To replace or not to replace: the signiﬁcance of …people.duke.edu/~kksmith/papers/tooth...

q 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3102-0009/$1.00

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

To replace or not to replace: the significance of reducedfunctional tooth replacement in marsupial andplacental mammals

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

Abstract.—Marsupial mammals are characterized by a pattern of dental replacement thought to beunique. 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. Inmarsupials, 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, thesuppression 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 thatdental 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 reproductivemode 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, butwe 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

Tooth replacement in marsupial mammalsdiffers from the condition generally believedto characterize eutherian mammals. In euthe-rian mammals, there are typically two gener-ations of incisors, canines, and most (or all)premolars. In contrast, marsupials typicallyhave two generations of functional teeth atonly one locus in each jaw quadrant, the lastpremolar (P3) (first noted by Flower [1867]).Some derived dasyurids have eliminated re-placement altogether. By definition, molarteeth are represented by only a single gener-ation in both clades. Studies of dental replace-ment in dryolestid eupantotheres (Martin1997), a Mesozoic taxon that represents anoutgroup to the Theria (Metatheria 1 Euthe-ria), show that the pattern commonly seen inliving eutherians is the primitive one.

Close examination of the development ofthe anterior dentition in a variety of marsu-

pials reveals that vestigial first generation(‘‘milk’’) incisors and canines are found inseveral marsupial families, including Macro-podidae (in Macropus giganteus Kirkpatrick1978), Dasyuridae (in Dasyurus quoll Luckett1989, and Sminthopsis virginiae Luckett andWoolley 1996), and Peramelidae (in PeramelesWilson and Hill 1897). Thus far, most detailedstudies of dental development of didelphids,generally considered to have the most primi-tive dentition of extant marsupials, havefailed to document incontrovertible evidenceof a vestigial first tooth generation. Thesestudies include several of Didelphis (Kukenthal1891; Rose 1892; Berkovitz 1978). However,Kozawa et al. (1998) claimed that Monodelphisdomestica has a much more complex set of suc-cessional homologies, with vestigial first gen-eration incisors at two loci and vestigial sec-ond generation teeth at three. Our own studiesof a more complete series of M. domesticafound no evidence for vestigial teeth. The ves-

325REDUCED TOOTH REPLACEMENT IN MAMMALS

tigial anterior teeth seen in the Australianfamilies are interpreted as evidence for theloss of a first generation of functional anteriorteeth present in the ancestry of marsupials.Thus, relative to the primitive therian condi-tion, marsupials have a distinctive, derivedpattern of reduced dental replacement.

Several workers have tied this derived pat-tern of dental replacement to the marsupialmode of reproduction and development. Wil-son and Hill (1897: p. 554) stated, ‘‘We believethat we are justified in seeking for the cause ofthe almost total suppression of the milk-teethin front of the last premolar, in the modifiedcondition of the mouth in the marsupialyoung in consequence of its peculiar adapta-tion to the sucking function.’’ Winge (1941)came to a similar conclusion, as did Ziegler(1971b: p. 240) who stated, ‘‘The selective fac-tors contributing to the suppression of thecomplete metatherian antemolar milk denti-tion except dP4 to a vestigial state are notknown for certain, although, as has often beensuggested, the phenomenon is very likely re-lated to the peculiar method of attachment ofthe newborn young to the nipple in the moth-er’s pouch.’’

More recently Luckett (1993: p. 195) alsoclaimed a link between the highly modifieddental development pattern and reproductivemode in marsupials. ‘‘(T)his modified anteri-or dentition is correlated with the prolongedlactation period of marsupials, especially withthe ‘period of fixation’ (Hill and O’Donoghue1913), during which the suckling young iscontinuously attached to the nipple for alengthy period of time. The well developedtongue and nipple fill the oral cavity duringthis period, and the continued pressure exert-ed by these structures probably has an effecton the developing tooth germs underlying theoral epithelium.’’

Because aspects of dental development andreplacement can be identified and studied infossils, the evolution of various conditionsmay be documented. Cifelli et al. (1996) de-scribed an immature specimen of Alphadonfrom the Late Cretaceous of North Americathat seems to show a dental replacement pat-tern similar to that seen in living dasyurids ordidelphids. On the basis of this specimen, Ci-

felli et al. (1996) argued that the marsupialtooth replacement pattern is of great antiquityand is found in some of the earliest marsupi-als. Cifelli and Muizon (1998) provide furtherevidence of the early appearance of the mar-supial dental replacement pattern in Creta-ceous and Paleocene marsupials. They de-scribed juvenile specimens of five marsupialspecies from the Paleocene of South Americaand found no evidence for tooth replacementanterior to the last premolar locus. They con-cluded that ‘‘(t)he pattern of postcanine erup-tion and replacement in the fossils is remark-ably similar to that of recent didelphids’’ (Ci-felli and Muizon 1998: p. 218). Furthermore,they emphasized the systematic significanceof that pattern: ‘‘Given the problematic natureof most dental and even basicranial featuresdefining Marsupialia (Muizon 1994), we sug-gest that the most robust test for assessing del-tatheroidean relationships will be provided byevidence from tooth replacement. In fact, inspite of the difficulties of observing it on fos-sils, it is probable that the pattern of tooth re-placement and eruption of living marsupialsrepresent one of the best metatherian syna-pomorphies (p. 218).’’ Rougier et al. (1998)demonstrated that the marsupial dental re-placement pattern is present in Deltatheridium,a deltatheroidean from the Late Cretaceous ofMongolia.

In addition to using this character in phy-logeny reconstruction, paleontologists haveused the hypothesized link between the de-rived marsupial tooth development patternand the distinct marsupial reproductive pat-tern to make inferences about the reproduc-tive patterns of fossil taxa. Cifelli et al. (1996:p. 717) argued on the basis of observing themarsupial tooth replacement pattern in Alpha-don ‘‘that at least some reproductive speciali-zations of marsupials, including nipple fixa-tion, were probably established during theMesozoic, earlier than previously suggested.’’Martin (1997) reported that dryolestid eupan-totheres from the Jurassic show unreducedtooth replacement (i.e., a pattern similar to eu-therians and different from marsupials) andconcluded, ‘‘Therefore, a marsupial reproduc-tive pattern most probably can be ruled out forLate Jurassic ‘eupantotheres’ with a plesio-

326 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH

morphous mode of tooth replacement’’ (p. 15).Rougier et al. (1998: p. 462) also commentedon the likely reproductive mode of deltather-oideans. ‘‘If the metatherian patterns of skulldevelopment, tooth replacement and repro-duction are correlated, deltatheroideans mayalready have possessed the basic marsupialreproductive pattern.’’

In this paper, we report observations ondental development and tooth eruption in thedidelphid Monodelphis domestica. We also pre-sent comparative data on tooth replacement inother mammals, both marsupial and placen-tal. We address the two major predictions ofthe hypothesis discussed above. First, we ex-amine the progress of dental developmentduring the period of fixation to see if odon-togenesis is suppressed during that develop-mental stage. This part of our study tests theexplicit hypothesis that the suppression ofdental replacement is a direct result of nippleattachment in marsupials. Second, we exam-ine whether the suppression of dental gener-ations is a unique character of marsupials.This part of our study allows us to determinewhether the evolution of the marsupial repro-ductive strategy is a necessary condition forthe evolution of the derived pattern of dentalreplacement observed.

Materials and Methods

Primary Study Species. The species studiedwas Monodelphis domestica, the gray short-tailed opossum, a small (80–130 g) didelphidmarsupial native to Brazil and Bolivia (Strei-lein 1982; Eisenberg and Redford 1999; No-wak 1999). The animals studied were from abreeding colony housed at Duke University.Colony husbandry is described by van Nieveltand Smith (2005). Pregnant females werechecked daily for the presence of a litter, so theage of all animals and specimens is known towithin 61 day. Young are born after a gesta-tion of 14.5 days and the day of birth is des-ignated as day 0 postnatal (0 P).

M. domestica possesses the didelphid adultdental formula: incisors 5 (upper)/4(lower),canines 1/1, premolars 3/3, molars 4/4. In thetext, upper teeth are designated by a numer-ical superscript (e.g., P3), lower teeth by a sub-script (e.g., P3). When both uppers and lowers

are referred to neither subscript nor super-script is used (e.g., P3). The homology of theteeth in the marsupial dentition has been con-troversial and there are several alternate no-menclatures (Flower 1867; Thomas 1887; Zie-gler 1971b; Archer 1978; Luckett 1993). As willbe seen below, in M. domestica, we were unableto detect a vestigial first generation of teeth.We hypothesize that the basic pattern of den-tal replacement is homologous in all marsu-pials, and we have followed the ontogeneti-cally based system of Luckett (1993). There-fore, following Luckett, we designate the teethfound in the adult dentition as follows: Theupper incisors are designated I1 to I5, the low-ers I1 to I4 (from mesial to distal). Canines aredesignated C1 and C1. Again following Luck-ett, premolars are designated dp1, dp2, andP3 (as Luckett argues that the functional adultteeth at the p1 and p2 position are from thefirst generation). Molars are designated M1 toM4. The single functional deciduous tooth ineach jaw quadrant is designated dp3. As istypical for marsupials, the premolars found inthe adult dentition are premolariform (i.e., notmolariform) and the deciduous premolar ismolariform. Note that antemolar teeth with aprefix ‘‘d’’ are considered to be from the firstor ‘‘deciduous’’ generation. Antemolar teethdesignated without a ‘‘d’’ prefix are consid-ered to be homologous with those of the sec-ond or ‘‘permanent’’ generation.

Development of Tooth Germs: Histological Spec-imens. Stages of dental development for allteeth present were determined in 17 ages be-tween day 14 embryonic (14 E) and day 35postnatal (35 P). In most cases a single speci-men of a given age was examined. Specimenswere fixed in 10% phosphate buffered forma-lin or Bodian’s fix (Humason 1979), decalci-fied, embedded in paraffin, and were seriallysectioned in a plane transverse to the jaws(coronal plane) at 8-12 m. Alternate slides werestained with Milligan’s trichrome or Weigert’shematoxylin counterstained with picropon-ceau (Humason 1979). The seven stages oftooth development recognized in this studyfollow the stages of Osborn (1981) and Ber-kovitz (1978): thickening of the free edge ofthe dental lamina (t.d.l.), bud, early cap, latecap, early bell, late bell with dentine (or pre-


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, primaryenamel 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 andenamel (or pre-enamel) present

dentine) only (abbreviated as ‘‘dentine’’), andlate bell with dentine and enamel (or pre-enamel) (abbreviated as ‘‘enamel’’). The stagesand the developmental events characterizingthem are shown in Table 1. The earliest stagerecognized (thickening of the free edge of thedental lamina) is somewhat subjective. It is anattempt to note the first visible signs of cel-lular proliferation in the dental lamina thatwill lead to a tooth germ at that position.

Eruption of Teeth and Development of Oral Be-havior. For the purposes of this paper, a toothwas considered to have erupted when anypart of its crown had pierced the gingiva(‘‘standard gingival emergence’’ of Smith etal. 1994). The age of gingival emergence wasdetermined by closely spaced (approximatelyevery other day) repeated observations of 14young from three litters. Average ages of gin-gival emergence (rounded to the nearest day)are reported here. Tooth eruption in M. do-mestica is examined in detail by van Nieveltand Smith (2005), where details of definitions,materials, methods, and statistics are report-ed.

Observations of aspects of the oral devel-opment of young in the colony were made onthe eruption study litters, on other litters oflive young, and on young taken for histolog-ical study. Some young between the ages of 37and 59 P were placed in proximity to variousfood items of varying hardness and difficulty(ferret chow pellets, live crickets, sliced apple,and sliced banana) in four experiments. Thereactions of the young to the food items were

noted. Other chance observations of earlyfeeding behavior were also recorded. The con-dition of the mammaries and nipples of themothers of four litters was also monitoredover the course of lactation in an effort to dis-cover when they had regressed to a nonpro-ducing condition. These observations werefairly subjective, as the regression of the mam-maries was a gradual process. It was noted atwhat ages the mammaries and nipples werefirst recorded as reducing in size, when theyappeared greatly reduced in size from thepeak size, and when they had returned to thesize typical of a nonbreeding, nonlactating fe-male.

Comparative Mammalian Tooth Replacement.To determine if the reduced functional toothreplacement seen in marsupials is exceptional,we searched the literature in order to delineatethe variation in functional tooth replacementpatterns in therian mammals. The choice oftaxa in the comparison group is not intendedto provide an exhaustive survey of the varia-tion of functional tooth replacement patternsin therian mammals, and the included speciesmay not be representative of other species inthe same family or order. Our sample includesthe full range of functional replacement fromthe maximum possible to none. We made aconcerted effort to collect all of the availabletooth replacement data for two groups, themusteloid carnivores and the talpid eulipo-typhlans, because these groups are well stud-ied and have diverse replacement patterns. Wefollow the recent phylogeny of Flynn et al.


(2000) in defining the Musteloidea as contain-ing the families Mustelidae and Procyonidae,as well as a separate family containing theskunks, the Mephitidae.

For the purposes of compiling the data onfunctional replacement, we considered onlytooth loci filled by one or two generations offunctional teeth. A tooth was considered ves-tigial if it did not consistently pierce the gin-giva, was shed after a very short period, orwas considered vestigial in the literature. Thedecision on whether or not to consider as ves-tigial diminutive teeth that did consistentlypierce the gums was somewhat subjective. Alocus was considered to have functional re-placement if it was filled by a functional toothin both the first and second generations. A lo-cus was not counted at all if it was filled onlyby vestigial teeth (of either or both genera-tions).

To compare animals with a range of dentalformulae, we calculated the percentage of thefunctional replacement for each dental field(incisor, canine, and premolar). This numberis equal to the number of tooth loci in eachfield that show functional replacement divid-ed by the number of loci that show at least onefunctional generation of teeth times 100%. Thefirst premolar locus in eutherians is exception-al in that it is replaced in few living taxa (Zie-gler 1971b; Luckett 1993). It has also been lostin many groups. Because of this, we have cho-sen to exclude the first premolar locus (P1) ofeutherian (placental) mammals from the cal-culations. Excluding the tooth at the P1 locusfrom the calculations has the effect of makingmore eutherian species appear to have com-plete (100%) functional premolar replacement.It therefore overestimates the differences be-tween eutherians and marsupials.

Two examples illustrate our method of cal-culating percentage of functional replace-ment. Canis familiaris (domestic dog) has a de-ciduous dental formula of di 3/3, dc 1/1, dp4/4 and a permanent dental formula of I 3/3,C 1/1, P 3/3, M 2/3. (The functional tooth atthe P1 locus is usually considered to be a tooth[dp1] from the deciduous dentition that is re-tained with the permanent dentition.) Allteeth are functional. The percentages of func-tional replacement are as follows: incisors: 6/

6 5 100%, canines: 2/2 5 100%, premolars: 6/6 5 100%. Note that if the P1 locus had beenincluded in the calculation, the premolar re-sult would have been 6/8 5 75%. Felis catus(domestic cat) has a deciduous dental formulaof di 3/3, dc 1/1, dp 3/2 and a permanentdental formula of I 3/3, C 1/1, P 3/2, M 1/1.However, dp2 is vestigial whereas P2 is re-duced in size but functional (Leche 1915). Thepercentages of functional replacement are asfollows: incisors: 6/6 5 100%, canines: 2/2 5100%, premolars: 4/5 5 80%.

Results

Development of Oral Behavior. M. domesticaneonates attach to a nipple shortly after birthand within three days their mouths are tightlybound to the swollen end of the nipple by aperidermal seal that closes the lips. Youngwere first observed to detach from and reat-tach to the teat about 12 days after birth. Thisis the period of fixation for M. domestica. By 13to 15 P the seal over the lips has broken downand the mouth opening begins to broaden toits full extent. Even though the young can de-tach and reattach to a nipple, our observationssuggest that considerable time is still spent ona teat. Before 31 P young were almost alwayson a teat when the cage was first opened andthe mother and young were examined in thenest. Between 31 and 44 P the percentage ofyoung on a teat declined, and after 44 P youngwere almost never found on a teat.

When the mother moves about the cage theyoung cling to her. This is accomplished bybiting down on a nipple or the fur and/orgripping with the hands, feet, and prehensiletail. We first observed young clinging to themother’s fur orally at 29 P. In slightly olderyoung that have well-erupted incisors, one canconfirm the incisors’ participation in this gripby gently pulling off a pup and seeing the pat-tern in the mother’s hair left by the incisors asthey ‘‘combed’’ it. This oral clinging of theyoung to the mother continues until indepen-dence.

Pups as young as 37 P sniff a favorite food(banana) and begin to masticate softer fruitsby 45 P. We have observed them consuminghard chow pellets by 47 P. Crickets were pre-sented to the young at 37, 51, and 59 P. The 37


P young did not react to the potential prey,whereas the 51 and 59 P young left alone withcrickets eventually captured and consumedthem. Initial attempts at prey capture wereclumsy; however, the young rapidly acquiredthe stereotypic response to prey seen in theadult (Ivanco et al. 1996). In sum, M. domesticayoung have acquired a full repertoire of adultfeeding behaviors sometime between 47 and51 P.

One aspect of weaning is the start of solidfood consumption, the other is the end ofsuckling. The size of the mammaries appearsto track the amount of milk consumed, as itdoes in Didelphis virginiana (Reynolds 1952). Inour sample of mothers, the mammary glandspeaked in size at around 51 P, were greatly re-duced in size by 58 to 69 P, and were reducedto the nonreproductive condition by 69 to 78P. If mammary size is an accurate indicator ofmilk consumption, consumption peaks andbegins to decline just as the young haveachieved a full range of feeding capabilitiesand is effectively over before 58 to 69 P, whenthe mammary tissue has mostly shrunk away.Young are routinely separated from the moth-er at eight weeks in laboratory colonies(VandeBerg 1999).

Development of Tooth Germs. We were ableto discern the initial thickening of the dentallamina at all tooth positions and were able totrace development through the deposition ofenamel at all but three posterior molar posi-tions and the replacement premolars. Theseresults are summarized graphically in Figure1. The states of development of representativeteeth near the middle (7 P) and at the end ofthe period of fixation (13 P) are shown in Fig-ures 2 and 3, respectively. As is well known,the marsupial neonate is highly altricial andcan be defined as being embryonic in mostfeatures, including the dentition. The only dis-cernible evidence of differentiation of teeth onthe day of birth is at the dp3 loci, with dp3 atbud stage and dp3 represented by a thickeningof the dental lamina. Relative to other teeth onthe same jaw (upper or lower), dp3 is alwaysthe first tooth to attain a particular stage.Within two days after birth, the followingteeth are discernible: I2–4, I2–5, C (upper andlower), dp2, and M1 (upper and lower), al-

though only dp3 has progressed beyond thebud stage. All teeth anterior (mesial) to dp3are discernible by 4 P. The replacement teethat the last premolar locus (P3) are first ob-served at 7 P as thickenings of the free edge ofthe dental lamina (Fig. 2E,F). By 13 P (Fig. 3)(the end of the period of fixation) all teeth an-terior to M3 in the lower jaw have begun cal-cification (late bell with dentine stage or later);all upper teeth anterior to M3 in the upper jaw,except for I1, have achieved at least early capstage.

In the incisor region, the first incisor initi-ates two to three days later than the more dis-tal incisors. I1 does catch up with the otherlower incisors and achieves late cap stage atabout the same time (10 P). The same is nottrue of I1. Though it achieves bud stage at thesame time as I2–3, it achieves all subsequentstages later than any other upper incisor. Thisdifference will persist through tooth eruption,where it will be even more pronounced. Afterthe bud stage, I4 is also relatively retardedcompared to I2–3,5.

The canines all appear within one day afterbirth. Within a jaw (upper or lower), the ca-nines are one of the two to four most advancedteeth at any given age. The upper and lowerfirst molars become discernible at about thesame time (2 P), quite early in the develop-ment of the dentition. In subsequent molars(M2–M3) the lower molar reaches a givenstage three to eight days before the upper mo-lar reaches the same stage. There is no visibletrace of M4 in the first 23 days after birth. M4

has achieved late cap stage in the 35 P speci-men.

The only definitive evidence of two gener-ations of teeth was found at the third premolarlocus, where the development of both dp3 andP3 were observed. The germ of P3 first ap-pears as a thickening of the free edge of thedental lamina between dp2 and dp3 by about7 P. There are no structures suggesting morethan one tooth generation at the canine ordp1–2 loci. In the absence of evidence of ves-tigial teeth, we assume that the generationalidentity of teeth is homologous with that ob-served in other marsupials (Luckett 1993).

Eruption of Teeth. Dental eruption in M. do-mestica is discussed in detail by van Nievelt


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 lowerteeth on the left and the upper teeth on the right. The dotted centerline represents the midline of the jaw and theteeth are in proximal-to-distal sequence from that line. The first six stages shown (t.d.l. to enamel) are the result ofexamination of a series of sectioned specimens and do not have confidence intervals. Also, the age of the start ofthese six earlier stages cannot be estimated accurately after 23 days because of larger gaps in the series after thatage. For clarity the early bell stage has been omitted. The age of eruption (first gingival emergence) is based onstudy of 14 individuals. The points are at the mean age of eruption and the error bars are 62 standard deviations.The lower gray area covers the period of fixation and the upper gray area represents the weaning period (from theearliest observed consumption of solid food to the rapid regression of the mammaries).


FIGURE 2. Development of representative antemolar teeth during the period of fixation (7 P) in M. domestica. Theseare frontal sections, oriented so that medial is to the right. Arrows indicate tooth germs. A, I2 at bud stage. B, I2 atearly cap. C, Upper canine at early cap. D, Lower canine at early cap. E, P3 as a thickening of the dental lamina; thestructure just lateral to P3 is the anterior tip of dp3. F, P3 as a thickening of the dental lamina; this section is anteriorto any part of dp3. G, dp3 at early bell. H, dp3 at early bell. Abbreviations: d 5 dentary (mandible) bone; e 5 oralepithelium; m 5 maxilla; p 5 premaxilla; t 5 tongue. Scale bars, 50 mm.


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 capstage. B, I2 at late bell; arrow points to dentine. C, Upper canine at late bell; arrow points to enamel. D, Lower canineat late bell; arrow points to dentine; enamel not visible. E, P3 at bud; note dp3 laterally. F, P3 at bud; this section isanterior to any part of dp3. G, dp3 at late bell; arrow points to enamel. H, dp3 at late bell; arrow points to enamel.Abbreviations as in Figure 2. Scale bars, 50 mm.


and Smith (2005) and shown graphically inFigure 1. Gingival emergence can be dividedinto five phases separated by lulls in eruptiveactivity. The first phase runs from about 32 to45 P. In this phase dp3 is, on average, the firsttooth to erupt, at about 32 P, closely followedby dp3. These teeth are followed by 17 othersin rapid succession until there are 19 teetherupted (per side) by day 45. These 19 teethinclude all incisors with the notable exceptionof I1, both upper and lower canines, dp1 todp3, M1–2, and M1. The second phase of erup-tion occurs between about 49 and 54 P, whenM2, I1, and M3 erupt. The third phase of erup-tion occurs between about 82 and 84 P. M4 andM3 erupt at that time. The fourth phase occursbetween about 108 and 112 P, when upper andlower P3 erupt. The fifth and last phase occursat approximately 126 P, when M4 erupts.

Eruption in the incisor region is notable forthe relatively late eruption of the first upperincisor. The lower incisors all erupt (between33 and 36 P) before any of the upper incisorserupt. I2 is the first upper incisor to erupt (at39 P) and is followed by I3–5 (between about 40and 45 P). I1 is the last incisor to erupt at 53 P,almost 9 days after the last of the other upperincisors, more than 14 days after the neigh-boring I2, and almost 20 days after the erup-tion of I1. The stages of eruption of I1 areshown in Figure 6. The late eruption of this in-cisor relative to its neighbors leaves a smallmedial gap which forms when the I2’s emergethrough the gums and closes fully when theI1’s are fully erupted at about 56 P. In Figure 6this gap is seen as an empty space, in life itcontains soft tissue.

Comparative Mammalian Tooth Replacement.Our survey of functional dental replacementin therian mammals shows that functional re-placement patterns are evolutionarily labileand quite variable. These patterns are shownin Table 2. Marsupials vary slightly: some de-rived species have lost all functional tooth re-placement, whereas primitive species retainreplacement at the P3 locus. Placental mam-mals show a much wider range of variation.Placentals displaying the primitive pattern offunctional tooth replacement, including hu-mans and many domestic animals, possessfull replacement of incisors, canines, and pre-

molars. Raccoons and several species of mus-telid show partial reduction of functional re-placement in the incisor region, yet these car-nivorans retain full replacement in the canineand premolar regions. Domestic cats, wildcats, and lions show full functional replace-ment of the incisors and canines, but at onlyfour of five premolar loci. Brown bears showreduced functional replacement in both the in-cisor and premolar regions. Rabbits retain fullreplacement in the premolar region, lose thecanine locus entirely, and show partial reduc-tion of functional replacement in the incisorregion. Some rodents retain full functional re-placement of premolars, while eliminatingfunctional replacement in the incisor regionand eliminating canines altogether. Finally, adiverse group of placental mammals are func-tionally monophyodont, having lost replace-ment altogether. These include the shrews,some moles, some bats, the striped skunk, thepinniped carnivores, toothed whales, theaardvark, and murid rodents.

Musteloids are notable because there is ex-tensive variation within this group (Fig. 4).Functional tooth replacement ranges fromcomplete to nonexistent both within the mus-teloid clade and among the outgroups.Among the musteloids the tayra (Eira barbara)exhibits complete replacement. It has full an-temolar replacement and retains each decid-uous tooth for at least two months (Poglayen-Neuwall and Poglayen-Neuwall 1976). In con-trast, the striped skunk (Mephitis mephitis) isfunctionally monophyodont. It does not erupta functional deciduous tooth at any position(Leche 1915; Verts 1967). Amongst the mus-teloid outgroups, pinnipeds do not have func-tional tooth replacement, whereas a canid likethe red fox (Vulpes vulpes) has full functionalreplacement.

Most members of the family Mustelidae inour sample possess full replacement of thepremolars and canines, but only partial func-tional replacement of the incisors. The exactpattern of functional replacement varies fromspecies to species. In the Eurasian badger (Me-les meles) di1 and di1–3 are vestigial, whiledi2–3, I1–3 and I1–3 are functional (Neal 1986). Inthe American badger (Taxidea taxus) and thethree species of Mustela represented in our


TA

BL

E2.

Fun

ctio

nal

toot

hre

pla

cem

ent

inth

eria

nm

amm

als.

Th

en

um

ber

sin

the

I(i

nci

sor)

,C

(can

ine)

and

P(p

rem

olar

)co

lum

ns

are

the

per

cen

tag

esof

fun

ctio

nal

toot

hre

pla

cem

ent

inth

atto

oth

fiel

d.

Kee

pin

min

dth

atth

ep

lace

nta

lP

1lo

cus

isn

otin

clu

ded

inth

eca

lcu

lati

onof

per

cen

tfu

nct

ion

alre

pla

cem

ent.

Abl

ank

spac

ein

dic

ates

ala

ckof

fun

ctio

nal

teet

hin

ato

oth

fiel

d.

Bol

dfa

cein

dic

ates

taxa

that

hav

ere

du

ced

fun

ctio

nal

rep

lace

men

t.Ta

xaar

ear

ran

ged

byor

der

;w

ith

inea

chor

der

taxa

are

arra

ng

edby

des

cen

din

gva

lue

ofin

ciso

rfu

nct

ion

alre

pla

cem

ent.

Ifa

ran

ge

isg

iven

for

ap

erce

nt

fun

ctio

nal

rep

lace

men

tva

lue,

this

may

rep

rese

nt

un

cert

ain

tyab

out

toot

hfu

nct

ion

,dif

fere

nce

sb

etw

een

two

sou

rces

,or

nat

ura

lva

riab

ilit

y.

Ord

erFa

mil

ySp

ecie

sC

omm

onn

ame

IC

PSo

urc

e

Mar

sup

ials

Did

elp

him

orp

hia

Did

elp

hid

aeD

idel

phis

vir

gin

ian

aV

irg

inia

op

oss

um

00

331,

2M

ono

delp

his

dom

esti

caG

ray

sho

rt-t

aile

do

po

ssu

m0

033

this

stu

dy

Pau

citu

ber

cula

taC

aen

oles

tid

aeC

aeno

lest

esco

nvel

atus

Bla

ckis

hsh

rew

op

oss

um

00

03

Das

yu

rom

orp

hia

Das

yu

rid

aeS

min

thop

sis

vir

gin

iae

Red

-ch

eek

edd

un

nar

t0

033

4D

asy

uru

sv

iver

rinu

sE

aste

rnq

uol

l0

00

5Sa

rcop

hil

ush

arr

isii

Tas

man

ian

dev

il0

00

6

Pla

cen

tals

Xen

arth

raD

asy

po

did

aeD

asy

pus

nove

mci

nctu

sN

ine-

ban

ded

arm

adil

lo.

887–

9A

fros

oric

ida

Ten

reci

dae

Mic

roga

lesp

p.Sh

rew

ten

recs

,sev

eral

spp.

100

100

100

10,

11O

ryzo

rict

este

trad

acty

lus

Fou

r-to

edri

cete

nre

c10

010

010

011

Pota

mog

ale

velo

xG

ian

tot

ter

shre

w10

010

010

011

Set

ifer

seto

sus

Gre

ater

hed

geh

ogte

nre

c10

010

010

010

,11

Ch

ryso

chlo

rid

aeA

mby

loso

mu

sho

tten

totu

sH

otte

nto

tgo

lden

mol

e10

010

010

011

Chr

ysoc

hlor

isas

iati

caC

ape

gold

enm

ole

100

100

100

11,

12C

hrys

ospa

lax

trev

elya

ni

Gia

nt

gold

enm

ole

100

100

100

11Te

nre

cid

aeTe

nre

cec

aud

atus

Tai

lles

ste

nre

c83

100

100

10,

11H

emic

ente

tes

sem

isp

ino

sus

Str

eak

edte

nre

c67

100

100

10,

11M

acro

scel

idea

Mac

rosc

elid

idae

Rhy

ncho

cyon

chry

sopy

gos

Gol

den

-ru

mp

edel

eph

ant

shre

w10

010

010

010

Tu

bu

lid

enta

taO

ryct

ero

pid

aeO

ryct

erop

usaf

erA

ard

var

k0

13H

yra

coid

eaP

roca

vii

dae

Pro

cavi

aca

pen

sis

Roc

kh

yra

x10

010

014

Eu

lip

oty

ph

laTa

lpid

aeN

euro

tric

hus

gibb

sii

Am

eric

ansh

rew

mol

e10

010

010

015

Uro

tric

hus

talp

oid

esJa

pan

ese

shre

wm

ole

100

100

6716

Sol

eno

do

nti

dae

Sol

eno

don

sp.

Sol

eno

do

n83

100

6710

,11

Eri

nac

eid

aeE

chin

oso

rex

gym

nura

Mo

on

rat

6710

067

10,

17H

ylo

my

ssu

illu

sS

ho

rt-t

aile

dg

ym

nu

re67

100

6710

,17

Eri

nac

eus

spp

.H

edg

eho

gs,

sev

eral

spp

.60

060

10,

17–1

9T

alp

idae

Sca

panu

sla

tim

anu

sB

road

-fo

ote

dm

ole

00

0–33

20C

ond

ylu

racr

ista

taS

tar-

no

sed

mol

e0

00

10,

19P

ara

sca

lop

sbr

ewer

iH

airy

-tai

led

mol

e0

00

21S

calo

pus

aqu

atic

usE

aste

rnm

ole

00

010

,19

Talp

aeu

ropa

eaE

uro

pea

nm

ole

00

019

,22

So

rici

dae

Sh

rew

s0

00

23


TA

BL

E2.

Con

tin

ued

.

Ord

erFa

mil

ySp

ecie

sC

omm

onn

ame

IC

PSo

urc

e

Ch

iro

pte

raV

esp

erit

ilio

nid

aeM

yoti

slu

cifu

gus

Lit

tle

bro

wn

bat

100

100

6724

Vesp

erti

lio

supe

ran

sA

sian

par

tico

lore

db

at10

010

050

–75

25A

ntro

zous

pall

idus

Pal

lid

bat

6010

075

26R

hin

olo

ph

idae

Hip

posi

dero

sca

ffer

Su

nd

eval

l’sro

un

dle

afb

at0

00

27R

hin

olop

hus

sp.

Ho

rses

ho

eb

at0

00

28M

egad

erm

atid

aeL

avia

fron

sYe

llo

w-w

ing

edb

at0

00

29C

arn

ivor

aC

anid

aeC

anis

fam

ilia

ris

Dom

esti

cd

og10

010

010

030

Can

ism

esom

elas

Bla

ck-b

acke

dja

ckal

100

100

100

31V

ulp

esvu

lpes

Red

fox

100

100

100

32P

rocy

onid

aeB

assa

risc

us

astu

tus

Rin

gta

il10

010

010

033

Bas

sari

scu

ssu

mic

hras

tiC

acom

ixtl

e10

010

010

034

Nas

ua

nar

ica

Wh

ite-

nos

edco

ati

100

100

100

35Po

tos

flav

osK

ink

ajou

100

100

100

36,

37M

ust

elid

aeE

ira

barb

ara

Tay

ra10

010

010

038

,39

Feli

dae

Feli

sca

tus

Do

mes

tic

cat

100

100

8039

Feli

ssi

lves

tris

Wil

dca

t10

010

080

40P

ant

hera

leo

Lio

n10

010

080

39P

rocy

on

idae

Pro

cyon

loto

rR

acco

on

6710

010

041

Urs

idae

Urs

usa

rcto

sB

row

nb

ear

6710

060

42M

ust

elid

aeE

nh

yd

ralu

tris

Sea

ott

er20

–60

100

100

43,

44M

eles

mel

esO

ldW

orl

db

adg

er33

100

100

45Ta

xide

ata

xus

Am

eric

anb

adg

er17

100

100

46M

uste

lav

ison

Am

eric

anm

ink

1710

010

047

,48

Mus

tela

lutr

eola

Eu

rop

ean

min

k17

100

100

49M

uste

lap

uto

rius

Eu

rop

ean

pol

ecat

/fer

ret

0–17

100

100

50,

51M

eph

itid

aeM

eph

itis

mep

hit

isS

trip

edsk

un

k0

00

52O

do

ben

idae

Wal

rus

00

053

,54

Ota

riid

aeS

eali

on

s0

00

53,

54P

ho

cid

aeE

arle

ssse

als

00

053

,54

Per

isso

dac

tyla

Eq

uid

aeE

quus

caba

llus

Ho

rse

100

010

055

Art

iod

acty

laB

ovid

aeB

osta

uru

sD

omes

tic

catt

le10

010

055

Cap

rahi

rcu

sD

omes

tic

goat

100

100

55ov

isar

ies

Dom

esti

csh

eep

100

100

55Su

idae

Su

ssc

rofa

Pig

100

100

100

55Ta

yass

uid

aePe

cari

taja

cuC

olla

red

pec

cary

100

100

100

56Sc

and

enti

aT

up

aiid

aeTu

paia

spp.

Tre

esh

rew

,sev

eral

spp.

100

100

100

10,

57


TA

BL

E2.

Con

tin

ued

.

Ord

erFa

mil

ySp

ecie

sC

omm

onn

ame

IC

PSo

urc

e

Pri

mat

esL

emu

rid

aeL

emu

rca

tta

Rin

g-t

aile

dle

mu

r10

010

010

058

Cal

litr

ich

idae

Cal

lith

rix

jacc

hus

Com

mon

mar

mos

et10

010

010

058

Sag

uin

us

fusc

icol

lis

Sad

dle

-bac

ked

tam

arin

100

100

100

58S

agu

inu

sn

igri

coll

isB

lack

-man

tle

tam

arin

100

100

100

58C

ebid

aeA

otu

str

ivir

gatu

sN

igh

tm

onke

y10

010

010

058

Sai

mir

isc

iure

us

Squ

irre

lm

onke

y10

010

010

058

Cer

cop

ith

ecid

aeM

acac

afa

scic

ula

ris

Cra

b-e

atin

gm

acaq

ue

100

100

100

58M

acac

afu

scat

aJa

pan

ese

mac

aqu

e10

010

010

058

Mac

aca

mu

latt

aR

hes

us

mac

aqu

e10

010

010

058

Papi

ocy

noce

phal

us

Sava

nn

ab

aboo

n10

010

010

058

Pon

gid

aeG

oril

lago

rill

aG

oril

la10

010

010

058

Pan

trog

lody

tes

Com

mon

chim

pan

zee

100

100

100

58Po

ngo

pygm

aeu

sO

ran

gu

tan

100

100

100

58H

omin

idae

Hom

osa

pien

sH

um

an10

010

010

058

Tar

siid

aeTa

rsiu

sba

nca

nus

Wes

tern

tars

ier

3310

067

59R

od

enti

aC

asto

rid

aeC

asto

rca

na

den

sis

Am

eric

anb

eav

er0

100

60S

ciu

rid

aeS

perm

oph

ilus

parr

yi

Arc

tic

gro

un

dsq

uir

rel

010

061

Th

ryo

no

my

idae

Th

ryon

omy

ssw

inde

ria

nus

Gre

ater

can

era

t0

062

Mu

rid

aeM

ice,

rats

063

Lag

om

orp

ha

Lep

ori

dae

Ory

ctol

agu

scu

nic

ulu

sD

om

esti

cra

bb

it33

100

64,

65

Sou

rces

:1.

(McC

rad

y19

38),

2.(P

etri

des

1949

),3.

(Lu

cket

tan

dH

ong

2000

),4.

(Lu

cket

tan

dW

ool

ley

1996

),5.

(Hil

lan

dH

ill

1955

),6.

(Gu

iler

and

Hed

dle

1974

),7.

(Mar

tin

1916

),8.

(Flo

wer

1868

),9.

(Sta

ng

let

al.1

995)

,10

.(L

ech

e18

97),

11.(

Lec

he

1907

),12

.(L

ech

e19

04),

13.(

An

thon

y19

34),

14.(

Fair

all

1980

),15

.(Z

ieg

ler

1971

a),1

6.(H

anam

ura

etal

.198

8),1

7.(L

ech

e19

02),

18.(

Kin

dah

l195

9b),

19.(

Lec

he

1895

),20

.(Z

ieg

ler

1972

),21

.(E

adie

1944

),22

.(M

ısek

and

Ster

ba

1989

),23

.(K

ind

ahl

1959

a),.

24.

(Fen

ton

1970

),25

.(K

oyas

uan

dM

uko

hya

ma

1992

),26

.(O

rr19

54),

27.

(Gau

nt

1967

),28

.(G

rass

e19

55),

29.

(Dor

st19

53),

30.(

Eva

ns

1993

),31

.(L

omb

aard

1971

),32

.(L

inh

art

1968

),33

.(P

og

laye

n-N

euw

all

and

Po

gla

yen

-Neu

wal

l199

3),3

4.(P

og

laye

n-N

euw

all1

995)

,35.

(Gom

pp

er19

95),

36.(

Po

gla

yen

-Neu

wal

l196

2),3

7.(P

og

laye

n-N

euw

all1

976)

,38.

(Po

gla

yen

-Neu

wal

lan

dP

og

laye

n-

Neu

wal

l19

76),

39.

(Lec

he

1915

),40

.(H

alte

nor

th19

62),

41.

(Mon

tgom

ery

1964

),42

.(D

ittr

ich

1960

),43

.(K

enyo

n19

69),

44.

(Sch

nei

der

1973

),45

.(N

eal

1986

),46

.(L

ong

1974

),47

.(A

uer

lich

and

Swin

dle

r19

68),

48.(

Kai

ner

1954

),49

.(M

osh

onk

in19

79),

50.(

Hab

erm

ehla

nd

Ro

ttch

er19

67),

51.(

Ber

kov

itz

and

Silv

erst

one

1969

),52

.(V

erts

1967

),53

.(K

ing

1983

),54

.(L

aws

1953

),55

.(G

etty

1975

),56

.(K

irk

pat

rick

and

Sow

ls19

62),

57.(

Kin

dah

l195

7),

58.

(Sm

ith

etal

.19

94),

59.

(Lu

cket

tan

dM

aier

1982

),60

.(v

anN

ost

ran

dan

dSt

eph

enso

n19

64),

61.(

Mit

chel

lan

dC

arse

n19

67),

62.(

van

der

Mer

we

2000

),63

.(M

oss

-Sal

enti

jn19

78),

64.(

Hir

sch

feld

etal

.197

3),6

5.(M

ich

aeli

etal

.19

80).


FIGURE 4. Phylogeny of musteloid carnivores showing functional tooth replacement. Phylogeny of the caniformcarnivores 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. Thecompleteness of tooth replacement at the incisor (I), canine (C), and premolar (P) loci is shown next to the taxonname. The loss or reduction of tooth replacement is apparently independently derived in multiple lineages. Sourcesof replacement information are listed in Table 2.

FIGURE 5. Phylogeny of the Talpidae showing function-al tooth replacement. This phylogeny follows that ofWhidden (2000), which is based on myological charac-ters. Uropsilus is a genus of nonfossorial Asiatic shrewmoles, generally placed into its own subfamily, theUropsilinae, for which we present tentative informationon functional replacement based on the studies of Zie-gler (1971a) and Thomas (1911). The subfamily Des-maninae contains two genera of desmans that are adapt-ed to aquatic life. Sources of replacement informationare listed in Table 2.

sample, (M. vison, M. lutreola, and M. putorius),di1–2 and di1–3 are vestigial, while di3, I1–3 andI1–3 are functional (Kainer 1954; Long 1965;Habermehl and Rottcher 1967; Auerlich andSwindler 1968; Berkovitz and Silverstone1969; Moshonkin 1979). According to Kenyon(1969) in the sea otter (Enhydra lutris) di1–2,di1–3 and I2 are vestigial, while di3, I1–3, and I1,3

are functional. (The designation of functionalversus vestigial incisors differs slightly fromthat of Scheffer [1951]), leading to the range offunctional replacement values shown in Table2.) To summarize, the general trend in mus-telids that reduce functional tooth replace-ment is to lose all functional lower deciduousincisors and one or two pairs of functionalcentral upper deciduous incisors.

Another phylogenetically constrained groupthat shows extensive variation in the degree offunctional replacement is the family Talpidae(moles, shrew moles, and desmans). In thecase of this family, functional replacementranges from full or nearly full to none or near-ly none, with all of the known variability inthe premolar field (Table 2, Fig. 5). When thepatterns of functional tooth replacement areplotted on the recent talpid phylogenies of


Whidden (2000) (Fig. 5) or Yates and Moore(1990), it can be seen that functional mono-phyodonty has probably evolved more thanonce. Soricidae (shrews), the sister group ofTalpidae in recent phylogenies (Asher 2001;Nikaido et al. 2001; Malia et al. 2002), has alsoentirely lost functional replacement.

Discussion

The Homology of Dental Generations in Mar-supials. We observe no evidence of two den-tal generations at the incisor, canine, or P1 andP2 loci in M. domestica. This is in agreementwith previous studies of Didelphis (Kukenthal1891; Rose 1892; Berkovitz 1978) but is in con-trast to several studies that have identifiedvestigial teeth at the incisor and canine loci ina variety of Australian marsupials (e.g., Wil-son and Hill 1897; Kirkpatrick 1978; Luckett1989, 1993; Luckett and Woolley 1996). Ourobservations of M. domestica also differ sub-stantially from those of Kozawa et al. (1998)on the same species. They examined a seriesof three specimens (12, 16, and 18 P) and claimto have found evidence for bud stage vestigialfirst-generation teeth at the I4 and I1 loci, a budstage vestigial second generation at I1, andsuccessional laminae lingual to dc1 and dc1.Our study of a more complete series did notconfirm the existence of any of these struc-tures. Vestigial incisors with dentine labial tothe definitive incisors have been observed re-cently in sectioned specimens of another di-delphid, Caluromys philander (van Nievelt per-sonal observation).

Vestigial teeth (which in some species arerepresented by little more than swellings ofthe dental lamina) at the incisor and canineloci have been interpreted by the above au-thors as representing the deciduous dentition,so that the functional, permanent teeth rep-resent a successional or second generation ofteeth. The apparent absence of even transitory,vestigial teeth in M. domestica makes unam-biguous identification of the generational ho-mology of these permanent teeth difficult.Luckett (1993: p. 196) claims that ‘‘it is impos-sible to have a secondary or successional toothwithout a deciduous predecessor.’’ If true, bydefinition the single generation of teeth ob-served in M. domestica would be considered to

be deciduous (and it is by this logic that Luck-ett identified the single generation of premo-lars at the first and second loci as deciduous).This would imply that the permanent teeth inM. domestica are not homologous with those ofAustralian marsupials.

However, we believe it is far more parsi-monious, and more consistent with generalpatterns of evolution, to assume that in somemarsupial taxa, such as M. domestica, the ves-tigial first generation seen in other marsupialshas been lost entirely. Therefore, the function-al, permanent teeth observed in M. domesticacan most reasonably be interpreted as beinghomologous with the functional permanentteeth observed in other marsupials. Becausewe cannot identify with absolute certaintywhich of two generations the single generationof teeth in M. domestica represents, we simplyrefer to these teeth as permanent. The issue ofgenerational homologies is a complex one, andthis paper does not attempt to resolve the is-sue. The more important point is that somemarsupials retain two developmental gener-ations, one of which is reduced and vestigial,whereas some retain only a single develop-mental generation; however, all marsupialspossess only a single functional generation atall but the p3 loci.

The Relation between Dental Development andthe Period of Fixation in Marsupials. Our ob-servations of the development of oral behaviorand tooth development in M. domestica dem-onstrate that there is no general suppressionof the process of odontogenesis during the pe-riod of fixation. The teeth at the lower incisor,upper and lower canine, and upper and lowerpremolar loci go through most stages of den-tal differentiation during the period of fixationand have begun calcification by its end (Fig. 3).The upper incisors are delayed relative to theother anterior teeth, but undergo all stages ofdental development during either the periodof fixation or while the young are still spend-ing considerable time on the nipple. Thus,dental development is not generally sup-pressed by suckling in M. domestica. Dentaldevelopment also occurs throughout the pe-riod of attachment in other marsupial species(Luckett 1993). There appears to be no func-tional or mechanical incompatibility between


dental development and the functional de-mands placed on the oral region during suck-ling by marsupials.

The development of the upper first incisorin M. domestica is consistently delayed relativeto all of the other incisors, and its eruption isrelatively late as well. I1 erupts around day 54at about the same time that the young are be-ginning to feed like an adult. For about twoweeks before weaning, this delay produces agap in the anterior dentition (Fig. 6). Luckettand Woolley (1996) also noted a delay in I1 de-velopment and eruption in the red-cheekeddunnart (Sminthopsis virginiae), and similarpatterns have been reported for the Tasmani-an devil (Sarcophilus laniarius) (Guiler andHeddle 1974), the Virginia opossum (Didelphisvirginiana) (McCrady 1938), and a variety ofother polyprotodont marsupials (Thomas1887). In at least S. virginiae, D. virginiana, andS. laniarius eruption is known to occur at aboutthe time of weaning and has been hypothe-sized to facilitate continued suckling by leav-ing a gap in the middle of the upper incisorsfor the nipple to fit into during the prewean-ing period (Winge 1941; Guiler and Heddle1974; Luckett and Woolley 1996).

Interestingly, the preweaning medial gap inthe incisors found in polyprotodont marsu-pials is found in modified form in the mustel-ids that have reduced functional incisor re-placement, such as the ferret illustrated in Fig-ure 6. In this case the small but functional di3

and the large dc1 do erupt, while the centralpairs of incisors are tiny and may or may notpierce the gums. This soft tissue-lined gappersists until the eruption of the functionalpermanent incisors shortly after weaning(Berkovitz and Silverstone 1969). Neal (1986)speculated that the gap in another mustelid,Meles meles, was ‘‘an adaptation for suckling.’’Incisor gaps during the suckling period havealso been reported for the brown bear (Ursusarctos) (Dittrich 1960) and the northern rac-coon (Procyon lotor) (Montgomery 1964).

Therefore, although it is possible that thedelay in eruption of I1 in Monodelphis domesticaand other polyprotodont marsupials is due tosuckling, two facts are important. First, thispattern is limited to a single tooth locus andcannot explain the general phenomenon of

suppression of anterior deciduous dentition inmarsupials. Second, seemingly similar adap-tations are seen in some eutherians. However,as suckling is universal for mammals, onemight expect some delay in eruption of thecentral incisors to be universal. We are awareof no particular adaptations for suckling in thetaxa in which incisor developmental delay hasbeen observed. It is therefore puzzling thatsuch adaptations appear to have a limited dis-tribution within the Theria.

We have discussed above the possibilitythat functional replacement of incisors may besuppressed because of interactions with thenipple in some marsupials and placentals. Bycontrast, some other taxa including most bats(Slaughter 1970; Vaughan 1970; Phillips 1971,2000; Czaplewski 1987) and some murid ro-dents (Lawrence 1941; Hamilton 1953; Brooks1972; Gilbert 1995) appear to have evolvedteeth with specialized morphologies that al-low the young to cling tenaciously to the nip-ple.

To summarize, development of the anteriordentition of M. domestica is not generally sup-pressed or delayed during suckling. The up-per incisors do show a transient delay in de-velopment (relative to the lower incisors), butthis perturbation is of brief duration, except inthe case of I1. The data presented here cannoteliminate the possibility that the pattern ofdental replacement observed in marsupials isrelated to their reproductive specializations,as craniofacial development is highly derived(Smith 2001) and it is possible that odonto-genesis is as well. If true, then, this providesfurther evidence that the marsupial reproduc-tive pattern is not primitive for therians, butin fact derived (Smith 2001). However, as themarsupial mode of reproduction appears tohave evolved only once, it is impossible to testthis hypothesis by comparative methods. It isclear that there is no general support for thehypothesis that there is a direct causal link be-tween marsupial suckling and the suppres-sion of anterior tooth development.

Loss of Functional Tooth Replacement in Theri-an Mammals. The survey of functional toothreplacement patterns in living placental mam-mals allows the marsupial tooth replacementpattern to be placed in the general context of


FIGURE 6. Closing of the incisor gap in an opossum and the ferret. Anterior views of the incisor regions showingthe 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 eachspecies 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 openslightly for this gap to open up because of the way that the lower teeth are positioned. Note that I1 protrudes slightlyabove 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 thedeciduous incisors except di3 are vestigial. D, Age 27 P (male, AvN 01-018). The large medial gap is formed betweenthe sturdy deciduous canines and the small but functional di3’s. In this case the gap is formed even with the jawsheld 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.


the range of replacement patterns seen in the-rian mammals. Data presented in Table 2demonstrate that the loss of deciduous teeth atvarious loci is common within eutherians andoccurs in many taxonomic groups. The onlyplacental mammal that possibly matches themarsupial functional replacement pattern (re-placement at only the last premolar locus) isthe broad-footed mole (Scapanus latimanus),but the functionality of the last premolars inthis species is not well known (Ziegler 1972).Even if there are no placental mammals thatexactly match the primitive marsupial pat-tern, marsupials fit within the range of livingplacental mammals (Table 2). In fact, the mar-supial pattern fits into the range of variationseen in the carnivore superfamily Mustelo-idea. Within this single superfamily one seesthe primitive eutherian condition of full re-placement, the loss of most functional replace-ment at the incisor loci, and even the loss of allfunctional replacement (Mephitis mephitis).The musteloids demonstrate that animalswith very different patterns of functionaltooth replacement can be fairly closely related,have similar adult morphologies, occupy asimilar adaptive niche, and share similar lifehistories.

The comparative data provided by placentalmammals strongly refute the hypothesis thatthe tooth replacement patterns seen in mar-supials are necessarily indicative of, or corre-lated with, the radical specializations associ-ated with the marsupial mode of reproduc-tion. Life history traits are neither a necessarynor a sufficient explanation of the mode ofdental replacement seen in marsupials.

Explanations for the Loss of Functional Replace-ment. We are not aware of any systematic at-tempt to explain the loss or reduction of func-tional tooth replacement in therian mammals,although many kinds of potential factors havebeen suggested. These include the loss oftooth loci, major modifications of the dentitionand dental development, factors related to theparticulars of life history and adaptations,functional demands during the normal re-placement period, phylogenetic history, andgrowth.

One potential factor is that dental replace-ment may be lost in the process of losing a

tooth at any given position. Loss of teeth atvarious loci is common in therians, and locithat are being reduced in size and importancemay possibly eliminate functional replace-ment as an intermediate stage on the way tofull elimination of the locus. Examples of thismight be the dp2/P2 locus in the domestic cator the unreplaced deciduous premolars ofbears. Murid rodents have eliminated caninesand premolars altogether and thus neithertooth generation erupts at these loci. Theyhave retained molars, but because molars donot undergo replacement, murids have nodental replacement at all.

Homodonty (all teeth with similar mor-phology), polydonty (more than the primitivenumber of teeth), simplification of the cusppatterns of the cheek teeth, and ever growingteeth are found in various combinations in aphylogenetically diverse assemblage of mam-mals. Presumably, changes to the primitivemammalian dental developmental programare required to create teeth or dentitions ofthese types. Such developmental changes ap-pear in some cases to be correlated with theloss of tooth replacement. The dentition of Or-ycteropus afer (the aardvark) is highly modifiedand this species exhibits a highly modifiedpattern of replacement. The functional teeth ofthis species, while varying in size, are mor-phologically simplified and similar. The func-tional dentition seen in the adult is reduced toI0/0, C0/0, P2/2, M3/3 (Anthony 1934) andthe functional teeth are ever growing, lackenamel, and have a peculiar ‘‘tubular’’ micro-structure (Broom 1909; Heuser 1913; Anthony1934). O. afer lacks functional tooth replace-ment altogether (Thomas 1890; Broom 1909;Anthony 1934) although several extra (poly-dont) premolar positions are indicated by thepresence of vestigial milk teeth (Broom 1909;Heuser 1913; Anthony 1934). The livingtoothed whales (Odontoceti) are typically ho-modont and polydont and lack tooth replace-ment (MacDonald 1984). However, primitivewhales (archaeocetes) were heterodont, werenot polydont, and underwent functional re-placement (Uhen 2000). The living pinnipedcarnivores tend toward homodonty in thepostcanine dentition and lack functional toothreplacement altogether (King 1983). The large,


ever growing incisors in both rabbits and ro-dents do not undergo functional replacement(Woodward 1894; Hirschfeld et al. 1973; Moss-Salentijn 1978).

However, major modifications of the devel-opmental program are not necessarily asso-ciated with the loss of functional replacement.Dasypus novemcinctus (the nine-banded arma-dillo) has a dentition as oddly specialized asthat of O. afer, yet it possesses functional, root-ed deciduous teeth that are subsequently re-placed at seven of the eight adult tooth posi-tions (Flower 1868; Martin 1916; Stangl et al.1995). In rabbits, the large, curved, ever grow-ing incisors are not functionally replaced, butthe smaller pair of upper incisors and the pre-molars are represented by rooted deciduousteeth that are replaced by rootless, ever grow-ing permanent teeth (Hirschfeld et al. 1973;Michaeli et al. 1980).

There may be features of an animal’s lifehistory and ecological adaptation that havesomehow led to selection against tooth re-placement. Both toothed whales and pinni-peds have lost functional replacement and ithas been suggested that this is related toaquatic predation. For example, Kubota et al.(2000) related the loss of functional replace-ment in Callorhinus ursinus (northern fur seal)and other pinnipeds to selection for adultfeeding behavior at an early age. They did notexplain why adult feeding behavior could notbe achieved with a smaller deciduous denti-tion. Size, too, has been suggested as a causalfactor in the loss of dental replacement. Blochet al. (1998) speculated that lack of functionalreplacement in living insectivores might berelated to small size, judging from the distri-bution of monophyodonty in living lipotyph-lans. They noted, however, that the Eocene in-sectivore Batodonoides vanhouteni may be thesmallest known mammal and that it had re-placement at least at the P4 locus. Ziegler(1971a) noted that lack of functional replace-ment was derived independently in all of thelineages of fossorial moles, but not in the lin-eages of semifossorial or nonfossorial shrewmoles. He felt that lack of replacement was aderived character somehow related to the sub-terranean lifestyle. Members of the other fos-sorial group for which we have data, Chry-

sochloridae (golden moles), have full function-al replacement, however.

Some degree of phylogenetic constraintmay operate as well. It is possible that oncetooth replacement is lost in a particular evo-lutionary lineage, it may be very difficult orimpossible for descendant species to regain it.Thus there may be species that might be pre-dicted to benefit from tooth replacement fortheoretical reasons, but do not have it becausetheir ancestors lost it.

Finally, we propose that growth of the bodyand jaws may be a factor in the reduction ofdiphyodonty in therian mammals, in part be-cause it appears to have been an importantfactor in the evolution of diphyodonty frompolyphyodonty. In nonmammalian vertebrates,tooth replacement is intimately related togrowth. Each successive generation of teeth isincrementally larger than the preceding oneas the animal undergoes slow growth for anindefinite period. Tooth wear is not consid-ered a major factor in replacement becauseteeth are usually shed before they are signif-icantly worn (reviewed in Berkovitz 2000). Ithas been argued that in mammals, lactation,in combination with the transition from slow,indeterminate growth to rapid growth to a de-terminate adult size, has led, in part, to a re-duction of tooth replacement (for exampleGow 1985; Zhang et al. 1998). A mammal pos-sessing both lactation and rapid determinategrowth requires a small set of teeth that fit ajuvenile sized jaw only briefly. The period oflactation, which requires no teeth, eliminatesthe need for functional replacement earlierduring growth or at a small size. The short pe-riod of rapid growth to an adult size elimi-nates the need for several successive genera-tions of intermediate sized teeth. In this waythe ancestor of therian mammals came to pos-sess a single generation of replacement teeth,which erupt when the jaw reaches a size largeenough to accommodate them. Molars, whichare not replaced, accommodate growth be-cause they erupt at the back of the tooth row,once space is available. This model does notignore the fact that other factors, such as theneed to maintain precise occlusion for theproper functioning of a shearing dentition


(Hopson 1973), may also have contributed toselection for reduced replacement.

The fossil evidence for this scenario is, un-surprisingly, meager, but Zhang et al. (1998)pointed out that a series of skulls of the EarlyJurassic mammaliaform Sinoconodon shows awide range of sizes, all with functional den-titions, whereas a series of skulls of anotherEarly Jurassic form Morganucodon varies littlein size. This difference can be interpreted asevidence that Sinoconodon underwent slow, in-determinate growth, whereas Morganucodongrew rapidly to an adult size. Sinoconodon isdefinitely polyphyodont and the evidence fortooth replacement in Morganucodon is consis-tent with diphyodonty.

Following this same line of reasoning, it ispossible that in some mammals the body andjaws reach adult size, or are large enough toaccommodate adult-sized teeth, before the an-imal requires a functional dentition. In thesecases, we might expect that dental replace-ment would be reduced from the diphyodontto the monophyodont condition (Mısek andSterba 1989). As yet, comparative data onbody and jaw growth and tooth eruption andreplacement are not available. If, however, arelation exists between these two processes,then the reduction of replacement to the func-tionally monophyodont condition, so commonin therian mammals, would merely be a con-tinuation of the same processes that led to theevolution of diphyodonty. If demonstrated, itwould do much to help us understand the ear-ly evolution of the mammalian lineage.

Unfortunately, none of the causal factorsdiscussed above appear to provide a goodgeneral explanation of the loss of functionalreplacement across therians. They are eitherad hoc explanations for single cases, coun-tered as general explanations by comparativedata, or lacking in supporting data. It maywell be that there is no single explanation forthe loss of tooth replacement, but instead, lossof functional replacement may have evolvedfor many reasons as mammals evolved theirgreat variety of dental adaptations.

Conclusions

Our major goal in this review has been two-fold. First, we point out that the loss of tooth

replacement in marsupials is neither unusualamong therian mammals nor highly correlat-ed with the extended period of nipple attach-ment in any obvious manner. Although allmarsupials may possess this derived pattern,and in fact, it may represent an important syn-apomorphy of the group, there is no evidencefor the conclusion that it is a clear indicationof any specific reproductive adaptation.

Second, we point out the enormous diver-sity in replacement pattern among eutherianmammals. It is possible that the loss of decid-uous dentition, or the evolution of monophyo-donty from diphyodonty, is simply an exten-sion of the primitive mammalian condition ofthe loss of dental generations. It may requireno special explanation, but simply accompanythe evolution of many types of dental and lifehistory adaptations.

Given this diversity, we urge caution inmaking inferences, based on dental replace-ment patterns, about behavior or life history oforganisms known only in the fossil record.

Acknowledgments

We thank R. F. Kay and V. L. Roth for com-ments on an earlier draft of this manuscript.J. Jernvall provided inspiration for the title.Thanks also to C. Schnurr and the other pos-sum wranglers who, at great personal risk totheir fingers, assisted in collecting the tootheruption data. T. A. Williams performed someof the feeding experiments and providedbehavioral observations. Special recognitionshould go to J. Wright, whose dissertation(Wright 1983) (available from University Mi-crofilms International) is a fabulous source ofinformation and references for anyone inter-ested in the deciduous dentition. This researchwas done in partial fulfillment of the re-quirements for a Ph.D. in Biological Anthro-pology and Anatomy at Duke University andA.F.H.v.N. is grateful for the financial supportof that department, his parents, and his wife.K.K.S., and the Monodelphis colony, was sup-ported by grants from the National ScienceFoundation.

Literature CitedAnthony, R. 1934. La dentition de l’orycterope: morphologie,

developpement, structure, interpretation. Annales des Sci-ences Naturelles, Zoologie series 10(tome 27):289–322.


Archer, M. 1978. The nature of the molar-premolar boundary inmarsupials and a reinterpretation of the homology of mar-supial cheekteeth. Memoirs of the Queensland Museum 18:157–164.

Asher, R. J. 2001. Cranial anatomy in tenrecid insectivorans:character evolution across competing phylogenies. AmericanMuseum of Natural History Novitates 3352:1–54.

Auerlich, R. J., and D. R. Swindler. 1968. The dentition of themink (Mustela vison). Journal of Mammalogy 49:488–494.

Berkovitz, B. K. B. 1978. Tooth ontogeny in Didelphis virginiana.Australian Journal of Zoology 26:61–68.

———. 2000. Tooth replacement patterns in non-mammalianvertebrates. Pp. 186–200 in M. F. Teaford, M. M. Smith, and M.W. J. Ferguson, eds. Development, function and evolution ofteeth. Cambridge University Press, Cambridge.

Berkovitz, B. K. B., and L. M. Silverstone. 1969. The dentition ofthe albino ferret. Caries Research 3:369–376.

Bloch, J., K. D. Rose, and P. D. Gingerich. 1998. New species ofBatodonoides (Lipotyphla, Geolabididae) from the early Eo-cene of Wyoming: smallest known mammal? Journal of Mam-malogy 79:804–827.

Brooks, P. M. 1972. Post-natal development of the African bushrat, Aethomys chrysophilus. Zoologica Africana 7:85–102.

Broom, R. 1909. On the milk dentition of Orycteropus. Annals ofthe South African Museum 5:381–384.

Cifelli, R. L., and C. de Muizon. 1998. Tooth eruption and re-placement pattern in early marsupials. Comptes Rendus del’Academie des Sciences, serie II, Sciences de la Terre et desPlanetes 326:215–220.

Cifelli, R. L., T. B. Rowe, W. P. Luckett, J. Banta, R. Reyes, and R.I. Howes. 1996. Fossil evidence for the origin of the marsupialpattern of tooth replacement. Nature 379:715–719.

Czaplewski, N. J. 1987. Deciduous teeth of Thyroptera tricolor.Bat Research News 28:23–25.

Dittrich, L. 1960. Milchgebissentwicklung und Zahnwechselbeim Braunbaren (Ursus arctos L.) und anderen Ursiden. Mor-phologisches Jahrbuch 101:1–142.

Dorst, J. 1953. Note sur la dentition d’un foetus de Lavia frons(Chiropteres, Megadermatides). Mammalia 17:83–84.

Dragoo, J. W., and R. L. Honeycutt. 1997. Systematics of mus-telid-like carnivores. Journal of Mammalogy 78:426–443.

Eadie, W. R. 1944. Tooth replacement in Brewer’s mole. Anatom-ical Record 89:357–360.

Eisenberg, J. F., and K. H. Redford. 1999. Mammals of the Neo-tropics, Vol. 1. The central neotropics. University of ChicagoPress, Chicago.

Evans, H. E. 1993. Miller’s anatomy of the dog. W. B. Saunders,Philadelphia.

Fairall, N. 1980. Growth and age determination in the hyrax Pro-cavia capensis. South African Journal of Zoology 15:16–21.

Fenton, M. B. 1970. The deciduous dentition and its replacementin Myotis lucifugus (Chiroptera: Vespertilionidae). CanadianJournal of Zoology 48:817–820.

Flower, W. H. 1867. On the development and succession of theteeth in the Marsupialia. Philosophical Transactions of theRoyal Society of London 157:631–641, plates XXIX, XXX.

———. 1868. On the development and succession of teeth in thearmadillos (Dasypodidae). Proceedings of the Zoological So-ciety of London 1868:378–380.

Flynn, J. J., M. A. Nedbal, J. W. Dragoo, and R. L. Honeycutt.2000. Whence the Red Panda? Molecular Phylogenetics andEvolution 17:190–199.

Gaunt, W. A. 1967. Observations upon the developing dentitionof Hipposideros caffer (Microchiroptera). Acta Anatomica 68:9–25.

Getty, R. 1975. The anatomy of the domestic animals. W. B.Saunders, Philadelphia.

Gilbert, A. N. 1995. Tenacious nipple attachment in rodents: the

sibling competition hypothesis. Animal Behaviour 50:881–891.

Gompper, M. E. 1995. Nasua narica. Mammalian Species 487:1–10.

Gow, C. E. 1985. Apomorphies of the Mammalia. South AfricanJournal of Science 81:558–560.

Grasse, P.-P. 1955. Traite de zoologie, Tome 17. Mammiferes.Masson, Paris.

Guiler, E. R., and R. W. L. Heddle. 1974. The eruption andgrowth of teeth in the Tasmanian devil, Sarcophilus harrissi(Marsupialia: Dasyuridae). Papers and Proceedings of theRoyal Society of Tasmania 108:137–140.

Habermehl, K. H., and D. Rottcher. 1967. Die Moglichkeiten derAltersbestimmung beim Marder und Iltis. Zeitschrift furJagdwissenschaft 13:89–102.

Haltenorth, T. 1962. Die Wildkatze. A. Ziemsen, Wittenberg.Hamilton, W. J., Jr. 1953. Reproduction and young of the Florida

wood rat, Neotoma f. floridiana (Ord). Journal of Mammalogy34:180–189.

Hanamura, H., Y. Uematsu, and T. Setoguchi. 1988. Replacementof the first premolars in Japanese shrew-moles (Talpidae: In-sectivora). Journal of Mammalogy 69:135–138.

Heuser, P. 1913. Uber die Entwicklung des Milchzahngebissesdes afrikanischen Erdferkels (Orycteropus capensis Geoffr.).Ein Beitrag zur Histologie der Zahnentwicklung der Eden-taten. Zeitschrift fur wissenschaftliche Zoologie 104:622–691.

Hill, J. P., and W. C. O. Hill. 1955. The growth-stages of thepouch-young of the Native Cat (Dasyurus viverrinus) togetherwith observations on the anatomy of the new-born young.Transactions of the Zoological Society of London 28:349–427.

Hill, J. P., and C. H. O’Donoghue. 1913. The reproductive cyclein the marsupial Dasyurus viverrinus. Quarterly Journal of Mi-croscopical Science 59:133–174.

Hirschfeld, Z., M. M. Weinreb, and Y. Michaeli. 1973. Incisors ofthe rabbit: morphology, histology, and development. Journalof Dental Research 52:377–384.

Hopson, J. A. 1973. Endothermy, small size, and the origin ofmammalian reproduction. American Naturalist 107:446–452.

Humason, G. L. 1979. Animal tissue techniques, 4th ed. W. H.Freeman, San Francisco.

Ivanco, T. L., S. M. Pellis, and I. Q. Whishaw. 1996. Skilled fore-limb movements in prey catching and in reaching by rats (Rat-tus norvegicus) and opossums (Monodelphis domestica): rela-tions to anatomical differences in motor systems. BehaviouralBrain Research 79:163–181.

Kainer, R. A. 1954. The gross anatomy of the digestive systemof the mink. I. The headgut and the foregut. American Journalof Veterinary Research 15:82–90.

Kenyon, K. B. 1969. The sea otter in the eastern Pacific Ocean.North American Fauna 68:1–352.

Kindahl, M. 1957. On the development of the tooth in Tupaia ja-vanica. Arkiv for Zoologi 10:463–479.

———. 1959a. Some aspects of the tooth development in the Sor-icidae. Acta Odontologica Scandinavica 17:203–237.

———. 1959b. The tooth development in Erinaceus europaeus.Acta Odontologica Scandinavica 17:467–489.

King, J. E. 1983. Seals of the world. British Museum (NaturalHistory), London.

Kirkpatrick, R. D., and L. K. Sowls. 1962. Age determination ofthe collared peccary by the tooth-replacement pattern. Jour-nal of Wildlife Management 26:214–217.

Kirkpatrick, T. H. 1978. The development of the dentition of Ma-cropus giganteus (Shaw): an attempt to interpret the marsupialdentition. Australian Mammalogy 2:29–35.

Koyasu, K., and M. Mukohyama. 1992. Dental morphology ofdeciduous teeth in the bat, Vespertilio orientalis. Pp. 115–123 inP. Smith and E. Tchernov, eds. Structure, function and evolu-tion of teeth. Freund, London.


Kozawa, Y., Y. Iwasa, and H. Mishima. 1998. Degeneration oftooth germ in the developing dentition of the gray short-tailed opossum (Monodelphis domestica) . European Journal ofOral Sciences 106(Suppl. 1):509–512.

Kubota, K., S. Shibanai, J. Kubota, and S. Togawa. 2000. Devel-opmental transition to monophyodonty in adaptation to ma-rine life by the northern fur seal, Callorhinus ursinus (Otari-idae). Historical Biology 14:91–95.

Kukenthal, W. 1891. Das Gebiß von Didelphys. AnatomischerAnzeiger 6:658–666.

Lawrence, B. 1941. Incisor tips of young rodents. Field Museumof Natural History Zoological Series 27:313–317.

Laws, R. M. 1953. The elephant seal (Mirounga leonina Linn.) I.Growth and age. Falkland Islands Dependencies Survey Sci-entific Reports 8:1–62.

Leche, W. 1895. Zur Entwicklungsgeschichte des Zahnsystemsder Saugethiere zugleich ein Beitrag zur Stammesgeschichtedieser Thiergruppe. Erwin Nagele, Stuttgart.

———. 1897. Zur Morphologie des Zahnsystems der Insectivo-ren. I. u. II. Anatomischer Anzeiger 13:1–11, 513–529.

———. 1902. Zur Entwicklungsgeschichte des Zahnsystems derSaugethiere II. Phylogenie 1.H. Die Familie der Erinaceidae.Zoologica, Stuttgart 37:1–103.

———. 1904. Uber Zahnwechsel bei Saugetiere im erwachsenenZustande. Zoologischer Anzeiger 27:219–222.

———. 1907. Zur Entwicklungsgeschichte des Zahnsystems derSaugetiere II. Phylogenie 2. Die Familien der Centetidae, So-lenodontidae und Chrysochloridae. Zoologica, Stuttgart 49:1–158.

———. 1915. Zur Frage nach der stammesgeschichtlichen Be-deutung des Milchgebisses bei den Saugetieren II. Viverridae,Hyaenidae, Felidae, Mustelidae, Creodonta. Zoologische Jahr-bucher. Abteilung fur Systematik, Geographie, und Biologieder Tiere 38:275–370.

Linhart, S. B. 1968. Dentition and pelage in the juvenile red fox(Vulpes vulpes). Journal of Mammalogy 49:526–528.

Lombaard, L. J. 1971. Age determination and growth curves inthe black-backed jackal, Canis mesomelas Schreber, 1775 (Car-nivora: Canidae). Annals of the Transvaal Museum 27:135–169.

Long, C. A. 1965. Comparison of juvenile skulls of the mustelidgenera Taxidea and Meles, with comments on the taxon Taxi-diinae Pocock. American Midland Naturalist 74:225–232.

———. 1974. Growth and development of the teeth and skull ofthe wild North American badger, Taxidea taxus . Transactionsof the Kansas Academy of Science 77:106–120.

Luckett, W. P. 1989. Developmental evidence for dental homol-ogies in the marsupial family Dasyuridae. Anatomical Record223:70A.

———. 1993. An ontogenetic assessment of dental homologiesin therian mammals. Pp. 182–204 in F. S. Szalay, M. J. Novacek,and M. C. McKenna, eds. Mammal phylogeny, Vol. 1. Meso-zoic differentiation, multituberculates, monotremes, earlytherians, and marsupials. Springer, New York.

Luckett, W. P., and N. Hong. 2000. Ontogenetic evidence for den-tal homologies and premolar replacement in fossil and extantcaenolestids (Marsupialia). Journal of Mammalian Evolution7:109–127.

Luckett, W. P., and W. Maier. 1982. Development of deciduousand permanent dentition in Tarsius and its phylogenetic sig-nificance. Folia Primatologica 37:1–36.

Luckett, W. P., and P. A. Woolley. 1996. Ontogeny and homologyof the dentition in dasyurid marsupials: development inSminthopsis virginiae. Journal of Mammalian Evolution 3:327–364.

MacDonald, D. W., ed. 1984. The encyclopedia of mammals.Facts on File, New York.

Malia, M. J., R. M. Adkins, and M. W. Allard. 2002. Molecular

support for Afrotheria and the polyphyly of Lipotyphla basedon analyses of the growth hormone receptor gene. MolecularPhylogenetics and Evolution 24:91–101.

Martin, B. E. 1916. Tooth development in Dasypus novemcinctus.Journal of Morphology 27:647–691.

Martin, T. 1997. Tooth replacement in late Jurassic Dryolestidae(Eupantotheria, Mammalia). Journal of Mammalian Evolu-tion 4:1–18.

McCrady, E., Jr. 1938. The embryology of the opossum. WistarInstitute of Anatomy, Philadelphia.

Michaeli, Y., Z. Hirschfeld, and M. M. Weinreb. 1980. The cheekteeth of the rabbit: morphology, histology and development.Acta Anatomica 106:223–239.

Mısek, I., and O. Sterba. 1989. Developmental anatomy of themole, Talpa europaea . X. Development of the dentition. FoliaZoologica 38:59–67.

Mitchell, O. G., and C. A. Carsen. 1967. Tooth eruption in theArctic ground squirrel. Journal of Mammalogy 48:472–474.

Montgomery, G. G. 1964. Tooth eruption in preweaned raccoons.Journal of Wildlife Management 28:582–584.

Moshonkin, N. N. 1979. Formation of the dental system in themink Lutreola lutreola. Zoologicheskii Zhurnal 58:1753–1756.

Moss-Salentijn, L. 1978. Vestigial teeth in the rabbit, rat andmouse: their relationship to the problem of lacteal dentitions.Pp. 13–29 in P. M. Butler and K. A. Joysey, eds. Development,function and evolution of teeth. Academic Press, London.

Muizon, C. de 1994. A new carnivorous marsupial from the Pa-laeocene of Bolivia and the problem of marsupial monophyly.Nature 370:208–211.

Neal, E. 1986. The natural history of badgers. Facts on File, NewYork.

Nikaido, M., K. Kawai, Y. Cao, M. Harada, S. Tomita, N. Okada,and M. Hasegawa. 2001. Maximum likelihood analysis of thecomplete mitochondrial genomes of eutherians and a reeval-uation of the phylogeny of bats and insectivores. Journal ofMolecular Evolution 53:508–516.

Nowak, R. M. 1999. Walker’s mammals of the world. Johns Hop-kins University Press, Baltimore.

Orr, R. T. 1954. Natural history of the pallid bat (Antrozous pal-lidus). Proceedings of the California Academy of Sciences 28:165–246.

Osborn, J. W., ed. 1981. Dental anatomy and embryology. Black-well Scientific, Oxford.

Petrides, G. A. 1949. Sex and age determination in the opossum.Journal of Mammalogy 30:364–378.

Phillips, C. J. 1971. The dentition of glossophagine bats: devel-opment, morphological characteristics, variation, pathology,and evolution. University of Kansas Museum of Natural His-tory, Miscellaneous Publications 54:1–138.

———. 2000. A theoretical consideration of dental morphology,ontogeny, and evolution in bats. Pp. 247–274 in R. A. Adamsand S. C. Pedersen, eds. Ontogeny, functional ecology, andevolution of bats. Cambridge University Press, Cambridge.

Poglayen-Neuwall, I. 1962. Beitrage zu einem Ethogramm desWickelbaren (Potos flavus Schreber). Zeitschrift fur Saugetier-kunde 27:1–44.

———. 1976. Zur Fortpflanzungsbiologie und Jugendentwick-lung von Potos flavus (Schreber 1774). Zoologische Garten 46:237–283.

———. 1995. Developmental data on Bassariscus sumichrasti(Carnivora: Procyonidae). Zoologische Garten 65:391–396.

Poglayen-Neuwall, I., and I. Poglayen-Neuwall. 1976. Postnataldevelopment of tayras, Eira barbara, in captivity. ZoologischeBeitrage 22:345–405.

———. 1993. Behavior, reproduction, and postnatal develop-ment of Bassariscus astutus (Carnivora; Procyonidae) in cap-tivity. Zoologische Garten 63:73–125.

Reynolds, H. C. 1952. Studies on reproduction in the opossum


(Didelphis virginiana). University of California Publications inZoology 52:223–284.

Rose, C. 1892. Uber die Zahnentwickelung der Beuteltiere. An-atomischer Anzeiger 7:639–650, 693–707.

Rougier, G. W., J. R. Wible, and M. J. Novacek. 1998. Implicationsof Deltatheridium specimens for early marsupial history. Na-ture 396:459–463.

Scheffer, V. B. 1951. Measurements of sea otters from westernAlaska. Journal of Mammalogy 32:10–14.

Schneider, K. B. 1973. Age determination of sea otter. Alaska De-partment of Fish and Game, Final Report, Federal Aid inWildlife Restoration, Projects W-17–4 and W-17–5, Job 8.10R:1–23.

Slaughter, B. H. 1970. Evolutionary trends of chiropteran den-titions. Pp. 51–83 in B. H. Slaughter and W. D. Walton, eds.About bats. Southern Methodist University Press, Dallas.

Smith, B. H., T. L. Crummett, and K. L. Brant. 1994. Ages oferuption of primate teeth: a compendium for aging individ-uals and comparing life histories. Yearbook of Physical An-thropology 37:177–231.

Smith, K. K. 2001. The evolution of mammalian development.Bulletin of the Museum of Comparative Zoology 156:119–135.

Stangl, F. B., Jr., S. L. Beauchamp, and N. G. Konermann. 1995.Cranial and dental variation in the 9-banded armadillo, Da-sypus novemcinctus, from Texas and Oklahoma. Texas Journalof Science 47:89–100.

Streilein, K. E. 1982. Behavior, ecology, and distribution of SouthAmerican marsupials. Special Publication of the PymatuningLaboratory of Ecology 6:231–250.

Thomas, O. 1887. On the homologies and succession of the teethin the Dasyuridae, with an attempt to trace the history of theevolution of mammalian teeth in general. PhilosophicalTransactions of the Royal Society of London B 178:443–462.

———. 1890. A milk dentition in Orycteropus. Proceedings of theRoyal Society of London 47:246–248.

———. 1911. The Duke of Bedford’s zoological exploration ofeastern Asia. XIII. On mammals from the provinces of Kan-su and Sze-chwan, western China. Proceedings of the Zoo-logical Society of London 1911:158–180.

Uhen, M. D. 2000. Replacement of deciduous first premolars anddental eruption in archaeocete whales. Journal of Mammal-ogy 81:123–133.

van der Merwe, M. 2000. Tooth succession in the greater canerat Thryonomys swinderianus (Temminck, 1827). Journal of Zo-ology 251:541–545.

van Nievelt, A. F. H., and K. K. Smith. 2005. Tooth eruption inMonodelphis domestica and its significance for phylogeny andnatural history. Journal of Mammalogy 86(2) (in press).

van Nostrand, F. C., and A. B. Stephenson. 1964. Age determi-nation for beavers by tooth development. Journal of WildlifeManagement 28:430–434.

VandeBerg, J. L. 1999. The laboratory opossum, Monodelphis do-mestica. Pp. 193–209 in T. B. Poole, ed. UFAW handbook on thecare and management of laboratory animals. Blackwell Sci-ence, Oxford.

Vaughan, T. A. 1970. The skeletal system. Pp. 97–138 in W. A.Wimsatt, ed. Biology of bats. Academic Press, New York.

Verts, B. J. 1967. The biology of the striped skunk. University ofIllinois Press, Urbana.

Whidden, H. P. 2000. Comparative myology of moles and thephylogeny of the Talpidae (Mammalia, Lipotyphla). Ameri-can Museum of Natural History Novitates 3294:1–53.

Wilson, J. T., and J. P. Hill. 1897. Observations upon the devel-opment and succession of the teeth in Perameles; together witha contribution to the discussion of the homologies of the teethin marsupial animals. Quarterly Journal of Microscopical Sci-ence 39:427–588, 8 plates.

Winge, H. 1941. The interrelationships of the mammalian gen-era, Vol. 1. C. A. Reitzel, Copenhagen.

Woodward, M. F. 1894. On the milk dentition of the Rodentia,with a description of a vestigial incisor in the mouse (Musmusculus). Anatomischer Anzeiger 9:619–631.

Wright, J. 1983. Biological significance of mammalian milkteeth. Ph.D. dissertation. Cornell University, Ithaca, N.Y.

Yates, T. L., and D. W. Moore. 1990. Speciation and evolution inthe family Talpidae (Mammalia: Insectivora). Pp. 1–22 in E.Nevo and O. A. Reig, eds. Evolution of subterranean mam-mals at the organismal and molecular levels. Wiley-Liss, NewYork.

Zhang, F.-K., A. W. Crompton, Z.-X. Luo, and C. R. Schaff. 1998.Pattern of dental replacement of Sinoconodon and its implica-tions for evolution of mammals. Vertebrata PalAsiatica 36:197–217.

Ziegler, A. C. 1971a. Dental homologies and possible relation-ships of recent Talpidae. Journal of Mammalogy 52:50–68.

———. 1971b. A theory of the evolution of therian dental for-mulas and replacement patterns. Quarterly Review of Biology46:226–249.

———. 1972. Milk dentition in the broad-footed mole, Scapanuslatimanus. Journal of Mammalogy 53:354–355.

To replace or not to replace: the signiﬁcance of …people.duke.edu/~kksmith/papers/tooth...

Documents

Transcript of To replace or not to replace: the signiﬁcance of …people.duke.edu/~kksmith/papers/tooth...