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Ontogeny of the nasopalatine duct in primates
Article first published online: 8 AUG 2003
Copyright © 2003 Wiley-Liss, Inc.
The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology
Volume 274A, Issue 1, pages 862–869, September 2003
How to Cite
Shimp, K. L., Bhatnagar, K. P., Bonar, C. J. and Smith, T. D. (2003), Ontogeny of the nasopalatine duct in primates. Anat. Rec., 274A: 862–869. doi: 10.1002/ar.a.10101
- Issue published online: 8 AUG 2003
- Article first published online: 8 AUG 2003
- Manuscript Accepted: 9 APR 2003
- Manuscript Received: 18 JUL 2002
- College of Health and Human Services, Slippery Rock University
- Bluntschli collection;
- Microcebus murinus;
- Microcebus myoxinus;
- nasopalatine duct;
- vomeronasal organ
Ecological explanations have been put forward to account for the precocious or delayed development of patency in ducts leading to the vomeronasal organ (VNO) in certain mammals. Perinatal function may be related, in part, to the patency or fusion of the vomeronasal and nasopalatine (NPD) ducts. However, few studies have focused on NPD development in primates, which generally have a prolonged period of dependence during infancy. In this study we examined 24 prenatal primates and 13 neonatal primates, and a comparative sample of fetal mice and insectivores. In embryonic and early fetal Microcebus murinus, the NPD was completely fused, whereas in fetuses of later stages the duct was partially fused or completely patent. M. myoxinus of all stages demonstrated some degree of NPD fusion. In all other prenatal primates, the NPD was fused to some extent. Four prenatal insectivores (Tenrec ecaudatus) showed some degree of NPD fusion. In Mus musculus at 19 days gestation, the NPD was patent, although the anatomically separate VNO duct was fused. T. ecaudatus and most of the neonatal primates revealed complete NPD patency. An exception was Saguinus geoffroyi, which exhibited fusion of the NPD near the VNO opening. These observations may relate to differences in perinatal VNO function. The differences noted in our study suggest that M. murinus and M. myoxinus may differ in perinatal VNO functionality and perhaps in related behavior. Observations of neonatal primates suggest that NPD patency may be relatively common at birth and could serve other purposes in addition to being an access route for VNO stimuli. Anat Rec Part A 274A:862–869, 2003. © 2003 Wiley-Liss, Inc.
At the base of the nasal septum in most mammals, and other vertebrates, paired accessory olfactory organs called the vomeronasal organ (VNO) are found (Broom, 1897; Wysocki et al., 1985). It has been suggested that these organs are involved in intraspecific communication related to territorial and sexual behavior through the reception of pheromones (Wysocki, 1979; Aujard, 1997). Since the nasopalatine duct (NPD) connects the VNO to the oral and nasal cavities in many mammals, it is a route for stimulus access. However, the NPD is not patent, or open for stimulus transmission, at all stages of development. It is unclear why in some mammals (e.g., cats and rats) the duct is patent during early fetal development, whereas other mammals (e.g., mice) do not have patent vomeronasal ducts until after birth (Coppola et al., 1993; Coppola and Millar, 1994; Wöhrmann-Reppening and Barth-Müller, 1994).
Ecological explanations have been put forward to account for the precocious or delayed development of patency in ducts leading to the VNO, such as the NPD, during prenatal ontogeny in certain mammals. One interpretation is that more rapid ductal development facilitates a more autonomous life immediately after birth, and hence altricial mammals experience slower maturation (Wöhrmann-Reppening and Barth-Müller, 1994). It has also been suggested that chemosensory reception can occur in utero (Coppola and Millar, 1994; Schaal et al., 1998), although there are indications that mammals may vary in the rate of maturation of the VNO (Tarozzo et al., 1998; Oikawa et al., 2001; Malz et al., 2002). Whereas variations in methods and selection of species leaves the issue of perinatal VNO function unresolved, fusion of the NPD at birth can at least rule out stimulus access to this chemosensory system.
While attempts have been made to explicate the significance of VNO and NPD development to later behavior, no studies have examined a prenatal series of primates. Compared to many mammals, primates are dependent during infancy (Nicolson, 1984; Derrickson, 1992). On the other hand, certain special senses, such as chemosensation, are well developed at birth (Schaal et al., 1998; Steiner et al., 2001). Furthermore, the VNOs of primates appear to vary in their morphological maturity at birth, with strepsirhines generally showing a better-developed neuroepithelium than haplorhines (Smith et al., 2002). Thus, primates provide an interesting test for the hypothesis that the maturation of the ducts leading to the VNO is related to the degree of infant dependency (Wöhrmann-Reppening and Barth-Müller, 1994). The focus of the present study was to examine the degree of NPD patency at different stages of development in primates, in order to determine the timing of stimulus access to the VNO.
MATERIALS AND METHODS
Twenty-four serially sectioned embryos and fetuses (Table 1) and 13 neonatal primates from 14 genera were examined for the current study (Table 2). A comparative sample comprising representatives from the orders Rodentia and Insectivora was also examined. The histologically sectioned prenatal primate slides were obtained from the Bluntschli collection, Department of Mammology, American Museum of Natural History. Neonatal primate cadavers were acquired from the Duke University Primate Center and the Cleveland Metroparks Zoo. Fetal mice series were available from previously sectioned specimens (Smith, unpublished data). Excluding the Bluntschli collection, tissues were prepared in the research laboratory at the School of Physical Therapy, Slippery Rock University.
|Specimen number||Species||CRL (mm)||Nasopalatine duct region|
|M23||Microcebus myoxinus (pygmy mouse lemur)||9.0||NF||NF||NF|
|M71||M. murinus (gray mouse lemur)||11.0||NF||NF||NF|
|A11||Avahi laniger (wooly lemur)||39.0||/||X||/|
|P23||Alouatta spp. (howler monkey)||29.0||X||X||X|
|AJ3||Mus musculus (house mouse)||?(19 days gest.)||O||NA||O|
|AJ4||Mus musculus||?(19 days gest.)||O||NA||O|
|I33||Tenrec ecaudatus (Madagascar hedgehog)||20.0||X||X||X|
|Specimen number||Species||CRL (mm)||Nasopalatine duct region|
|P1690||Cheirogaleus medius (dwarf lemur)||61.54||O||O||O|
|P384||Mirza coquereli (Coquerel's dwarf lemur)||69.40||O||O||O|
|P3097||Galago moholi (Mohol's galago)||56.84||O||O||O|
|P3080||Galagoides demidoff (dwarf galago)||51.79||O||O||O|
|Em1||Eulemur mongoz (mongoose lemur)||?||O||O||O|
|P6778||Eulemur macao (black lemur)||101.58||O||O||O|
|Cg1||Colobus guereza (colobus monkey)||?||O||NA||O|
|SG3||Saguinus geoffroyi (Geoffroy's tamarin)||?||O||X||O|
|LR1||Leontopithecus rosalia (Golden lion tamarin)||95.32||O||O||O|
|I49||Tenrec ecaudatus (Madagascar hedgehog)||?||O||O||O|
The Bluntschli collection was assembled by Hans Bluntschli during the early 20th century, and includes primates and insectivores collected in Madagascar and South America. Specimens were serially sectioned at 8–40 μm in the transverse, frontal, and sagittal planes, and stained with hematoxylin-eosin or other stains. Included with the collection were specimen data cards indicating measures such as “total overall length,” which is equivalent to crown–rump length (CRL), based on archived photographs of embryos/fetuses. Selected specimens from the Bluntschli collection were initially examined by one of the authors (T.D.S.). Specimens representing the full CRL range of each species were examined when a complete series of the NPD and VNO could be clearly seen. All pertinent sections of the NPD, and every third to fifth section of the VNO were photographed using Pixera Visual Communication Suite 2.0 (Pixera Corporation, Los Gatos, CA) and an Olympus BX50 photomicroscope (Olympus, Melville, NY). Images were stored as tagged image format files (TIFFs), and all files containing the NPD region were examined by one of the authors (K.L.S.) in the School of Physical Therapy, Slippery Rock University.
In the specimens that were sectioned for the present study, an entire half head, including the nasal septum, was removed from perinatal primate cadavers that had been stored in 10% buffered formalin. The heads were decalcified in formic acid-sodium citrate solution. The tissues were then embedded in paraffin and serially sectioned in the coronal plane at 10–12 μm. Every fifth section was mounted on glass slides and alternately stained using the Gomori one-step trichrome procedure or hematoxylin-eosin. In the region of the NPD, intervening sections were mounted for examination. The sections were examined with a Leica photomicroscope or as TIFF files. To assess the complete fusion, partial fusion, and patency of the NPD, we divided it into palatal, middle, and nasal regions (Fig. 1; also see Smith et al. (2001a) for the NPD location in the sagittal plane). The criteria for partial fusion are given in Figure 1 for the entirety of the NPD. The criteria for patency and complete fusion are shown in Figure 2. The estimated age and CRL are shown in Table 1 for the prenatal species, and in Table 2 for the neonatal species.
There was a distinct difference in NPD prenatal development between the two prenatal species of mouse lemurs (Fig. 2). In Microcebus myoxinus, 9-mm embryos had not yet formed the NPD. All fetuses of 12–31 mm exhibited a completely or partially fused NPD in the palatal, middle, and nasal areas (Figs. 2 and 3). One of the two 32-mm M. myoxinus had a patent NPD in the lower region. While M. murinus with a CRL of 11 or 16 mm either had not yet developed an NPD or maintained a completely fused one, those with a CRL of 28.5–37 mm exhibited patency or partial fusion in the three previously determined regions (Table 1). A notable difference was seen between M. murinus and M. myoxinus regarding the CRL at which communication to the nasal cavity vs. the NPD was seen. In M. murinus, the VNO opened at the level of the nasal cavity in an 11-mm embryo, whereas this communication was seen at 9-mm CRL in M. myoxinus (Fig. 2a and b). In larger specimens (≥16 mm in M. murinus, and ≥12 mm in M. myoxinus), the VNO opened directly into the NPD (Fig. 2c). In the majority of other prenatal primates, the middle and nasal portions of the NPD were completely fused, with the exception of Avahi laniger (Fig. 4a), which possessed a partially fused nasal portion. The development of the palatal area of the NPD varied among the primates, showing complete fusion in Avahi laniger and Aloutta sp. (Fig. 4b), partial fusion in Saimiri sciureus (Fig. 4c and d), and patency in Aotus vociferans.
Three prenatal insectivores (Tenrec ecaudatus (CRL = 20–23 mm)) had completely fused NPDs in the three regions, and one (CRL = 23.5 mm) showed partial fusion and patency in the palatal and nasal area, respectively. In Mus musculus at 19 days gestation, the NPD was patent, although the duct to the VNO was completely fused (in agreement with Coppola et al. (1993)). Examination of a variety of neonatal primates (including Cheirogaleus medius, Mirza coquereli (Fig. 5a), Galago moholi, Galagoides demidoff, Eulemur mongoz, Colobus guereza, Leontopithecus rosalia (Fig. 5b and c)) and one insectivore (T. ecaudatus; Fig. 5f) revealed patency in all sections of the NPD (Fig. 5). The only exceptions were Saguinus geoffroyi (Fig. 5d and e), which exhibited fusion of the middle portion, and C. guereza, for which analysis of the middle portion was not applicable due to absence of the VNO.
Considering the anatomical position of the NPD in many primates, the degree of its patency dictates the potential for stimulus access to the VNO. Our study revealed differences (patency vs. fusion) in the NPD among prenatal primates (Figs. 3 and 4), whereas the NPD was patent in most neonates examined. Since not all mammals have the same degree of NPD patency near the time of birth, it has also been hypothesized that mammals that undergo precocious NPD development (i.e., earlier patency) are likely to be able to lead an autonomous life more quickly (Wöhrmann-Reppening and Barth-Müller, 1994). As mammals with highly dependent infants and (usually) patent NPDs, primates appear to contradict this view. It should be noted that Wöhrmann-Reppening and Barth-Müller's (1994) hypothesis specifically focuses on prenatal events pertaining to the juncture of the NPD and VNO duct (see Smith and Bhatnagar (2000) for further details on this development in prenatal mouse lemurs). Previous studies (Coppola et al., 1993; Coppola and Millar, 1994), as well as the current results, indicate that patency of the communication of the VNO with the nasal cavity (directly or indirectly via the NPD) may occur prenatally in some mammals or perinatally in others, regardless of the precociality/atriciality of the infants.
Schaal et al. (1998, 2001) proposed that prenatal experiences with chemical stimuli contribute to the canalization of sensory and motivational organization after birth. The timing of VNO ductal patency during gestation has been shown to vary among rodents (Coppola et al., 1993; Coppola and Millar, 1994); thus, the time at which VNO receptors may encounter stimuli differs. Interestingly, mice show evidence of prenatal differentiation of VNO receptors (Tarozzo et al., 1998) before the VNO duct is patent. In the present study, S. geoffroyi was the only primate that exhibited fused NPDs at birth. Specifically, the duct remained fused near its communication with the VNO. Clearly, the timing of NPD patency differs among callitrichids, and further examinations of more taxa will reveal how much variation exists. At present, it is interesting to note that the species with later patency of the NPD (S. geoffroyi), appeared to have less sensory epithelium in the VNO at birth (Smith et al., 2002, HB:2003; unpublished data).
It is possible that NPD patency is significant for reasons other than VNO function. Near-term mice and a neonatal insectivore showed similarities in NPD patency, regardless of whether the NPD and VNO communicated in the species. Similar to our findings on C. guereza, Zingeser (1984) and Maier (1997) showed that the NPD exhibits early patency in other catarrhine primates where no communication between NPD and VNO exists. Likewise, in bats, which also show a great deal of variability in VNO development, open and well developed NPDs have been reported in groups lacking the VNO, such as in the families Pteropodidae, Vespertilionidae, and Natalidae (Bhatnagar, 1980). Other variations have also been reported. For example, in Macrotus a VNO is present but the NPD is absent (Bhatnagar, 1980). Our findings suggest that NPD patency may be common in primates at birth. Conversely, in prenatal stages the NPD exhibits fusion for at least part of development.
Since ductal patency occurs at different stages even for two closely related Microcebus species (Figs. 2 and 3), it is possible that VNO chemoreception begins at different stages of development. However, little information is available regarding ecological and behavioral differences among different species of Microcebus to provide a context for such differences. Furthermore, recent field and museum work has identified at least one, and as many as six, new species of Microcebus (Rasoloarison et al., 2000; Schwab, 2000). There is no doubt that Bluntschli did indeed collect two distinct species of Microcebus. Developmental aspects of the VNO are commonly used to stage embryos (Bossy, 1980). The two species of Microcebus examined in the present study clearly had distinct body sizes relative to the timing of VNO development (Fig. 2). Provided the two species of Microcebus are identical to those examined by Schwab (2000), it is interesting that in a species reported to have a more solitary lifestyle (M. myoxinus), the NPD becomes patent later in development (Schwab, 2000). In contrast, there is a possibility that stimulus access to the VNO develops earlier in M. murinus, a species characterized by relatively large group sizes (Schwab, 2000). Nonetheless, these data provide evidence of a striking developmental difference between closely related species. The two species also have different prenatal lengths of the VNO; however, this may relate to body-size differences during growth (Smith et al., 2001b).
Primates present a dichotomy regarding the altricial–precocial spectrum (Starck and Ricklefs, 1998). Sensory organs in general are highly precocious at birth. However, infants are highly dependent on prenatal care (Nicolson, 1984; Derrickson, 1992). Considering these characteristics, our data conflict with the idea that precocious VNO function relates to early autonomy (Wöhrmann-Reppening and Barth-Müller, 1994). Some other behavior (e.g., social or familial interaction) may relate to the timing of NPD patency and stimulus access to the VNO. Alternately, NPD patency ultimately may prove relevant to functions other than access to VNO stimuli, or the timing of patency might relate more strongly to events during palatogenesis.
Experimental data indicate that VNO may function primarily in the perception of pheromones for intraspecific communication linked to territorial, aggressive, and sexual behaviors (Wysocki, 1979), and the VNO of adult M. murinus likely has such functions (Aujard, 1997). However, our data and those from other studies (Coppola et al., 1993; Coppola and Millar, 1994) reveal the possibility of a more precocious (perhaps even prenatal) VNO function in some species. Unfortunately, whether early social interactions (e.g., familial bonding and competition) are linked to VNO function is unclear. For example, it appears that some mammals do not depend on the VNO for certain perinatal interactions (Hudson and Distel, 1986; Coppola, 2001). Further studies may help explain the differences in the timing of NPD and VNO duct patency among different species.
The authors thank R. Randall and R.D.E. MacPhee of the Department of Mammalogy, AMNH, for arranging access to the Bluntschli collection. We also are grateful to P.M. Mikkelsen for allowing the use of her microscopic imaging system for examination of the series. This is Duke University Primate Center publication #731.
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