeerJ ,DOI10.7717/peerj.5639 24/27
PAGE 25
MahoneyJA,PosamentierH.1975. Theoccurrenceofthenativerodent Pseudomys gracilicaudatus Gould,1845Rodentia:MuridaeinNewSouthWales. Australian Mammalogy 1 :333. MoroD,CampbellNJH,ElphinstoneMS,BaverstockPR.1998. TheThevenardIsland Mouse:historicandconservationimplicationsfrommorphologicalandgenetic variationin Leggadina mitochondrialDNAsequence-variation.Pacific. Conservation Biology 4 :282DOI10.1071/PC980282. MoroD,KuttAS.2008. Northernshort-tailedmouseLeggadinalakedownensisWatts, 1976.In:VanDyckSM,StrahanR,eds. ThemammalsofAustralia .ThirdEdition. Sydney:ReedNewHolland,583. MusserGG.1981. ThegiantratofFloresanditsrelativeseastofBorneoandBali. Bulletin oftheAmericanMuseumofNaturalHistory 169 :67. MusserGG,CarletonMD.2005. SuperfamilyMuroidea.In:WilsonDE,ReederDM, eds. MammalspeciesoftheworldataxonomicandgeographicreferenceVolume2 . ThirdEdition.Baltimore:JohnsHopkinsUniversity,894. PriceGJ.2008a. Isthemodernkoala Phascolarctoscinereus aderiveddwarfofaPleistocenegiant?Implicationsfortestingmegafaunaextinctionhypotheses. Quaternary ScienceReviews 27 :2516DOI10.1016/j.quascirev.2008.08.026. PriceGJ.2008b. Taxonomyandpalaeobiologyofthelargest-evermarsupial, Diprotodon Owen1838Diprotodontidae,Marsupialia. ZoologicalJournaloftheLinneanSociety ofLondon 153 :389DOI10.1111/j.1096-3642.2008.00387.x. PriceGJ.2012a. Long-termtrendsinlineage`health'oftheAustraliankoalaMammalia, Phascolarctidae:usingpaleo-diversitytoprioritizespeciesforconservation.In: LouysJC,ed. Paleontologyinecologyandconservation .Berlin,Heidelberg:SpringerVerlag,171. PriceGJ.2012b. Plio-PleistoceneclimateandfaunalchangeincentraleasternAustralia. Episodes 35 :160. PriceGJ.2013. Quaternary.In:JellPA,ed. GeologyofQueensland .Queensland: GeologicalSurveyofQueensland,653. PriceGJ,FengY-X,ZhaoJ-X,WebbGE.2013. DirectUThdatingofvertebratefossils withminimumsamplingdestructionandapplicationtomuseumspecimens. QuaternaryGeochronology 18 :1DOI10.1016/j.quageo.2013.07.003. PriceGJ,HocknullSA.2011. Invictokoalamonticola gen.etsp.nov.Phascolarctidae, Marsupialia,aPleistoceneplesiomorphickoalaholdoverfromOligoceneancestors. JournalofSystematicPalaeontology 9 :327DOI10.1080/14772019.2010.504079. PriceGJ,LouysJ,CrambJ,FengY-X,ZhaoJ-X,HocknullSA,WebbGE,NguyenAD, Joannes-BoyauR.2015. TemporaloverlapofhumansandgiantlizardsVaranidae; SquamatainPleistoceneAustralia. QuaternaryScienceReviews 125 :98 DOI10.1016/j.quascirev.2015.08.013. PriceGJ,PiperKJ.2009. GigantismoftheAustralian Diprotodon Owen1838Marsupialia,DiprotodontoideathroughthePleistocene. JournalofQuaternaryScience 24 :1029DOI10.1002/jqs.1285. Crambetal., PeerJ ,DOI10.7717/peerj.5639 25/27
PAGE 26
PriceGJ,ZhaoJ-X,FengY-X,HocknullSA.2009. NewrecordsofPlio-Pleistocene koalasfromAustralia:palaeoecologicalandtaxonomicimplications. Recordsofthe AustralianMuseum 61 :39. PrideauxG,WarburtonN.2009. Bohranullarbora sp.nov.asecondtree-kangaroo Marsupialia:MacropodidaefromthePleistoceneoftheNullarborPlain, WesternAustralia. RecordsoftheWesternAustralianMuseum 25 :165 DOI10.18195/issn.0312-3162.25.2009.165-179. ReidJRW.2008. Centralshort-tailedMouse Leggadinaforresti Thomas,1906.In: VanDyckSM,StrahanR,eds. ThemammalsofAustralia .ThirdEdition.Sydney: ReedNewHolland,581. RichTH.1991. ThehistoryofmammalsinTerraAustralis.In:Vickers-RichP, MonaghanJM,BairdRF,RichTH,eds. VertebratepalaeontologyofAustralasia . Melbourne:PioneerDesignStudio,893. RideWDL.1970. AguidetothenativemammalsofAustralia .Melbourne:Oxford UniversityPress. RoweKC,AplinKP,BaverstockPR,MoritzC.2011. Recentandrapidspeciationwith limitedmorphologicaldisparityinthegenus Rattus . SystematicBiology 60 :188 DOI10.1093/sysbio/syq092. RoweKC,RenoML,RichmondDM,AdkinsRM,SteppanSJ.2008. PliocenecolonizationandadaptiveradiationsinAustraliaandNewGuineaSahul:multilocussystematicsoftheoldendemicrodentsMuroidea:Murinae. MolecularPhylogenetics andEvolution 47 :84DOI10.1016/j.ympev.2008.01.001. SmissenPJ,RoweKC.2018. RepeatedbiometransitionsintheevolutionofAustralian Rodents. MolecularPhylogeneticsandEvolution 128 :182 DOI10.1016/j.ympev.2018.07.015. StartAN,BurbidgeAA,McDowellMC,McKenzieNL.2012. Thestatusofnon-volant mammalsalongarainfallgradientinthesouth-westKimberleyWesternAustralia. AustralianMammalogy 34 :36. SteppanSJ,AdkinsRM,SpinksPQ,HaleC.2005. MultigenephylogenyoftheOld Worldmice,Murinae,revealsdistinctgeographiclineagesandthedecliningutility ofmitochondrialgenescomparedtonucleargenes. MolecularPhylogeneticsand Evolution 37 :370DOI10.1016/j.ympev.2005.04.016. TateGHH.1951. ResultsoftheArchboldExpeditions.TherodentsofAustraliaand NewGuinea. BulletinoftheAmericanMuseumofNaturalHistory 97 :183. ThomasO.1906. OnmammalsfromnorthernAustraliapresentedtotheNational MuseumbySirWm.Ingram,Bt.andtheHon.JohnForrest. Proceedingsofthe ZoologicalSocietyofLondon 1906 :536. ThomasO.1910. ThegenericarrangementoftheAustralianmurineshitherto referredto``Mus''. TheAnnalsandMagazineofNaturalHistory 6 :603 DOI10.1080/00222931008692890. TravouillonKJ,HandSJ,ArcherM,BlackKH.2014. Earliestmodernbandicootand bilbyMarsupialia,PeramelidaeandThylacomyidaefromtheMioceneofthe Crambetal., PeerJ ,DOI10.7717/peerj.5639 26/27
PAGE 27
RiversleighWorldHeritageArea,northwesternQueensland,Australia. Journalof VertebratePaleontology 34 :375DOI10.1080/02724634.2013.799071. TylerM,ArcherM,GodthelpH.1994. FrogsfromaPlio-PleistocenesiteatFloraville Station,NorthwesternQueensland. RecordsoftheSouthAustralianMuseum 27 :169. VanDyckS,GyntherI,BakerA.2013. FieldcompaniontotheMammalsofAustralia . Sydney:NewHollandPublishers. WattsCHS.1976. Leggadinalakedownensis ,anewspeciesofmuridrodentfromnorth Queensland. TransactionsoftheRoyalSocietyofSouthAustralia 100 :105. WattsCHS,AslinHJ.1981. TherodentsofAustralia .Sydney:AngusandRobertson Publishers. Crambetal., PeerJ ,DOI10.7717/peerj.5639 27/27
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