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Evolution of Dental Replacement in Mammals

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Evolution of Dental Replacement in Mammals EVOLUTION OF DENTAL REPLACEMENT IN MAMMALS ZHE-XI LUO Section of Vertebrate Paleontology, Carnegie Museum of Natural History, 4400 Forbes Avenue, Pittsburgh, PA 15213 ZOFIA KIELAN-JAWOROWSKA Instytut Paleobiologii PAN, ul. Twarda 51/55 PL-00-818 Warszawa, Poland RICHARD L. CIFELLI Oklahoma Museum of Natural History, 2401 Chautauqua, Norman, OK 73072 ABSTRACT We provide a review of dental replacement features in stem stem clades of crown mammals including multituberculates and clades of mammals and an hypothetical outline for the evolution eutriconodonts have an antero-posterior sequential and diphy- of replacement frequency, mode, and sequence in early mam- odont replacement of premolars. By contrast, stem taxa of the malian evolution. The origin of mammals is characterized by a trechnotherian clade (Zhangheotherium, Dryolestes, and Slaugh- shift from a primitive pattern of multiple, alternating replace- teria) are characterized by an alternating (p2 → p4 → p3) and ments of all postcanines in most cynodonts to a derived pattern diphyodont replacement, a condition that is shared by basal eu- of single, sequential replacement of postcanines. The stem mam- therians. The sequential replacements of premolars in most extant mal Sinoconodon, however, retained some primitive replacement placentals (either antero-posteriorly p2 → p3 → p4 as in ungu- features of cynodonts. The clade of Morganucodon 1 crown lates and carnivores, or postero-anteriorly p4 → p3 → p2 as in mammals is characterized by the typical mammalian diphyodont some insectivores) would represent secondarily derived condi- replacement in which antemolars are replaced by one generation tions within eutherians. The single replacement of P3/p3 of meta- in antero-posterior sequence, but molars are not replaced. The therians is the most derived for all therian mammals. INTRODUCTION Mammals differ from their phylogenetic rela- Diphyodont dental replacement of mammals is a tivesÐnonmammalian cynodontsÐin their greatly major apomorphy because it is certainly correlated reduced number of successional teeth per tooth lo- with the determinate growth pattern of the skull, cus. Living mammals have two generations of teeth and partly correlated with lactation, which is the (diphyodonty) at most, whereas nonmammalian cy- most important mammalian characteristic (Pond, nodonts had multiple generations of tooth replace- 1977; Tyndale-Biscoe and Renfree, 1987; Jenkins, ment sustained throughout life (polyphyodonty). 1990; and Zeller, 1999). Nursing of the neonates by Mammalian dental replacement is limited partly by maternal milk has had a profound impact on mam- a delay in the onset of dental eruption in neonates malian growth patterns and on development of nu- that nurse on maternal milk. During lactation, the merous apomorphies in dentition and skull, such as: toothless neonates can achieve a considerable the reduced replacement of the postcanines, devel- amount of cranial growth at a rapid rate before erup- opment of precise molar occlusion, formation of the tion of the ®rst generation of deciduous teeth dentary-squamosal temporomandibular joint, as ®rst (Brink, 1956; Hopson, 1973; Pond, 1977; Luckett, pointed out by Brink (1956) and elaborated by 1993). The mammalian dental replacement is also many others (Hopson and Crompton, 1969; Romer, reduced partly by an early termination of dental re- 1970; Ziegler, 1971; Hopson, 1971; Pond, 1977; placement related to the determinate skull growth Kermack and Kermack, 1984; Gow, 1985; Cromp- in mammals. Prior to weaning, the rate of skull ton and Hylander, 1986; Luckett, 1993; Luo, 1994; growth exceeds that of the postcranial skeleton. Af- Crompton, 1995). ter weaning the rate of skull growth slows down. The complex phenomenon of dental replacement The termination of the skull growth usually coin- can be broken down to several basic morphological cides with eruption of the last molar (Pond, 1977). elements. (1) Replacement frequencyÐnumber of 159 160 BULLETIN CARNEGIE MUSEUM OF NATURAL HISTORY NO. 36 successional teeth at each tooth locus, especially (3) Direction or sequence of replacement: antero- whether replacement occurred in the posterior mo- posterior versus postero-anterior. In this study we lariforms. The rate of dental replacement is directly will attempt to outline these main features of the correlated with the patterns of skull growth. (2) dental replacement patterns in cynodont-mammal Mode of replacement: alternating versus sequential. evolution. DENTAL REPLACEMENT OF EXTANT MAMMALS Placentals (Fig. 1).ÐThe diphyodont dental re- vores, none of the premolars is replaced and the placement in most living placental mammals is entire postcanine series is monophyodont (Osborn, characterized by a single replacement of deciduous 1971; Bloch et al., 1998). The embryonic precursors (``milk'') incisors, canines, and premolars by a sec- to the deciduous antemolars in the highly altricial ond generation of permanent incisors, canines and neonates are reabsorbed before eruption (Church- premolars. Molars are part of the permanent denti- ®eld, 1990; Nowak, 1991). As a result, these small tion and are never replaced (Ziegler, 1971; Williams insectivores have only a one generation of function- et al., 1989; Nowak, 1991; Evans, 1995). al postcanine teeth (monophyodonty). The same There are several well-known exceptions to this monophyodont condition appears to be also present typical diphyodont pattern among the placentals. As in some geolabidid insectivores of the Late Creta- the antemolar replacement has some degree of ho- ceous and early Tertiary (Lillegraven et al., 1981), moplasy, it can vary among genera of the same fam- although not in others (Bloch et al., 1998). Other ily. In some very small soricid and talpid insecti- exceptions to the typical placental diphyodont den- tition can be seen in the anteaters (myrmecophagid xenarthrans) and the pangolins (manid pholidotans). These mammals are toothless and rely on the tongue to feed on ants and other insects. Adult mysticete whales have baleen for ®lter feeding instead of teeth ← Fig. 1.ÐComparison of dental replacement between nonmam- malian cynodonts and extant therian mammals. A. The nonmam- malian cynodont Pachygenelus (from Crompton and Luo, 1993: ®g. 4.14). B. The eutherian Canis latrans (coyote): aboveÐde- ciduous lower dentition of a juvenile (based on Carnegie Mu- seum CM 8653); belowÐpermanent dentition of an adult (CM 7365). C. The metatherians Alphadon (modi®ed from Clemens, 1966, and Cifelli et al., 1996). Teeth in light gray: erupting/suc- cessor teeth (5 permanent teeth after eruption). Dark gray: de- ciduous predecessor teeth yet to be replaced. Gray/hatched: de- ciduous predecessor teeth in alternate positions, yet to be re- placed. Unshaded: permanent teeth. Abbreviations: di, deciduous incisor; dc, deciduous canine; dp, deciduous premolars; dpc, de- ciduous postcanines; m, molars; pc, postcanines; rpc, replacing postcanines. Most nonmammalian cynodonts (except gompho- donts and tritylodontids) are characterized by alternating replace- ments of all teeth for multiple generations, in correlation with indeterminate growth of the jaw. The deciduous postcanines are replaced at every other, or every third tooth position in the same replacement wave (as seen in Pachygenelus). As the successor tooth tends to be larger than the predecessor tooth in each tooth position, the jaw had to grow in length to accommodate the larg- er replacement teeth in cynodonts, as in extant diapsids. In most extant placental mammals, there is only one generation of re- placement for the antemolars but no replacement of molars (as seen in Canis). Tooth replacement is more reduced in metathe- rians (as seen in Alphadon), postcanine replacement only occurs in the ultimate premolar P3/p3. 2004 LUO ET AL.ÐEVOLUTION OF DENTAL REPLACEMENT IN MAMMALS 161 (Nowak, 1991). Nonetheless, most placental mam- latter two taxa do not seem to represent the gener- mals have a diphyodont dentition in which all de- alized condition of most early Tertiary mammals. ciduous antemolars (including the premolars or Given the distribution of these characteristics, it is ``milk molars'') are replaced by the successional clear that primitively the placental crown group as and permanent teeth. This generalized placental a whole has sequential replacement of premolars, condition is less specialized than those of extant but it is not clear whether the antero-posterior di- marsupials and monotremes. rection, or the postero-anterior direction would pre- The sequence of replacement of premolars is also sent the ancestral condition of all extant placentals. variable among various extant placental groups. In Metatherians (Fig. 1C).ÐIn metatherians includ- the talpid insectivore Scapanus, the eruption of de- ing extant marsupials, only the ultimate premolar ciduous premolars and their replacement occur ear- (P3/p3) has both an erupted deciduous tooth and a lier in the ultimate premolar locus than the more successor tooth (Luckett, 1993; Cifelli et al., 1996; anterior premolar loci (Zielger, 1971). The same Rougier et al., 1998). Other antemolars have only postero-anterior sequences of premolar shedding one generation of functional teeth in most marsu- and eruption also occur in the chrysochlorid Er- pials. The ®rst and second premolars have the erupt- emitalpa (Kindahl, 1963), the macroscelidid Ele- ed deciduous teeth retained in adults, without re- phantulus (Kindahl, 1957), and in some lipotyph- placing successors. The incisors and canines
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