Observations on the vomeronasal organ of prenatal Tarsius bancanus borneanus with implications for ancestral morphology

Abstract

Adult primates have at least five known phenotypes of vomeronasal organ (VNO), ranging from the typical morphology seen in most other mammals to complete absence. With such morphological disparity, the phylogenetic value and any inferences on ancestral VNO morphology of the primate VNO are left uncertain. The present study investigated the VNO of embryonic and fetal Tarsius bancanus borneanus (n = 4) in comparison with prenatal specimens from four other species of primates in an effort to clarify adult morphological variations. In all except one of the fetal primates, the VNO communicated to the nasopalatine duct. One exception occurred in the largest fetal Tarsius (25 mm crown-rump length), in which the VNO communicated with the nasal cavity alone. The vomeronasal neuroepithelium was well differentiated from a thinner, non-sensory epithelium in all Tarsius and New World monkeys studied, as well as late embryonic and fetal Microcebus myoxinus. In anterior sections, this neuroepithelium was found in a more superior location in Tarsius and New World monkeys compared with Microcebus myoxinus. In all primates, masses of cell bodies were found superior to the VNO, intermingled with nerve fibres. These morphologically resembled luteinizing hormone-releasing hormone neurons described in other mammals, including humans, suggesting that a primitive association of these neurons with the VNO may exist in all primate taxa. The present study revealed that prenatal similarities exist in Tarsius and New World primates in VNO epithelial morphology. However, these are transient stages of morphology. If tarsiers and anthropoids do represent a clade (Haplorhini), then the atypical morphology seen in adult tarsiers and New World monkeys probably represents the adult VNO morphology of a haplorhine common ancestor.

Fig. 1

In one of the 20-mm CRL Tarsius, a groove (*) was seen that connected posteriorly with the intersection of the vomeronasal duct (open arrows) and nasopalatine duct (NPD, a,b). The largest fetal tarsier (25 mm CRL) had a fused vomeronasal duct that did not communicate with the nasopalatine duct (d), which was found more anteriorly (c). In addition, this specimen had a more superiorly positioned epithelial tube (*), located just above the vomeronasal cartilages (VNC, c,d). Microcebus had an embryonic VNO opening (open arrow) into the nasal cavity alone (e, 9-mm CRL embryo), but in fetuses (f, 33-mm CRL) the VNO opened directly into the nasopalatine duct. NS = nasal septum. Scale bars: a–d = 400 µm; e = 200 µm; f = 100 µm.

Fig. 2

Organization of the vomeronasal organ epithelium at the 25th (top row), 50th (middle row) and 75th (bottom row) percentiles of VNO length. The left column (a–c) shows a 25-mm CRL Tarsius bancanus, the middle column (d–f) shows a 25-mm CRL Saimiri sciureus, and the right column (g–i) shows a 15-mm CRL Microcebus myoxinus. Scale bar = 100 µm.

Fig. 3

(a) An 8-mm CRL Microcebus myoxinus, showing the openings of the vomeronasal organ (VNO) with nerves and masses of paravomeronasal ganglia (open arrows); the similar cells were visible in association with the VNO itself in 9-mm embryos (b) and larger embryos (c, 13-mm CRL) of Microcebus. Note the mediolateral differentiation in the 13-mm CRL embryo, with a pronounced neuroepithelium medially (*, c). Anteriorly, the Saimiri sciureus embryo (d) had a more superiorly positioned neuroepithelium (*) and masses of paravomeronasal ganglia. (e) A 13-mm CRL embryonic tarsier had a similarly positioned neuroepithelium. A 20-mm CRL tarsier (f–j) had numerous neuronal cell bodies and ganglia visible in association with nerves (NN) anterior to the VNO (f and inset, g). (h) The posterior half of the VNO in the 20-mm fetal tarsier revealed a pronounced neuroepithelium (*) medially, with a thin lateral non-sensory epithelium (NSE, i). Ganglia and cells of neuroblastic appearance were visible superior to the VNO (open arrow, h, and enlarged in j). NS = nasal septum, VNC = vomeronasal cartilage. Scale bars: a,d = 150 µm; b,c,e,j = 100 µm; f = 500 µm; g,i = 50 µm; h = 200 µm.