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The Significance of Reduced Functional Paleobiology, 31(2), 2005, pp. 324±346 To replace or not to replace: the signi®cance of reduced functional tooth replacement in marsupial and placental mammals Alexander F. H. van Nievelt and Kathleen K. Smith Abstract.ÐMarsupial mammals are characterized by a pattern of dental replacement thought to be unique. The apparent primitive therian pattern is two functional generations of teeth at the incisor, canine, and premolar loci, and a series of molar teeth, which by de®nition are never replaced. In marsupials, the incisor, canine, and ®rst and second premolar positions possess only a single func- tional generation. Recently this pattern of dental development has been hypothesized to be a syn- apomorphy of metatherians, and has been used to diagnose taxa in the fossil record. Further, the suppression of the ®rst generation of teeth has been linked to the marsupial mode of reproduction, through the mechanical suppression of odontogenesis during the period of ®xation of marsupials, and has been used to reconstruct the mode of reproduction of fossil organisms. Here we show that dental development occurs throughout the period of ®xation; therefore, the hypothesis that odon- togenesis is mechanically suppressed during this period is refuted. Further, we present compar- ative data on dental replacement in eutherians and demonstrate that suppression of tooth replace- ment is fairly common in diverse groups of placental mammals. We conclude that reproductive mode is neither a necessary nor a suf®cient explanation for the loss of tooth replacement in mar- supials. We explore possible alternative explanations for the loss of replacement in therians, but we argue that no single hypothesis is adequate to explain the full range of observed patterns. Alexander F. H. van Nievelt.* Department of Biological Anthropology and Anatomy, Box 90383, Duke University, Durham, North Carolina 27708 Kathleen K. Smith. Department of Biology, Box 90338, Duke University, Durham, North Carolina 27708. E-mail: [email protected] *Present address: Department of Biology, Box 90338, Duke University, Durham, North Carolina 27708. E-mail: [email protected] Accepted: 28 June 2004 Introduction pials reveals that vestigial ®rst generation (``milk'') incisors and canines are found in Tooth replacement in marsupial mammals several marsupial families, including Macro- differs from the condition generally believed podidae (in Macropus giganteus Kirkpatrick to characterize eutherian mammals. In euthe- 1978), Dasyuridae (in Dasyurus quoll Luckett rian mammals, there are typically two gener- 1989, and Sminthopsis virginiae Luckett and ations of incisors, canines, and most (or all) Woolley 1996), and Peramelidae (in Perameles premolars. In contrast, marsupials typically Wilson and Hill 1897). Thus far, most detailed have two generations of functional teeth at studies of dental development of didelphids, only one locus in each jaw quadrant, the last generally considered to have the most primi- premolar (P3) (®rst noted by Flower [1867]). tive dentition of extant marsupials, have Some derived dasyurids have eliminated re- failed to document incontrovertible evidence placement altogether. By de®nition, molar of a vestigial ®rst tooth generation. These teeth are represented by only a single gener- studies include several of Didelphis (KuÈ kenthal ation in both clades. Studies of dental replace- 1891; RoÈse 1892; Berkovitz 1978). However, ment in dryolestid eupantotheres (Martin Kozawa et al. (1998) claimed that Monodelphis 1997), a Mesozoic taxon that represents an domestica has a much more complex set of suc- outgroup to the Theria (Metatheria 1 Euthe- cessional homologies, with vestigial ®rst gen- ria), show that the pattern commonly seen in eration incisors at two loci and vestigial sec- living eutherians is the primitive one. ond generation teeth at three. Our own studies Close examination of the development of of a more complete series of M. domestica the anterior dentition in a variety of marsu- found no evidence for vestigial teeth. The ves- q 2005 The Paleontological Society. All rights reserved. 0094-8373/05/3102-0009/$1.00 REDUCED TOOTH REPLACEMENT IN MAMMALS 325 tigial anterior teeth seen in the Australian felli et al. (1996) argued that the marsupial families are interpreted as evidence for the tooth replacement pattern is of great antiquity loss of a ®rst generation of functional anterior and is found in some of the earliest marsupi- teeth present in the ancestry of marsupials. als. Cifelli and Muizon (1998) provide further Thus, relative to the primitive therian condi- evidence of the early appearance of the mar- tion, marsupials have a distinctive, derived supial dental replacement pattern in Creta- pattern of reduced dental replacement. ceous and Paleocene marsupials. They de- Several workers have tied this derived pat- scribed juvenile specimens of ®ve marsupial tern of dental replacement to the marsupial species from the Paleocene of South America mode of reproduction and development. Wil- and found no evidence for tooth replacement son and Hill (1897: p. 554) stated, ``We believe anterior to the last premolar locus. They con- that we are justi®ed in seeking for the cause of cluded that ``(t)he pattern of postcanine erup- the almost total suppression of the milk-teeth tion and replacement in the fossils is remark- in front of the last premolar, in the modi®ed ably similar to that of recent didelphids'' (Ci- condition of the mouth in the marsupial felli and Muizon 1998: p. 218). Furthermore, young in consequence of its peculiar adapta- they emphasized the systematic signi®cance tion to the sucking function.'' Winge (1941) of that pattern: ``Given the problematic nature came to a similar conclusion, as did Ziegler of most dental and even basicranial features (1971b: p. 240) who stated, ``The selective fac- de®ning Marsupialia (Muizon 1994), we sug- tors contributing to the suppression of the gest that the most robust test for assessing del- complete metatherian antemolar milk denti- tatheroidean relationships will be provided by tion except dP4 to a vestigial state are not evidence from tooth replacement. In fact, in known for certain, although, as has often been spite of the dif®culties of observing it on fos- suggested, the phenomenon is very likely re- sils, it is probable that the pattern of tooth re- lated to the peculiar method of attachment of placement and eruption of living marsupials the newborn young to the nipple in the moth- represent one of the best metatherian syna- er's pouch.'' pomorphies (p. 218).'' Rougier et al. (1998) More recently Luckett (1993: p. 195) also demonstrated that the marsupial dental re- claimed a link between the highly modi®ed placement pattern is present in Deltatheridium, dental development pattern and reproductive a deltatheroidean from the Late Cretaceous of mode in marsupials. ``(T)his modi®ed anteri- Mongolia. or dentition is correlated with the prolonged In addition to using this character in phy- lactation period of marsupials, especially with logeny reconstruction, paleontologists have the `period of ®xation' (Hill and O'Donoghue used the hypothesized link between the de- 1913), during which the suckling young is rived marsupial tooth development pattern continuously attached to the nipple for a and the distinct marsupial reproductive pat- lengthy period of time. The well developed tern to make inferences about the reproduc- tongue and nipple ®ll the oral cavity during tive patterns of fossil taxa. Cifelli et al. (1996: this period, and the continued pressure exert- p. 717) argued on the basis of observing the ed by these structures probably has an effect marsupial tooth replacement pattern in Alpha- on the developing tooth germs underlying the don ``that at least some reproductive speciali- oral epithelium.'' zations of marsupials, including nipple ®xa- Because aspects of dental development and tion, were probably established during the replacement can be identi®ed and studied in Mesozoic, earlier than previously suggested.'' fossils, the evolution of various conditions Martin (1997) reported that dryolestid eupan- may be documented. Cifelli et al. (1996) de- totheres from the Jurassic show unreduced scribed an immature specimen of Alphadon tooth replacement (i.e., a pattern similar to eu- from the Late Cretaceous of North America therians and different from marsupials) and that seems to show a dental replacement pat- concluded, ``Therefore, a marsupial reproduc- tern similar to that seen in living dasyurids or tive pattern most probably can be ruled out for didelphids. On the basis of this specimen, Ci- Late Jurassic `eupantotheres' with a plesio- 326 A. F. H. VAN NIEVELT AND KATHLEEN K. SMITH morphous mode of tooth replacement'' (p. 15). are referred to neither subscript nor super- Rougier et al. (1998: p. 462) also commented script is used (e.g., P3). The homology of the on the likely reproductive mode of deltather- teeth in the marsupial dentition has been con- oideans. ``If the metatherian patterns of skull troversial and there are several alternate no- development, tooth replacement and repro- menclatures (Flower 1867; Thomas 1887; Zie- duction are correlated, deltatheroideans may gler 1971b; Archer 1978; Luckett 1993). As will already have possessed the basic marsupial be seen below, in M. domestica, we were unable reproductive pattern.'' to detect a vestigial ®rst generation of teeth. In this paper, we report observations on We hypothesize that the basic pattern of den- dental development and tooth eruption in the tal replacement is homologous in all marsu- didelphid Monodelphis domestica. We also pre- pials, and we have followed the ontogeneti- sent comparative data on tooth replacement in cally based system of Luckett (1993). There- other mammals, both marsupial and placen- fore, following Luckett, we designate the teeth tal. We address the two major predictions of found in the adult dentition as follows: The the hypothesis discussed above. First, we ex- upper incisors are designated I1 to I5, the low- amine the progress of dental development ers I1 to I4 (from mesial to distal). Canines are 1 during the period of ®xation to see if odon- designated C and C1.
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