ontogenetic evidence for dental homologies and premolar replacement in fossil and extant...

Journal of Mammalian Evolution, Vol. 7, No. 2, 2000

1064-7554/ 00/ 0600-0109$18.00/ 0 2000 Plenum Publishing Corporation

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Ontogenetic Evidence for Dental Homologies andPremolar Replacement in Fossil and Extant Caenolestids(Marsupialia)

W. Patrick Luckett1,3 and Nancy Hong2

It is generally accepted that the South American marsupial family Caenolestidae is characterizedin part by the absence or noneruption of the third deciduous premolar (dP3) in both jaws,although juvenile stages have rarely been identified in extant or fossil representatives of thefamily. Published illustrations of the dentary of the Miocene caenolestid Stilotherium suggestedto us, however, that P3 erupted relatively late during ontogeny, after the eruption of M4. Inextant marsupials, this eruption sequence appears to represent the plesiomorphic state and thispattern is generally associated with the eruption of dP3 earlier in ontogeny, and its subsequentreplacement by the erupting P3. Therefore, we suspected that a dP3 erupted in earlier ontogeneticstages of caenolestids; to test this hypothesis we searched the mammalogy collections of threemuseums for evidence of dP3 in juvenile specimens of caenolestids. Examination of more than180 specimens of the three extant genera of caenolestid marsupials resulted in the identificationof only nine juvenile or subadult stages of dental eruption. Seven specimens of Caenolestes andRhyncholestes corroborated our hypotheses of late eruption of P3 in Caenolestidae. In addition,the two youngest specimens of Caenolestes possessed a tiny, rudimentary dP3, measuring about0.4 to 0.5 mm in greatest length, associated with a mesiolingual eruption pit containing theapex of the larger P3 in very early phases of eruption above the alveolar margins. The tiny dP3is clearly nonfunctional in occlusion, and it is questionable whether it erupted above the gunmargins in life. Comparison of the dentaries of subadult caenolestids with four dentaries of theMiocene genus Stilotherium corroborated our initial impression that the fossil genus exhibitedevidence of a late-erupting P3, comparable to the condition in extant caenolestids. We suggestthat examination of other specimens of juvenile dentitions, skulls, and skeletons in museumcollections can provide additional insight into the developmental and evolutionary biology ofmammals.

KEY WORDS: marsupials; dental ontogeny; deciduous premolars; Caenolestidae.

INTRODUCTION

The South American marsupial family Caenolestidae includes three extant genera(Caenolestes, Lestoros, Rhyncholestes) and a number of Miocene (Santacrucian) gen-

1 Department of Anatomy, University of Puerto Rico, Medical Sciences Campus, San Juan 00936-5067, PuertoRico.

2 Caribbean Primate Research Center Museum, University of Puerto Rico, Medical Sciences Campus, San Juan,Puerto Rico.

3 To whom correspondence should be addressed. E-mail: p [email protected]

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era, including Stilotherium (see Marshall, 1980 for an excellent summary of fossilcaenolestids). The family is generally placed in a separate order or infraorder Paucitu-berculata, distinct from Didelphidae or Didelphoidea (Aplin and Archer, 1987; Marshallet al., 1990; Szalay, 1994), although both higher taxa are clustered usually within themarsupial cohort Ameridelphia. The Miocene-Recent caenolestids are characterized byan enlarged anterior lower incisor; however, the homologies of this large incisor (as I1

or l2 of the primitive marsupial condition) are unclear (see Ride, 1962; Marshall, 1980).In his diagnosis of the family Caenolestidae, Marshall (1980) considered the prob-

able absence of dP3 in both jaws as a derived attribute of the family. This was based inpart on the earlier report by Archer (1978) that he was unable to find any evidence oftooth replacement in more than 150 specimens of caenolestids examined. In support ofthis hypothesis, Marshall (1980) noted also that no evidence of dP3 or premolar erup-tion had been detected in fossil caenolestids. Studies of dental ontogeny (Luckett, 1993)suggest, however, that dP3 develops in both jaws of all extant marsupials, as it does inthe ancestral marsupial morphotype. Therefore, it seems likely that dP3 develops duringearly ontogeny in all caenolestids, although it could undergo regression and resorptionwithout eruption, a possibility also considered by Archer (1978). Unfortunately, there areno histological studies of dental development in young extant caenolestids to test thishypothesis and, indeed, there have been few juvenile specimens collected during fieldstudies (e.g., Kelt and Martınez, 1989).

In the absence of histological studies of early dental ontogeny, an alternate methodis available to test the likelihood of dP3 eruption in caenolestids. An extensive surveyof dental eruption and dP3 replacement patterns in juvenile and subadult skulls of mostfamilies and genera of extant marsupials (Luckett, 1994; Luckett and Hong, in prep.)demonstrates that the late eruption of P3 and its displacement of dP3 (concomitant withor later than eruption of M4) probably represent the primitive or ancestral condition forMarsupialia; this hypothesis is consistent with the meager evidence from the fossil record(Cifelli et al., 1996; Cifelli and Muizon, 1998). If true, then evidence for the late erup-tion of P3 in extant or fossil caenolestids (and other marsupials) could be taken as anindirect indication that this was replacing a previously erupted dP3. On the other hand, iferuption of P3 is precocious in caenolestids or other marsupials (concomitant with erup-tion of M2 or M3), this might be indicative of the vestigial development and possiblenoneruption of dP3, correlated with precocious eruption of the successor P3; this is thecase for some extant marsupials (e.g., Dasyurus) for which adequate ontogenetic data areavailable (Luckett, 1993, 1994; Luckett and Hong, in prep.). This working hypothesis ispotentially of great value for the study of marsupial fossils, as in some cases it can pro-vide indirect evidence for the earlier presence (or not) of an erupted dP3. The presentstudy provides a test of this hypothesis in a marsupial family whose dental ontogeny isalmost completely undocumented. Interestingly, Lonnberg (1921, p. 72) mentioned briefly(but did not illustrate) a “young male” specimen of Caenolestes, in which M4 had notyet erupted and P3 was in an early eruptive phase. He interpreted this as evidence thatP3 is a successor tooth in this genus, “having displaced a predecessor.” This importantobservation seems to have gone unnoticed by subsequent investigators.

Following the initial description by Ameghino (1887) of the Miocene (Santacru-cian) fossil Stilotherium dissimile as a member of the marsupial family Microbiotheriidae,it was subsequently recognized that Santacrucian taxa with an enlarged anterior lower

Dental Homologies in Caenolestids 111

incisor (“I1”) but an otherwise relatively complete dentition (including Stilotherium)should be placed in a separate family Garzonidae (Ameghino, 1894). At about the sametime, evidence of extant caenolestids in South America was rediscovered by Thomas(1895), following the earlier, preliminary report of Tomes (1863). Comparison of the fos-sil garzonids and the newly described extant Caenolestes by Thomas (1895) and Ame-ghino (1897) led both investigators to realize that these taxa belonged in the same family,which was subsequently recognized as the family Caenolestidae [see Sinclair (1906) andMarshall (1980) for further discussion of the history of caenolestid systematics].

Our examination of the illustration by Marshall (1980; his Fig. 6) of the nearly com-plete mandibular dentition of the Miocene caenolestid Stilotherium dissimile suggested tous that P3 was not fully erupted in this jaw, whereas M1−4 had completed their eruption.This same specimen (MACN A-8464) had been illustrated previously by Reig (1955)and by Pascual and Herrera (1975), but none of these authors commented on the appar-ent incomplete eruption of P3 in this jaw. If late eruption of P3 indeed occurred in thisrelatively plesiomorphous Miocene caenolestid, then the possibility exists that the sameeruption pattern might occur in extant caenolestids. The present study was undertaken totest the hypothesis of late replacement of dP3 by P3 in extant and fossil caenolestids.

MATERIALS AND METHODS

Specimens of all three genera of extant caenolestids were examined in the mammal-ogy collections of the American Museum of Natural History, New York (AMNH), theField Museum of Natural History, Chicago (FMNH), and the National Museum of Natu-ral History, Washington D.C. (USNM). The presumed juvenile specimen of Caenolestes,described briefly by Lonnberg (1921), was borrowed from the Swedish Museum of Natu-ral History (NRM), through the courtesy of Dr. Bo Fernholm and Ms. Rita Larje. When-ever possible, both the greatest length (GL) and the basal length (BL) of each juvenileand subadult skull, and selected adult skulls, were measured with Mitutoyo Digimaticcalipers to the nearest 0.01 mm [see Fig. 17 of Hershkovitz (1992) for an outline schemefor these measurements on marsupial skulls]. In addition, casts of two dentaries of theMiocene caenolestid Stilotherium dissimile (MACN A-5700, MACN A-8464) were exam-ined in the collections of the Department of Vertebrate Paleontology, American Museumof Natural History. The fossil casts are of specimens housed in the Ameghino Collectionof the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina (MACN); fortu-nately, one of these (MACN A-8464) is the same subadult dentary illustrated by Marshall(1980). Through the courtesy of Dr. Jose Bonaparte, we borrowed three additional fos-sil dentaries of Stilotherium from the MACN for comparison with the casts. Collectiondata for all these fossil specimens of Stilotherium, from the Santa Cruz Formation ofPatagonia, southern Argentina, are summarized by Marshall (1982, p. 69).

Dental homologies and terminology for extant and fossil marsupials used here fol-low Luckett (1993), i.e., P3 replaces dP3, and the anterior two premolar loci in adultthree-premolared marsupials are unreplaced deciduous teeth (dP1, dP2). For purposes ofthis study, juvenile skulls were considered as those in which M4 was not erupted in bothjaws, whereas subadults may have M4 erupted, but P3 is not completely erupted. Cam-era lucida drawings were made of selected jaws and dentitions of juvenile and subadultextant caenolestids, and of several specimens of the fossil genus Stilotherium. One den-

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tary of Caenolestes convelatus (FMNH 94948) was photographed with a scanning elec-tron microscope (SEM) at the Field Museum of Natural History, through the collaborationof Dr. Bruce Patterson and Ms. Betty Strack. For comparison, juvenile and subadult den-titions of most other genera of extant marsupials have been examined, as part of ourongoing study of dental eruption and replacement in marsupials.

RESULTS

Although specimens of extant caenolestids are well represented in the mammalogycollections of the Field Museum of Natural History, the American Museum of NaturalHistory, and the National Museum of Natural History, only a few representatives of juve-nile or subadult dentitions are found in these collections. Nevertheless, evidence for theoccurrence of dP3 and its late replacement in Caenolestes is clearly documented. Amongmore than 180 skulls of caenolestids examined, only nine specimens could be consideredjuvenile or subadult, based on the extent of dental eruption. No juvenile or subadult speci-mens of Lestoros inca were found, and only a single subadult Rhyncholestes raphanuruswas identified, in which M4 was about half-erupted. Therefore, the following descrip-tions are based primarily on ontogenetic stages from several species of Caenolestes. Thespecies and subspecies of Caenolestes recognized in our study are those of Bublitz (1987);this is the same scheme currently in use at the FMNH, where most of the juvenile andsubadult specimens from our study are located.

Premolar Replacement in Caenolestids

Evidence for the relatively late eruption of P3, after the eruption of M4, is docu-mented in a small series of lower jaws in Caenolestes (Table I). In constrast, there is lessevidence for the eruption of P3, because of the general trend in didelphids, caenolestids,dasyurids, and peramelids for the earlier eruption of P3 in the upper jaw than in the den-tary. Different species of Caenolestes and Rhyncholestes are clustered together in thisanalysis and in Table I, because there do not appear to be any significant differencesin the pattern and sequence of eruption of P3 and M4 in the few immature specimensavailable.

Definite evidence for the occurrence of dP3 was found in a juvenile male skull ofCaenolestes convelatus convelatus (FMNH 94948), in which M1-3 were erupted in bothjaws and the upper canine was almost completely erupted. In this specimen, P3 is about1/ 2–2/ 3 erupted on the right side of the maxilla (Fig. 1 and Table I); this tooth hasfallen out on the left side and its roots remain open and incompletely formed. There isno trace of a displaced dP3. The M4 region is represented only by a tiny, shallow alveolusbilaterally; comparison with later stages suggests that the missing M4 had not yet begunerupting (see below).

In the lower jaw, M4 has almost completed its eruption, whereas P3 has not yet begunto erupt (Fig. 2). A moderate-sized eruption pit occurs in the bone between the erupted dP2

and M1 and the apex of the unerupted P3 is evident at or just below the alveolar marginsof the eruption pit bilaterally. Careful examination of the right side of the dentary revealsthat a tiny remnant of dP3 (0.4 mm long) is adherent to the dried connective tissue thatoverlies the eruption pit for P3 (Figs. 3, 4, and 5). The tiny dP3 apparently lacks distinct


Fig. 1. Juvenile skull of Caenolestes convelatus (FMNH 94948), with erupting P3 in right maxilla, and withM3 almost completely erupted.

roots; its slender, tapered base is attached only to the dried tissue that partially surroundsthe margins of the eruption pit. The apex of the tiny tooth is covered with shiny, refractileenamel, and there is evidence for the formation of several cusplike elevations on a taller,mesial trigonid and a lower, distal talonid (Fig. 5). Because of the essentially horizon-tal orientation of this rootless tooth, it is difficult to confirm the number and pattern ofthe tiny cusps, without dislodging the tooth from its precarious attachment. No trace of a

Fig. 2. Juvenile left dentary of Caenolestes convelatus (FMNH 94948), lingual view, in which M1−4 are erupted(M3−4 region not shown), whereas P3 has not yet begun to emerge above the alveolar margins (note the apexof P3 within alveolus and the absence of dP3 on this side).

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Table I. Juvenile and Subadult Specimens of Caenolestid Dentitions

SkullSpecies GL BL

(specimen no., sex) (mm) (mm) P3 M4 dP3 P3 M4

C. convelatus 28.07 25.02 1/ 2 Probably Tiny (0.4 Not AlmostFMNH 94948, M Erupted not mm) erupting fully

erupting eruptedC. convelatus 29.80 — Almost Not Tiny (not Very early Erupted

NRM A580074, M fully erupting measured) eruptingerupted

C. fuliginosus 26.95 — Almost Very — Very early EruptedFMNH 70858, M fully early erupting

erupted eruptingC. fuliginosus 27.96 — Almost Early — 2/ 3–3/ 4 Erupted

FMNH 92299, M fully erupting Eruptederupted

C. caniventer 30.57 26.94 Almost Early — 3/ 4 Erupted EruptedFMNH 81459, M fully erupting

eruptedC. fuliginosus Broken — Erupted Almost — 2/ 3 Erupted Erupted

FMNH 70859, M fullyerupted

C. caniventer 30.70 27.23 Erupted 1/ 2 Erupted — Almost EruptedFMNH 81460, M fully

erupted

Dental H

omologies in C

aenolestids115

C. fuliginosus 28.53 25.42 Erupted Erupted — Almost EruptedFMNH 70888, F fully

eruptedR. raphanurus 29.72 26.81 Erupted 1/ 2 Erupted — Erupted Erupted

FMNH 129828, FR. raphanurus 31.56 29.09 Erupted Erupted — Erupted Erupted

FMNH 129834, FC. caniventer 32.95 30.40 Erupted Erupted — Erupted Erupted

FMNH 81457, FC. convelatus 33.34 30.91 Erupted Erupted — Erupted Erupted

FMNH 53288, FC. fuliginosus 31.57 28.36 Erupted Erupted — Erupted Erupted

FMNH 70847, MStilotherium dissimile — — — — — Almost Erupted

MACN A-8464, ? fullyerupted

Stilotherium dissimile — — — — — Almost EruptedMACN A-8465, ? fully

eruptedStilotherium dissimile — — — —- — Erupted Erupted

MACN A-5700, ?

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Fig. 3. Juvenile right dentary of Caenolestes convelatus (FMNH 94948), showing an enlarged view ofthe dP2–M1 region (oblique bucco-occlusal view). Note the apex of the unerupted P3 (arrow) and thetiny dP3 immediately anterior to it. Dried connective tissue (*) partially surrounds the eruption pit forP3 and the tiny dP3 is loosely adherent to this.

Fig. 4. Juvenile right dentary of Caenolestes convelatus (FMNH 94948), showing an enlarged view ofthe dP2–M1 region (lingual view). The apex of the unerupted P3 is evident and the base of the tinyoverlying dP3 is not seen in this view.


Fig. 5. Scanning electron micrograph of juvenile right dentary of Caenolestes convelatus (FMNH 94948), inlinguo-occlusal view (cf. Fig. 4). The tiny dP3 (arrow) overlies the apex of P3 and these teeth are flanked bydP2 (left) and M1 (right). Note the tiny cusplike elevations on the possible trigonid (lower left) and talonid(upper right) of dP3. Scale bar c 0.1 mm.

tiny dP3 is found on the left side of the jaw; this is probably due to the “more efficient”cleaning of dried tissue from the margins of the eruption pit on this side.

The occurrence of such a tiny rudiment of dP3 in a single specimen of Caenolestesraises doubts concerning whether this is a typical or an atavistic remnant of the decid-uous premolar. Fortunately, the specimen of C. convelatus from the Swedish Museum ofNatural History (NRM A580074) exhibits a similar, but slightly advanced, state of erup-tion of the premolars, in comparison to the FMNH specimen. Although the specimenswere collected 47 years apart, both came from the region of Gualea in Ecuador and areallocated to the same species.

M1-3 are erupted in both jaws of NRM A580074, and the tiny M4 is not erupting. Asin the FMNH juvenile specimen, the molar cusps are relatively unworn. In the maxilla, P3

is almost completely erupted, although its apex is still lower than that of M1 and its buccalcingulum is just above the alveolar margins (Fig. 6). Initial examination of the eruptingtooth and adjacent alveolar margins with a dissecting microscope revealed no trace of arudimentary dP3, in agreement with Lonnberg’s (1921) observation. However, during thecourse of preparing the camera lucida drawing, we observed a tiny, refractile, enamel-covered fragment adhering to the distobuccal side of the erupting right P3, and wedgedbetween P3 and M1 (Fig. 6). We suggest that this is an apical remnant of a rudimentarydP3, which was in the process of being displaced by the erupting P3.

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Fig. 6. Juvenile left maxilla of Caenolestes convelatus (NRM A580074) with P3 erupting between dP2 (left)and M1 (right). Note the tiny, enamel-covered apical fragment (arrow) of a possible dP3, adhering to the disto-buccal side of the erupting P3. Scale bar c 1 mm.

In the lower jaw, M4 is erupted, whereas the apex of P3 is only just above the alveolarmargins, in a very early stage of eruption (Fig. 7). On the right side a tiny calcified dP3

overlies the distobuccal side of the apex of the early erupting P3 (Fig. 8). The tiny toothis triangular and somewhat elonate anteroposteriorly and has a globular apex. It adheresto the dried, transparent remnants of the gingival tissue, and distinct roots are apparentlylacking. The precise shape and dimensions of this dental rudiment are unclear; any furthercleaning or exposure would probably result in its loss. There is no trace of a tiny dP3 onthe left side; this may be correlated with the somewhat greater degree of eruption of P3

on this side.In later stages of ontogeny examined, P3 has nearly completed its eruption process,

while the small M4 is in early phases of eruption (Table I). Because of the later eruption

Fig. 7. Juvenile right dentary of Caenolestes convelatus (NRM A580074), buccal view, showing the eruptionpit for P3 (arrow) between dP2 (right) and M1 (left). The apex of P3 is evident in the eruption pit. Note thefour tiny teeth lying between dP2 and the enlarged anterior incisor. Scale bar c 1 mm.


Fig. 8. Juvenile right dentary of Caenolestes convelatus (NRM A580074), showing an enlarged view of thedP2–M1 region, in bucco-occlusal view. A tiny dP3 (arrow) overlies the distobuccal apex (A) of the earlyerupting P3. Scale bar c 1 mm.

of P3 in the lower jaw, its progress is documented better in our small series. In the dentaryof a juvenile male Caenolestes fuliginosus (FMNH 70858), the apex of P3 is in a veryearly eruption phase (Fig. 9), whereas the small M4 is completely erupted. In all laterphases of P3 eruption in the dentary (Fig. 10), M4 is also completely erupted (Table I).

In the single subadult stage of Rhyncholestes raphanurus (FMNH 129828) available,P3 is erupted in both jaws, whereas the small M4 is only about 1/ 2–2/ 3 erupted (Table I).This stage is most similar to that seen in Caenolestes caniventer FMNH 81460, in whichP3 is completely erupted, whereas the small M4 is about 1/ 2 erupted and P3 is almostfully erupted. There are slight differences regarding whether M4 or P3 is the last toothto complete eruption in Caenolestes (and in Rhyncholestes); this may be related in someway to the small size of M4 in caenolestids. As in other three-premolared marsupials,

Fig. 9. Juvenile right dentary of Caenolestes fuliginosus (FMNH 70858), in lingual view, showing an earlyerupting P3.

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Fig. 10. Subadult right dentaries of Caenolestes fuliginosus (FMNH70888 above, FMNH 70859 below), showing an enlarged view of thedP2–M1 region, in lingual view. In these different phases of nearly com-plete eruption of P3, note the crowding and slight rotation of this tooth,between dP2 and M1.

there is no evidence for any replacement occurring at the dP1 or dP2 positions in ourlimited ontogenetic series.

Study of four dentaries from the Miocene caenolestid Stilotherium dissimile confirmsour initial impression, gained from examination of Fig. 6 in Marshall (1980), that eruptionof P3 is not completed in the lower jaw of this genus until after the eruption of M4, similarto the condition in extant Caenolestes. In the nearly intact right dentary of MACN A-8464, M1−4 are fully erupted, whereas the base of P3 was not yet completely erupted(Figs. 11 and 12). The apex of P3 lies somewhat lower than the apex of the trigonidcusps of M1, and the posterior half of the lingual cingulum of P3 does not extend abovethe level of the alveolar margins (Fig. 11). The erupting P3 is crowded between dP2

and M1; consequently, the posterior shelf of P3 partly underlies the anterior end of M1,and P3 is somewhat rotated buccolingually (Figs. 11 and 12). The degree of eruption ofP3 is slightly less advanced in MACN A-8464, compared with Caenolestes fuliginosusFMNH 70859 and 70888 (cf. Figs. 10, 11, and 12). In keeping with the subadult nature ofthis Stilotherium jaw, the molar cusps are relatively unworn. The left dentary of MACNA-8464 is more damaged, with the anterior premolars being represented only by alveoli.Nevertheless, P3 exhibits a similar eruptive phase to that on the more complete right side.Examination of a second subadult dentary of Stilotherium (MACN A-8465) reveals thata virtually identical pattern of late-erupting P3 occurs in this specimen, in which M1−4

are completely erupted.


Fig. 11. Right dentaries of two specimens of the Miocene caenolestid Stilotherium dissimile, in lingual view.Above is MACN A-8464, with a nearly complete dentition, missing only the tiny “second” incisor (*). P3 hasalmost completely erupted, but its lingual cingulum is not yet exposed distally. Note the crowding of P3 betweendP2 and M1. Below is MACN A-5700, a partial adult dentary (M3−4 lost), with P3 completely erupted (andpartly displaced out of its alveoli). Note the greater wear on the molar crowns of this more mature specimen,compared to MACN A-8464.

The cast of the partial right dentary of MACN A-5700 bears erupted C, dP2, P3, andM1−2 (Figs. 11 and 12). Alveoli are also present for the missing dP1 and M3. The den-tary is missing posterior to the anterior alveolus for M3 and anterior to the erupted C. Bycomparison with MACN A-8464 and A-8465, and with other dentaries of Stilotheriumfigured by Ameghino (1897, 1903, 1906), it is almost certain that M3−4 were fully eruptedin this specimen. P3 is completely erupted in this adult dentary; there is no crowding of

Fig. 12. Right dentaries of two specimens of the Miocene caenolestid Stilotherium dissimile, in buccal view.MACN A-8464 (above) and MACN A-5700 (below). Note the difference in crowding of P3 in the subadultspecimen above and the adult below compared to Fig. 11.

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this tooth between dP2 and M1 and there is no obvious rotation of P3 buccolingually. Theapex of P3 is elevated above the apex of the trigonid cusps of M1 (as it is in adult extantcaenolestids) and the buccal and lingual cingula of P3 are completely exposed above thealveolar margins. During the fossilization process, P3 became displaced slightly out of itsalveoli; nevertheless, when the crown heights of P3 and M1 are measured from the levelof the base of their buccal cingula, the premolar height still exceeds that of M1. In thisadult specimen, the molar cusps exhibit more wear and are lower in height than those ofthe subadults (MACN A-8464, A-8465).

A comparison of the P3–M1 relationships in these two ontogenetic stages ofStilotherium dissimile corroborates the hypothesis for late eruption of P3 in this fossilspecies, after the eruption of M4. It seems probable that the eruption pattern of P3 inStilotherium is comparable to that in the upper jaws of extant caenolestids, although fewupper dentitions are known for Stilotherium; we have not yet examined fossil maxillae.

Homologies of Lower Incisors in Caenolestids

The homologies of the enlarged, anterior lower incisors of fossil and Recentcaenolestids are unclear, in comparison with didelphids and the ancestral marsupial mor-photype. The last common ancestor of known fossil and extant marsupials is believedto have possessed an adult dental formula of: 5–1–3–4/ 4–1–3–4; this is identical to thepattern in extant didelphids. Most extant and fossil caenolestids (including Stilotherium)have a maximum incisor count of 4/ 3. In the dentary the enlarged, procumbent anteriorincisor is followed by four tiny, unicuspid teeth, generally interpreted to represent twoincisors, dC, and dP1 (Figs. 2, 7, 9, and 11). However, at least two adult specimens ofCaenolestes appear to have four lower incisors. One of these is an adult male of C. fuligi-nosus, mentioned briefly by Osgood (1921, p. 112). This specimen (FMNH 18603) bearsan additional, tiny unicuspid tooth in the anterior portion of the right dentary, resulting ina presumed dental formula in the lower jaw of 4–1–3–4 (Fig. 13). Between the enlargedanterior incisor (I1?) and the small, somewhat elongate dP2 lie five tiny, unicuspid teeth;these may represent I2−4, dC, and dP1. In contrast, the left dentary bears only four tinyunicuspids, similar to the condition in most other extant caenolestids. Such meager andunilateral evidence does not clarify whether the “extra” tiny tooth represents a remnantof the ancestral incisor formula or whether it is an atavism.

DISCUSSION

The observations of the present study confirms the occurrence of a small dP3 duringontogeny in extant caenolestids, as well as its likely presence in the relatively plesiomor-phic Miocene genus Stilotherium. In Caenolestes, this tiny deciduous tooth is already ina late phase of regression, and it is unlikely that it “erupts” above the gingival surface ofthe oral cavity or plays any functional role in occlusion. Evidence for the occurrence ofdP3 is mainly restricted to the lower jaw in our limited ontogenetic series, due to the latereruption of P3 in the dentary than in the maxilla, similar to the condition in didelphids,dasyurids, and peramelids. In the earliest ontogenetic stage available (FMNH 94948), thetiny dP3 is barely above the alveolar margins of the dentary, overlying the apex of theunerupted P3. The lack of distinct roots and the adherence of the tiny tooth to dried soft


Fig. 13. Adult right dentary of Caenolestes fuliginosus (FMNH 18603), buccal view. Note the occurrence offive tiny, unicuspid teeth between the enlarged anterior incisor and dP2; the left half of the dentary containsonly four tiny teeth (the usual number in extant caenolestids). Scale bar c 1 mm.

tissues overlying the apex of P3 suggest that the rudimentary dP3 may have been pushedabove the alveolar margins during the early preeruptive movements of P3. It was, indeed,fortuitous for our study that the dried gingival tissue had not been cleaned completelyfrom the area of the eruption pit for P3 in this juvenile specimen, or from the slightlymore mature NRM specimen; if it had been, the tiny dP3 would almost certainly havebeen lost with it. Such rudimentary teeth, measuring less than 0.5 mm in greatest length,are unlikely to be seen by the unaided eye; even when viewed under a dissecting micro-scope, we failed to note the presence of the tiny dP3 fragment initially in the maxilla ofNRM A580074. Moreover, Lonnberg (1921) found no evidence of the tiny dP3 rudimentduring his original study of the latter specimen; it is unclear whether he examined thejaws with a microscope. Nevertheless, his astute prediction of the probable occurrence ofdP3 in this genus has proved to be correct by our investigation, based, in part, on carefulstudy of his own specimen.

Although the rudimentary dP3 in both jaws of Caenolestes (and presumably in otherextant caenolestids) do not function in mastication, this does not result in acceleratederuption of the successor P3. This contrasts with the condition in some dasyurids (e.g.,Dasyurus viverrinus), in which a rudimentary but calcified dP3 develops but does noterupt usually. In this dasyurid genus there is accelerated development and eruption of P3in both jaws; in the upper jaw its eruption is completed before that of M2 in at least twospecies of Dasyurus (Luckett, 1993 and unpublished observations; see also Merchant etal., 1984).

In addition to its common function as the first molariform tooth to develop and eruptin didelphids, phalangeroids, and macropodoids, dP3 plays another important role in allknown extant marsupials for which there are adequate histological stages of ontogeny(including Dasyurus), regardless of whether this tooth erupts or not. The lingual succes-sional lamina of dP3 serves as the epithelial source for the development of the P3 budin all cases where there has been careful study of closely graded ontogenetic series (seeLuckett, 1993 and Luckett and Woolley, 1996 for a summary of the available evidence).Therefore, it is unlikely that dP3 is “absent” during the ontogeny of any extant marsu-pial [contra Archer (1978) and Marshall (1980) for caenolestids]; if P3 occurs, then it isvirtually certain that dP3 develops and gives rise to its successor P3, regardless of the

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subsequent fate of dP3 (either eruption or resorption). From a biological and evolutionaryperspective, it is important to distinguish between the development and the eruption ofdP3; development can terminate in eruption or noneruption and resorption.

Paradoxically, the initial evidence for the likely occurrence of dP3 in caenolestidscame to us by viewing the excellent camera lucida illustration by Marshall (1980, his Fig.6) of a dentary (MACN A-8464) of the Miocene caenolestid Stilotherium. His figure,as well as the earlier one by Reig (1955) of the same specimen, suggested to us thatMACN A-8464 represents a subadult dentary, in which P3 had not quite completed itseruption, although M4 was fully erupted. Based on our unpublished observations of P3eruption in all families and most genera of extant marsupials, this pattern of late eruptionof P3, following that of M4 (at least in the lower jaw), probably represents the primitivemarsupial condition; this pattern is associated with the replacement of an erupted dP3 byP3 in both jaws. In the case of caenolestids, the condition in the fossil Stilotherium ledto the search and discovery of the tiny dP3 in extant Caenolestes.

Examination of the original, relatively simple drawings of the dentary of Stilotheriumdissimile by Ameghino (1897, Fig. 75; 1903, Fig. 92; 1906, Fig. 196) suggests that hisoft-reproduced figure was based, at least in part, on MACN A-8464 and/ or A-8465. Iftrue, we have had indirect evidence for the probable occurrence of dP3 in caenolestidsfor more than 100 years, without it being recognized as such. Marshall (1982), basedon his personal examination of multiple specimens of Stilotherium in Buenos Aires, alsosuggested that the nearly complete dentary of Stilotherium, illustrated several times byAmeghino, was MACN A-8465, although the latter specimen is now fragmentary, con-sisting only of the region containing P3–M4. Marshall (1982, p. 69) acknowledged that theincisor and premolar region in Ameghino’s figures of Stilotherium “may have been basedon MACN 8464, but this is less certain.” Based on our observation of a similar phase oflate-erupting P3 in both of these subadult dentaries, we suspect that both specimens wereused by Ameghino (1897 and later) in making a composite figure for illustration.

In any case, our observations on Stilotherium suggest that many other juvenile fossilspecimens of marsupials (and eutherians) lie unrecognized or unstudied in museum col-lections. Such juvenile fossils can contribute significantly to our understanding of dentaleruption, replacement, and evolution in mammals [see Luckett and Hong (1998) for anexample of the value of juvenile fossil specimens in the study of artiodactyl and cetaceanphylogenetic relationships].

In many marsupials with a late-erupting P3, the displaced dP3 is a well developed,molariform tooth, as in didelphids. In most peramelids and some dasyurids, however, thedP3 has become reduced and nonmolariform; the greatest range of variation occurs indasyurids. The retention of late eruption of P3 in caenolestids, associated with the derivedcondition of a greatly reduced dP3 that probably does not erupt, is a combination not foundin other marsupial families for which adequate data are available. Further investigationof other juvenile caenolestids, including histological studies of early stages, is required todetermine whether this developmental pattern is uniquely derived within Marsupialia.

Incisor Homologies in Caenolestids

In the absence of histological evidence from earlier ontogenetic stages, it is impos-sible to tell which incisor locus is “missing” in the dentary of extant caenolestids and


in Stilotherium. The occurrence of an additional tiny tooth in the dentary, between theenlarged anterior incisor and the moderate-sized dP2, has been reported in two specimensof Caenolestes (Bensley, 1903; Osgood, 1921). The British Museum specimen (numbernot given) illustrated by Bensley (1903) possesses the additional tooth bilterally, whereasthe specimen (FMNH 18603) mentioned, but not illustrated by Osgood (1921; see ourFig. 13), bears the additional tiny tooth only on the right side. Such limited evidence,coupled with the lack of histological examination of any juvenile caenolestid dentaries,makes it difficult to assess whether the additional tiny tooth represents an incisor locuswhich does not normally erupt, or whether it is just a supernumerary tooth in these twospecimens. Until preserved juvenile caenolestids are identified in museum or universitycollections and sectioned serially, it is unlikely that we can evaluate confidently the I1or I2 homologies of the enlarged, procumbent anterior incisor of caenolestids, as notedearlier by Ride (1962).

In contrast, ontogenetic studies of the anterior dentition in Australian diprotodontiansindicate that the enlarged lower incisor in this group is derived from the second devel-oping tooth position in the dentary, rather than the first [see Woodward, 1893; Berkovitz,1968; Kirkpatrick, 1969; also Luckett and Renfree, unpublished]. However, because it isunclear which incisor locus has been lost in dasyuroid and perameloid marsupials, com-pared to didelphids and microbiotheriids, incisor homologies still remain uncertain for allfamilies of Australian marsupials. Because of the scarcity of intact anterior jaws and den-titions for fossil marsupials in Australia, the available fossil evidence offers no resolutionto this dilemma [see Godthelp et al. (1999) for a recent discussion].

A final comment is warranted concerning the original report by Archer (1978) thathe was unable to detect any evidence of tooth replacement in more than 150 specimensof caenolestids examined by him. Unfortunately, he did not specify whether juvenile orsubadult specimens were present in his sample; if only adult skulls are present in collec-tions, they would not be expected to furnish such evidence. Our examination of more than180 caenolestid skulls revealed only nine immature specimens and this was both unex-pected and frustrating for the investigation. Clearly, one must be cautious in interpretingnegative evidence of any kind; this is particularly true when searching for ontogeneticevidence in extant and fossil mammals.

ACKNOWLEDGMENTS

We thank the following museum curators and personnel, whose help made this studypossible: Dr. Bruce Patterson and William Stanley (Field Museum of Natural History,Chicago); Dr. Richard Tedford, Dr. Nancy Simmons, John Alexander, Helmut Sommer,and Darrin Lunde (American Museum of Natural History, New York), and Dr. RichardThorington and Ms. Linda Gordon (National Museum of Natural History). The valu-able juvenile Caenolestes specimen was graciously loaned from the Swedish Museumof Natural History (Stockholm) by Dr. Bo Fernholm and Ms. Rita Larje. Special thanksgo to Dr. Jose Bonaparte (Museo Argentino de Ciencias Naturales, Buenos Aires) forthe loan of four specimens of Stilotherium, and to Dr. Guillermo Rougier (University ofLouisville) for hand-carrying these valuable fossils from Buenos Aires to New York forour study. The manuscript was improved by constructive comments from Drs. RichardCifelli, Jean-Louis Hartenberger, and an anonymous reviewer.

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