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Dental Development, Homologies and Primate Phy'logeny Jeffrey H

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Dental Development, Homologies and Primate Phy'logeny Jeffrey H DentalDevelopment, Homologies and Primate Phy'logeny Jeffrey H. Schwartz,.l5260,Department of Anthropology,University of Pittsburgh, Pittsburgh,PA andSection of VertebrateFossils, CarnegieMuseum of NaturalHjstory, Pittsburgh, PA Received May L2, L978 ABSTRACTComparison of sequencesof dental developmentand eruption of fossil andextant primatesas well as'insectivoresstrongly suggeststhat the commonly accepteddental homologies,the reconstructionof the ancestral_primatemorpho- type as well as the phylogeneticrelationships of primatesshould be revised. tt js suggestedthat variousprimates (e.g.Tarsius) haveretained the prim'i- tive mammaliancharacteristic of five premolarloci, but lost the jncisors front the 0ther primates(e.9. anddeveloped the canineat the of iaw. 'lost Strepsirhini) retained the primitive incisor-caninecornplex and pre- molars. In addition, it appearsthat the molar region of Catarrhini is not homologouswith that of other primates. t( tk Introduction Recentdescriptions of fossil Eutheriawh'ich unquest'ionably .l975)possessed five pairs of premolars(Clemens,197.3; L'illegraven,.l969; McKenna, demanda revision of the dental formula(3.1.4.3/3..l.4.3) conrmonly accepted as primitive for eutheriansand identificat'ion of the loci whichmay have beeninvolved in reductionof premolarnumber within. the variousmarnna'lian groups (9f: McKenna, 1975). Specimensof Kenrclg:lql (McKenna,1975) and Gypsonictops (Clemens, 1973.;Li1iegraven,l96,gl@demonstratelossofaprernoTarTromwithin the set of five premolars. McKenna(.l975) has arguedthat th'is tooth was dP3. Inherentin the needto recognizethat premo'larloss mayoccur at different loci rlithin or at the extrem'itiesof the premolarset is that of determin'ing mechanismswhich produce Such dental reductiOn,i.e., tooth "loss." From developmentalstudies of tooth replacementin the multi-toothed,polyphyodont reptile Lacertavivipara (Osborn,l97l), it'is clear that tooth "loss" is not ju;t theffivme-n[ and, thus, non-appearanceof a structure. It jn- volvesforces or fields of inhibit'ion whichprevent either total growthand the tooth (Butler,1939; Grijndberg,.|95?, eruption.1963; or proper.|973).calcificat'ion of 0sborn', l^lithregard to incompleteca'lcification, the vestigia]_ structure is resorbed(Grijneberg, 1952,'1963;0sborn, l97l) andthus, for all intents and purposes,has been"lost." Simplistically, the reptilian condi- tion (i.e. multiple successjvewaves of replacementof large numbersof teeth) could havebeen converted to that of mammalsby inhib'iting mostt{aves of dental developmentas well as the numberof successfu'llydevelop'ing teeth. That teeth, moreaccurate'ly, are inhibited from completedevelopment rather than strictly "lost" (andthus potentiil tooth loci of the dental laminaare not "lost") js implied by the secondariiyderived multi-toothed condition of cetaceans. Contrastedwith reptjles, mammalsare characterizedby havingmaximaliy two sets of post-natalteeth: deciduouspredecessors and permanent success- ors (Peyer,tgOA). Themolars are the result of the sameinteractions ,|939',I956; which premolar (Butler, producedeciduous .l958a,incisor, .l958b, canjne.l959a, and .l959b,1967; teeth .l970, .|973; kinoant,1957, 0sborn, l97l' Evolutionary Thecry 4zL-'32 (September, 1978) The editors Lhank E. Delson, K.D. Rose, and another referee for help in eval-uating this paper. G) 1978, the author SCl{l'fARTZ peyer, 1968). Therefore, a permanentset of teeth that would have rep'laced tfrl m6tars has been inhibited. Furthermore,with regard to deciduousinci- sors, caninesand premolars that are succeededby permanentteeth, there are var.iitions of the conrmonone-to-one replacement which should be noted. D.ifferentialTooth Replacement and lgg![Lgls. Whenthere is a difference betwe reptaFinglFm-anent teeth of the sameset during ontogeny,the decreasehas beenin the number-ofpermanent teeth. An .it..fi" exafrpt!is found'in Lep'ilemur(the sportive lemur)in whicha pair of uitimately shedand un- J.iiarorr upirerincisors .|974a). devei@ an-ilerupt but are replaced(Slhwartz, 0ther examplesof differential tooth replacement ur!, t) ine indriines (Propithegus, andAvahi), jn wh'ichfour deci9ugu:_ .Ifrdri (Schwartz, io*." premotarsare shedanAreTTaced-EFonly .l958a),.Taipatwo permalen!_PlgTolars .l958b),.Nolharctus 1g74b)';2) Elephantulus(Kindahl, (Kindahl, (G;#;y;,tffiii.iii.r,i.in,lgii),Tfi_whichon1ythepostEiffir-e of four deciduousprffiars'are repiacedby permanentpremolars; and 3) Tarsius iiig."i )-i; ;hi;h irre tee*r usualiv aetlneit.is the uppbrlateraj incisorfTfiE- jow6r premolars replaceteeth incisor andthe upperand.|948; lower anterior,l974a). do not nor u". r.epiaced(Dahlberg, Schwartz, With regard.tothe non- replacing-unreplaceclteet[ of Tarsius, they shouldbe viewedas deciduous,not peiran.ni teeth, becausethey aie ThEfirst to developand_erupt.and therefore function wjth b6th "proper"ieqiduous and permanentsets of teeth (cf. Dah'lberg' i94g; iifrwartz,lgT4'a,iSZSal.t This 'is sjmilar to the situation in Notharctus, Adaois.Elephantuius-ina Tal6a, jn whichit is the anteriormostdeciduffi pre- rffi" *rrm-mt-nit funcffiiF with the other deciduousteeth but is retained with the permanentset. pt "t f Wtr4q odr- f**it Pf "l print of rad'iographof a iuvenj'leTar:'ius sPectrum (RM &-Fjqurel: Postiive lgg1d; approx. xZj-sfiowingre]ativ6 states of dental devejop-nrenfrn-a'eruption. OFi-inOhb9 a"e retainedind will functionwjth the variously developingand .r'lpiing p$rmanentteeth; as definedhere, the permanentpremolars develop and'eru[t in the order P2+ P5'r P4. **************rk*********************Jr*****:k************************************ lCartmill and Kay (.l978) have argued that the occasional development'infetal tarsjers of rudimentarydenta'l nuUOinsat the loci of what are here regarded as deciduousteeth indicates that the fetal "teeth" are really deciduousteeth inO-if'ui the latter are permanentteeth. In reviewing this phenomenonin iarsius and other mammals,Schwartz (ms.b) pointed out that there is a funda- nffiOiii.".n.. betweenfetally initiated dental nubb'insand post-nata'l1y ."Jpting teeth: the former are developmentallyvery incompleteand do not function, whereasthe latter have completecrowns and roots and do function in masticat.ion. There maybe two sets of post-nata'l1y functignlng teeth, which are the deciduousand permanentdentit'ions, and the variably initiated dental nubbins are pre-natal or pre-deciduousteeth, as they are commonlyrefeffed to in Homosapiens. DENTAL DEVELOPMENTAND PRIMATES Fromthe above,two s'ignificant generalizationscan be made. First, in the adult Talpa, Elephantulus,Notharctus, Adapig (and, presumably,otl.rer four-premola?Ei''a@ afrffio-lar teeth are a m'ixed(decid- uousand permanent) dentit'ion. Theseteeth are not serially homologousand cannotbe undifferentiai'ly lumpedtogether for purposesof either biolog'ica'l oF-Fh-togeneticcons jderation. Thus,s'imp1e dental formulaesuch as 2.1.4.3/2.1.4.3for mostadapids, or unmod'ifiedstatements such as "...the three premolarsof Tarsius...," are mislead'ing. Thesecond generali2ation .l939,Concerns .l956; the evidence.l952,for tooth.|963; "loss." (e.9. Various.l973) studies Butler, Grtlneberg, 0sborn,.1971 , c]early demonitratethat the non-appearanceof a tooth (tooth "loss) is causedby fields of jnhibition which, at somestage of tooth development(e.g. follicle, bud, crown)interfere w'ith the propergrowth of a tooth, resu'lting in jts resorption. If a tooth subjectedto forces of inhibition doesdevelop (the to a certain.|963)) minimum threshold "quasi-continuous"trait of Grtlneberg (1952, sufficient for it .|939,to erupt,.|956, it.l963). will be diminutive, stuntedor malformed(ibid.; also Butler, 0n a macroscopic1eve1, observation-6Fthelatter (i.e. a stuntedtooth) wouldindicate a locus of tooth inh'ibition and, perhapseventually, tooth "loss." However,tooth "loss" can occurwithout necessarilyobserv'ing a precedingdiminution of a tooth (Schwartz,1974c). Thefirst genera'lization--occurrenceof a mixed(decid- uousand permanent) dentition in the adult--imp'liesthat tooth "loss" can occur phy'logeneticallyin the following fashionby: 1) developingand eruptinga ieti auoustooth and j nhibi ti ng i ts permanentsuccessor; 1a ) possib'ly reta'in- inq the deciduoustooth to functionrrtith the permanentmem[ers of its set; and2) 'inhibiting the deciduoustooth (see Kindahl,1967).t Step "1a" need .notnecessarily occur. This modelapp'l'ies, for examp'le,to the derivation of the s'ister-taxa LepiI emurand Meqal adapi s . The majorit7-6T-ffipsi rhlieEfffih-thropoidea develop two pairs of dec'iduousupper incisors that are repiacedby two pairs of permanentteeth; this representsthe primitive state. Thecond'ition jn Lepilemur:could have beenderived by: 1) eruption andsupsequent shedding of two pairs of decid- uousupper jncisors (e.g. dla anddID).and.inhibit'ion of one pair of the permanentreplacements (la for example);2) completeinhibition of the i***********************tr**********************************t?rk***dr************** 2thi, sequencefollows from the developmentaldependence of the permanenttooth (cf. '1958;Kindahl, cit.; on its deciduous.|958): predecessor GrUneberg,1952, E1. Peyer, i.e., 1) the developmentof a deciduous-!oo!lis seenas a rr5-u6'-atthe free edgeof the dental lamina;2) asrthe deciduoustooth develops, jt sendsoff a "stali," (the gubernaculum)at the endof whichthe permanent successordevelops. Molars,for example,are deciduousteeth 'in that they developfrom the free edgeof the dental laminaand are not replacedby other teeth; obviously,development of
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