Toothcomb origins: Support for the grooming hypothesis

Debate over the original adaptive significance of the lemuriform toothcomb, whether it was principally a grooming organ or a scraper-feeding tool, currently hinges upon the functional morphology of the lower incisors and canines of lemurs and lorises, and the fossil adapids thought to be their ancestors or structural prototypes. We suggest that the morphology of the upper incisors and the oronasal complex of the latter, given the context of a more general theory of incisor evolution within the primates, exhibits preadaptive conditions foreshadowing the emergence of the toothcomb and also evidence of strepsirhine monophyly. We find in all underived lemuriforms and in most fossil adapids where the elements are known, a striking continuity in upper incisor form, including such derived features as an interincisal diastema, strong central incisor prong, low-crowned morphology and reduced premaxillary size. The pattern suggests a basic strepsirhine reduction in the functional significance of the anterior dentition in feeding and harvesting roles. These features may be related to a novel connection of the rhinarium with the vomeronasal organ via a sulcate pair of labial folds, which serves as a component of a specialized behavioral-physiological complex dealing with olfactory communication. Rather than being the anatomical nucleus of this system, the toothcomb may have been added secondarily in the lemuriform descendants of the preadapted adapids, possibly as a device to stimulate glandular secretion of pheromones by direct pressure, and to simultaneously distribute odorants through the fur.     

Morphometrics of the anterior dentition in strepsirhine primates

Size variations in the anterior dentition were analyzed for 26 species of strepsirhine primates. The upper and lower incisor rows of strepsirhines, like those of anthropoid primates, scale isometrically with body size. Within the order Primates, strepsirhines exhibit the smallest incisors relative to body size, followed in increasing size by tarsiers, platyrrhines, and catarrhines. If the lateral teeth of the indriid toothcomb are interpreted as incisors and not canines, correlations between mandibular tooth size variables and body weight are maximized. The upper incisors of strepsirhines are extremely small and frequently widely separated, most likely to minimize occlusion with the toothcomb. Species deviations for assorted size variables of the anterior dentition generally fail to reflect functional variations in the use of the anterior teeth; some of the variables, however, do reflect taxonomic differences within the Strepsirhini. Although toothcomb size variations among extant strepsirhines are more readily interpreted in terms of gum feeding and bark scraping than they are in terms of grooming, anterior dental morphology as a whole is more easily explained by a grooming hypothesis when existing models of toothcomb origins are considered.     

The anatomical relations of the ductus vomeronasalis and the occurrence of taste buds in the papilla palatina of Nycticebus coucang (primates, prosimiae) with remarks on strepsirrhinism.

Nycticebus coucang is typically strepsirrhine. This condition is basically the same in all prosimians except Tarsius. The rhinarium shows a labial part; the marked furrow in its median plane clefts the margin of the upper lip. The latter is attached to the gum between the median incisors by means of paired folds (not corresponding to a frenulum labii superioris). The labial cleft is continued in the sulcus papillae palatinae. The ductus vomeronasalis opens into the ductus nasoplatinus which, in turn, enters the aboral part of the sulcus palatinus. Thus strepsirrhinism provides, occasionally, an open communication of the olfactory systems (nose, vomeronasal organ) with the environment in front of the rhinarium. Strepsirrhine primates possess an internarium very similar to the one of platyrrhine monkeys. The shape of the nostrils is not characteristics for strepsirrhinism. A split-lip condition is likely ancestral to the complete lip condition, since it is found in several stems of mammals, especially in archaic forms. Strepsirrhinism, such as in lemuroid prosimians, is probably just one case of the primitive split-lip condition. Therefore, a median furrow in the external hairy skin of the upper lip, found in some platyrrhine monkeys, could be a rudiment of a cleft, indicating that a kind of a split lip condition was ancestral to the undivided lips of platyrrhine monkeys. Taste buds occur in the epithelium of the lateral surface of the papilla palatina of Nycticebus. Other lorisid prosimians have not been studied in this respect. The taste buds test water soluble substances entering the sulcus either way. These substances may come from the environment entering the sulcus through the labial cleft.     

On the vomer in Acrochordidae (Reptilia: Serpentes), and its cladistic significance

It is reported that in certain features the form of the vomer is significantly different in Caenophidia than in Henophidia (except acrochordids). In Henophidia the vomer typically has one or a few apertures for the exit of the vomeronasal nerve from the bony surround of the vomeronasal organ, well- or moderately-developed vertical and horizontal (palatal) posterior laminae, and only a partially-developed cup-like enclosure for the vomeronasal organ. In Caenophidia the vomer typically has very many tiny foramina for the passage of the vomeronasal nerve, the horizontal posterior lamina in particular is much reduced or absent, and the vomer forms a globular enclosure for the vomeronasal organ. A comparison with the vomer in lizards suggests that the henophidian type of vomer is primitive within snakes and the caenophidian type is derived. Scolecophidia are not discussed. The vomer in acrochordids closely resembles that of Caenophidia, and this form of vomerine morphology is proposed as a synapomorphy indicating the strict monophyly of the group acrochordids-Caenophidia. The acrochordids have been treated very differently by various snake taxonomists and their phyletic position has always been highly problematical. The synapomorphy proposed herein contributes to a solution of this problem.     

Molecular and evolutionary analyses of formyl peptide receptors suggest the absence of VNO-specific FPRs in primates

Formyl peptide receptors (FPRs) were observed to expand in rodents and were recently suggested as candidate vomeronasal chemo-sensory receptors. Since vomeronasal chemosensory receptors usually underwent positive selection and evolved concordantiy with the vomeronasal organ (VNO) morphology, we surveyed FPRs in primates in which VNO morphology is greatly diverse and thus it would provide us a clearer view of VNO-FPRs evolution. By screening available primate genome sequences, we obtained the FPR repertoires in representative primate species. As a result, we did not find FPR family size expansion in primates. Further analyses showed no evolutionary force variance between primates with or without VNO structure, which indicated that there was no functional divergence among primates FPRs. Our results suggest that primates lack the VNO-specific FPRs and the FPR expansion is not a common phenomenon in mammals outside rodent lineage, regardless of VNO complexity.     

The structure of the nasal chemosensory system in squamate reptiles. 2. Lubricatory capacity of the vomeronasal organ

The vomeronasal organ is a poorly understood accessory olfactory organ, present in many tetrapods. In mammals, amphibians and lepidosaurian reptiles, it is an encapsulated structure with a central, fluid-filled lumen. The morphology of the lubricatory system of the vomeronasal organ (the source of this fluid) varies among classes, being either intrinsic (mammalian and caecilian amphibian vomeronasal glands) or extrinsic (anuran and urodele nasal glands). In the few squamate reptiles thus far examined, there are no submucosal vomeronasal glands. In this study, we examined the vomeronasal organs of several species of Australian squamates using histological, histochemical and ultrastructural techniques, with the goal of determining the morphology of the lubricatory system in the vomeronasal organ. Histochemically, the fluid within the vomeronasal organ of all squamates is mucoserous, though it is uncertain whether mucous and serous constituents constitute separate components. The vomeronasal organ produces few secretory granules intrinsically, implying an extrinsic source for the luminal fluid. Of three possible candidates, the Harderian gland is the most likely extrinsic source of this secretion.     

Lemuriform origins as viewed from the fossil record

Fossils relevant to lemuriform origins are reviewed. Omanodon seems very close to the other early tooth-combed lemuriforms Karanisia, Wadilemur and Saharagalago, whereas Bugtilemur is rejected from the Lemuriformes. The Djebelemurinae, including Djebelemur and 'Anchomomys' milleri, are considered as stem lemuriforms preceding tooth comb differentiation; they are shown to be very distinct from European adapiforms. With tooth-combed lemuriforms present in Africa around 40 million years ago, and stem lemuriforms without tooth combs present on the same continent around 50-48 million years ago, a reasonable scenario can be proposed: tooth comb differentiation and lemuriform dispersal to Madagascar between 52-40 million years ago. The possible significance of Plesiopithecus for daubentoniid origins is raised. A critique of molecular dates is presented in the light of the fossil record. Azibiids are possibly early African prosimians. The timing of the dispersal of primates to Africa and the problem of strepsirhine origins are briefly examined.     

New ways to go—nasal floor structures as channelling system for vomeronasal stimuli in the shrew (<Emphasis Type="Italic">Sorex araneus</Emphasis>, Mammalia)

The mammalian lateral nasal gland (LNG, also called Steno’s gland) is known to be one source of so-called odorant-binding proteins, which are suggested to work as vehicles to carry chemosensory stimuli within the nasal cavity in order to guide them to olfactory and vomeronasal sensory neurons. Up to now, a largely unattended and unanswered question is how the secretions of the LNG migrate between the glandular opening at the upper edge of the anterior lateral nasal wall and the more caudally located vomeronasal organ. In order to address this issue, the functional morphology of the rostral nasal cavity of Sorex araneus was investigated histologically. Special interest was laid on the opening region of the LNG in the vestibular region of the nose and its topological connection to a hitherto largely unnoticed nasal concha, the atrioturbinate. It appears that the atrioturbinate serves as a specialised channel that directs the secretions of the LNG pointedly towards the entrance of the vomeronasal organ. In addition, it was observed that—contrary to previous reports—the LNG in Sorex araneus is anatomically clearly separated from the maxillary sinus gland and does not invade the maxillary sinus.     

Organization of the vomeronasal organ in a plethodontid salamander

Salamanders in the family Plethodontidae show a unique behavior (nose-tapping) and have unique structures (nasolabial grooves) that may be used specifically to convey chemicals to the vomeronasal organ. The nasal structure of Plethodon cinereus was studied to determine if there is enhanced development of the vomeronasal organ compared with other salamander families that would correlate with use of these unique features. The vomeronasal organ in salamanders is found in a ventrolateral diverticulum of each main olfactory organ. P. cinereus has a more anteriorly placed vomeronasal organ within the diverticulum, and the posterior limit of each nasolabial groove is adjacent to the anterior limit of the vomeronasal organs. This suggests that the grooves deliver chemicals preferentially to the vomeronasal organs instead of to the main olfactory organs. In addition, the vomeronasal sensory epithelium is thickest anteriorly and is at its thinnest at about the level corresponding to the location of the vomeronasal organ in other salamander families. These adaptations suggest a specific mechanism of odorant delivery to the vomeronasal organ in plethodontid salamanders not found in other salamander families.     

Development of the nasal chemosensory organs in two terrestrial anurans: the directly developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), and the metamorphosing toad, Bufo americanus (Anura: Bufonidae)

Nearly all vertebrates possess an olfactory organ but the vomeronasal organ is a synapomorphy for tetrapods. Nevertheless, it has been lost in several groups of tetrapods, including aquatic and marine animals. The present study examines the development of the olfactory and vomeronasal organs in two terrestrial anurans that exhibit different developmental modes. This study compares the development of the olfactory and vomeronasal organs in metamorphic anurans that exhibit an aquatic larva (Bufo americanus) and directly developing anurans that have eliminated the tadpole (Eleutherodactylus coqui). The olfactory epithelium in larval B. americanus is divided into dorsal and ventral branches in the rostral and mid-nasal regions. The larval olfactory pattern in E. coqui has been eliminated. Ontogeny of the olfactory system in E. coqui embryos starts to vary substantially from the larval pattern around the time of operculum development, the temporal period when the larval stage is hypothesized to have been eliminated. The nasal anatomy of the two frogs does not appear morphologically similar until the late stages of embryogenesis in E. coqui and the terminal portion of metamorphosis in B. americanus. Both species and their respective developing offspring, aquatic tadpoles and terrestrial egg/embryos, possess a vomeronasal organ. The vomeronasal organ develops at mid-embryogenesis in E. coqui and during the middle of the larval period in B. americanus, which is relatively late for neobatrachians. Development of the vomeronasal organ in both frogs is linked to the developmental pattern of the olfactory system. This study supports the hypothesis that the most recent common ancestor of tetrapods possessed a vomeronasal organ and was aquatic, and that the vomeronasal organ was retained in the Amphibia, but lost in some other groups of tetrapods, including aquatic and marine animals.     

The study of animal bones from archaeological sites. By Raymond E. Chaplin. ix + 170 pp., figures,tables, bibliography,index. Seminar press,London. 1971. $5.75 (cloth)

A review of the literature reveals a long history of disagreement on the interpretation of the lower deciduous and permanent dentition of the Indriidae. This disagreement has centered on the existence and/or replacement of a canine as a member of the indriid toothcomb. The presence of a pair of canines in the toothcomb of lemurids and lorisids has rarely been questioned, and there is no evidence to indicate that this interpretation is incorrect. There has, however, been no consistency nor substantiating evidence presented for any interpretation of the indriid toothcomb. By comparing the morphology of the teeth of the lemurid, lorisid, and indriid toothcomb, both deciduous and permanent, comparing the mode of dental development in these three families, identifying the indriid lower deciduous dentition, and by relating the data to an ontogenetic and phylogenetic framework, this study proposes: (1) in all three families, the lateral teeth of the toothcomb are canines, (2) the dental formula for the lower deciduous teeth of indriids is 1.1.4, (3) the dental formula for the lower permanent teeth of indriids is 1.1.2.3, and (4) that decrease in number of incisors during primate evolution was most likely I1 to I2 to I3.     

Morphology of the Harderian gland of some Australian geckos

This study of the morphology, histology, histochemistry, and ultrastructure of the Harderian gland in Geckos (Squamata, Gekkota) revealed previously unreported variation. The gecko Harderian gland is unlike that of other squamates in that each cell of the secretory epithelium has both lipid and protein secretory granules. Lipid secretion has not been reported previously for the squamate Harderian gland. The structure of the protein granules resembles that described for a scincomorph lizard (Podarcis, Lacertidae). Differences between representatives of the subfamilies Gekkoninae and Diplodactylinae suggest possible phylogenetic constraints in the structure or function of Harderian glands within gekkotan lineages. The structural relationship between the Harderian gland and the lacrimal duct supports previous suggestions of a possible functional link between the Harderian gland and the vomeronasal organ. J Morphol 231:253–259, 1997. © 1997 Wiley-Liss, Inc.     

Identification and characterization of new protein chemoattractants in the frog skin secretome

The vomeronasal organ is a chemosensory organ present in most vertebrates and involved in chemical communication. In the last decade, the deciphering of the signal transduction process of this organ has progressed. However, less is known about the vomeronasal organ ligands and their structure-function relationships. Snakes possess a highly developed vomeronasal system that is used in various behaviors such as mating, predator detection, or prey selection, making this group a suitable model for study of the vomeronasal chemoreception. In this work, we used a proteomics approach to identify and characterize proteins from frog cutaneous mucus proteome involved in prey recognition by snakes of the genus Thamnophis. Herein we report the purification and characterization of two proteins isolated from the frog skin secretome that elicit the vomeronasal organ-mediated predatory behavior of Thamnophis marcianus. These proteins are members of the parvalbumin family, which are calcium-binding proteins generally associated to muscular and nervous tissues. This is the first report that demonstrates parvalbumins are not strictly restricted to intracellular compartments and can also be isolated from exocrine secretions. Purified parvalbumins from frog muscle and mucus revealed identical chemoattractive properties for T. marcianus. Snake bioassay revealed the Ca(2+)/Mg(2+) dependence of the bioactivity of parvalbumins. So parvalbumins appear to be new candidate ligands of the vomeronasal organ.     

Presence of the vomeronasal system in aquatic salamanders

Previous reports have indicated that members of the proteid family of salamanders lack a vomeronasal system, and this absence has been interpreted as representing the ancestral condition for aquatic amphibians. I examined the anatomy of the nasal cavities, nasal epithelia, and forebrains of members of the proteid family, mudpuppies (Necturus maculosus), as well as members of the amphiumid and sirenid families (Amphiuma tridactylum and Siren intermedia). Using a combination of light and transmission electron microscopy, I found no evidence that mudpuppies possess a vomeronasal system, but found that amphiuma and sirens possess both vomeronasal and olfactory systems. Amphiumids and sirenids are considered to be outgroups relative to proteids; therefore, these data indicate that the vomeronasal system is generally present in salamanders and has been lost in mudpuppies. Given that the vomeronasal system is generally present in aquatic amphibians, and that the last common ancestor of amphibians and amniotes is believed to have been fully aquatic, I conclude that the vomeronasal system arose in aquatic tetrapods and did not originate as an adaptation to terrestrial life. This conclusion has important implications for the hypothesis that the vomeronasal organ is specialized for detection of non-volatile compounds.     

Deviant anatomy of the olfactory system of the Malagasy frog Mantidactylus betsileanus (Anura: Mantellidae)

Frogs of the family Mantellidae are endemic to Madagascar and the Comoran island of Mayotte. Like many other animals in this biogeographical region, they have passed through millions of years of isolated evolution which led to ecological, physiological and anatomical specialization. The present study compares the intranasal anatomy of a mantellid, the Malagasy Common Marsh Frog (Mantidactylus betsileanus Boulenger, 1882) with that of the Malaysian Green Flying Frog (Rhacophorus reinwardtii Schlegel, 1840), a representative of the sister group of mantellids (the family Rhacophoridae). Histological examination revealed that the structure of the nasal cavities of M. betsileanus strongly deviates from the usual nasal morphology of anurans. In the typical condition, to which also R. reinwardtii conforms, the two parts of the nasal cavity (main chamber and accessory chambers), containing two different chemosensory systems (main olfactory organ and vomeronasal organ respectively), are connected by a slit-like longitudinal opening. In M. betsileanus, this elongated opening is almost completely reduced. Therefore, main chamber and accessory nasal chambers are markedly separated anatomically, leading to an enhanced spatial segregation of the two different organs of smell. Whether these anatomical alterations correspond to a more significant role of vomeronasal perception and might be related to the presence of characteristic pheromone-producing femoral glands in mantellid frogs requires further study.     

Olfactory and vomeronasal systems of caecilians (Amphibia: Gymnophiona)

The morphology of both the main nasal cavity and the vomeronasal organ differs among species representing six families of caecilians. The main nasal cavity is either divided or undivided. The vomeronasal organ differs in position (mediolateral, lateral), size (large vomeronasal organ in the aquatic species), and shape (mediolateral extension, vomeronasal organ with a lateral rostral projection). The great amount of respiratory epithelium of the main nasal cavity, the large vomeronasal organ, and its extensive innervation in typhlonectids may reflect both phylogeny and habitat adaptation, for these taxa are secondarily aquatic or semiaquatic and have several concomitant morphological and physiological modifications. The vomeronasal organ is associated with the caecilian tentacle as the tentacular ducts open into it. This association is further evidence for the involvement of the caecilian tentacle in vomeronasal chemoperception and may represent the mechanism by which these animals smell though the main nasal cavity is closed during burrowing or swimming. Labelings of primary olfactory and vomeronasal projections by means of horseradish peroxidase reaction reveal that the pattern of vomeronasal projections is similar in Ichthyophis kohtaoensis, Dermophis mexicanus, and Typhlonectes natans, even though T. natans possess stronger vomeronasal projections relative to olfactory projections than I. kohtaoensis and D. mexicanus. However, there are differences with respect to the patterns of olfactory projections. The olfactory projection of I. kohtaoensis is characterized by many displaced glomeruli. T. natans has the smallest olfactory projection. The nervus terminalis is associated with the olfactory system as shown by selective labelings of olfactory projections. Six characters potentially useful for phylogenetic analysis emerge from this study of comparative morphology. The characters were subjected to analysis using PAUP to see (1) if any resolution occurred and (2) if any groups were distinguished, whether they corresponded to phylogenetic arrangements based on other morphological characters. The characters are too few to produce nested dichotomous sets for all cases, but they do support the two typhlonectid genera examined and Dermophis and Gymnopis as sister taxa discrete from other groups, and they show that species within genera cluster together.     

Modulation of serum testosterone and autonomic function through stimulation of the male human vomeronasal organ (VNO) with pregna-4,20-diene-3,6-dione

In mammals, external chemosensory signals from conspecifics of the opposite sex acting on vomeronasal organ receptors can modulate the release of gonadotropins. There is developmental, anatomical and functional evidence showing that the human vomeronasal organ (VNO) has the characteristics of a chemosensory organ. We have been using naturally occurring human pheromones to serve as models for designing novel synthetic compounds that we call vomeropherins². In previous publications we reported that vomeropherin pregna-4,20-diene-3,6-dione (PDD) delivered to the VNO of normal female and male human volunteers significantly affected male subjects only, decreasing respiration and cardiac frequency, augmenting alpha brain waves, and significantly decreasing serum luteinizing hormone (LH) and follicle stimulating hormone (FSH). Results of the present work confirm that PDD produces a local dose-dependent effect in the male human VNO. This is followed by a mild parasympathomimetic effect characterized by 10% increase of vagal tone, together with decreased frequency of electrodermal activity events. Furthermore, PDD locally delivered to the male human VNO significantly decreases serum LH and testosterone (p<0.01). The present results contribute additional evidence supporting the functionality of the human VNO and its repercussions in autonomic and psychophysiological functions, as well as in neuroendocrine secretions.     

Chiropteran vomeronasal complex and the interfamilial relationships of bats

Within the extant orders of living mammals, the distribution of the vomeronasal organ (VNO) and associated structures is very stable, being universally present in the vast majority or universally absent in cetaceans and sirenians. Chiroptera is the most noteworthy exception, with variation in the absence or presence of the vomeronasal complex occurring even at the species level in some instances. The VNO and/or its component structures, such as the accessory olfactory bulb, were studied in serially sectioned snouts and brains from 114 genera and 292 species representing all extant chiropteran families except Myzopodidae and Antrozoidae. Taxa were scored for the following characters: (1) degree of formation of the vomeronasal epithelial tube, (2) shape of the vomeronasal cartilage, (3) occurrence of the nasopalatine duct, and (4) occurrence of the accessory olfactory bulb. To reconstruct the evolutionary history of the bat vomeronasal complex, the distributions of these four characters were mapped, using the computer program MacClade, onto chiropteran phylogenies in the literature derived from other data sets. In all phylogenies, these four characters exhibit a high degree of homoplasy, only part of which is accounted for by several polymorphic taxa. However, perhaps the most remarkable result is that in the most parsimonious solutions the absence of the vomeronasal epithelial tube and accessory olfactory bulb is identified as primitive for Chiroptera, with both structures reevolving numerous times: such a scenario would be unique to bats among mammals. An alternative, though less parsimonious interpretation, which does not require reevolution of this very complex system, is that a well-developed vomeronasal epithelial tube is primitive for Chiroptera, as in nearly all other orders of mammals, but has been reduced or lost in the majority of families. Explication of the peculiar evolutionary history of the vomeronasal system in bats awaits studies on the adult morphology in the more than 630 species not yet examined and, in particular, on ontogeny, which to date is known for only a handful of taxa.A preliminary account of this research was presented at the Tenth International Bat Research Conference and Twenty-Fifth North American Bat Research Symposium held at Boston University, Massachusetts, on 6–11 August 1995.     

Strong links between genomic and anatomical diversity in both mammalian olfactory chemosensory systems

Mammalian olfaction comprises two chemosensory systems: the odorant-detecting main olfactory system (MOS) and the pheromone-detecting vomeronasal system (VNS). Mammals are diverse in their anatomical and genomic emphases on olfactory chemosensation, including the loss or reduction of these systems in some orders. Despite qualitative evidence linking the genomic evolution of the olfactory systems to specific functions and phenotypes, little work has quantitatively tested whether the genomic aspects of the mammalian olfactory chemosensory systems are correlated to anatomical diversity. We show that the genomic and anatomical variation in these systems is tightly linked in both the VNS and the MOS, though the signature of selection is different in each system. Specifically, the MOS appears to vary based on absolute organ and gene family size while the VNS appears to vary according to the relative proportion of functional genes and relative anatomical size and complexity. Furthermore, there is little evidence that these two systems are evolving in a linked fashion. The relationships between genomic and anatomical diversity strongly support a role for natural selection in shaping both the anatomical and genomic evolution of the olfactory chemosensory systems in mammals.