As author of the booklet (Evidence for Design) I would like to reply to my (anonymous) critic.
Sadly, his/her review is full of errors.
The opening quotation about the prevalence of belief in evolution is not in the booklet at all! It is taken from the publisher's web page introduction to the booklet.
Secondly, anyone can quote short extracts from a copyright book for review purposes.
Thirdly, the reviewer has completely misread the sentence which includes the word 'baffled'. The imaginary schoolboy in chapter one is baffled, not by the complexities of the living world, but by the illogical arguments used by his biology teacher to explain the origin of life. The evolutionary theory he was being taught did not make sense.
Regrettably, the reviewer makes no attempt whatever to answer the arguments used in the booklet - for example, how, by evolution alone, a tube could arise within the thickness of the eyelid, running down to the inside of the throat to drain away the tears that are essential to the health of the eye. All he does is to mock and sneer at faith in a Designer.
Lastly, the booklet does not say, as he/she claims, that throughout history mankind has not believed in evolution. It says that until the last 100 years or so men believed in a supreme being. Of course, if you accept unaided evolution as the explanation for life, the ultimate logic is that you would deny the existence of God. But some evolutionists, theistic evolutionists, still believe in God.
One has to observe that ex Christadelphians seem to be a very unhappy crowd of people, full of bitterness, and without hope.
With regard to David's question about the evolution of the Nasolacrimal duct in primates; that is an "argument from incredulity" for design and as such it is a logical fallacy. Therefore it does not require an answer. David has made a technical blunder in this debate, just as he has made a series of technical and actual blunders in his book.
He won't understand what I have just written, because if he did, he would not have made the mistake in the first place. He obviously is not skilled in debating evolution/creation at an informed level. A skilled debater at this level would know that his opponent would not have to answer the question and indeed he would not expect him to, nor would he ask the question, in front of university trained biologists or even philosophers.
Nevertheless I am going to do something that I very rarely do and I am going to give him the answer. He will understand the short answer but not the long answer. He might understand the slightly longer answer; or he might not. But that will illustrate to him that he is completely out of his depth peddling the sort of air-head trash contained in his book and that he should stick to a subject that he knows something about.
The short and simple answer to David's question regarding the evolution of the Nasolacrimal duct in primates is that we evolved from fish and therefore land based tetrapods needed a way to keep their eyes moist, as if they were submerged in water, even though they were living in the air. Rather than waste that moisture, the Lacrimal duct evolved to reuse it efficiently by draining it into the nasal cavities. This also assisted in promoting the sense of smell in land based animals; it added moisture to the inside of the nasal cavities.
How anatomical features in general evolve is a different question. That question is answered in mountains of literature, books and papers on the subject of evolution. It would take me approximately a year to explain that answer to someone like David Pearce. He will have to do what I did and that is to study the subject in depth.
The slightly longer and more complex answer is that Tetrapods are equipped with a lacrimal duct, or tear duct that has an internal connection with the choana. It is possible that the choana started as a natural crack between maxilla and premaxilla because of an incomplete fusion in air-breathing animals. If this gap got wider and deeper with time, the frontal part of it would have to fuse together to avoid weakening the upper jaw, creating a small opening on the upper lip. Some more migrating, and this gap would meet the anterior pair of the external nasal openings. The posterior pair of the openings was then free to form the lacrimal duct if a migration caused them to come in contact with the eyes.
The longer answer is given in the following paper.
Ontogeny of the nasolacrimal duct in primates: functional and phylogenetic implications
The ontogeny of the nasolacrimal ducts (NLD) and canals (NLC) are investigated in strepsirrhine and haplorhine primates. Developmental series of serially sectioned fetal, perinatal and adult specimens, in combination with juvenile and adult skulls subjected to high-resolution computed tomography, reveal that the vertical NLC and NLD of adult tarsiers and anthropoids are produced by the degeneration of a more horizontal anterior arm of the NLD that is present only transiently in haplorhines, but is maintained throughout life in strepsirrhines. This degeneration manifests as an ‘unzipping’ of the anterior arm by means of progressive enlargement (in a rostral direction) of a caudally placed opening of the NLD (at the base of the vertical NLC), followed by breakdown of the resulting epithelial groove. The similar mode by which the anterior arm of the membranous NLD degenerates in tarsiers and anthropoids strongly suggests that the conditions in these two taxa are homologous, and provides additional evidence for a monophyletic Haplorhini. The functional relationship between the nasolacrimal duct and the vomeronasal organ is reviewed in light of this evidence, and it is suggested that these changes in the haplorhine NLD were functionally linked to the development of anatomical haplorhinism of the oronasal complex.
Keywords: anthropoid, haplorhine, nasolacrimal, tarsier, vomeronasal
The primate order is divided by most systematists into two monophyletic suborders: Strepsirrhini (lemurs, lorises and galagos) and Haplorhini (tarsiers and anthropoids), originally named for their external nasal anatomy (Pocock, 1918). An alternative classification, grouping tarsiers with strepsirrhines, has historically been based on their gradistic similarity (e.g. Fleagle, 1999), but a monophyletic suborder Prosimii has also gained some support in recent years (Murphy et al. 2001; Seiffert et al. 2003; Eizirik et al. 2004). Although the shape of the nostrils alone has proven to be an unreliable differentia of the two clades (Hofer, 1979), several other aspects of nasal anatomy serve as well-documented synapomorphies of Haplorhini (Hill, 1955; Cave, 1967, 1973; Hofer, 1977; Cartmill & Kay, 1978; Maier, 1980). Despite the phylogenetic significance of the primate nasal region, the morphology of the nasolacrimal duct (NLD) has received little attention.
Like most mammals, strepsirrhines possess a naked wet rhinarium that connects to the oral cavity via a median cleft or philtrum in the upper lip, which is tethered to the gums by a frenulum (for reviews, see Beard, 1988; Martin, 1990). Through this channel, odorant molecules that collect on the rhinarium drain between a gap separating the upper central incisors to reach the oral cavity. The median cleft continues posteriorly within the oral cavity, typically ending as Y-shaped channels bilateral to the incisive papilla, which covers the entrance to the nasopalatine ducts. Thus, odorant molecules dissolved in fluid medium on the rhinarium can ultimately reach the vomeronasal organs (VNO), which open into the nasopalatine ducts (Hill, 1955; Schilling, 1970; Hofer, 1980; Maier, 1980; Starck, 1984; Wöhrmann-Repenning & Bergmann, 2001; Evans, 2003). In strepsirrhines, the nasolacrimal duct empties its contents into the anterior end of the nasal vestibule, and contributes to the moistness of the rhinarium (a small portion of these fluids is absorbed by the lining of the NLD; Paulsen, 2003). In as much as moisture on the rhinarium is an integral part of the functional complex of the VNO just described (herein the ‘rhinarium–philtrum–papilla’ or RPP system), the NLD is a critical component of this system (for a review, see Hillenius & Rehorek, 2005). This functional significance of the NLD has not been emphasized by primatologists, but has been discussed in studies contrasting the functional morphology of the VNO in mammals and non-mammalian tetrapods (e.g. Negus, 1958; Hillenius, 2000; Hillenius & Rehorek, 2005).
In haplorhines, a major rearrangement of nasal morphology has occurred (Pocock, 1918; Hill, 1955; Hofer, 1980; Maier, 1980; Starck, 1984). The naked rhinarium is completely lost. A now hair-covered upper lip is freed from the gums (and hence mobile), and there is no interincisor gap, so that the RPP system is completely dismantled. Although it has only been alluded to previously (Woollard, 1925; Hill, 1955; Starck, 1960, 1984; Maier, 1980), the NLD is also rearranged in haplorhines so that it opens in a much more caudal position rather than into the nasal vestibule.
The spatial associations of the NLD in the two primate suborders have not yet been the subject of detailed comparative anatomical or developmental study. Here we document the development of the NLD in sectioned rostra of perinatal, infant and adult haplorhines, and discuss the phylogenetic and functional implications of these findings.
Materials and methods
Nasal fossae of 88 primate specimens were examined. Of these, 36 were serially sectioned nasal fossae (see Table 1), including those of 21 strepsirrhines, 12 anthropoids and four tarsiers. Tissues of perinatal primates were obtained from animals that died naturally in captivity, and specimens were initially frozen or fixed by immersion in 10% buffered formalin (see Table 1). Adult tissues were obtained from animals in primate laboratories that were killed elsewhere after unrelated studies. Three specimens were sectioned fetuses available from the Hubrecht Laboratorium. All perinatal primates were collected by the Duke University Primate Center, where they died naturally after birth or were stillbirths. Thus, they represent a mixed-age ‘perinatal sample’. Of the two perinatal Tarsius syrichta, one was smaller and was found within an amnionic sac. The specimens were probably of different stages of development (late fetal and neonatal) but no data exist to provide precise ages.
Age group, preservation and source of the primate species investigated by serial sectioning
The entire head, one-half of the head (bisected sagittally), or the nasal region was processed in perinatal and adult primates (see Smith et al. 2003b). Tissues were decalcified in a formic acid solution (formic acid–sodium citrate or Cal-Ex II: Fisher Scientific), dehydrated in a graded ethanol series, cleared in xylene, embedded in paraffin and serially sectioned in the coronal plane at 10–12 µm. Every tenth section was mounted on glass slides and alternately stained with haematoxylin-eosin and Gomori trichrome procedures. Hubrecht specimens had previously been sectioned at 15 µm in the coronal or horizontal planes, mounted on glass slides and stained with haematoxylin-eosin. The tissues were examined for morphology of the NLD using a Leica photomicroscope. Each series was examined at ×25–×630.
Additionally, 52 juvenile, subadult and adult osteological specimens of Eulemur, Loris, Microcebus, Tarsius, Saguinus, Leontopithecus, Lagothrix, Alouatta, Cebus, Callicebus, Saimiri, Cacajao, Aotus, Callimico and Hylobates were subjected to high-resolution X-ray computed tomography (for details, see Rossie, 2006). These data were viewed as stacks of coronal slices of varying thickness using ImageJ software. Voxblast Light was used to generate three-dimensional reconstructions of these data in which the nasolacrimal canal is highlighted.
In our perinatal and fetal specimens of Nycticebus and Otolemur, the duct passes inferiorly from the lacrimal sac, running anteroinferiorly along the lateral aspect of the cartilaginous paries nasi (Figs 1 and and2).2). Upon reaching the inferior border of the paries nasi, it runs anteriorly in the horizontal sulcus that separates the paries nasi and lamina transversalis anterior. The nasal orifice of the duct is found just inside the external nares, inferior to the atrioturbinal in neonates. This basic arrangement appears to be universal among strepsirrhines, and is illustrated for reference here in adult and perinatal specimens of Otolemur spp. (Fig. 1A–F). In the fetal Nycticebus, the membranous duct extends even further anteriorly – about 10 µm beyond the premaxilla, opening medial to the marginoturbinal (Fig. 2A).
Strepsirrhine and anthropoid nasolacrimal ducts. (A–D) The typical passage of the nasolacrimal duct (nld) in strepsirrhines is shown from anterior to posterior in a perinatal Otolemur garnetti. (A) A coronal section just posterior to the opening ...
Nycticebus coucang. (A) Coronal section just anterior to the premaxilla in a 25-mm crown–rump length (CRL) Nycticebus coucang, showing the opening of the NLD (*) just inferomedial to the marginoturbinal (mgt). (B) A section 1.2 mm posterior to ...
In adults, the precise course of the bony nasolacrimal canal depends on details of nasal cavity development in different species, but the nasal orifice remains beneath the atrioturbinal, anterior to the maxilloturbinal (Fig. 1E). When a maxillary sinus is present (e.g. in Eulemur, Fig. 3), the canal is overtaken by the expansion of the sinus so that its posterior portion runs within the roof of the sinus. In species without a sinus (e.g. Loris), the NLD runs along the wall of the recessus lateralis. In nearly all forms (with and without a sinus, short or long snouted), its anterior portion runs within the base of the maxilloturbinal before entering the inferior meatus beneath the atrioturbinal (Fig. 3). The duct continues for a distance anterior to this as a membranous duct within the lamina propria of the nasal cavity so that the nasal orifice of the duct is well anterior to the opening of the bony canal. This anterior position of the NLD opening was referred to by Starck (1960) as a ‘primary’ opening, because it is clearly plesiomorphic, and was contrasted with a ‘secondary’ position of the opening (described below). Herein, we employ the terms ‘narial’ (primary) and ‘meatal’ (secondary), following Göbbel (2002).
Strepsirrhine nasolacrimal duct. Three-dimensional reconstruction of adult Eulemur fulvus (A) and Microcebus (D) skulls showing course of the osseous NLC (solid white) and membranous NLD (dashed lines). Coronal sections (B,C) through the rostrum of Eulemur ...
In adult anthropoids (Figs 1G,H and and4),4), the NLD (and bony canal) descends vertically from the lacrimal foramen (which lies within the orbit) to open beneath the maxilloturbinal. In some specimens, it actually runs slightly posteroinferiorly so that the nasal orifice is somewhat caudal to the lacrimal foramen (Figs 1G,H and and4),4), but in all cases the nasal orifice is caudal to the nasopalatine duct. This position is the ‘secondary’ opening of (Starck, 1960), but will be referred to as a ‘meatal’ opening herein. The developmental process that leads to this caudal position of the NLD nasal orifice is revealed by our younger specimens.
Haplorhine nasolacrimal duct. Three-dimensional reconstruction of juvenile (A) and adult (B) Leontopithecus and adult Tarsius (E), and coronal slices of juvenile (C) and adult (D) Leontopithecus through the NLC. Dashed lines in A and E represent the position ...
In perinatal specimens, the NLD descends inferiorly from the orbit, running along the lateral side of the cartilaginous paries nasi, and enters the nasal capsule beneath the maxilloturbinal (Fig. 5). This proximal arm of the NLD foreshadows the adult course of the duct. The nasal orifice, when patent, is found at its inferior end (the orifice can remain sealed by a thin sheet of epithelium until near birth as in humans; Schaeffer, 1920). Upon entering the nasal cavity, the duct turns roughly 90°, and continues rostrally as an epithelial structure running horizontally within the mucosa of the inferior meatus. This anterior arm of the duct follows the course of the anterior portion of the duct in strepsirrhines: running below the cartilage of the maxilloturbinal/paries nasi, and eventually between the inferior edge of the pars anterior and the dorsal edge of the lamina transversalis anterior. The size and presence of this distal arm is variable among specimens, as well as bilaterally within each specimen in our sample. It is usually canalized, but never bears an opening at its anterior end. The nasal orifice of the NLD is located at the fulcrum of the proximal and distal arms of the duct.
Leontopithecus rosalia. Coronal sections of a 3-day-old Leontopithecus rosalia (A–D), showing the passage of the membranous anterior arm of the NLD within the mucosa of the wall of the inferior meatus. Note the anterior blind ending (A, *), the ...
The developmental fate of this dead-end anterior arm is best exemplified in Leontopithecus (Fig. 5). In neonates (3–4 days postpartum), the nasal orifice of the duct takes the form of an anteroposteriorly orientated slit, between 100 and 250 µm in length (Fig. 5C). The blind anterior arm of the duct extends roughly 100–200 µm anterior to the orifice. By 9 days postpartum (Fig. 5E–I), the slit-like orifice of the duct has expanded anteriorly to a length of over 300 µm, essentially ‘unzipping’ the anterior arm of the duct so that it is converted into an open groove. This open groove appears to degenerate subsequently, as no traces of it are found in a 4-month-old specimen, leaving only the posteriorly positioned orifice at the end of the vertical osseous nasolacrimal canal that is seen in adults (Fig. 5J–L). Saguinus and Callithrix also conform to this pattern of development according to our material.
As in anthropoids, the NLD in perinatal and fetal tarsiers descends from the lacrimal foramen, which lies just anterior to the medial rim of the orbit, along a short and nearly vertical route on the lateral surface of the pars intermedia of the nasal capsule to open beneath the maxilloturbinal (Figs 6 and and7).7). This opening is near the coronal plane of the nasopalatine duct, at the inferior end of what will become the osseous nasolacrimal canal. This vertical orientation and relatively caudal position of the NLD orifice is the same as that found in anthropoids.
Tarsius syrichta. (A) Coronal section of a late fetal Tarsius syrichta, showing the anterior arm of the nasolacrimal duct (NLD) at the level of the nasopalatine duct (NPD). Note the NLD is patent on the right side of the image. On the left side, it is ...
Tarsius bancanus. (A) Horizontal section through the nasal fossa of a 20-mm crown–rump length (CRL) Tarsius bancanus, showing a partially patent NLD on the left side of the figure and the blind ending of the NLD on the right. (B) Horizontal section ...
In prenatal tarsiers and the smaller perinatal tarsier (Tarsius bancanus, T. syrichta, respectively), after entering the nasal cavity the NLD continues anteriorly along the same horizontal path as in strepsirrhines and anthropoids. As in anthropoids, this anterior arm of the duct ends blindly without opening into the nasal vestibule (Fig. 6A). These epithelial anterior arms, devoid of orifices (Fig. 7A,C), extend no further anteriorly than the maxilloturbinal (compare with Nycticebus, Fig. 2A).
In the larger perinatal T. syrichta, the anterior arm has degenerated and is represented by only an isolated 50-µm piece of the ‘unzipped’ epithelial groove (described above in anthropoids) lying on the inferior surface of the root of the maxilloturbinal (Fig. 6F). Anterior and posterior to this fragment of the epithelial groove there is no visible membranous NLD (e.g. note absence of duct remnants at level of nasopalatine duct in Fig. 6E; cf. Fig. 2B).
The development of the NLD is most well documented in humans, whose facial morphology is highly autapomorphic among primates. Nonetheless, the underlying developmental processes documented in humans appear to hold for other primates. In early fetal development the NLD begins as an ‘epithelial cord’ or long strand of surface epithelial cells that invaginates at the junction of the lateral nasal process and maxillary process of the embryonic midface (Schaeffer, 1920; Sperber, 1989; Larsen, 1997). At this union, the epithelial cord arises from a transient groove (the naso-optic fissure) that connects the medial margin of the eye to the lateral margin of the anterior nares (Schaeffer, 1920). The precise manner in which the epithelial cord subsequently ‘canalizes’, or becomes patent internally as a duct, has been the subject of some disagreement, but most studies agree that the process is often incomplete at birth (see Schaeffer, 1920; Sevel, 1981; Sperber, 1989; de la Cuadra-Blanco et al. 2006). Instead, the nasal orifice remains covered by a thin layer of epithelium, the lacrimonasal membrane, until around the time of birth or slightly thereafter (as in our Saguinus specimens), at which point it ruptures, completing the communication between orbit and nasal cavity. As the present study has shown, in both strepsirrhines and haplorhines this epithelial cord, and the membranous duct that it gives rise to, extend further anterior than will the osseous nasolacrimal canal of adults. Whereas in strepsirrhines this original length of the duct is maintained into adulthood, it is considerably shorter in adult haplorhines, but the reasons for this difference, and its phylogenetic and functional significance, have not been investigated previously.
Our results corroborate previous accounts of NLD morphology in strepsirrhines (e.g. Eloff, 1951; Starck, 1962; Maier, 1980), and affirm their similarity to those found in Scandentia (Zeller, 1987) and other mammals that lack radical specializations of the rostrum (Roux, 1947; Asher, 1998). Accordingly, we regard this morphology, and its pattern of development, as the primitive condition for primates (if not eutherians). The NLD morphology described above for haplorhines is therefore a derived condition, and may constitute a significant synapomorphy of that group.
A few authors have mentioned the caudal position of the nasal opening of the NLD in tarsiers (e.g. Woollard, 1925; Hill, 1955), but without describing its course in any detail, or mentioning the similarity to anthropoids. More recently, Maier (1980: 222) has noted that a caudal position of the opening, beneath the maxilloturbinal, was a derived feature of tarsiers and anthropoids, but did not describe the structure in detail. However, in Starck's (1984: 282) thorough description of the tarsier nasal cavity, it was noted that in adults ‘the rostral part of the NLD is reduced’, and represented by ‘epithelial rests’, and that the NLD opens beneath the maxilloturbinal in a ‘secondarily’ caudal position in the plane of the nasopalatine duct. Assuming that the term ‘epithelial rests’ was meant to refer to epithelial remains or vestiges, our findings confirm these observations. The isolated fragment of ‘unzipped’ epithelial groove found in our larger perinatal Tarsius syrichta corresponds to the epithelial fragments noted by Starck (1984), and the presence of these fragments indicates that the same unzipping and degeneration process as was seen in anthropoids is responsible for the adult morphology of tarsiers.
The conditions encountered in our anthropoids also reconcile what might appear to be contradictory accounts of the anterior extent of the NLD (e.g. Frets, 1913; Maier, 1980). As noted above, Maier (1980) regarded a caudal opening of the NLD to be a synapomorphy of haplorhines, but sectioned rostra of fetal anthropoids reported elsewhere (e.g. Ateles; Frets, 1913) clearly showed the membranous distal arm of the nasopalatine duct (NPD) extending anteriorly along the usual strepsirrhine course (at the junction of the paries nasi and anterior transverse lamina). The terminus of this anterior arm of the duct was not described by Frets (1913), but Starck (1973) described a similar duct in a fetal chimpanzee that ended blindly near the level of the nasal vestibule. The nasal orifice in this specimen was located posteriorly, at the end of the vertically orientated nasolacrimal canal, as it is in our platyrrhine specimens. On the basis of the developmental pattern documented here for callitrichines and Tarsius, it appears that haplorhines develop a strepsirrhine-like anterior arm of the NLD early in fetal ontogeny but, once the orifice at the base of the nasolacrimal canals (NLC) opens, the epithelial duct anterior to this point begins to degrade, beginning with an ‘unzipping’ process achieved by expanding the anteroposterior length of the duct's nasal orifice (Fig. 8). This process explains the presence of the anterior NLD extension seen in some fetal and infant anthropoid specimens, as well as the meatal position of the nasal orifice in adults. The fact that the same process (unzipping and degeneration of the anterior arm) appears to be responsible for the distinctive position of the NLD orifice in tarsiers and anthropoids strongly suggests that the condition is homologous in the two lineages.
Schematic illustration of the ‘unzipping’ process in a haplorhine. (A) Side view of skull showing position of NLD and eye (e). (B) Bisected skull showing nasal cavity structures. (C) bisected skull showing course of the prenatal/perinatal ...
Having documented the proximate reason for the distinctive caudal position of the NLD in haplorhines, it may be of interest to consider the ultimate cause of this change. Consideration of the functional role of the NLD in a broader phylogenetic framework suggests a likely explanation. The NLD of strepsirrhines, like that of many other mammals, opens into the anterior part of the nasal vestibule, and in some cases reaches the ventral surface of the nares, thereby delivering its fluid contents to the surface of the naked rhinarium (Bang & Bang, 1959; Evans & Christensen, 1979; Nickel et al. 1979; Zeller et al. 1993; Hillenius, 2000). This arrangement is an essential difference between the VNO system of mammals and non-mammalian tetrapods (Hillenius & Rehorek, 1997, 2005; Hillenius, 2000). In the primitive tetrapod condition, exemplified by lepidosaurs, turtles and amphibians, the NLD opens in close proximity to (if not into) the VNO duct (Pratt, 1948; Dawley & Bass, 1988; Hillenius & Rehorek, 1997, 2005; Hillenius, 2000), and its fluid contents are thought to aid in either transferring odorants into the VNO (Broman, 1920; Pratt, 1948; Negus, 1958; Bellairs, 1970; Rehorek, 1997) or the chemical processing of these signals (e.g. Bellairs & Boyd, 1950; Halpern, 1992). In squamates, Pratt (1948) described this as a ‘continuous current mechanism’, by which the NLD delivers a constant supply of fluids that flow past the mouth of the VNO. Evidence for a functional relationship between the NLD and VNO is not limited to these structural correlations. Experimental work on squamates (Rehorek et al. 2000), caecilians (Schmidt & Wake, 1990) and anurans (Hillenius et al. 2001) has shown that orbital fluids tagged with chemical or radioactive markers are later found inside the VNO.
In most mammals, the VNO no longer receives a direct flow of NLD fluids. Instead, the fluids take a circuitous course: exiting the nasal cavity through the nares to reach the neomorphic naked rhinarium where they entrain odorant molecules that adhere to its surface, then running down the philtrum between the central incisors and onto the papilla in the oral roof (Schilling, 1970; Maier, 1980; Wöhrmann-Repenning, 1980; Asher, 1998; Hillenius & Rehorek, 2005). From here the odorants can be drawn up into the nasopalatine duct, within which the VNO ducts open (Schilling, 1970; Maier, 1980; Wöhrmann-Repenning, 1980; Poran et al. 1993; Asher, 1998; Hillenius & Rehorek, 2005). The precise mechanism of the latter process is debated but either the behaviour known as flehmen (see Estes, 1972; Wöhrmann-Repenning, 1991), or a pump action produced by changes in the volume of blood vessels that surround the VNO is thought to be responsible (e.g. Dagg & Taub, 1970; Schilling, 1970). This RPP system is widespread in mammals (though not ubiquitous), and is certainly the primitive condition for eutherian mammals. Several groups of mammals have disrupted the RPP system, either by changing the spatial relations of the NPD and VNO duct (e.g. bats, rodents, equids) or by partially fusing their fetal maxillary processes for various reasons (e.g. labial mobility in ungulates; Boyd, 1932). However, only in haplorhine primates is the naked rhinarium completely lost (Boyd, 1932). Only in haplorhines, then, is the role of the NLD in moistening the rhinarium lost as well.
In light of the available evidence, we can infer the following sequence of evolutionary changes in haplorhines. In the haplorhine common ancestor, the maxillary processes fused completely during ontogeny such that the naked rhinarium was replaced by hairy skin, the upper central incisors were tightly appressed in the midline, and the upper lip was no longer tethered tightly to the gums by a frenulum (Martin, 1990). Whether the selective advantage of this change lay in the mobility of the lip or in the construction of the incisors is not clear, but the effect was the obliteration of the RPP system. As a result, haplorhines reverted to an essentially non-mammalian method of introducing chemical stimulants to the VNO through the nasal cavity. Without a moist rhinarium, inspiration of chemical stimulants would place them primarily on the mucosa lining the respiratory portion of the nasal passages, i.e. on the maxilloturbinal and inferior meatus. If the nasal opening of the NLD were repositioned posteriorly so as to open into the inferior meatus, just beneath the maxilloturbinal's base, then its fluid contents could help to wash chemical stimuli inferiorly into the region of the NPD in which the openings to the VNO are found. Such an arrangement would also benefit from moving the openings of the VNO to a more dorsal position, near the nasal opening of the NPD, and these two conditions are precisely those found in extant tarsiers and platyrrhines (this study; Smith et al. 2003a,b).
Although the VNO and the accessory olfactory bulb (AOB) to which it projects are both lost in catarrhines, they are present and ‘functional’ in tarsiers and platyrrhines (Maier, 1980; Stephan et al. 1981; Martin, 1990). The tarsier VNO is odd in that it is lined almost entirely with neuroepithelium (Wöhrmann-Repenning & Bergmann, 2001; Smith et al. 2003a), and in both tarsiers and platyrrhines the AOB is relatively small compared with overall brain volume (Martin, 1990). Regardless, the degree to which the VNO is of lesser significance in tarsiers and platyrrhines compared with strepsirhines is uncertain, and the present argument implies that there was selective pressure in stem haplorhines for structural modifications that would salvage the function of the VNO. Whether this reprise of the ‘continuous current’ mechanism was somehow less efficient than the RPP system is also unclear, but it is obviously a compromise solution.
The possibility that the rearrangement of the NLD in haplorhines is associated with a reduced emphasis on vomerolfaction receives some support, by analogy, from recent research on Microchiroptera (Göbbel, 2002). A functioning VNO combined with a narial opening of the NLD appears to be the plesiomorphic state among chiropterans (as in primates), but both elements have been transformed in various microchiropteran lineages (Wible & Bhatnagar, 1996; Göbbel, 2002). The anterior portion of the NLD has been reduced in at least four microchiropteran lineages (Göbbel, 2002). In some, the result is a meatal opening near the level of the NPD (e.g. Thyropteridae, Natalidae), or at the dorsal mouth of the NPD (Furipteridae, Rhinolophinae), yielding conditions resembling those of haplorhines. In more extreme cases (nycterids, phyllostomids, mormoopids and noctilionids), the NLD is either absent or cystic (blind-ending) (Bhatnagar & Kallen, 1974; Göbbel, 2002). Reconstructing the sequence of changes in VNO morphology in such a speciose order is complicated by sampling issues (see Wible & Bhatnagar, 1996), and attempting to associate these changes with those in the NLD system is necessarily tenuous. Nonetheless, it is notable that all four clades in which the NLD is truncated also undergo either loss of neuroepithelia from the VNO or complete loss of the VNO (Wible & Bhatnagar, 1996; Göbbel, 2002). In some of these groups, the nasolacrimal duct is reduced (e.g. phyllostomids) before the VNO loses neuroepithelium (mormoopids and noctilionids). In at least a broad sense, the association between reorientation of the NLD and reduction of vomerolfaction may hold within Microchiroptera as it does in Haplorhini, but the direction of causality is unclear at present. Further study of these associations, as well as their relationship to the sometimes dramatic transformations of the external rhinarium in bats, could be of interest in this regard.
Fetal, perinatal and adult strepsirrhines possess an obliquely or subhorizontally orientated nasolacrimal canal, and a horizontal NLD extending anterior to this. Haplorhines are characterized by a vertically orientated proximal arm of the NLD that corresponds to the osseous NLC. In fetal and perinatal specimens, an epithelial NLD extends anterior to this horizontally. This structure degenerates subsequently, leaving only the vertical NLD and NLC in adults.
The relatively caudal position of the nasal orifice of the NLD in haplorhines is a synapomorphy that is functionally related to the loss of the naked rhinarium and philtrum. The loss of the naked rhinarium removed the need for a NLD that delivered its contents to the rostral end of the nasal vestibule, and the loss of the RPP system of delivering odorants to the VNO appears to have necessitated a reversion to reliance on access through the nasal passages. This was facilitated by a more dorsal opening of the VNO, at the nasal end of the nasopalatine ducts, and a repositioning of the nasolacrimal canal so that it opens into the inferior meatus near the coronal plane of the NPD where it would wash odorant molecules from the sidewalls of the respiratory portion of the nasal cavity into the mouth of the NPD and VNO below. This method of delivering odorant molecules to the VNO is reminiscent of the strategy employed by many non-mammalian tetrapods, and may be less effective than the typical eutherian RPP system. If so, this may explain the reduced role of the VNO in haplorhines that is inferred from the relatively small accessory olfactory bulb in tarsiers and platyrrhines, and the loss of this structure as well as the VNO in catarrhines.
As the reorientation of the NLD in haplorhines is part of a larger functional complex, it might be argued that it should not be counted as an additional independent character that would add to the already impressive list of haplorhine synapomorphies. If nothing else, it adds an element of complexity to the nasal morphology shared by the two groups, and strengthens the argument for the homology of these similarities. Those who support a monophyletic Prosimii (e.g. Eizirik et al. 2004) must invoke homoplasy in the evolution of this entire set of features. More importantly, the vertical nasolacrimal canal of haplorhines is a condition that could potentially be documented in fossil taxa.
We thank Alan Walker and Tim Ryan for sharing HRXCT scans of Microcebus. All other computed tomography was performed at the HRXCT lab, University of Texas, Austin. We thank C. J. Bonar of the Cleveland Metroparks zoo for making some of the perinatal tissues available. S. Combes and J. Ives of Duke University Primate Center arranged for the availability of strepsirrhine primate cadavers used in this study. Finally, we are grateful to J. Narraway of the Hubrecht Laboratorium for making the fetal tarsiers and slow loris available for our study. This work was conducted in part during a Rea Postdoctoral Fellowship awarded to J.B.R. Other funding was provided by NSF grant BCS-0100825 to J.B.R., and by grants from Slippery Rock University to T.D.S. This is Duke University Primate Center publication no. 1004.
- Asher RJ. Morphological diversity of anatomical strepsirrhinism and the evolution of the lemuriform toothcomb. Am J Phys Anthropol. 1998;105:355–367. [PubMed]
- Bang BG, Bang FB. A comparative study of the vertebrate nasal chamber in relation to upper respiratory infections. Bull Johns Hopkins Hosp. 1959;104:107–149. [PubMed]
- Beard KC. The phylogenetic significance of strepsirhinism in Paleogene primates. Int J Primatol. 1988;9:83–96.
- Bellairs ADA, Boyd JD. The lachrymal apparatus in lizards and snakes. II. The anterior part of the lachrymal duct and its relationship with the palate and with the nasal and vomeronasal organs. Proc Zool Soc Lond. 1950;120:269–309.
- Bellairs ADA. The Life of Reptiles. New York: Universe Books; 1970.
- Bhatnagar KP, Kallen FC. Morphology of the nasal cavities and associated structures in Artibeus jamaicensis and Myotis lucifungus. Am J Anat. 1974;139:167–190. [PubMed]
- Boyd JD. The classification of the upper lip in mammals. J Anat. 1932;67:409–416. [PMC free article] [PubMed]
- Broman I. Das Organon Vomero-Nasale Jacobsoni – ein Wassergeruchsorgan! Arb Anat Inst Wiesbaden (Anat H Abt I) 1920;58:137–191.
- Cartmill M, Kay RF. Craniodental morphology, tarsier affinities, and primate suborders. In: Chivers DJ, Joysey KA, editors. Recent Advances in Primatology. Vol. 3. London: Academic Press; 1978. pp. 205–214.
- Cave AJE. Observations on the platyrrhine nasal fossa. Am J Phys Anthropol. 1967;26:277–288. [PubMed]
- Cave AJE. The primate nasal fossa. Biol J Linn Soc Lond. 1973;5:377–387.
- de la Cuadra-Blanco C, Peces-Peña MD, Jáñez-Escalada L, Mérida-Velasco JR. Morphogenesis of the human excretory lacrimal system. J Anat. 2006;209:127–135. [PMC free article] [PubMed]
- Dagg AI, Taub A. Flehmen. Mammalia. 1970;34:686–695.
- Dawley EM, Bass AH. Organization of the vomeronasal organ in a plethodontid salamander. J Morph. 1988;198:243–255.
- Eizirik E, Murphy WJ, Springer MS, O'Brien SJ. Molecular phylogeny and dating of early primate divergences. In: Ross CF, Kay RF, editors. Anthropoid Origins: New Visions. New York: Kluwer Academic Press; 2004. pp. 45–64.
- Eloff FC. On the organ of Jacobson and the nasal floor cartilages in the chondrocranium of Galago senegalensis. Proc Zool Soc Lond. 1951;1951:651–655.
- Estes RD. The role of the vomeronasal organ in mammalian reproduction. Mammalia. 1972;36:315–341.
- Evans C. Vomeronasal Chemoreception in Vertebrates: a Study of the Second Nose. London: Imperial College Press; 2003.
- Evans HE, Christensen GC. Miller's Anatomy of the Dog. 2. Philadelpia: Saunders; 1979.
- Fleagle JG. Primate Adaptation and Evolution. San Diego: Academic Press; 1999.
- Frets GP. Beiträge zur vergleichenden Anatomie und Embryologie der Nase der Primaten. II. Die Regio ethmoidalis des Primordialcraniums mit Deckknochen von einigen Platyrrhinen Affen. Gegenbaurs Morph Jahrb. 1913;45:557–726.
- Göbbel L. Ontogenetic and phylogenetic transformations of the lacrimal-conducting apparatus among Microchiroptera. Mamm Biol. 2002;67:338–357.
- Halpern M. Nasal chemical senses in reptiles: structure and function. In: Gans C, Crew D, editors. Biology of the Reptilia Physiology E, Hormones, Brain and behavior. Vol. 18. Chicago: University Chicago Press; 1992. pp. 424–532.
- Hill WCO. Primates, Comparative Anatomy and Taxonomy II Haplorhini: Tarsioidea. Edinburgh: Edinburgh University Press; 1955.
- Hillenius WJ, Rehorek SJ. Harderian gland and vomeronasal organ – an ancient collaboration? Am Zool. 1997;37:60A.
- Hillenius WJ. Septomaxilla of nonmammalian synapsids: Soft-tissue correlates and a new functional interpretation. J Morph. 2000;245:29–50. [PubMed]
- Hillenius WJ, Watrobski LK, Rehorek SJ. Passage of tear duct fluids through the nasal cavity of frogs. J Herp. 2001;35:701–704.
- Hillenius WJ, Rehorek SJ. From the eye to the nose: ancient orbital to vomeronasal communication in tetrapods? In: Mason RT, LeMaster MP, Müller-Schwarze D, editors. Chemical Signals in Vertebrates 10. New York: Springer; 2005. pp. 228–241.
- Hofer HO. The anatomical relations of the Ductus vomeronasalis and the occurrence of taste buds in the Papilla palatina of Nycticebus coucang (Primates, Prosmiae) with remarks on strepsirhinism. Gegenbaurs Morph Jahrb. 1977;123:836–856. [PubMed]
- Hofer HO. The external nose of Tarsius bancanus borneanus Horsfield, 1821 (Primates, Tarsiiformes) Folia Primatol. 1979;32:180–192. [PubMed]
- Hofer HO. The external anatomy of the oro-nasal region of primates. Z Morph Anthropol. 1980;71:233–249. [PubMed]
- Larsen WJ. Human Embryology. London: Churchill Livingstone; 1997.
- Maier W. Nasal structures in Old and New World primates. In: Ciochon R, Chiarelli AB, editors. Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum; 1980. pp. 219–241.
- Martin RD. Primate Origins and Evolution: a Phylogenetic Reconstruction. Princeton: Princeton University Press; 1990.
- Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ. Molecular phylogenetics and the origins of placental mammals. Nature. 2001;409:614–618. [PubMed]
- Negus V. The Comparative Anatomy and Physiology of the Nose and Paranasal Sinuses. London: Livingstone; 1958.
- Nickel R, Schummer A, Seiferle E. The Viscera of the Domestic Animals. 2. Berlin: Verlag Paul Parey; 1979.
- Paulsen F. The human nasolacrimal ducts. Adv Anat Embryol Cell Biol. 2003;170:1–106. [PubMed]
- Pocock RI. On the external characters of the lemurs and Tarsius. Proc Zool Soc Lond. 1918;1918:19–53.
- Poran NS, Vandoros A, Halpern M. Nuzzling in the gray short-tailed opossum I: delivery of odors to vomeronasal organ. Physiol Behav. 1993;53:959–967. [PubMed]
- Pratt CWM. The morphology of the ethmoidal region of Sphenodon and lizards. Proc Zool Soc Lond. 1948;118:171–201.
- Rehorek SJ. Squamate Harderian gland: an overview. Anat Rec. 1997;248:301–306. [PubMed]
- Rehorek SJ, Hillenius WJ, Quan W, Halpern M. Passage of the Harderian gland secretions to the vomeronasal organ of Thamnosis spp. (Serpentes, Colubridae) Can J Zool. 2000;78:1284–1288.
- Rossie JB. Ontogeny and homology of the paranasal sinuses in Platyrrhini (Mammalia: Primates) J Morph. 2006;267:1–40. [PubMed]
- Roux GH. The cranial development of certain Ethiopian ‘insectivores’ and its bearing on the mutual affinities of the group. Acta Zool. 1947;28:165–397.
- Rowe N. Pictorial Guide to Living Primates. New York: Pogonias Press; 1996.
- Schaeffer JP. The Nose, Paranasal Sinuses, Nasolacrimal Passageways, and Olfactory Organ in Man. Philadelphia: P. Blakiston's Son; 1920.
- Schilling A. L'organe de Jacobson du lémurien malgache Microcebus murinus (Miller, 1907) Mém Mus Natn Hist Nat Paris (ns), A (Zool) 1970;61:203–280.
- Schmidt A, Wake MH. Olfactory and vomeronasal systems of Caecilia. J Morph. 1990;205:255–268.
- Seiffert ER, Simons EL, Attia Y. Fossil evidence for an ancient divergence of lorises and galagos. Nature. 2003;422:421–424. [PubMed]
- Sevel D. Development and congenital abnormalities of the nasolacrimal apparatus. J Pediatr Ophthalmol Strabismus. 1981;18:13–19. [PubMed]
- Smith TD, Siegel MI, Bhatnagar KP. Observations on the vomeronasal organ of prenatal Tarsius bancanus borneanus with implications for ancestral morphology. J Anat. 2003a;203:473–481. [PMC free article] [PubMed]
- Smith TD, Bhatnagar KP, Bonar CJ, Shimp KL, Mooney MP, Siegel MI. Ontogenetic characteristics of the vomeronasal organ in Saguinus geoffroyi and Leontopithecus rosalia with comparisons to other primates. Am J Phys Anthropol. 2003b;121:342–353. [PubMed]
- Sperber GH. Craniofacial Embryology. Boston: Wright; 1989.
- Starck D. Das Cranium eines Schimpansenfetus (Pan troglodytes[Blumenbach 1799]) von 71 mm SchStlg., nebst Bemerkungen über die Körperform von Schimpansenfeten. Gegenbaurs Morph Jahrb. 1960;100:559–647.
- Starck D. Das Cranium von Propithecus spec. (Prosimiae, Lemuriformes, Indriidae) Bibl Primat. 1962;1:163–196.
- Starck D. The skull of the fetal chimpanzee (chondrocranium and development of osteocranium) In: Bourne GH, editor. The Chimpanzee. Basel: Karger; 1973. pp. 1–33.
- Starck D. The nasal cavity and nasal skeleton of Tarsius. In: Niemitz C, editor. Biology of Tarsiers. Stuttgart: Fischer Werlag; 1984. pp. 275–290.
- Stephan H, Frahm H, Baron G. New and revised data on Volumes of brain structures in insectivores and primates. Folia Primatol. 1981;35:1–29. [PubMed]
- Wible JR, Bhatnagar KP. Chiropteran vomeronasal complex and the interfamilial relationships of bats. J Mamm Evol. 1996;3:285–314.
- Wöhrmann-Repenning A. The relationship between Jacobson's organ and the oral cavity in a rodent. Zool Anz. 1980;204:391–399.
- Wöhrmann-Repenning A. Functional aspects of the vomeronasal complex of mammals. Zool Jb Anat. 1991;121:71–80.
- Wöhrmann-Repenning A, Bergmann M. The vomeronasal complex in strepsirhine primates and Tarsius. Mamm Biol. 2001;66:257–258.
- Woollard HH. The anatomy of Tarsius spectrum. Proc Zool Soc Lond. 1925;70:1071–1184.
- Zeller U. Morphogenesis of the mammalian skull with special reference to Tupaia. In: Kuhn H-J, Zeller U, editors. Morphogenesis of the Mammalian Skull. Hamburg: Parey; 1987. pp. 17–50.
- Zeller U, Wible JR, Elsner M. New ontogenetic evidence on the septomaxilla of Tamandua and Choloepus (Mammalia, Xenarthra), with a reevaluation of the homology of the mammalian septomaxilla. J Mammal Evol. 1993;1:31–46.