Paleobiology, 31(2), 2005, pp. 324–346

To replace or not to replace: the significance of reduced functional tooth replacement in marsupial and placental mammals

Alexander F. H. van Nievelt and Kathleen K. Smith

Abstract.—Marsupial mammals are characterized by a pattern of dental replacement thought to be unique. The apparent primitive therian pattern is two functional generations of teeth at the incisor, canine, and premolar loci, and a series of molar teeth, which by definition are never replaced. In marsupials, the incisor, canine, and first and second premolar positions possess only a single func- tional generation. Recently this pattern of dental development has been hypothesized to be a syn- apomorphy of metatherians, and has been used to diagnose taxa in the fossil record. Further, the suppression of the first generation of teeth has been linked to the marsupial mode of reproduction, through the mechanical suppression of odontogenesis during the period of fixation of marsupials, and has been used to reconstruct the mode of reproduction of fossil organisms. Here we show that dental development occurs throughout the period of fixation; therefore, the hypothesis that odon- togenesis is mechanically suppressed during this period is refuted. Further, we present compar- ative data on dental replacement in eutherians and demonstrate that suppression of tooth replace- ment is fairly common in diverse groups of placental mammals. We conclude that reproductive mode is neither a necessary nor a sufficient explanation for the loss of tooth replacement in mar- supials. We explore possible alternative explanations for the loss of replacement in therians, but we argue that no single hypothesis is adequate to explain the full range of observed patterns.

Alexander F. H. van Nievelt.* Department of Biological Anthropology and Anatomy, Box 90383, Duke University, Durham, North Carolina 27708 Kathleen K. Smith. Department of Biology, Box 90338, Duke University, Durham, North Carolina 27708. E-mail: [email protected] *Present address: Department of Biology, Box 90338, Duke University, Durham, North Carolina 27708. E-mail: [email protected]

Accepted: 28 June 2004

Introduction pials reveals that vestigial first generation (‘‘milk’’) incisors and canines are found in Tooth replacement in marsupial mammals several marsupial families, including Macro- differs from the condition generally believed podidae (in Macropus giganteus Kirkpatrick to characterize eutherian mammals. In euthe- 1978), Dasyuridae (in Dasyurus quoll Luckett rian mammals, there are typically two gener- 1989, and Sminthopsis virginiae Luckett and ations of incisors, canines, and most (or all) Woolley 1996), and Peramelidae (in Perameles premolars. In contrast, marsupials typically Wilson and Hill 1897). Thus far, most detailed have two generations of functional teeth at studies of dental development of didelphids, only one locus in each jaw quadrant, the last generally considered to have the most primi- premolar (P3) (first noted by Flower [1867]). tive dentition of extant marsupials, have Some derived dasyurids have eliminated re- failed to document incontrovertible evidence placement altogether. By definition, molar of a vestigial first tooth generation. These teeth are represented by only a single gener- studies include several of Didelphis (Ku¨ kenthal ation in both clades. Studies of dental replace- 1891; Ro¨se 1892; Berkovitz 1978). However, ment in dryolestid eupantotheres (Martin Kozawa et al. (1998) claimed that Monodelphis 1997), a Mesozoic taxon that represents an domestica has a much more complex set of suc- outgroup to the Theria (Metatheria ϩ Euthe- cessional homologies, with vestigial first gen- ria), show that the pattern commonly seen in eration incisors at two loci and vestigial sec- living eutherians is the primitive one. ond generation teeth at three. Our own studies Close examination of the development of of a more complete series of M. domestica the anterior dentition in a variety of marsu- found no evidence for vestigial teeth. The ves-

᭧ 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3102-0009/$1.00 REDUCED TOOTH REPLACEMENT IN MAMMALS 325 tigial anterior teeth seen in the Australian felli et al. (1996) argued that the marsupial families are interpreted as evidence for the tooth replacement pattern is of great antiquity loss of a first generation of functional anterior and is found in some of the earliest marsupi- teeth present in the ancestry of marsupials. als. Cifelli and Muizon (1998) provide further Thus, relative to the primitive therian condi- evidence of the early appearance of the mar- tion, marsupials have a distinctive, derived supial dental replacement pattern in Creta- pattern of reduced dental replacement. ceous and Paleocene marsupials. They de- Several workers have tied this derived pat- scribed juvenile specimens of five marsupial tern of dental replacement to the marsupial species from the Paleocene of South America mode of reproduction and development. Wil- and found no evidence for tooth replacement son and Hill (1897: p. 554) stated, ‘‘We believe anterior to the last premolar locus. They con- that we are justified in seeking for the cause of cluded that ‘‘(t)he pattern of postcanine erup- the almost total suppression of the milk-teeth tion and replacement in the fossils is remark- in front of the last premolar, in the modified ably similar to that of recent didelphids’’ (Ci- condition of the mouth in the marsupial felli and Muizon 1998: p. 218). Furthermore, young in consequence of its peculiar adapta- they emphasized the systematic significance tion to the sucking function.’’ Winge (1941) of that pattern: ‘‘Given the problematic nature came to a similar conclusion, as did Ziegler of most dental and even basicranial features (1971b: p. 240) who stated, ‘‘The selective fac- defining Marsupialia (Muizon 1994), we sug- tors contributing to the suppression of the gest that the most robust test for assessing del- complete metatherian antemolar milk denti- tatheroidean relationships will be provided by tion except dP4 to a vestigial state are not evidence from tooth replacement. In fact, in known for certain, although, as has often been spite of the difficulties of observing it on fos- suggested, the phenomenon is very likely re- sils, it is probable that the pattern of tooth re- lated to the peculiar method of attachment of placement and eruption of living marsupials the newborn young to the nipple in the moth- represent one of the best metatherian syna- er’s pouch.’’ pomorphies (p. 218).’’ Rougier et al. (1998) More recently Luckett (1993: p. 195) also demonstrated that the marsupial dental re- claimed a link between the highly modified placement pattern is present in Deltatheridium, dental development pattern and reproductive a deltatheroidean from the Late Cretaceous of mode in marsupials. ‘‘(T)his modified anteri- Mongolia. or dentition is correlated with the prolonged In addition to using this character in phy- lactation period of marsupials, especially with logeny reconstruction, paleontologists have the ‘period of fixation’ (Hill and O’Donoghue used the hypothesized link between the de- 1913), during which the suckling young is rived marsupial tooth development pattern continuously attached to the nipple for a and the distinct marsupial reproductive pat- lengthy period of time. The well developed tern to make inferences about the reproduc- tongue and nipple fill the oral cavity during tive patterns of fossil taxa. Cifelli et al. (1996: this period, and the continued pressure exert- p. 717) argued on the basis of observing the ed by these structures probably has an effect marsupial tooth replacement pattern in Alpha- on the developing tooth germs underlying the don ‘‘that at least some reproductive speciali- oral epithelium.’’ zations of marsupials, including nipple fixa- Because aspects of dental development and tion, were probably established during the replacement can be identified and studied in Mesozoic, earlier than previously suggested.’’ fossils, the evolution of various conditions Martin (1997) reported that dryolestid eupan- may be documented. Cifelli et al. (1996) de- totheres from the Jurassic show unreduced scribed an immature specimen of Alphadon tooth replacement (i.e., a pattern similar to eu- from the Late Cretaceous of North America therians and different from marsupials) and that seems to show a dental replacement pat- concluded, ‘‘Therefore, a marsupial reproduc- tern similar to that seen in living dasyurids or tive pattern most probably can be ruled out for didelphids. On the basis of this specimen, Ci- Late Jurassic ‘eupantotheres’ with a plesio- 326 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH morphous mode of tooth replacement’’ (p. 15). are referred to neither subscript nor super- Rougier et al. (1998: p. 462) also commented script is used (e.g., P3). The homology of the on the likely reproductive mode of deltather- teeth in the marsupial dentition has been con- oideans. ‘‘If the metatherian patterns of skull troversial and there are several alternate no- development, tooth replacement and repro- menclatures (Flower 1867; Thomas 1887; Zie- duction are correlated, deltatheroideans may gler 1971b; Archer 1978; Luckett 1993). As will already have possessed the basic marsupial be seen below, in M. domestica, we were unable reproductive pattern.’’ to detect a vestigial first generation of teeth. In this paper, we report observations on We hypothesize that the basic pattern of den- dental development and tooth eruption in the tal replacement is homologous in all marsu- didelphid Monodelphis domestica. We also pre- pials, and we have followed the ontogeneti- sent comparative data on tooth replacement in cally based system of Luckett (1993). There- other mammals, both marsupial and placen- fore, following Luckett, we designate the teeth tal. We address the two major predictions of found in the adult dentition as follows: The the hypothesis discussed above. First, we ex- upper incisors are designated I1 to I5, the low- amine the progress of dental development ers I1 to I4 (from mesial to distal). Canines are 1 during the period of fixation to see if odon- designated C and C1. Again following Luck- togenesis is suppressed during that develop- ett, premolars are designated dp1, dp2, and mental stage. This part of our study tests the P3 (as Luckett argues that the functional adult explicit hypothesis that the suppression of teeth at the p1 and p2 position are from the dental replacement is a direct result of nipple first generation). Molars are designated M1 to attachment in marsupials. Second, we exam- M4. The single functional deciduous tooth in ine whether the suppression of dental gener- each jaw quadrant is designated dp3. As is ations is a unique character of marsupials. typical for marsupials, the premolars found in This part of our study allows us to determine the adult dentition are premolariform (i.e., not whether the evolution of the marsupial repro- molariform) and the deciduous premolar is ductive strategy is a necessary condition for molariform. Note that antemolar teeth with a the evolution of the derived pattern of dental prefix ‘‘d’’ are considered to be from the first replacement observed. or ‘‘deciduous’’ generation. Antemolar teeth designated without a ‘‘d’’ prefix are consid- Materials and Methods ered to be homologous with those of the sec- Primary Study Species. The species studied ond or ‘‘permanent’’ generation. was Monodelphis domestica, the gray short- Development of Tooth Germs: Histological Spec- tailed opossum, a small (80–130 g) didelphid imens. Stages of dental development for all marsupial native to Brazil and Bolivia (Strei- teeth present were determined in 17 ages be- lein 1982; Eisenberg and Redford 1999; No- tween day 14 embryonic (14 E) and day 35 wak 1999). The animals studied were from a postnatal (35 P). In most cases a single speci- breeding colony housed at Duke University. men of a given age was examined. Specimens Colony husbandry is described by van Nievelt were fixed in 10% phosphate buffered forma- and Smith (2005). Pregnant females were lin or Bodian’s fix (Humason 1979), decalci- checked daily for the presence of a litter, so the fied, embedded in paraffin, and were serially age of all animals and specimens is known to sectioned in a plane transverse to the jaws within Ϯ1 day. Young are born after a gesta- (coronal plane) at 8-12 ␮. Alternate slides were tion of 14.5 days and the day of birth is des- stained with Milligan’s trichrome or Weigert’s ignated as day 0 postnatal (0 P). hematoxylin counterstained with picropon- M. domestica possesses the didelphid adult ceau (Humason 1979). The seven stages of dental formula: incisors 5 (upper)/4(lower), tooth development recognized in this study canines 1/1, premolars 3/3, molars 4/4. In the follow the stages of Osborn (1981) and Ber- text, upper teeth are designated by a numer- kovitz (1978): thickening of the free edge of ical superscript (e.g., P3), lower teeth by a sub- the dental lamina (t.d.l.), bud, early cap, late script (e.g., P3). When both uppers and lowers cap, early bell, late bell with dentine (or pre- REDUCED TOOTH REPLACEMENT IN MAMMALS 327

TABLE 1. Stages of tooth development recognized in histological material.

Stage Key features Thickening of dental lamina (t.d.l.) Thickening of epithelially derived dental lamina, earliest mor- phological indication of tooth germ Bud Tooth germ a spherical to ovoid ball of epithelial cells, sur- rounded by a conspicuous condensation of mesenchyme Early cap Enamel organ invaginates and takes on a cap shape, primary enamel knot may be seen Late cap Enamel organ still cap shaped, stellate reticulum begins forma- tion Early bell Enamel organ achieves bell shape, odontoblasts begin to differ- entiate Late bell with dentine only (dentine) Deposition of calcified begins, only dentine (or pre-dentine) pres- ent Late bell with enamel (enamel) Deposition of calcified tissues continues, both dentine and enamel (or pre-enamel) present

dentine) only (abbreviated as ‘‘dentine’’), and noted. Other chance observations of early late bell with dentine and enamel (or pre- feeding behavior were also recorded. The con- enamel) (abbreviated as ‘‘enamel’’). The stages dition of the mammaries and nipples of the and the developmental events characterizing mothers of four litters was also monitored them are shown in Table 1. The earliest stage over the course of lactation in an effort to dis- recognized (thickening of the free edge of the cover when they had regressed to a nonpro- dental lamina) is somewhat subjective. It is an ducing condition. These observations were attempt to note the first visible signs of cel- fairly subjective, as the regression of the mam- lular proliferation in the dental lamina that maries was a gradual process. It was noted at will lead to a tooth germ at that position. what ages the mammaries and nipples were Eruption of Teeth and Development of Oral Be- first recorded as reducing in size, when they havior. For the purposes of this paper, a tooth appeared greatly reduced in size from the was considered to have erupted when any peak size, and when they had returned to the part of its crown had pierced the gingiva size typical of a nonbreeding, nonlactating fe- (‘‘standard gingival emergence’’ of Smith et male. al. 1994). The age of gingival emergence was Comparative Mammalian Tooth Replacement. determined by closely spaced (approximately To determine if the reduced functional tooth every other day) repeated observations of 14 replacement seen in marsupials is exceptional, young from three litters. Average ages of gin- we searched the literature in order to delineate gival emergence (rounded to the nearest day) the variation in functional tooth replacement are reported here. Tooth eruption in M. do- patterns in therian mammals. The choice of mestica is examined in detail by van Nievelt taxa in the comparison group is not intended and Smith (2005), where details of definitions, to provide an exhaustive survey of the varia- materials, methods, and statistics are report- tion of functional tooth replacement patterns ed. in therian mammals, and the included species Observations of aspects of the oral devel- may not be representative of other species in opment of young in the colony were made on the same family or order. Our sample includes the eruption study litters, on other litters of the full range of functional replacement from live young, and on young taken for histolog- the maximum possible to none. We made a ical study. Some young between the ages of 37 concerted effort to collect all of the available and 59 P were placed in proximity to various tooth replacement data for two groups, the food items of varying hardness and difficulty musteloid carnivores and the talpid eulipo- (ferret chow pellets, live crickets, sliced apple, typhlans, because these groups are well stud- and sliced banana) in four experiments. The ied and have diverse replacement patterns. We reactions of the young to the food items were follow the recent phylogeny of Flynn et al. 328 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

(2000) in defining the Musteloidea as contain- 6 ϭ 100%, canines: 2/2 ϭ 100%, premolars: 6/ ing the families Mustelidae and Procyonidae, 6 ϭ 100%. Note that if the P1 locus had been as well as a separate family containing the included in the calculation, the premolar re- skunks, the Mephitidae. sult would have been 6/8 ϭ 75%. Felis catus For the purposes of compiling the data on (domestic cat) has a deciduous dental formula functional replacement, we considered only of di 3/3, dc 1/1, dp 3/2 and a permanent tooth loci filled by one or two generations of dental formula of I 3/3, C 1/1, P 3/2, M 1/1. functional teeth. A tooth was considered ves- However, dp2 is vestigial whereas P2 is re- tigial if it did not consistently pierce the gin- duced in size but functional (Leche 1915). The giva, was shed after a very short period, or percentages of functional replacement are as was considered vestigial in the literature. The follows: incisors: 6/6 ϭ 100%, canines: 2/2 ϭ decision on whether or not to consider as ves- 100%, premolars: 4/5 ϭ 80%. tigial diminutive teeth that did consistently pierce the gums was somewhat subjective. A Results locus was considered to have functional re- Development of Oral Behavior. M. domestica placement if it was filled by a functional tooth neonates attach to a nipple shortly after birth in both the first and second generations. A lo- and within three days their mouths are tightly cus was not counted at all if it was filled only bound to the swollen end of the nipple by a by vestigial teeth (of either or both genera- peridermal seal that closes the lips. Young tions). were first observed to detach from and reat- To compare animals with a range of dental tach to the teat about 12 days after birth. This formulae, we calculated the percentage of the is the period of fixation for M. domestica.By13 functional replacement for each dental field to 15 P the seal over the lips has broken down (incisor, canine, and premolar). This number and the mouth opening begins to broaden to is equal to the number of tooth loci in each its full extent. Even though the young can de- field that show functional replacement divid- tach and reattach to a nipple, our observations ed by the number of loci that show at least one suggest that considerable time is still spent on functional generation of teeth times 100%. The a teat. Before 31 P young were almost always first premolar locus in eutherians is exception- on a teat when the cage was first opened and al in that it is replaced in few living taxa (Zie- the mother and young were examined in the gler 1971b; Luckett 1993). It has also been lost nest. Between 31 and 44 P the percentage of in many groups. Because of this, we have cho- young on a teat declined, and after 44 P young sen to exclude the first premolar locus (P1) of were almost never found on a teat. eutherian (placental) mammals from the cal- When the mother moves about the cage the culations. Excluding the tooth at the P1 locus young cling to her. This is accomplished by from the calculations has the effect of making biting down on a nipple or the fur and/or more eutherian species appear to have com- gripping with the hands, feet, and prehensile plete (100%) functional premolar replacement. tail. We first observed young clinging to the It therefore overestimates the differences be- mother’s fur orally at 29 P. In slightly older tween eutherians and marsupials. young that have well-erupted incisors, one can Two examples illustrate our method of cal- confirm the incisors’ participation in this grip culating percentage of functional replace- by gently pulling off a pup and seeing the pat- ment. Canis familiaris (domestic dog) has a de- tern in the mother’s hair left by the incisors as ciduous dental formula of di 3/3, dc 1/1, dp they ‘‘combed’’ it. This oral clinging of the 4/4 and a permanent dental formula of I 3/3, young to the mother continues until indepen- C 1/1, P 3/3, M 2/3. (The functional tooth at dence. the P1 locus is usually considered to be a tooth Pups as young as 37 P sniff a favorite food [dp1] from the deciduous dentition that is re- (banana) and begin to masticate softer fruits tained with the permanent dentition.) All by 45 P. We have observed them consuming teeth are functional. The percentages of func- hard chow pellets by 47 P. Crickets were pre- tional replacement are as follows: incisors: 6/ sented to the young at 37, 51, and 59 P. The 37 REDUCED TOOTH REPLACEMENT IN MAMMALS 329

P young did not react to the potential prey, though only dp3 has progressed beyond the whereas the 51 and 59 P young left alone with bud stage. All teeth anterior (mesial) to dp3 crickets eventually captured and consumed are discernible by 4 P. The replacement teeth them. Initial attempts at prey capture were at the last premolar locus (P3) are first ob- clumsy; however, the young rapidly acquired served at 7 P as thickenings of the free edge of the stereotypic response to prey seen in the the dental lamina (Fig. 2E,F). By 13 P (Fig. 3) adult (Ivanco et al. 1996). In sum, M. domestica (the end of the period of fixation) all teeth an- young have acquired a full repertoire of adult terior to M3 in the lower jaw have begun cal- feeding behaviors sometime between 47 and cification (late bell with dentine stage or later); 51 P. all upper teeth anterior to M3 in the upper jaw, One aspect of weaning is the start of solid except for I1, have achieved at least early cap food consumption, the other is the end of stage. suckling. The size of the mammaries appears In the incisor region, the first incisor initi- to track the amount of milk consumed, as it ates two to three days later than the more dis- does in Didelphis virginiana (Reynolds 1952). In tal incisors. I1 does catch up with the other our sample of mothers, the mammary glands lower incisors and achieves late cap stage at peaked in size at around 51 P, were greatly re- about the same time (10 P). The same is not duced in size by 58 to 69 P, and were reduced trueofI1. Though it achieves bud stage at the to the nonreproductive condition by 69 to 78 same time as I2–3, it achieves all subsequent P. If mammary size is an accurate indicator of stages later than any other upper incisor. This milk consumption, consumption peaks and difference will persist through tooth eruption, begins to decline just as the young have where it will be even more pronounced. After achieved a full range of feeding capabilities the bud stage, I4 is also relatively retarded and is effectively over before 58 to 69 P, when compared to I2–3,5. the mammary tissue has mostly shrunk away. The canines all appear within one day after Young are routinely separated from the moth- birth. Within a jaw (upper or lower), the ca- er at eight weeks in laboratory colonies nines are one of the two to four most advanced (VandeBerg 1999). teeth at any given age. The upper and lower Development of Tooth Germs. We were able first molars become discernible at about the to discern the initial thickening of the dental same time (2 P), quite early in the develop- lamina at all tooth positions and were able to ment of the dentition. In subsequent molars trace development through the deposition of (M2–M3) the lower molar reaches a given enamel at all but three posterior molar posi- stage three to eight days before the upper mo- tions and the replacement premolars. These lar reaches the same stage. There is no visible results are summarized graphically in Figure trace of M4 in the first 23 days after birth. M4 1. The states of development of representative has achieved late cap stage in the 35 P speci- teeth near the middle (7 P) and at the end of men. the period of fixation (13 P) are shown in Fig- The only definitive evidence of two gener- ures 2 and 3, respectively. As is well known, ations of teeth was found at the third premolar the marsupial neonate is highly altricial and locus, where the development of both dp3 and can be defined as being embryonic in most P3 were observed. The germ of P3 first ap- features, including the dentition. The only dis- pears as a thickening of the free edge of the cernible evidence of differentiation of teeth on dental lamina between dp2 and dp3 by about the day of birth is at the dp3 loci, with dp3 at 7 P. There are no structures suggesting more bud stage and dp3 represented by a thickening than one tooth generation at the canine or of the dental lamina. Relative to other teeth on dp1–2 loci. In the absence of evidence of ves- the same jaw (upper or lower), dp3 is always tigial teeth, we assume that the generational the first tooth to attain a particular stage. identity of teeth is homologous with that ob- Within two days after birth, the following served in other marsupials (Luckett 1993). 2–5 teeth are discernible: I2–4,I , C (upper and Eruption of Teeth. Dental eruption in M. do- lower), dp2, and M1 (upper and lower), al- mestica is discussed in detail by van Nievelt 330 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

FIGURE 1. Dental development in Monodelphis domestica. This graphic representation of dental development in M. domestica shows the first 60 days after birth. Tooth positions are represented on the horizontal axis, with the lower teeth on the left and the upper teeth on the right. The dotted centerline represents the midline of the jaw and the teeth are in proximal-to-distal sequence from that line. The first six stages shown (t.d.l. to enamel) are the result of examination of a series of sectioned specimens and do not have confidence intervals. Also, the age of the start of these six earlier stages cannot be estimated accurately after 23 days because of larger gaps in the series after that age. For clarity the early bell stage has been omitted. The age of eruption (first gingival emergence) is based on study of 14 individuals. The points are at the mean age of eruption and the error bars are Ϯ2 standard deviations. The lower gray area covers the period of fixation and the upper gray area represents the weaning period (from the earliest observed consumption of solid food to the rapid regression of the mammaries). REDUCED TOOTH REPLACEMENT IN MAMMALS 331

FIGURE 2. Development of representative antemolar teeth during the period of fixation (7 P) in M. domestica. These 2 are frontal sections, oriented so that medial is to the right. Arrows indicate tooth germs. A, I at bud stage. B, I2 at early cap. C, Upper canine at early cap. D, Lower canine at early cap. E, P3 as a thickening of the dental lamina; the 3 3 structure just lateral to P is the anterior tip of dp .F,P3 as a thickening of the dental lamina; this section is anterior 3 ϭ ϭ to any part of dp3.G,dp at early bell. H, dp3 at early bell. Abbreviations: d dentary (mandible) bone; e oral epithelium; m ϭ maxilla; p ϭ premaxilla; t ϭ tongue. Scale bars, 50 ␮m. 332 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

FIGURE 3. Development of representative antemolar teeth at the end of the period of fixation (13 P) in M. domestica. These are frontal sections, oriented so that medial is to the right. Arrows indicate tooth germs. A, I2 at late cap stage. B, I2 at late bell; arrow points to dentine. C, Upper canine at late bell; arrow points to enamel. D, Lower canine 3 3 at late bell; arrow points to dentine; enamel not visible. E, P at bud; note dp laterally. F, P3 at bud; this section is 3 anterior to any part of dp3.G,dp at late bell; arrow points to enamel. H, dp3 at late bell; arrow points to enamel. Abbreviations as in Figure 2. Scale bars, 50 ␮m. REDUCED TOOTH REPLACEMENT IN MAMMALS 333 and Smith (2005) and shown graphically in molars. Raccoons and several species of mus- Figure 1. Gingival emergence can be divided telid show partial reduction of functional re- into five phases separated by lulls in eruptive placement in the incisor region, yet these car- activity. The first phase runs from about 32 to nivorans retain full replacement in the canine 45 P. In this phase dp3 is, on average, the first and premolar regions. Domestic cats, wild tooth to erupt, at about 32 P, closely followed cats, and lions show full functional replace- by dp3. These teeth are followed by 17 others ment of the incisors and canines, but at only in rapid succession until there are 19 teeth four of five premolar loci. Brown bears show erupted (per side) by day 45. These 19 teeth reduced functional replacement in both the in- include all incisors with the notable exception cisor and premolar regions. Rabbits retain full of I1, both upper and lower canines, dp1 to replacement in the premolar region, lose the 1 dp3, M1–2,andM. The second phase of erup- canine locus entirely, and show partial reduc- tion occurs between about 49 and 54 P, when tion of functional replacement in the incisor 2 1 M ,I,andM3 erupt. The third phase of erup- region. Some rodents retain full functional re- tion occurs between about 82 and 84 P. M4 and placement of premolars, while eliminating M3 erupt at that time. The fourth phase occurs functional replacement in the incisor region between about 108 and 112 P, when upper and and eliminating canines altogether. Finally, a lower P3 erupt. The fifth and last phase occurs diverse group of placental mammals are func- at approximately 126 P, when M4 erupts. tionally monophyodont, having lost replace- Eruption in the incisor region is notable for ment altogether. These include the shrews, the relatively late eruption of the first upper some moles, some bats, the striped skunk, the incisor. The lower incisors all erupt (between pinniped carnivores, toothed whales, the 33 and 36 P) before any of the upper incisors aardvark, and murid rodents. erupt. I2 is the first upper incisor to erupt (at Musteloids are notable because there is ex- 39 P) and is followed by I3–5 (between about 40 tensive variation within this group (Fig. 4). and45P).I1 is the last incisor to erupt at 53 P, Functional tooth replacement ranges from almost 9 days after the last of the other upper complete to nonexistent both within the mus- incisors, more than 14 days after the neigh- teloid clade and among the outgroups. boring I2, and almost 20 days after the erup- Among the musteloids the tayra (Eira barbara) 1 tion of I1. The stages of eruption of I are exhibits complete replacement. It has full an- shown in Figure 6. The late eruption of this in- temolar replacement and retains each decid- cisor relative to its neighbors leaves a small uous tooth for at least two months (Poglayen- medial gap which forms when the I2’s emerge Neuwall and Poglayen-Neuwall 1976). In con- through the gums and closes fully when the trast, the striped skunk (Mephitis mephitis)is I1’s are fully erupted at about 56 P. In Figure 6 functionally monophyodont. It does not erupt this gap is seen as an empty space, in life it a functional deciduous tooth at any position contains soft tissue. (Leche 1915; Verts 1967). Amongst the mus- Comparative Mammalian Tooth Replacement. teloid outgroups, pinnipeds do not have func- Our survey of functional dental replacement tional tooth replacement, whereas a canid like in therian mammals shows that functional re- the red fox (Vulpes vulpes) has full functional placement patterns are evolutionarily labile replacement. and quite variable. These patterns are shown Most members of the family Mustelidae in in Table 2. Marsupials vary slightly: some de- our sample possess full replacement of the rived species have lost all functional tooth re- premolars and canines, but only partial func- placement, whereas primitive species retain tional replacement of the incisors. The exact replacement at the P3 locus. Placental mam- pattern of functional replacement varies from mals show a much wider range of variation. species to species. In the Eurasian badger (Me- 1 Placentals displaying the primitive pattern of les meles)di and di1–3 are vestigial, while 2–3 1–3 functional tooth replacement, including hu- di ,I and I1–3 are functional (Neal 1986). In mans and many domestic animals, possess the American badger (Taxidea taxus)andthe full replacement of incisors, canines, and pre- three species of Mustela represented in our 334 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH 1, 2 3 4 5 6 7–9 13 16 10, 11 10, 17 10, 17 this study 10, 11 10, 11 10, 17–19 20 10, 19 21 10, 19 19, 22 23 88 ement. A blank space Ͼ arranged by order; within each order 60 0 60 emolar) columns are the percentages of functional . hant shrew 100 100 100 10 mole 100 100 100 15 elep golden mole 100 100 100 11 rt-tailed opossum 0 0 33 golden mole 100 100 100 11 n-rumped golden mole 100 100 100 11, 12 Rock hyraxAmerican shrew Japanese shrew moleSolenodonMoonratShort-tailed gymnure 100 100 100 67 83 100 67 67 100 100 67 100 14 67 67 Aardvark 0 Nine-banded armadillo Virginia opossumGray sho Blackish shrew opossumRed-cheeked dunnartEastern quollTasmanian devil 0 0Four-toed rice 0 tenrecGiant otter 0 shrewGreater 0 hedgehog tenrecHottentot 0Cape 0 0Giant 0 33 Tailless tenrec 100 33 Streaked 100 tenrec 0 0Golde 100 100 100 0 100 0 100 100 11 100 10, 11 83 67Hedgehogs, several 11 spp Broad-footed mole 100Star-nosed mole 100Hairy-tailed moleEastern mole 100 European 100 mole 0 0 0 0 0 0 0 0–33 0 0 0 0 0 0 0 ntal P1 locus is not included in the calculation of percent functional replac mispinosus ement. If a range is given for a percent functional replacement value, this may represent uncertainty . mcinctus . sp spp spp. Shrew tenrecs, several spp. 100 100 100 10, 11 nove Procavia capensis Neurotrichus gibbsii Urotrichus talpoides Solenodon Echinosorex gymnura Hylomys suillus Erinaceus Orycteropus afer Didelphis virginiana Monodelphis domestica Caenolestes convelatus Sminthopsis virginiae Dasyurus viverrinus Sarcophilus harrisii Dasypus Microgale Oryzorictes tetradactylus Potamogale velox Setifer setosus Ambylosomus hottentotus Chrysochloris asiatica Chrysospalax trevelyani Tenrec ecaudatus Hemicentetes se Rhynchocyon chrysopygos Scapanus latimanus Condylura cristata Parascalops breweri Scalopus aquaticus Talpa europaea rian mammals. The numbers in the I (incisor), C (canine) and P (pr field. Boldface indicates taxa that have reduced functional replacement. Taxa are idae idae ement in the idae field. Keep in mind that the place idae nrecidae tooth Solenodontidae Erinaceidae Chrysochlor Tenrecidae Talpidae Soricidae Shrews 0 0 0 differences between two sources, or natural variability. ion, ement in that Order Family Species Common name I C P Source icida Te 2. Functional tooth replac DidelphimorphiaPaucituberculata Didelphidae Dasyuromorphia Caenolestidae Dasyuridae Xenarthra Dasypodidae ABLE HyracoideaEulipotyphla Procavi Talp Tubulidentata Orycteropidae about tooth funct tooth replac taxa are arranged by descending value of incisor functional replac indicates a lack of functional teeth in a tooth T Marsupials Placentals Afrosor Macroscelidea Macroscelid REDUCED TOOTH REPLACEMENT IN MAMMALS 335 28 29 39 40 39 41 42 43, 44 45 46 47, 48 49 50, 51 52 53, 54 53, 54 53, 54 55 24 25 26 27 Yellow-winged batDomestic dogBlack-backed jackalRed foxRingtailCacomixtleWhite-nosed coatiKinkajouTayra 0Domestic cat 100Wild cat 100Lion 0 100Raccoon 100Brown bearSea 100 100 otter 0 Old World 100 badger 100 100 100American 100 31 badgerAmerican mink 100 30 100 100European mink 100 100European 100 polecat/ferretStriped 100 skunk 100 100 35 100 100 100 100 32 34 33 100 100 33 100Horse 0–17 67 67 80 100 17 20–60Domestic cattle 36, 100 37 100 100Domestic 100 100 goat 100 17 100 100Domestic 80 sheep 17 38, 39 Pig 100 100 100 100 Collared peccary 60 100 100 80 100 0 100 100 0 100 100 100 100 0 100 100 0 100 100 100 100 100 55 100 55 100 55 56 100 55 Horseshoe bat 0 0 0 Little brown batAsian particolored batPallid batSundevall’s roundleaf bat 100 0 100 100 100 50–75 0 60 67 0 100 75 . sp mephitis spp. Tree shrew, several spp. 100 100 100 10, 57 Lavia frons Canis familiaris Canis mesomelas Vulpes vulpes Bassariscus astutus Bassariscus sumichrasti Nasua narica Potos flavos Eira barbara Felis catus Felis silvestris Panthera leo Procyon lotor Ursus arctos Enhydra lutris Meles meles Taxidea taxus Mustela vison Mustela lutreola Mustela putorius Mephitis Equus caballus Bos taurus Capra hircus ovis aries Sus scrofa Pecari tajacu Tupaia Myotis lucifugus Vespertilio superans Antrozous pallidus Hipposideros caffer Rhinolophus idae idae idae idae idae Megadermatidae Procyon Mustel Felidae Procyonidae Ursidae Mustelidae Mephitidae OdobenidaeOtariidaePhocidaeSuidae Tayassuidae Walrus Sea lions Earless seals 0 0 0 0 0 0 0 0 0 Rhinolophidae Order Family Species Common name I C P Source 2. Continued. ABLE Carnivora Can PerissodactylaArtiodactyla Equidae Scandentia Bov Tupai T Chiroptera Vesperitilionidae 336 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH 57), 59 60 61 62 63 64, 65 1973), 65. (Michaeli feld et al. ´ 1955), 29. (Dorst 1953), 30. (Evans 1993), 31. (Lombaard 1971), 62), 37. (Poglayen-Neuwall 1976), 38. and (Poglayen-Neuwall Poglayen- he 1902), 18. (Kindahl 1959b), 19. (Leche 1895), 20. (Ziegler 1972), 21. (Eadie 1973), 45. (Neal 1986), 46. (Long 1974), 47. (Auerlich and Swindler 1968), 48. (Kainer neider Ring-tailed lemurCommon marmosetSaddle-backed tamarinBlack-mantle tamarinNight monkeySquirrel monkeyCrab-eating macaqueJapanese macaque 100 100 100Rhesus macaqueSavanna baboon 100 100Gorilla 100 100Common chimpanzee 100Orangutan 100 100 100Human 100 100 100Western tarsier 100 100 100 58 58 American 58 beaver 100 100Arctic 100 ground 58 squirrel 100Greater 100 cane 100 100 rat 100 100 100Domestic rabbit 58 100 100 100 58 58 100 58 100 100 100 100 0 33 58 0 58 100 58 100 100 100 0 100 100 100 33 67 58 100 58 100 100 58 0 100 1996), 5. (Hill and Hill 1955), 6. (Guiler and Heddle 1974), 7. (Martin 1916), 8. (Flower 1868), 9. (Stangl et al. 1995), 1964), 61. (Mitchell and Carsen 1967), 62. (van der Merwe 2000), 63. (Moss-Salentijn 1978), 64. (Hirsch Luckett and Woolley ephenson ygmaeus 1964), 42. (Dittrich 1960), 43. (Kenyon 1969), 44. (Sch 2000), 4. ( rkovitz and Silverstone 1969), 52. (Verts 1967), 53. (King 1983), 54. (Laws 1953), 55. (Getty 1975), 56. (Kirkpatrick and Sowls 1962), 57. (Kindahl 19 Lemur catta Callithrix jacchus Saguinus fuscicollis Saguinus nigricollis Aotus trivirgatus Saimiri sciureus Macaca fascicularis Macaca fuscata Macaca mulatta Papio cynocephalus Gorilla gorilla Pan troglodytes Pongo p Homo sapiens Tarsius bancanus Castor canadensis Spermophilus parryi Thryonomys swinderianus Oryctolagus cuniculus gomery Luckett and Hong ¨ttcher 1967), 51. (Be 1962), 41. (Mont cidae idae 1982), 60. (van Nostrand and St idae enorth eporidae Callitrich Cebidae Cercopithe Pongidae Hominidae Tarsiidae Sciuridae Thryonomyidae Muridae Mice, rats 0 Luckett and Maier ´sek and Sterba 1989), 23. (Kindahl 1959a),. 24. (Fenton 1970), 25. (Koyasu and Mukohyama 1992), 26. (Orr 1954), 27. (Gaunt 1967), 28. (Grasse Order Family Species Common name I C P Source 2. Continued. Sources: 1. (McCrady 1938), 2. (Petrides 1949), 3. ( ABLE 58. (Smith et al. 1994), 59. ( 1954), 49. (Moshonkin 1979), 50. (Habermehl and Ro et al. 1980). T Primates Lemur RodentiaLagomorpha Castoridae 32. (Linhart 1968), 33. (Poglayen-Neuwall andNeuwall 1976), Poglayen-Neuwall 1993), 39. 34. (Poglayen-Neuwall (Leche 1995), 35. 1915), L (Gompper 40. 1995), (Halt 36. (Poglayen-Neuwall 19 10. (Leche 1897), 11. (Leche1944), 1907), 22. 12. (Leche (Mı 1904), 13. (Anthony 1934), 14. (Fairall 1980), 15. (Ziegler 1971a), 16. (Hanamura et al. 1988), 17. (Lec REDUCED TOOTH REPLACEMENT IN MAMMALS 337

FIGURE 4. Phylogeny of musteloid carnivores showing functional tooth replacement. Phylogeny of the caniform carnivores including the Musteloidea following the phylogenies of Dragoo and Honeycutt (1997) and Flynn et al. (2000). The tayra (Eira barbara) was not included in those phylogenies and its placement here is conjectural. The completeness of tooth replacement at the incisor (I), canine (C), and premolar (P) loci is shown next to the taxon name. The loss or reduction of tooth replacement is apparently independently derived in multiple lineages. Sources of replacement information are listed in Table 2.

sample, (M. vison, M. lutreola,andM. putorius), 1–2 3 1–3 di and di1–3 are vestigial, while di ,I and

I1–3 are functional (Kainer 1954; Long 1965; Habermehl and Ro¨ttcher 1967; Auerlich and Swindler 1968; Berkovitz and Silverstone 1969; Moshonkin 1979). According to Kenyon (1969) in the sea otter (Enhydra lutris)di1–2, 3 1–3 di1–3 and I2 are vestigial, while di ,I ,andI1,3 are functional. (The designation of functional versus vestigial incisors differs slightly from that of Scheffer [1951]), leading to the range of functional replacement values shown in Table 2.) To summarize, the general trend in mus- telids that reduce functional tooth replace- ment is to lose all functional lower deciduous incisors and one or two pairs of functional central upper deciduous incisors. Another phylogenetically constrained group that shows extensive variation in the degree of FIGURE 5. Phylogeny of the Talpidae showing function- functional replacement is the family Talpidae al tooth replacement. This phylogeny follows that of Whidden (2000), which is based on myological charac- (moles, shrew moles, and desmans). In the ters. Uropsilus is a genus of nonfossorial Asiatic shrew case of this family, functional replacement moles, generally placed into its own subfamily, the Uropsilinae, for which we present tentative information ranges from full or nearly full to none or near- on functional replacement based on the studies of Zie- ly none, with all of the known variability in gler (1971a) and Thomas (1911). The subfamily Des- the premolar field (Table 2, Fig. 5). When the maninae contains two genera of desmans that are adapt- ed to aquatic life. Sources of replacement information patterns of functional tooth replacement are are listed in Table 2. plotted on the recent talpid phylogenies of 338 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

Whidden (2000) (Fig. 5) or Yates and Moore be deciduous (and it is by this logic that Luck- (1990), it can be seen that functional mono- ett identified the single generation of premo- phyodonty has probably evolved more than lars at the first and second loci as deciduous). once. Soricidae (shrews), the sister group of This would imply that the permanent teeth in Talpidae in recent phylogenies (Asher 2001; M. domestica are not homologous with those of Nikaido et al. 2001; Malia et al. 2002), has also Australian marsupials. entirely lost functional replacement. However, we believe it is far more parsi- monious, and more consistent with general Discussion patterns of evolution, to assume that in some The Homology of Dental Generations in Mar- marsupial taxa, such as M. domestica, the ves- supials. We observe no evidence of two den- tigial first generation seen in other marsupials tal generations at the incisor, canine, or P1 and has been lost entirely. Therefore, the function- P2 loci in M. domestica. This is in agreement al, permanent teeth observed in M. domestica with previous studies of Didelphis (Ku¨kenthal can most reasonably be interpreted as being 1891; Ro¨se 1892; Berkovitz 1978) but is in con- homologous with the functional permanent trast to several studies that have identified teeth observed in other marsupials. Because vestigial teeth at the incisor and canine loci in we cannot identify with absolute certainty a variety of Australian marsupials (e.g., Wil- which of two generations the single generation son and Hill 1897; Kirkpatrick 1978; Luckett of teeth in M. domestica represents, we simply 1989, 1993; Luckett and Woolley 1996). Our refer to these teeth as permanent. The issue of observations of M. domestica also differ sub- generational homologies is a complex one, and stantially from those of Kozawa et al. (1998) this paper does not attempt to resolve the is- on the same species. They examined a series sue. The more important point is that some of three specimens (12, 16, and 18 P) and claim marsupials retain two developmental gener- to have found evidence for bud stage vestigial ations, one of which is reduced and vestigial, 4 first-generation teeth at the I and I1 loci, a bud whereas some retain only a single develop- stage vestigial second generation at I1,and mental generation; however, all marsupials 1 successional laminae lingual to dc and dc1. possess only a single functional generation at Our study of a more complete series did not all but the p3 loci. confirm the existence of any of these struc- The Relation between Dental Development and tures. Vestigial incisors with dentine labial to the Period of Fixation in Marsupials. Our ob- the definitive incisors have been observed re- servations of the development of oral behavior cently in sectioned specimens of another di- and tooth development in M. domestica dem- delphid, Caluromys philander (van Nievelt per- onstrate that there is no general suppression sonal observation). of the process of odontogenesis during the pe- Vestigial teeth (which in some species are riod of fixation. The teeth at the lower incisor, represented by little more than swellings of upper and lower canine, and upper and lower the dental lamina) at the incisor and canine premolar loci go through most stages of den- loci have been interpreted by the above au- tal differentiation during the period of fixation thors as representing the deciduous dentition, and have begun calcification by its end (Fig. 3). so that the functional, permanent teeth rep- The upper incisors are delayed relative to the resent a successional or second generation of other anterior teeth, but undergo all stages of teeth. The apparent absence of even transitory, dental development during either the period vestigial teeth in M. domestica makes unam- of fixation or while the young are still spend- biguous identification of the generational ho- ing considerable time on the nipple. Thus, mology of these permanent teeth difficult. dental development is not generally sup- Luckett (1993: p. 196) claims that ‘‘it is impos- pressed by suckling in M. domestica. Dental sible to have a secondary or successional tooth development also occurs throughout the pe- without a deciduous predecessor.’’ If true, by riod of attachment in other marsupial species definition the single generation of teeth ob- (Luckett 1993). There appears to be no func- served in M. domestica would be considered to tional or mechanical incompatibility between REDUCED TOOTH REPLACEMENT IN MAMMALS 339 dental development and the functional de- suppression of anterior deciduous dentition in mands placed on the oral region during suck- marsupials. Second, seemingly similar adap- ling by marsupials. tations are seen in some eutherians. However, The development of the upper first incisor as suckling is universal for mammals, one in M. domestica is consistently delayed relative might expect some delay in eruption of the to all of the other incisors, and its eruption is central incisors to be universal. We are aware relatively late as well. I1 erupts around day 54 of no particular adaptations for suckling in the at about the same time that the young are be- taxa in which incisor developmental delay has ginning to feed like an adult. For about two been observed. It is therefore puzzling that weeks before weaning, this delay produces a such adaptations appear to have a limited dis- gap in the anterior dentition (Fig. 6). Luckett tribution within the Theria. and Woolley (1996) also noted a delay in I1 de- We have discussed above the possibility velopment and eruption in the red-cheeked that functional replacement of incisors may be dunnart (Sminthopsis virginiae), and similar suppressed because of interactions with the patterns have been reported for the Tasmani- nipple in some marsupials and placentals. By an devil (Sarcophilus laniarius) (Guiler and contrast, some other taxa including most bats Heddle 1974), the Virginia opossum (Didelphis (Slaughter 1970; Vaughan 1970; Phillips 1971, virginiana) (McCrady 1938), and a variety of 2000; Czaplewski 1987) and some murid ro- other polyprotodont marsupials (Thomas dents (Lawrence 1941; Hamilton 1953; Brooks 1887). In at least S. virginiae, D. virginiana,and 1972; Gilbert 1995) appear to have evolved S. laniarius eruption is known to occur at about teeth with specialized morphologies that al- the time of weaning and has been hypothe- low the young to cling tenaciously to the nip- sized to facilitate continued suckling by leav- ple. ing a gap in the middle of the upper incisors To summarize, development of the anterior for the nipple to fit into during the prewean- dentition of M. domestica is not generally sup- ing period (Winge 1941; Guiler and Heddle pressed or delayed during suckling. The up- 1974; Luckett and Woolley 1996). per incisors do show a transient delay in de- Interestingly, the preweaning medial gap in velopment (relative to the lower incisors), but the incisors found in polyprotodont marsu- this perturbation is of brief duration, except in pials is found in modified form in the mustel- thecaseofI1. The data presented here cannot ids that have reduced functional incisor re- eliminate the possibility that the pattern of placement, such as the ferret illustrated in Fig- dental replacement observed in marsupials is ure 6. In this case the small but functional di3 related to their reproductive specializations, and the large dc1 do erupt, while the central as craniofacial development is highly derived pairs of incisors are tiny and may or may not (Smith 2001) and it is possible that odonto- pierce the gums. This soft tissue-lined gap genesis is as well. If true, then, this provides persists until the eruption of the functional further evidence that the marsupial reproduc- permanent incisors shortly after weaning tive pattern is not primitive for therians, but (Berkovitz and Silverstone 1969). Neal (1986) in fact derived (Smith 2001). However, as the speculated that the gap in another mustelid, marsupial mode of reproduction appears to Meles meles, was ‘‘an adaptation for suckling.’’ have evolved only once, it is impossible to test Incisor gaps during the suckling period have this hypothesis by comparative methods. It is also been reported for the brown bear (Ursus clear that there is no general support for the arctos) (Dittrich 1960) and the northern rac- hypothesis that there is a direct causal link be- coon (Procyon lotor) (Montgomery 1964). tween marsupial suckling and the suppres- Therefore, although it is possible that the sion of anterior tooth development. delay in eruption of I1 in Monodelphis domestica Loss of Functional Tooth Replacement in Theri- and other polyprotodont marsupials is due to an Mammals. The survey of functional tooth suckling, two facts are important. First, this replacement patterns in living placental mam- pattern is limited to a single tooth locus and mals allows the marsupial tooth replacement cannot explain the general phenomenon of pattern to be placed in the general context of 340 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

FIGURE 6. Closing of the incisor gap in an opossum and the ferret. Anterior views of the incisor regions showing the condition of that region while there is a median incisor gap, just after that gap closes, and the adult condition. Skulls were photographed with the jaws held closed and the cheek teeth in occlusion. Scale bars, 1 mm, with each species at a constant scale. A–C, The gap formed between the I2’s and how it is closed by the eruption of I1 in M. domestica. A, Age 45 P (male, KKS-99003). Observe the wide gap between the I2’s. The jaw would have to open slightly for this gap to open up because of the way that the lower teeth are positioned. Note that I1 protrudes slightly above the alveolar bone. B, Age 55 P (male, KKS-99017). I1 now closes the gap. C, Age 140 P (male, AvN 01-050). The adult condition, in which the incisors as a whole have spread out, but in which there is no median gap. D–F, The median gap in the incisor region of a ferret, Mustela putorius. In the ferret the gap is formed because all of the deciduous incisors except di3 are vestigial. D, Age 27 P (male, AvN 01-018). The large medial gap is formed between the sturdy deciduous canines and the small but functional di3’s. In this case the gap is formed even with the jaws held fully closed. Vestigial deciduous incisors can be seen medial to di3 and a single vestigial lower incisor is visible. E, Age 50 P (male, AvN 01-012). Incisor gap closed by eruption of permanent incisors. F, Adult female (AvN 00- 005). All specimens are currently housed in the laboratory of K.K.S. at Duke University. REDUCED TOOTH REPLACEMENT IN MAMMALS 341 the range of replacement patterns seen in the- tooth at any given position. Loss of teeth at rian mammals. Data presented in Table 2 various loci is common in therians, and loci demonstrate that the loss of deciduous teeth at that are being reduced in size and importance various loci is common within eutherians and may possibly eliminate functional replace- occurs in many taxonomic groups. The only ment as an intermediate stage on the way to placental mammal that possibly matches the full elimination of the locus. Examples of this marsupial functional replacement pattern (re- might be the dp2/P2 locus in the domestic cat placement at only the last premolar locus) is or the unreplaced deciduous premolars of the broad-footed mole (Scapanus latimanus), bears. Murid rodents have eliminated canines but the functionality of the last premolars in and premolars altogether and thus neither this species is not well known (Ziegler 1972). tooth generation erupts at these loci. They Even if there are no placental mammals that have retained molars, but because molars do exactly match the primitive marsupial pat- not undergo replacement, murids have no tern, marsupials fit within the range of living dental replacement at all. placental mammals (Table 2). In fact, the mar- Homodonty (all teeth with similar mor- supial pattern fits into the range of variation phology), polydonty (more than the primitive seen in the carnivore superfamily Mustelo- number of teeth), simplification of the cusp idea. Within this single superfamily one sees patterns of the cheek teeth, and ever growing the primitive eutherian condition of full re- teeth are found in various combinations in a placement, the loss of most functional replace- phylogenetically diverse assemblage of mam- ment at the incisor loci, and even the loss of all mals. Presumably, changes to the primitive functional replacement (Mephitis mephitis). mammalian dental developmental program The musteloids demonstrate that animals are required to create teeth or dentitions of with very different patterns of functional these types. Such developmental changes ap- tooth replacement can be fairly closely related, pear in some cases to be correlated with the have similar adult morphologies, occupy a loss of tooth replacement. The dentition of Or- similar adaptive niche, and share similar life ycteropus afer (the aardvark) is highly modified histories. and this species exhibits a highly modified The comparative data provided by placental pattern of replacement. The functional teeth of mammals strongly refute the hypothesis that this species, while varying in size, are mor- the tooth replacement patterns seen in mar- phologically simplified and similar. The func- supials are necessarily indicative of, or corre- tional dentition seen in the adult is reduced to lated with, the radical specializations associ- I0/0, C0/0, P2/2, M3/3 (Anthony 1934) and ated with the marsupial mode of reproduc- the functional teeth are ever growing, lack tion. Life history traits are neither a necessary enamel, and have a peculiar ‘‘tubular’’ micro- nor a sufficient explanation of the mode of structure (Broom 1909; Heuser 1913; Anthony dental replacement seen in marsupials. 1934). O. afer lacks functional tooth replace- Explanations for the Loss of Functional Replace- ment altogether (Thomas 1890; Broom 1909; ment. We are not aware of any systematic at- Anthony 1934) although several extra (poly- tempt to explain the loss or reduction of func- dont) premolar positions are indicated by the tional tooth replacement in therian mammals, presence of vestigial milk teeth (Broom 1909; although many kinds of potential factors have Heuser 1913; Anthony 1934). The living been suggested. These include the loss of toothed whales (Odontoceti) are typically ho- tooth loci, major modifications of the dentition modont and polydont and lack tooth replace- and dental development, factors related to the ment (MacDonald 1984). However, primitive particulars of life history and adaptations, whales (archaeocetes) were heterodont, were functional demands during the normal re- not polydont, and underwent functional re- placement period, phylogenetic history, and placement (Uhen 2000). The living pinniped growth. carnivores tend toward homodonty in the One potential factor is that dental replace- postcanine dentition and lack functional tooth ment may be lost in the process of losing a replacement altogether (King 1983). The large, 342 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH ever growing incisors in both rabbits and ro- sochloridae (golden moles), have full function- dents do not undergo functional replacement al replacement, however. (Woodward 1894; Hirschfeld et al. 1973; Moss- Some degree of phylogenetic constraint Salentijn 1978). may operate as well. It is possible that once However, major modifications of the devel- tooth replacement is lost in a particular evo- opmental program are not necessarily asso- lutionary lineage, it may be very difficult or ciated with the loss of functional replacement. impossible for descendant species to regain it. Dasypus novemcinctus (the nine-banded arma- Thus there may be species that might be pre- dillo) has a dentition as oddly specialized as dicted to benefit from tooth replacement for that of O. afer, yet it possesses functional, root- theoretical reasons, but do not have it because ed deciduous teeth that are subsequently re- their ancestors lost it. placed at seven of the eight adult tooth posi- Finally, we propose that growth of the body tions (Flower 1868; Martin 1916; Stangl et al. and jaws may be a factor in the reduction of 1995). In rabbits, the large, curved, ever grow- diphyodonty in therian mammals, in part be- ing incisors are not functionally replaced, but cause it appears to have been an important the smaller pair of upper incisors and the pre- factor in the evolution of diphyodonty from molars are represented by rooted deciduous polyphyodonty. In nonmammalian vertebrates, teeth that are replaced by rootless, ever grow- tooth replacement is intimately related to ing permanent teeth (Hirschfeld et al. 1973; growth. Each successive generation of teeth is Michaeli et al. 1980). incrementally larger than the preceding one There may be features of an animal’s life as the animal undergoes slow growth for an history and ecological adaptation that have indefinite period. Tooth wear is not consid- somehow led to selection against tooth re- ered a major factor in replacement because placement. Both toothed whales and pinni- teeth are usually shed before they are signif- peds have lost functional replacement and it icantly worn (reviewed in Berkovitz 2000). It has been suggested that this is related to has been argued that in mammals, lactation, aquatic predation. For example, Kubota et al. in combination with the transition from slow, (2000) related the loss of functional replace- indeterminate growth to rapid growth to a de- ment in Callorhinus ursinus (northern fur seal) terminate adult size, has led, in part, to a re- and other pinnipeds to selection for adult duction of tooth replacement (for example feeding behavior at an early age. They did not Gow 1985; Zhang et al. 1998). A mammal pos- explain why adult feeding behavior could not sessing both lactation and rapid determinate be achieved with a smaller deciduous denti- growth requires a small set of teeth that fit a tion. Size, too, has been suggested as a causal juvenile sized jaw only briefly. The period of factor in the loss of dental replacement. Bloch et al. (1998) speculated that lack of functional lactation, which requires no teeth, eliminates replacement in living insectivores might be the need for functional replacement earlier related to small size, judging from the distri- during growth or at a small size. The short pe- bution of monophyodonty in living lipotyph- riod of rapid growth to an adult size elimi- lans. They noted, however, that the Eocene in- nates the need for several successive genera- sectivore Batodonoides vanhouteni maybethe tions of intermediate sized teeth. In this way smallest known mammal and that it had re- the ancestor of therian mammals came to pos- placement at least at the P4 locus. Ziegler sess a single generation of replacement teeth, (1971a) noted that lack of functional replace- which erupt when the jaw reaches a size large ment was derived independently in all of the enough to accommodate them. Molars, which lineages of fossorial moles, but not in the lin- are not replaced, accommodate growth be- eages of semifossorial or nonfossorial shrew cause they erupt at the back of the tooth row, moles. He felt that lack of replacement was a once space is available. This model does not derived character somehow related to the sub- ignore the fact that other factors, such as the terranean lifestyle. Members of the other fos- need to maintain precise occlusion for the sorial group for which we have data, Chry- proper functioning of a shearing dentition REDUCED TOOTH REPLACEMENT IN MAMMALS 343

(Hopson 1973), may also have contributed to replacement in marsupials is neither unusual selection for reduced replacement. among therian mammals nor highly correlat- The fossil evidence for this scenario is, un- ed with the extended period of nipple attach- surprisingly, meager, but Zhang et al. (1998) ment in any obvious manner. Although all pointed out that a series of skulls of the Early marsupials may possess this derived pattern, Jurassic mammaliaform Sinoconodon shows a and in fact, it may represent an important syn- wide range of sizes, all with functional den- apomorphy of the group, there is no evidence titions, whereas a series of skulls of another for the conclusion that it is a clear indication Early Jurassic form Morganucodon varies little of any specific reproductive adaptation. in size. This difference can be interpreted as Second, we point out the enormous diver- evidence that Sinoconodon underwent slow, in- sity in replacement pattern among eutherian determinate growth, whereas Morganucodon mammals. It is possible that the loss of decid- grew rapidly to an adult size. Sinoconodon is uous dentition, or the evolution of monophyo- definitely polyphyodont and the evidence for donty from diphyodonty, is simply an exten- tooth replacement in Morganucodon is consis- sion of the primitive mammalian condition of tent with diphyodonty. the loss of dental generations. It may require Following this same line of reasoning, it is no special explanation, but simply accompany possible that in some mammals the body and the evolution of many types of dental and life jaws reach adult size, or are large enough to history adaptations. accommodate adult-sized teeth, before the an- Given this diversity, we urge caution in imal requires a functional dentition. In these making inferences, based on dental replace- cases, we might expect that dental replace- ment patterns, about behavior or life history of ment would be reduced from the diphyodont organisms known only in the fossil record. to the monophyodont condition (Mı´sek and Acknowledgments Sterba 1989). As yet, comparative data on body and jaw growth and tooth eruption and We thank R. F. Kay and V. L. Roth for com- replacement are not available. If, however, a ments on an earlier draft of this manuscript. relation exists between these two processes, J. Jernvall provided inspiration for the title. then the reduction of replacement to the func- Thanks also to C. Schnurr and the other pos- tionally monophyodont condition, so common sum wranglers who, at great personal risk to in therian mammals, would merely be a con- their fingers, assisted in collecting the tooth tinuation of the same processes that led to the eruption data. T. A. Williams performed some evolution of diphyodonty. If demonstrated, it of the feeding experiments and provided would do much to help us understand the ear- behavioral observations. Special recognition ly evolution of the mammalian lineage. should go to J. Wright, whose dissertation Unfortunately, none of the causal factors (Wright 1983) (available from University Mi- discussed above appear to provide a good crofilms International) is a fabulous source of general explanation of the loss of functional information and references for anyone inter- replacement across therians. They are either ested in the deciduous dentition. This research ad hoc explanations for single cases, coun- was done in partial fulfillment of the re- tered as general explanations by comparative quirements for a Ph.D. in Biological Anthro- data, or lacking in supporting data. It may pology and Anatomy at Duke University and well be that there is no single explanation for A.F.H.v.N. is grateful for the financial support the loss of tooth replacement, but instead, loss of that department, his parents, and his wife. of functional replacement may have evolved K.K.S., and the Monodelphis colony, was sup- for many reasons as mammals evolved their ported by grants from the National Science great variety of dental adaptations. Foundation.

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