close

Вход

Забыли?

вход по аккаунту

?

Perinatal size and maturation of the olfactory and vomeronasal neuroepithelia in lorisoids and lemuroids.

код для вставкиСкачать
American Journal of Primatology 69:74–85 (2007)
RESEARCH ARTICLE
Perinatal Size and Maturation of the Olfactory and
Vomeronasal Neuroepithelia in Lorisoids and Lemuroids
TIMOTHY D. SMITH1,2, LAURA J. ALPORT3, ANNE M. BURROWS2,4,
KUNWAR P. BHATNAGAR5, JOHN C. DENNIS6, PRAPHUL TULADHAR1,
6
AND EDWARD E. MORRISON
1
School of Physical Therapy, Slippery Rock University, Slippery Rock, Pennsylvania
2
Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania
3
Department of Anthropology, University of Texas at Austin, Austin, Texas
4
Department of Physical Therapy, Duquesne University, Pittsburgh, Pennsylvania
5
Department of Anatomical Sciences and Neurobiology, University of Louisville School of
Medicine, Louisville, Kentucky
6
Department of Anatomy, Physiology and Pharmacology, College of Veterinary Medicine,
Auburn University, Auburn, Alabama
Explanations for the chemosensory abilities of newborn mammals focus
primarily on food (milk) acquisition and communication (e.g., maternal–
infant bonding). However, the relative importance of the main and
accessory (vomeronasal) olfactory systems is hypothesized to differ at
birth between altricial and precocial mammals. Strepsirrhines (lemurs
and lorises) possess main and accessory olfactory systems, and vary in
life-history traits related to infant dependency and maturation. Accordingly, this study examines the size and maturational characteristics of
vomeronasal (VNNE) and olfactory (OE) neuroepithelia in strepsirrhines.
Serially sectioned heads of 18 infant cadavers were examined microscopically for neuroepithelial distribution. Measurements were taken on
the length of the nasal fossa on one side that was occupied by VNNE and
OE. The data were corrected for body size using the cranial length or
body mass, and were then examined for correlation with several lifehistory variables, as well as activity pattern. In addition, immunohistochemistry was used to identify cells in the VNNE and OE that express
olfactory marker protein (OMP), a marker of mature olfactory neurons.
Relative OE extent was not significantly correlated with any of the lifehistory variables. Relative VNNE length was negatively correlated with
relative gestation length and relative neonatal mass (Po0.05). However,
when we corrected for phylogenetic relationships, we found no significant
correlations between either of the neuroepithelial measurements and lifehistory variables. Immunohistochemical findings suggest that OE has
more OMP-reactive cells than VNNE in all species. OMP-reactive cells
Contract grant sponsor: Slippery Rock University; Contract grant sponsor: Federal Aviation
Administration; Contract grant number: 01-6-022; Contract grant sponsor: U.S. Army Robert
Morris Acquisition Center; Contract grant number: N66001-1099-0072.
Correspondence to: Timothy D. Smith, School of Physical Therapy, Slippery Rock University,
Slippery Rock, PA 16057. E-mail: tdsmith@gmail.com
Received 5 July 2005; revised 23 October 2005; revision accepted 25 October 2005
DOI 10.1002/ajp.20328
Published online in Wiley InterScience (www.interscience.wiley.com).
r 2006 Wiley-Liss, Inc.
Perinatal Size and Maturation of the Olfactory / 75
appear to be less numerous in diurnal species compared
nocturnal species. These results indicate that the VNNE
relatively longer at birth in altricial species. However, it
uncertain how phylogeny and/or ontogeny may explain these
Am. J. Primatol. 69:74–85, 2007. c 2006 Wiley-Liss, Inc.
Key
words: accessory olfaction;
ontogeny; precocial
chemosensation;
to most
may be
remains
findings.
development;
INTRODUCTION
Most mammals can be developmentally categorized as altricial (helpless, with
eyes closed) or precocial (mobile and alert at a very early age) according to their
degree of dependency at birth [Grand, 1992]. The rate of maturation of the
olfactory system is known to vary between these categories. Behaviorally, it is
known that precocial mammals may be able to develop bonds with the mother at a
relatively early age based on the availability of olfactory cues [Jäckel & Trillmich,
2003]. The rate at which the main olfactory bulbs acquire an adult-like
organization differs between precocial and altricial mice (i.e., they are more
organized at an earlier postnatal age in precocial mammals) [Brunjes, 1983; Leon
et al., 1984]. Similar differences in the accessory olfactory bulb may exist between
altricial (most mice) and precocial (pigs and sheep) mammals [Salazar & Sánchez
Quinteiro, 2003; Salazar et al., 2003; 2004]. Studies have revealed stark
developmental and functional contrasts; however, some apparently contradictory
findings have been reported for altricial mammals. For instance, the potential for
chemostimulus access to the vomeronasal organ differs between rats and mice
[Coppola et al., 1993; Coppola & Millar, 1994]. Thus, it is possible that not all
chemical senses, or not all aspects of them, vary similarly among altricial
mammals. Alternately, olfactory maturation may not categorically relate to
altriciality or precociality, but to specific life-history traits that help to define
these categories.
Virtually no work has assessed components of the main olfactory system
(MOS; see Table I) or accessory olfactory system (AOS) in a broad taxonomic
sample of newborn primates [Shimp et al., 2003]. Primates are variously
considered to be precocial [Martin, 1990] or altricial [Nicolson, 1984] depending
on the criteria used to categorize them. When both neural and somatic
development are considered together, primates are considered intermediate in
the spectrum, with poor neuromotor function but relatively well-developed
special senses [Derrickson, 1992; Grand, 1992; Mennella et al., 2001; Schaal et al.,
2001, 2003]. These characteristics make primates a unique testing group to
TABLE I. Abbreviations of Terms Used in Text
AOS, accessory olfactory system
CAIC, comparative analysis of independent contrasts
MOS, main olfactory system
NFL, nasal fossa length
OE, olfactory neuroepithelium
OMP, olfactory marker protein
PrIn, prosthion-inion length
VNNE, vomeronasal neuroepithelium
VNNEL, vomeronasal neuroepithelium length
Am. J. Primatol. DOI 10.1002/ajp
76 / Smith et al.
determine which attributes of the neonatal lifestyle may relate to variation in
olfactory structures at birth. Within the primate order, Strepsirrhini are known
to possess a demonstrably functional MOS and AOS [Aujard, 1997; Dennis et al.,
2004; Hedewig, 1980; Smith et al., 2001], and thus they are the focus of our study.
In the present investigation we asked whether peripheral olfactory structures
vary in association with life-history traits that relate to infant maturation and
dependency. We also asked whether MOS or AOS characteristics vary in
association with diurnality, cathemerality, and nocturnality, because activity
patterns are frequently associated with primate olfactory abilities [Martin, 1990].
To address these questions, we analyzed the relative size (i.e., corrected for body
size) of the peripheral receptor organs for the MOS and AOS (olfactory (OE) and
vomeronasal (VNNE) neuroepithelia, respectively) in a sample of infant
strepsirrhines. These variables were tested for associations with four characteristics that define altriciality/precociality: relative neonatal body size, gestation
length, nest use/non-use, and lactation period [Martin, 1990; Grand, 1992; Ross,
2001; Ross, 2003]. These four life-history variables were selected because they
vary across primate taxa more than other defining characteristics of precociality.
Because early maturation of the MOS and AOS has been associated with infant
precociality by some authors [Evans, 2003; Wöhrmann-Repenning & BarthMüller, 1994], we predicted that primates with longer gestation, later weaning
age, relatively larger neonatal weights, and lack of nest use would have relatively
better developed olfactory structures at birth. More specifically, we predicted that
more precocial primates would have relatively larger neuroepithelia with a
relatively larger proportion of mature olfactory neurons, as evidenced by
expression of olfactory marker protein (OMP).
MATERIALS AND METHODS
A sample of 18 infant strepsirrhine primates was studied (Table II). The
sample included four species of galagids, three species of cheirogaleids, six species
of lemurids, and one indriid. All of the primates died of natural causes at the Duke
University Primate Center (DUPC), Durham, North Carolina. Most specimens
were originally fixed and stored in formalin. In three cases, specimens were
obtained as deep frozen cadavers, and were immediately fixed in formalin. Prior
to dissection, gross measurements were taken of each specimen, including cranial
length (prosthion-inion). Subsequent procedures involving preparation of heads
for serial sectioning (in the coronal plane at 10–12 mm) and staining were
previously described in detail by Smith et al. [2002, 2004]. In the present study, at
least every fifth section was mounted on glass slides for analysis. In addition,
selected unstained sections were mounted for immunohistochemical study (see
below).
For quantitative study, each stained section was examined with a Leica
DMLB photomicroscope. Measurements of chemosensory neuroepithelial length
were carried out as follows: Every 10th section of the nasal fossa was examined for
the presence of VNNE or OE (because of the potentially small length of the
VNNE, every fifth section was examined near the anterior and posterior points,
for greater accuracy). These neuroepithelia differed from the epithelium of the
remainder of the nasal cavity in that they possessed numerous rows of round, pale
receptor nuclei. This epithelium was adjacent to nonsensory types of epithelia
that were devoid of receptor neuron nuclei. This included the low, usually
nonciliated pseudostratified epithelium found dorsolaterally in the vomeronasal
organ, or the pseudostratified columnar respiratory epithelium (the latter
Am. J. Primatol. DOI 10.1002/ajp
f
m
–
m
m
m
m
f
f
f
m
f
m
m
f
–
m
m
a
a
a
a
a
a
a
a
a
a
a
b
a
a
b
b
a
a
Preservationa Sexb
0
1
0
2
0
1
0
5
1
0
0
1
0
1
1
2
0
0
C
N
C
N
C
C
C
C
C
N
N
N
N
N
N
N
N
C
132
123
135
110
120
129
129
135
135
142.5
142.5
132.5
132.5
62
60
87
87
140
0.1337
–0.0257
–0.0287
0.1107
–0.0068
–0.0711
–0.0264
0.0174
0.0174
0.1457
0.1457
–0.0552
–0.0552
0.0008
–0.1091
–0.1102
–0.1102
0.0275
140
45
135
92
159.00
135.00
152.00
142
142
132
132
108.3
108.3
61
40
86
86
181.5
36.02
24.81
35.67
21.05
44.32
48.41
43.31
43.25
40.25
38.08
40.26
46.02
47.94
24.93
19.41
27.02
25.52
49.26
3.1
1.9
3.2
1.6
3
3.096
3.1
2.3
1.45
2.55
1.35
3.4
3.35
2.7
2.85
4.1
3.75
3.4
0.230
0.218
0.215
0.216
0.196
0.170
0.203
0.153
0.101
0.219
–
–
0.172
0.310
0.401
0.414
0.408
0.170
10.8
6.58
11.34
6.2
–
11.7
10.2
8.9
6.5
7.4
–
–
10.1
7.7
5.6
7.7
7
10.9
0.800
0.756
0.850
0.838
–
0.642
0.667
0.594
0.474
0.635
–
–
0.518
0.884
0.789
0.778
0.761
0.545
c
b
Preservation: a, immersed in formalin after death; b, frozen and later immersed in formalin.
Sex: m, male; f, female.
Age: day 0 denotes newborn or stillborn.
d
Data on nest use/carry from Ross [2001]: N, nest; C, carried. All other life history variables were obtained or calculated from Kappeler & Pereira [2003]; supplemented by data
from Nash [1993] and Lindenfors [2002].
Relative neonatal weight, residuals of log10 neonatal mass against log10 adult female mass; PrIn, prosthion-inion length; –, no data available; OE, olfactory neuroepithelium (from
one side of the nasal fossa); VNNEL, vomeronasal neuroepithelium length (from one side of the nasal fossa); NFL, nasal fossa length.
a
Eulemur fulvus
Eulemur macaco
Eulemur mongoz
Lemur catta
Lemur catta
Hapalemur griseus
Hapalemur griseus
Varecia variegata
Varecia variegata
Cheirogaleus medius
Microcebus murinus
Mirza coquereli
Mirza coquereli
Propithecus
verreauxi
Galagoides
demidoff
Galago moholi
Otolemur
crassicaudatus
Otolemur garnettii
Species
OE
OE
Relative Weaning
VNNEL VNNEL/ extent
extent/
Age
Nest/ Gestation neonatal
age
(days)c carryd (days)d
weight
(days)d PrIn (mm) (mm) NFL ratio (mm) NFL ratio
TABLE II. Preservation, Sex, Age Group, Cranial Length, and Neuroepithelial Measurements Used in the Study
Perinatal Size and Maturation of the Olfactory / 77
Am. J. Primatol. DOI 10.1002/ajp
78 / Smith et al.
possessing short cilia), which generally abutted the OE. The anterior start points
and posterior end points were recorded as section numbers. The difference
between the start- and end-point section numbers was multiplied by the section
thickness in each specimen to obtain the length of the VNNE and the
anteroposterior extent of the OE.
For analysis, activity patterns were categorized as diurnal, cathemeral, or
nocturnal [Rowe, 1996]. Data on life-history variables for each species, including
neonatal body mass, female body mass, length of gestation (days), age at weaning
(days), and nest use/non-use, were collected from the literature (mainly Ross
[2001] and Kappeler and Pereira [2003], supplemented by data from Nash [1993]
and Lindenfors [2002]). All continuous data were log10 transformed.
To correct for differences in body size, residuals were calculated with leastsquares regressions. As a measure of neonatal body mass relative to the size of the
mother, residuals were calculated for neonatal and adult female body mass
(referred to as the relative neonatal body mass). Both gestation length and
weaning age were significantly correlated with prosthion-inion length (PrIn)
(r 5 0.758, Po0.001; r 5 0.885, Po0.001, respectively). Therefore, residuals were
calculated for gestation length and PrIn, and for weaning age and PrIn (hereafter
termed the relative gestation length and relative weaning age). OE was also
significantly correlated with PrIn (r 5 0.77, Po0.001). Thus, residuals were
calculated for OE and PrIn. VNNEL was not correlated with PrIn (r 5 0.15,
P40.05). In this case, absolute VNNEL and residuals for VNNEL and PrIn were
analyzed.
Continuous variables were analyzed using Pearson correlation tests
(Table III). Categorical variables were tested using Mann-Whitney U-tests and
Kruskal-Wallis tests. To correct for the effects of phylogeny, we also analyzed the
data with a comparative analysis of independent contrasts (CAIC) using CAIC
software from Purvis and Rambaut [1995] with the associated phylogeny. Branch
lengths were not included. Significance was set at Po0.05.
Selected specimens (those found to have little or no artifactual damage to the
VNNE or OE) were used for immunohistochemistry. Mounted tissue sections
were deparaffinized in Hemo-D (Scientific Safety Products, Keller, TX), hydrated
to distilled water (dH2O). To abolish endogenous peroxidase-like activity, the
sections were incubated in absolute methanol made to 0.9% hydrogen peroxide
(H2O2) for 20 min at room temperature (23.5–251C). Subsequently the tissues
were washed in dH2O and then in 10 mM phosphate-buffered saline (PBS)
(2.7 mM KCl, 137 mM NaCl) (Sigma, St. Louis, MO). The tissues were incubated
TABLE III. Pearson Correlation Coefficients of the Log10 and Relative VNNE and
Relative OE Length Measurements with Life History Variables
Life history variable
Relative gestation length
Relative weaning age
Relative neonatal mass
Log10 VNNEL
Relative VNNE length
r 5 –0.512
r 5 –0.517
r 5 –0.049 ns
r 5 –0.587
r 5 –0.050 ns
r 5 –0.614
Relative OE extent
r 5 –0.125 ns
r 5 0.094 ns
r 5 –0.126 ns
Po0.05.
Po0.01.
VNNEL, length of vomeronasal neuroepithelium (mm); OE extent, anteroposterior extent of olfactory
neuroepithelium (mm); PrIn, prosthion-inion distance (mm); relative VNNE length, log10VNNEL – log10PrIn
residual; relative OE extent, log10OE extent – log10PrIn residual; relative gestation length, log10gestation (days) –
log10PrIn residual; relative weaning age, log10weaning age (days) – log10PrIn residual; relative neonatal mass,
log10female neonatal mass – log10adult, nonpregnant female mass residual; ns, not significant at Po0.05.
Am. J. Primatol. DOI 10.1002/ajp
Perinatal Size and Maturation of the Olfactory / 79
TABLE IV. Reactivity to Olfactory Marker Protein
Species
Eulemur macaco
Lemur catta
Microcebus murinus
Mirza coquereli
Galago moholi
Otolemur garnetti
VNNE
Reference figure
OE
Reference figure
1
–a/1
11
–
11
11
—
2b (newborn); 2c (5-day-old)
—
—
—
2a
11
1
11
11
11
11
—
2e (5-day-old)
—
—
—
2d
a
No reactivity in newborn; few reactive cells in 5-day-old infant.
11, numerous reactive cells; 1, few reactive cells; –, no reactive cells.
for 20 min in the appropriate blocking solution (5% normal serum (Sigma) of the
species in which the secondary antibody was made and 2.5% BSA (Sigma) in
PBS), and then washed briefly in PBS. The tissue sections were left overnight in
the primary antibody (OMP), which was appropriately diluted in blocking
solution. OMP is a neuronal marker of mature olfactory neurons [Margolis, 1980].
The sections were treated with biotinylated secondary antibodies (Vector,
Burlingame, CA) diluted 1:200, and then treated with ABC Elite reagent (Vector),
reacted with diaminobenzidine (Vector), dehydrated, and mounted with VectaMount (Vector). Alexa-conjugated secondaries (Molecular Probes, Carlsbad, CA)
were diluted at 1:500, mounted with VectaShield (Vector), and sealed with clear
nail polish. Sections were microscopically examined and described regarding the
density of OMP (1) cells. Specimens were rated relative to each other as having
numerous, few, or no reactive cells in the OE/VNNE (Table IV).
RESULTS
In all of the strepsirrhine neonates/infants examined in this study, VNNE
length ranged from 1.35 to 4.1 mm and OE extent ranged from 5.6 to 11.7 mm
(Table II). Proportionally, VNNE length ranged from 15% (L. catta) to 41%
(M. coquereli) of the nasal fossa length, and OE extent ranged from 52%
(V. variegata) to 88% (C. medius) of nasal fossa length. Scatterplots of absolute
measurement values (Fig. 1) showed a linear relationship of OE extent and
cranial length, whereas VNNE length was more variable. Notably, the VNNEs of
the cheirogaleids were similar to or longer than those of larger strepsirrhines
(Fig. 1).
Log10 and relative VNNE length were both significantly (Po0.05) negatively
correlated with relative gestation length and relative neonatal mass (Table III,
Fig. 1). No other correlations were significant (Table III). Mann-Whitney U-tests
revealed no significant difference in log10 VNNE length (Z 5 –0.134, P40.05),
relative VNNE length (Z 5 –0.267, P40.05), or relative OE extent (Z 5 –1.04,
P40.05) between infant strepsirrhines that were kept in nests and those that
were carried only. Kruskal Wallis tests indicated no significant differences
(P40.05) between strepsirrhines with different activity patterns in VNNE or OE
measurements. There were no significant associations between the life-history
Fig. 1. Scatterplots of absolute VNNE length (a) and absolute OE extent (b) against cranial length
(prosthion-inion) in strepsirrhines. Filled symbols indicate primates that use nests, and open
symbols indicate non-nesting species. Scatterplots of relative VNNE length (c, e, and g), and
relative OE extent (d, f, and h) against relative gestation length (c and d), relative weaning age
(e and f), and relative neonatal mass (g and h).
Am. J. Primatol. DOI 10.1002/ajp
80 / Smith et al.
Am. J. Primatol. DOI 10.1002/ajp
Perinatal Size and Maturation of the Olfactory / 81
Fig. 2. Immunoreactivity of OMP in the VNNE (a–c) and OE (d and e) of selected strepsirrhines.
Open arrows indicate reactive receptor neurons. Otolemur garnetti (a) had more numerous OMP
(1) cells in the VNNE than Lemur catta at birth (b, no reactive cells) and at 5 days of age (c, only a
few reactive cells). In O. garnetti (d) and 5-day-old L. catta (e), OMP(1) cells were more numerous
in the OE than in the VNNE. ON, olfactory nerves; VNC, vomeronasal cartilage; VNN, vomeronasal
nerves. Scale bars 5 100 mm. [Color figure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]
variables and the anatomical variables when phylogeny was accounted for using
an analysis of independent contrasts.
Immunohistochemical findings are presented in Table IV and Fig. 2. The
highest density of OMP-reactive VNNE/OE neurons appeared to occur in the two
galagids analyzed. as well as in Microcebus murinus. In contrast, two lemurids
studied appeared to have a lower density of OMP-reactive cells in the OE or
VNNE (Table IV, Fig. 2b,c, and e), and M. coquereli showed no OMP-reactivity
in the VNNE. Most species showed a relatively higher reactive-cell density in the
OE compared to the VNNE (Fig. 2a,b,c,d,e).
DISCUSSION
Several lines of evidence indicate that the ontogeny of the MOS and AOS
varies among mammals. Histochemical and morphological indicators have been
used to assess the appearance of ‘‘adult-like’’ olfactory structures during various
subadult stages [Brunjes, 1983; Leon et al., 1984; Salazar et al., 2003, 2004]. Some
studies have linked morphological maturation to the timing of initial olfactory
Am. J. Primatol. DOI 10.1002/ajp
82 / Smith et al.
performance. In the spiny mouse (Acomys cahirinus), a rare example of a highly
precocial rodent, both morphological and behavioral indicators point to the
development of olfactory functionality at a relatively early age compared to other
rodents [Leon et al., 1984; Porter & Ruttle, 1975]. According to Leon et al. [1984],
the timing of behavioral indicators of olfactory competence, such as the first
response to maternal odors, appears to relate to the same stage of olfactory bulb
maturation in different species of rodents. Based on morphological evidence, a
precocious functionality of the AOS was also suggested for pigs and sheep [Salazar
et al., 2003, 2004; Wöhrmann-Repenning & Barth-Müller, 1994]. The selection for
characteristics relating to early olfactory function (particularly AOS) may be
linked to an early ‘‘autonomous lifestyle’’ in some mammals [WöhrmannRepenning & Barth-Müller, 1994]. Because primates are moderately precocial
mammals [Grand, 1992] and vary with regard to life-history characteristics
[Martin, 1990], they provide a valuable model for investigating whether early
development of olfactory structures is linked to specific life-history variables.
Based on the traditional analyses presented herein, the VNNE shows a clear
(negative) association with relative gestation length and relative neonatal mass.
Conversely, analyses of independent contrasts revealed no significant associations. Thus, the results of our traditional analyses may reflect phylogenetic
characteristics. In particular, gestation length may be especially subject to
phylogenetic inertia [Martin et al., 2005]. Indeed, cheirogaleids cluster as a group
with a long VNNE, moderately extensive OE distribution, and short gestation
relative to body size. However, because of our small sample size, very few
contrasts were generated. The apparent trends seen in scatterplots (e.g., both
lemurids and galagids appeared to have negative associations of VNNE length
and OE extent with relative gestation length) suggest that further work with
larger samples is required.
Although phylogeny may play an important role in the association between
the VNNE and precociality, we can suggest an adaptive basis for these results.
First, limitations in the present study should be noted. Previous studies that
quantified the VNNE and OE frequently used measurements such as length or
volume as a proxy for receptor neuron population size. Linear distance
measurements are thought to relate less closely to neuronal numbers than other
measurements, such as volume [Dawley, 1998]. Moreover, it has been argued
elsewhere that neuronal density is a critical variable in comparisons of
chemosensory structures [Smith et al., 2004]. Indeed, the OE of neonatal
Microcebus murinus was qualitatively described by Smith and Bhatnagar [2004]
as being comparatively densely packed with neuronal nuclei, which indicates that
the volume measurements may accordingly correspond to relatively large
numbers of receptor cells. Data on a subset of specimens used in this study
(i.e., those suitable for three-dimensional reconstruction (T.D. Smith, unpublished data from six specimens)), indicate that VNNE length is highly correlated
with the cube root of the VNNE volume (r 5 0.9286). A smaller data set available
for OE surface area suggests a somewhat poorer relationship between OE extent
and the square root of the OE surface area, perhaps owing to the more
complicated distribution of the OE along turbinals and in recesses. Thus, the
degree to which VNNE length and OE extent relate to neuronal numbers is
unknown and potentially quite important.
With the above caveats in mind, the findings of the present study suggest that
relative to body size, small neonates born after a short gestation have the largest
VNNE. Our results are in contrast to findings on total brain mass, which show
positive associations with life-history variables such as lifespan and age at first
Am. J. Primatol. DOI 10.1002/ajp
Perinatal Size and Maturation of the Olfactory / 83
reproduction (with gestation length showing a poorer correlation [Deaner et al.,
2003]). This contrast to findings on total brain mass suggests that the negative
association found in this study may be an adaptive pattern. It is possible that
species with more altricial life-history traits use a more developed AOS in order to
form mother–infant bonds. This appears to differ with suggestions that the AOS
is particularly important for precocial infants [Evans, 2003; WöhrmannRepenning & Barth-Müller, 1994]. However, previous studies did not explicitly
test for a positive association between specific life-history variables and the
VNNE. In addition, it is possible that the AOS functions uniquely, in a temporal
sense, in primates. In support of this possibility, immunohistochemical findings
suggest that there are different degrees of maturation among species and between
the two olfactory systems. The apparent differences in OMP-reactive cell density
most likely reflects differences in the number of mature receptor neurons in the
AOS compared to the MOS. Certain species had very few OMP-reactive cells at
birth in the VNNE (Lemur catta had none at day 0, although few OMP-reactive
cells were seen in a 5-day-old L. catta), whereas OMP reactivity was more
widespread in the OE.
As an aside, this and other studies support the idea that the timing of VNNE
maturation varies among primates [Dennis et al., 2004; Evans, 2003]. A clear
pattern is difficult to discern in primates at this point, and it is premature to
suggest an association with life-history traits or activity pattern. Immunohistochemical studies of a larger range of taxa will be crucial to determine whether
such relationships exist. Finally, since some variables cannot be controlled in
studies involving animals that died natural deaths in captivity, additional
analyses are needed to verify our results.
Further investigation into the relationship between chemosensory function
and the life-history characteristics of primates may reveal important associations.
It is known that the MOS and AOS vary differently in association with social
behavior [Alport, 2004]. Our results suggest the same is true of the association
between the MOS and AOS and certain life-history variables. Thus, further
studies must illuminate the relationship of the partially overlapping, distinctive
functions of the AOS, MOS, and gustation with life history, social behavior,
and diet.
ACKNOWLEDGMENTS
The authors acknowledge grant support from Slippery Rock University (to
T.D.S.) and the U.S. Army Robert Morris Acquisition Center (]N66001-1099-0072
to E.E.M.). We thank C.J. Bonar for providing access to a neonatal specimen of
Eulemur mongoz, and B. Docherty for help with staining some of the slides. The
authors are grateful to Dr. Frank Margolis for the generous gift of the anti-OMP
antisera used in this study, and to two anonymous reviewers for their comments.
This is DUPC publication ]1000.
REFERENCES
Alport LJ. 2004. Comparative analysis of the
role of olfaction and the neocortex in
primate intrasexual competition. Anat Rec
281A:1182–1189.
Aujard F. 1997. Effect of vomeronasal organ
removal on male socio-sexual responses to
female in a prosimian primate (Microcebus
murinus). Physiol Behav 62:1003–1008.
Brunjes PC. 1983. Olfactory bulb maturation
in Acomys cahirinus: is neural growth
similar in precocial and altricial murids?
Brain Res 284:335–341.
Coppola DM, Budde J, Millar LC. 1993. The
vomeronasal duct has protracted postnatal
development in the mouse. J Morph 218:
59–64.
Am. J. Primatol. DOI 10.1002/ajp
84 / Smith et al.
Coppola DM, Millar LC. 1994. Stimulus access
to the accessory olfactory system in the
prenatal and perinatal rat. Neuroscience
60:463–468.
Dawley EM. 1998. Species, sex, and seasonal
differences in VNO size. Microsc Res
Technol 41:506–518.
Deaner RO, Barton RA, van Schaik CP. 2003.
Primate brains and life histories: renewing
the connection. In: Kappeler PM, Pereira
ME, editors. Primate life histories and
socioecology. Chicago: University of Chicago
Press. p 233–265.
Dennis JC, Smith TD, Bhatnagar KP, Bonar
CJ, Burrows AM, Morrison EE. 2004.
Expression of neuron-specific markers by
the vomeronasal neuroepithelium in six
primate species. Anat Rec 281A:1190–1200.
Derrickson EM. 1992. Comparative reproductive strategies of altricial and precocial
mammals. Func Ecol 6:57–65.
Evans C. 2003. Vomeronasal chemoreception
in vertebrates. A study of the second nose.
London: Imperial College Press. 265p.
Grand TI. 1992. Altricial and precocial mammals: a model for neural and muscular
development. Zoo Biol 11:3–15.
Hedewig R. 1980. Vergleichende anatomische
untersuchungen an den Jacobsonschen organen von Nycticebus coucang Boddaert,
1785 (Prosimiae, Lorisidae) und Galago
crassicaudatus E. Geoffroy, 1812 (Prosimiae, Lorisidae). II. Galago crassicaudatus.
Gegenbaurs Morphol Jahrb 126:676–722.
Jäckel M, Trillmich F. 2003. Olfactory individual recognition of mothers by young
guinea-pigs (Cavia porcellus). Ethology 109:
197–208.
Kappeler PM, Pereira ME. 2003. Primate life
histories and socioecology. Chicago: University of Chicago Press. 395p.
Leon M, Coopersmith R, Ulibarri C, Porter
RH, Powers JB. 1984. Development of
olfactory bulb organization in precocial
and altricial rodents. Brain Res 314:45–53.
Lindenfors P. 2002. Sexually antagonistic
selection on primate size. J Evol Biol 15:
595–607.
Margolis FL. 1980. A marker protein for the
olfactory chemoreceptor neuron. In: Bradshaw RA, Schneider D, editors. Proteins
of the nervous system. New York: Raven
Press. p 59–84.
Martin RD. 1990. Primate origins and evolution: a phylogenetic reconstruction. Princeton: Princeton University Press. 804p.
Martin RD, Genoud M, Hemelrijk CK. 2005.
Problems of allometric scaling analysis:
examples from mammalian reproductive
biology. J Exp Biol 208:1731–1747.
Mennella JA, Jagnow CP, Beauchamp GK.
2001. Prenatal and postnatal flavor learning
by human infants. Pediatrics 107:E88.
Am. J. Primatol. DOI 10.1002/ajp
Nash LT. 1993. Juveniles in nongregarious
primates. In: Pereira ME, Fairbanks LA,
editors. Juvenile primates: life history,
development, and behavior. Oxford: Oxford
University Press. p 119–137.
Nicolson NA. 1984. Infants, mothers, and
other females. In: Smuts BA, Cheney DL,
Seyfarth RM, Wrangham RW, Struhsaker
TT, editors. Primate societies. Chicago:
University of Chicago Press. p 330–342.
Porter RH, Ruttle K. 1975. The responses
of one-day old Acomys cabirinus pups
to naturally occurring chemical stimuli.
Z Tierpsychol 38:154–162.
Purvis A, Rambaut A. 1995. Comparative
analysis by independent contrasts (CAIC):
an Apple Macintosh application for analysing comparative data. Comp Appl Biosci
11:247–251.
Ross C. 2001. Park or ride? Evolution of infant
carrying in primates. Int J Primatol 22:
749–771.
Ross C. 2003. Life history, infant care strategies, and brain size in primates. In: Kappeler PM, Pereira ME, editors. Primate life
histories and socioecology. Chicago: University of Chicago Press. p 266–284.
Rowe N. 1996. Pictorial guide to living
primates. New York: Pogonias Press. 263p.
Salazar I, Sánchez Quinteiro P. 2003. Differential development of binding sites for four
lectins in the vomeronasal system of juvenile
mouse: from the sensory transduction site to
the first relay stage. Brain Res 979:15–26.
Salazar I, Lombardero M, Aleman N, Sánchez
Quinteiro P. 2003. Development of the
vomeronasal receptor epithelium and the
accessory olfactory bulb in sheep. Microsc
Res Tech 61:438–447.
Salazar I, Sánchez Quinteiro P, Lombardero
M, Aleman N, Fernandez de Troconiz P.
2004. The prenatal maturity of the accessory olfactory bulb in pigs. Chem Senses 29:
3–11.
Schaal B, Coureaud G, Marlier L, Soussignan
R. 2001. Fetal olfactory cognition preadapts
neonatal behavior in mammals. In: Marchlewska-Koj A, Lepri JJ, Müller-Schwarze
D, editors. Chemical signals in vertebrates
IX. New York: Kluwer Academic/Plenum
Publishers. p 197–204.
Schaal B, Coureaud G, Langlois D, Ginies C,
Semon E, Perrier G. 2003. Chemical and
behavioural characterization of the rabbit
mammary pheromone. Nature 424:68–72.
Shimp KL, Bhatnagar KP, Bonar CJ, Smith
TD. 2003. Ontogeny of the nasopalatine
duct in primates. Anat Rec 274A:862–869.
Smith TD, Siegel MI, Bhatnagar KP. 2001.
A reappraisal of the vomeronasal system
of catarrhine primates: ontogeny, morphology, functionality, and persisting questions. Anat Rec (New Anat) 265:176–192.
Perinatal Size and Maturation of the Olfactory / 85
Smith TD, Bhatnagar KP, Shimp KL,
Kinzinger JH, Bonar CJ, Burrows AM,
Mooney MP, Siegel MI. 2002. Histological
definition of the vomeronasal organ
in humans and chimpanzees with a comparison to other primates. Anat Rec 267:
166–176.
Smith TD, Bhatnagar KP. 2004. Microsmatic
primates: reconsidering how and when size
matters. Anat Rec 279B:24–31.
Smith TD, Bhatnagar KP, Tuladhar P, Burrows
AM. 2004. Distribution of olfactory epithelium in the primate nasal cavity: are ‘‘microsmia’’ and ‘‘macrosmia’’ valid morphological
concepts? Anat Rec 281A:1173–1181.
Wöhrmann-Repenning A, Barth-Müller U.
1994. Functional anatomy of the vomeronasal complex in the embryonic development
of the pig (Sus-scrofa dom.). Acta Theriol
39:313–323.
Am. J. Primatol. DOI 10.1002/ajp
Документ
Категория
Без категории
Просмотров
3
Размер файла
209 Кб
Теги
perinatal, neuroepithelial, vomeronasal, lemuroids, maturation, size, lorisoids, olfactory
1/--страниц
Пожаловаться на содержимое документа