ARTÍCULO
Supernumerary teeth in Necromys lasiurus (Rodentia, Cricetidae): the first record in sigmodontinae
Gustavo Simões Libardi* and Alexandre Reis Percequillo
Departamento de Ciências Biológicas, Escola Superior de Agricultura "Luiz de Queiroz". Universidade de São Paulo, Av. Pádua Dias, 11, Caixa Postal 9, 13418-900, Piracicaba, São Paulo, Brazil [correspondence: Alexandre Percequillo <percequillo@usp.br>].
* Present address: Unidad de Investigación Diversidad, Sistemática y Evolución, Centro Nacional Patagónico, Boulevard Almirante Brown 2915, Casilla de Correo 128, 9120 Puerto Madryn, Chubut, Argentina.
Recibido 18 abril 2014.
Aceptado 3 julio 2014.
Editor asociado: UFJ Pardiñas
ABSTRACT.
There are several kinds of anomalies related to the teeth reported in mammals, and one of them is known as supernumerary teeth and is commonly noticed in the literature, being reported in nearly all orders of mammals. Here, we report the occurrence of supernumerary molars in the sigmodontine rodent Necromys lasiurus, a common and widespread small rodent of tribe Akodontini. In order to assess the patterns of morphometric variation of N. lasiurus in eastern South America, we examined the skulls of 1763 specimens. The supernumerary molars were found in 2 individuals, which represent a frequency of 0.11%. The origin of supernumerary teeth started a long discussion on tooth homology, whether this anomaly is a result of heredity, a mutation or an atavism. Based on the morphologies presented by the extra teeth encountered in N. lasiurus and on the evidences and hypothesis available in the literature, we consider that the presence of these supernumerary molars in one of the studied animals could be considered an atavism, and we also consider the extra molar presented by the other specimen is a malformation, due to some kind of random process occurred in later stages of the development of distal dental germ. To the best of our knowledge, this represents the first record of supernumerary molars in the subfamily Sigmodontinae and one of the few known cases in rodents.
RESUMO.
Dentes supranumerários em Necromys lasiurus (Rodentia, Cricetidae): primeiro registro em Sigmodontinae.
Diversos tipos de anomalias dentárias já foram descritas para mamíferos e uma delas é conhecida como dente supranumerário comumente reportada na literatura para quase todas as ordens de mamíferos. No presente trabalho apresentamos a ocorrência de molares extras em Necromys lasiurus, uma espécie de pequeno roedor sigmodontíneo comum e amplamente distribuído, membro da tribo Akodontini. Durante o levantamento de dados para avaliação morfométrica da variação da espécie no leste da América do Sul, foram examinados os crânios de 1763 espécimes. Os dentes supranumerários foram encontrados em dois indivíduos, representando 0.11% da amostra investigada. A ocorrência dos dentes supranumerários há muito tempo levanta questões acerca da homologia dentária, das mutações e dos atavismos que podem estar relacionados à origem desta anomalia. Baseados na morfologia apresentada pelos molares extra numerários de N. lasiurus, nós consideramos que a presença dos mesmos em um dos espécimes é um atavismo, e no outro, tratase de uma malformação devido a um processo de origem tardia no desenvolvimento das gemas dentárias. Com base em nosso conhecimento de outras espécies e em toda a revisão bibliográfica, a ocorrência dos dentes supranumerários em N. lasiurus tratase dos primeiros registros da anomalia para a subfamília Sigmodontinae e um dos poucos já registrados para a ordem Rodentia.
Key words: Akodontini; Brazil; Development; Extra teeth; Molar; Premolar.
Palavras-chave: Akodontini; Brasil; Dentes extras; Desenvolvimento; Molar; Prémolar.
INTRODUCTION
There are several kinds of anomalies related to the teeth reported in mammals captured in nature, such as congenital agenesis (Smith et al., 1977; Beaver et al., 1981; Stewart and Stewart, 1987); irregular placement (Heran 1970; Beaver et al., 1981; Smith et al., 1977); divided tooth and other crown anomalies (Van Gelder and McLaughlin, 1961; Wolsan, 1983; Stewart and Stewart, 1987; Smith et al., 1977; Angelici and Luiselli, 1999); post trauma repair (Graipel et al., 1997), and many others (see Smith et al., 1977, and Winer et al., 2012, for more examples).
One of them is known as supernumerary teeth and is commonly noticed in the literature, being reported in nearly all orders of mammals, mostly in Didelphimorphia (Takahashi, 1974; Moraes et al., 2001), Pilosa (McAfee and Naples, 2012), Primates (Berkovitz and Musgrave, 1971; Wolsan, 1984; see also Smith et al., 1977), Soricomorpha (Hooper, 1946; Feldhamer and Stober, 1993), Chiroptera (Ramírez-Pulido and Müdespacher, 1987; Rui and Drehmer, 2004), Carnivora (Paradiso, 1966; Beaver et al., 1981; Stewart and Stewart, 1987; Drehmer and Ferigolo, 1996; Graipel et al., 1997; Andersone and Ozolins, 2000; Peters et al., 2013; Winer et al., 2012), Artiodactyla (Knowlton and Glazener, 1965; Chaplin and Atkinson, 1968; Pekelharing, 1968; Zurowski, 1970; Steele and Parama, 1979; Natsume et al., 2005), and Rodentia, both extant (Johnson, 1952; Krutzsch, 1953; Dearden, 1954; Harris and Fleharty, 1962; Sheppe, 1964; Sofaer and Shaw, 1971; Goodwin, 1998; Angelici and Luiselli, 1999) and extinct (Goodwin, 1998; Arnal and Vucetich, 2011). The occurrence of supernumerary teeth in rodents is generally related to extra molars placed posteriorly the toothrow (Johnson, 1952; Sofaer and Shaw, 1971) and is comparatively rarer in natural populations other than Carnivora (Wolsan, 1984), which is the group with higher number of documented cases in literature.
In the present contribution we report the occurrence of supernumerary molars in the sigmodontine rodent Necromys lasiurus (Lund, 1840). This species is a common and widespread small rodent of tribe Akodontini that inhabits preferentially open vegetation areas, on the Caatinga, Cerrado, and Chaco biomes, as well as grasslands and shrublands that occur in the central portion of South America (Musser and Carleton, 2005). However, being an extremely versatile rodent, this species is also found in transitional areas, margins of forests and secondary forests, as well as anthropogenic habitats, like plantations and pastures (Mares et al., 1986; Henriques et al., 1997; Pardiñas et al., in press).
MATERIALS AND METHODS
In order to assess the patterns of morphometric variation of N. lasiurus in Brazil, we examined the skulls of 1763 specimens deposited in the following Brazilian collections: Universidade Estadual do Mato Grosso, Cuiabá (UFMT); Universidade Federal de Lavras, Lavras (CMUFLA); Universidade Federal de Minas Gerais, Belo Horizonte (UFMG); Museu de Ciências Naturais, Pontíficia Universidade Católica, Belo Horizonte (MCN-M); Museu de História Natural Capão da Imbuia, Curitiba (MHNCI); Museu Nacional da Universidade Federal do Rio de Janeiro, Rio de Janeiro (MN); Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP); Museu de Zoologia da Universidade Estadual de Campinas (ZUEC); and Museu de Ciências Naturais, Universidade Luterana do Brasil, Canoas (MCNU).
The nomenclature employed for dental morphology follows Reig (1977) and dental measurements (length of upper molar series) are accordingly to Percequillo et al. (2008). For age determination we followed Libardi (2013) and Voss (1991), and recognized 5 classes defined by tooth eruption and wear of major cusps, lophs and flexi.
In order to compare the length of the supernumerary toothrows to regular series presented by the same individuals and by other specimens, we calculated the descriptive statistics (mean, standard deviation, minimum and maximum values) and designed a boxplot graph, using the descriptive information of length of toothrow from individuals with supernumerary molars and from some selected samples. We gathered individuals of the same age class and same or nearby localities of the specimens with extra teeth to avoid the effects of other variation factors that could mislead the interpretation of the comparisons of the toothrow length, once the species seems to present age variation and geographic structure in toothrow and other skull dimensions, as highlighted by Macêdo and Mares (1987) and Libardi (2013). A list of the specimens employed in comparisons from the same and nearby localities where the individuals with supernumerary teeth were found is provided in the Appendix.
We calculated the frequency of occurrence of extra teeth in N. lasiurus by simply dividing the number of specimens captured in nature presenting the oral feature by the total number of analyzed individuals, and therefore multiplying by 100 in order to obtain a value expressed in percentage. We also provide a list of frequencies and extra teeth positions on several mammalian orders, including Rodentia, in order to compare our findings to some described throughout in past decades for mammals. Some orders were not assessed due to the few information available or due to the unique nature of their dentition, as Cingulata and Cetacea.
We expressed the value of the frequencies of the revised literature, when available, in percentage as it appears in the article; when it was not directly informed, we applied here the same method as to N. lasiurus; when no information on total number of analyzed individuals were available, we did not calculate any frequency, providing then a "?" symbol.
The positions of extra teeth in each mammalian species revised are based on the accuracy of the information of the descriptions and figures provided by the authors. It is important to emphasize that we used the same nomenclature employed for the mammalian species in the articles.
RESULTS
The supernumerary molars were found in 2 individuals out from a sampling of 1763 specimens of N. lasiurus, which represent a frequency of 0.11%. The specimen MN 44035 is an adult male age class 2, collected at Gleba José Nani (also Bairro Santa Luzia), Caçapava municipality, São Paulo state, Brazil (23°06'S, 47°36'W; see Weksler and Bonvicino, 2005), collected on May 7, 1973, during the field survey performed by the Campaign for Combating Schistosomiasis (CACEsq). The MN 44035 present 2 extra teeth, one at each upper toothrow, at the distal end of dental series (Figs. 1A and 1B). The extra teeth are molar-like, covered by enamel, present reduced wear and no dentine exposition, peg-like, with no lophs or flexi discernible on molar topography and completely aligned with the other molars of both toothrows; these supernumerary teeth exhibit the crown positioned slightly higher than the remaining teeth (Fig. 2A). All remaining teeth show reduced wear and present a typical configuration of other specimens of N. lasiurus from other localities observed with similar molar wear. The total length of the upper right toothrow is 5.29 mm (ca. 4.60 mm without the extra molar) and of the upper left toothrow is 5.25 mm (ca. 4.48 mm without the extra molar). The mandible does not show any supernumerary teeth and all molars present the typical morphology. Both upper and lower series occluded perfectly, with the supernumerary teeth being positioned posteriorly to the lower third molars. It was also noted that the presence of the extra teeth did not cause any kind of injury on the other teeth, as well as no evidence of excessive wear on the posterior surface of the lower third molar, or even on the hard palate.
Fig. 1. Necromys lasiurus: Occlusal view of the left upper toothrow of specimens MN 44035 (A, right; B, left), from Caçapava, São Paulo; and UFMT 839 (C, right; D, left), from Rio Juruena, Mato Grosso, presenting the supernumerary molars, distally to other tooth; length of molar series provided in Table 1. Scale = 1 mm.
Fig. 2. Necromys lasiurus: Lingual lateral view of the upper left toothrow of specimens MN 44035, from Caçapava, São Paulo, and UFMT 839, from Rio Juruena, Mato Grosso, both presenting the supernumerary distal molars. It is possible to observe the occlusal surface of the extra teeth positioned above the surface of the other teeth; length of molar series provided in Table 1. Scale = 1 mm.
The individual UFMT 839 is an adult, age class 3, presents no information on sex, and was collected at Rio Juruena, Sapezal municipality, Mato Grosso state, Brazil (13º27'24"S, 59º00'07"W) on August 22, 2006. In this specimen, there is only 1 extra tooth in the left upper toothrow, also positioned at the distal end of this dental series (Figs. 1C and 1D). The extra tooth is molar-like, enameled, with some wear on occlusal surface and small dentine exposition, with no lophs or flexi visible and its crown is positioned slightly higher than the remaining of molar series (Fig. 2B). The extra to oth is erupted transversally towards the labial direction, and the entire toothrow is unaligned, producing no precise occlusion of the upper and lower molar series. Moreover, the alveolus of the third tooth and the supernumerary tooth are confluent and very wide, probably with some maxillary bone reabsorption. The lack of alignment of the toothrow, especially the supernumerary tooth, suggests that there could have been some injury to the gum and the roots during the chewing movements. The total length of the upper right toothrow is 4.56 mm and of the upper left toothrow is 5.17 mm (ca. 4.56 mm without the extra molar).
We compared the length of the molar series of the specimens MN 44035 and UFMT 839 to the toothrow length of syntopic individuals, from Caçapava and Rio Juruena with the same molar wear (Table 1 and Fig. 3). Due to the existence of only 1 specimen with normal dentition from Caçapava, we decided to generate a boxplot considering also the individuals from Estação Biológica de Boracéia, Salesópolis, São Paulo state, the best available sample in the region, and which is nearly 60 km to the south of Caçapava. Table 1 shows the results of the descriptive statistics: in all comparisons, the molar series with extra molars are consistently longer than regular molar series with three teeth. It is also interesting to notice that the measurements of the right normal series of specimen UFMT 839 and of the molar series of MN 44035 excluding the extra teeth are within the limits of variation of samples employed in comparisons.
Table 1. Descriptive statistics of the toothrow lengths of the samples of Necromys lasiurus which presented normal molars and of the molar rows of the individuals with supernumerary molars. The "*" indicates absolute values; N = sampling number; SD = standard deviation. All measurements are provided in millimiters.
Fig. 3. Individual values and box-plot of the length of the upper toothrows of MN 44035 and UFMT 839 and of individuals from the same (Caçapava and Rio Juruena) and near localities (Boracéia) without supranumerary teeth for Necromys lasiurus. The black dashes represent the individual values for individual specimens or the mean value for samples; the gray boxes represent the quartiles and the whiskers represent the maximum and minimum values of each sample.
DISCUSSION
The frequency of occurrence of the supernumerary teeth in N. lasiurus is low (0.11%), and we are confident that this represents information for the species (and not for a restricted sample), since the sample we studied is quite robust and presents specimens throughout the distribution of the species. It is noteworthy that this frequency is smaller than those frequencies exhibited by many other species: apparently in felids, which experienced drastic reductions on the number of post canine teeth, the expression of supernumerary teeth (especially molars) is more common than in other groups; in marsupials, which present complete dentitions with all possible teeth, the frequency is similar to that observed in N. lasiurus. The position of the extra teeth found in N. lasiurus is also congruent to the other cases in Rodentia (Table 2).
Table 2. Frequencies and kinds of extra teeth found in other mammalian taxa disponible in literature. The superscripted and subscripted numbers indicate the upper and lower teeth, respectively, when it was posible to determine their position precisely; n.c. = not comparable.
The origin of supernumerary teeth started a long discussion on tooth homology (Wolsan, 1984; Peterkova et al., 2006; see also Hinton, 1923 for former hypothesis), whether this anomaly is a result of heredity, a mutation or an atavism. The present dentition of muroid rodents is currently understood as a result of the loss of the canines, incisors and premolars, and only the molars and a pair of incisors remained (see Peterkova et al., 2006). Nevertheless, the occurrence of extra molars posterior to the current third molar, raised the hypothesis that the first molar could be a modified premolar and the dental formula of rodents would be 1 incisor, 1 premolar and 2 molars (premolar theory): therefore, the extra tooth would represent the expression of a suppressed third molar during development (Johnson, 1952; Sheppe, 1964). Based on the timing of developmental patterns of the cheekteeth of embryos of Mus musculus in comparison to the timing of human embryos, Peterkova et al. (2006) suggest that the rodent M1, M2 and M3 teeth could correspond to the human dP3, dP4 and M1, respectively. This configuration would explain the presence of supernumerary teeth in the posteriormost portion of the maxillary.
The supernumerary teeth found in MN 44035 are nearly conventional, being aligned and symmetrically bilateral. This configuration could result of heredity (see Sofaer and Shaw, 1971), once the symmetry in position and morphology between the extra teeth suggests that their formation occurred before the differentiation of both sides of maxillae, so resulting from a genetically inducted formation process of the tooth germ instead of developmental interferences, mutation or random split of one single germ (Wolsan, 1984; Goodwin, 1998). Although the possibility of these extra teeth to have hereditary origins, we did not find any other N. lasiurus specimen from Caçapava and nearby localities, which counted 75 individuals (Appendix). This information, together with all the records we gathered from available bibliography (Table 2), is in agreement with the statement that supernumerary teeth are rare in natural populations of sigmodontine rodents.
In the other hand, the asymmetric eruption of the extra molar and the lack of alignment of toothrow found in UFMT 839 seem to be related to other random developmental or mutation processes (Wolsan, 1984:131; Goodwin, 1998). The occurrence of abnormal morphologies and unusual patterns of eruption is far more common in literature than the configuration observed in specimen MN 44035 (e. g., Harris and Fleharty, 1962; Smith et al., 1977; Graipel et al., 1997; Andersone and Ozolins, 2000; Winer et al., 2012).
Based on the morphologies presented by the extra teeth encountered in N. lasiurus and on the evidences and hypothesis available in the literature, we consider more likely that the supernumerary molars of specimen MN 44035 is in fact a result of genetic heredity (based on Sofaer and Shaw, 1971), once its alignment with the molar series, which is also well developed, suggests they originated at the earlier stages of embryonic development. Thus, if the hypothesis advocated by Johnson (1952) and Peterkova et al. (2006), in which the present dentition of muroid rodents is composed by the dP3, dP4 and M1 of the basic eutherian dentition, are true, the presence of these supernumerary molars in this specimen of N. lasiurus could be considered an atavism, i.e., the reappearance of a lost ancestral character (Peterkova et al., 2006). We also consider that the extra molar presented by the specimen UFMT 839 is a malformation, due to some kind of stochastic process during later stages of development of the distal tooth germ (see Glasstone, 1952; Wolsan, 1984:131), rather than earlier developmental process like reported by Sofaer and Shaw (1971). We cannot hypothesize if in this case the origin of supernumerary tooth is related or not to any kind of atavism, and if it is related to the hypothesis proposed by Johnson (1952) or Peterkova et al. (2006).
As observed in other species of rodents (Table 2), the positions of supernumerary teeth in both N. lasiurus specimens are posterior to the "normal" molar series, and therefore if we accept the conventional hypothesis that rodent molars are M1, M2 and M3, these teeth would represent a "fourth molar" due to the origin of a new dental germ, an unlikely event. However, if we accept the hypothesis regarding the dental formula of rodents, composed by the dP3, dP4 and M1, as valid (Johnson, 1952; Peterkova et al., 2006), these extra teeth would be the M2. As such, their presence could be more likely explained and would adjust adequately to the recurrent expression of supernumerary teeth in the same position for the order Rodentia, in natural populations; experimental breeding revealed that this seems to be the tendency in Oryzomys palustris (Sofaer and Shaw, 1971). The fewer cases of occurrence of extra teeth in other positions reported for Rodentia (Goodwin, 1998:1166) are more difficult to relate to this pattern and also to atavistic origins, compared to the occurrence of the distal extra molars. Nevertheless, Rodrigues et al. (2011) have reported a special case of continuous dental replacement in the African molerat Heliophobius argenteocinereus (Rodentia: Bathyergidae), which is related to the supernumerary molars. As the authors claim, this kind of unique teeth replacement system, which occurs also only in the species of the manatee genus Trichechus and in the pygmy rock-wallaby Petrogale concinna, is a convergent mechanism which combines specific dental traits, as dental mesial drift, delayed eruption and the occurrence of supernumerary molars. In the H. argenteocinereus case, the supernumerary molars emerge in the distal portion of toothrows continuously and drift anteriorly as the frontal teeth are worn and atrophied and, subsequently, reabsorbed (see Rodrigues et al., 2011). Although it is difficult to determine the number of teeth, the occurrence of extra teeth agrees with the general pattern observed in Rodentia, with extra teeth emerging distally.
The occurrence of supernumerary teeth in N. lasiurus seems to be an odd event in the subfamily Sigmodontinae. Although one of the authors (ARP) personally analyzed nearly 7000 individuals of several species of the tribe Oryzomyini, no extra teeth were observed. U. F. J. Pardiñas (pers. comm.) reported to us the occurrence of extra molars in the same position and presenting similar morphology as presented the individual MN 44035, in a partial skull of Abrothrix olivacea (Sigmodontinae, Abrotrichini) found by D. Procopio in an owl pellet from Southern Patagonia. The only other records on literature are from experimental colonies of rice rats (Sofaer and Shaw, 1971).
CONCLUSIONS
To the best of our knowledge, this represents the first record of supernumerary molars in wild-caught specimens in the subfamily Sigmodontinae and one of the few known cases in rodents, and it is very likely that these teeth represent a vestigial structure. Considering the complex and poorly understood history of the evolutionary pathways on the origin and evolution of mammalian dentition, we hope that this contribution provide useful information on the knowledge of this important subject.
ACKNOWLEDGEMENTS
We are thankful to all curators and responsible staff of the collections visited, and especially to J. A. Oliveira and R. V. Rossi, curators of MN-UFRJ and UFMT, respectively, for providing us the material with extra teeth for detailed analysis. We are also grateful to Ulyses F. J. Pardiñas for sharing his information on extra teeth in genus Abrothrix. At last, we would like to acknowledge L. Soilbenzon and 2 anonymous reviewers for their suggestion for the improvement of this contribution. This work received financial support from CAPES and FAPESP (Process 09/16009-1).
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Specimens examined of genus Necromys employed in quantitative and qualitative comparisons in this study; the symbol * indicates that the specimen was used in the boxplot comparisions.
Caçapava (23º06'S; 45º43'W; Weksler and Bonvicino, 2005): MN 24193, 24194; also includes Gleba José Nani and José Nani, Bairro Sta. Luzia MN 44033*, 44035*.
Fazenda Mombaça, Pindamonhangaba (22º55'S; 45º27'W in Pindamonhangaba - IBGE): MN 44036.
Faz. Sto. Ângelo, Represa de Americana, Sumaré (22º49'S; 47º15'W in Sumaré - IBGE): MN 24187.
Guararema (23º25'S; 46º02'W; Weksler and Bonvicino, 2005): ZUEC 1402, 1410, 1414.
Ribeirão da Lagoa, Boracéia, Salesópolis (23º38'S; 45º52'W; Percequillo, 1998): MZUSP 10746, 10757, 10765*, 10766, 10770*, 10771*, 10815*, 10824, 10828*, 10831, 10832, 10834*, 10835*, 10836, 10837, 10840, 10842, 10844*, 10846, 10848, 10851, 10855, 10857*, 10861, 10862*, 10863*, 10865, 10867*, 10868*, 10877, 10879*, 10886, 10892*, 10893, 10894, 10897, 10899*, 10905, 10918*, 10919, 10920, 10927, 10945, 21196.
Rio Juruena, Sapezal (13º27'24"S, 59º00'07"W): UFMT 832*, 839*, 849*, 856*, 4012*.
São Luís do Paraitinga (23º13'S; 45º18'W in São Luís do Paraitinga - IBGE): ZUEC 2421, 2422, 2423, 2424, 2425.
Taubaté (23º01'S; 45º32'W in Taubaté - IBGE): ZUEC 1405, 1409, 1413; also includes Bairro do Barranco: MZUSP 11211, 11227; Faz. Antonio Taino (Foco 30): MN 24185; Gleba Paulo Japonês, Bairro Barranco: MN 44029, 44030, 44031, 44034, 44037, 44039, 44040, 44043, 44044, 44050, 60426.