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Diurnality and cone photopigment polymorphism in strepsirrhines Examination of linkage in Lemur catta.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 122:66 –72 (2003)
Diurnality and Cone Photopigment Polymorphism in
Strepsirrhines: Examination of Linkage in Lemur catta
Gerald H. Jacobs1* and Jess F. Deegan II2
1
Neuroscience Research Institute and Department of Psychology, University of California, Santa Barbara,
California 93106
2
Department of Psychology, California State University, Bakersfield, California 93311
KEY WORDS
lemurs; cones; electroretinogram; opsins; primate evolution
ABSTRACT
Trichromatic color vision is routine
among catarrhine primates, but occurs only as a variant
form of color vision in some individuals in most platyrrhine genera. This arises from a fundamental difference in
the organization of X-chromosome cone opsin genes in
these two lineages: catarrhines have two opsin genes specifying middle- and long-wavelength-sensitive cone pigments, while platyrrhines have only a single gene. Some
female platyrrhine monkeys achieve trichromacy because
of a species polymorphism that allows the possibility of
different opsin gene alleles on the two X-chromosomes.
Recently, a similar opsin gene polymorphism was detected
in some diurnal strepsirrhines, while at the same time
appearing to be absent in any nocturnal genera. The aim
of this study was to assess whether cone pigment polymorphism is inevitably linked to diurnality in strepsirrhines.
Cone photopigments were measured in a species usually
classified as diurnal, the ring-tailed lemur (Lemur catta),
using electroretinogram flicker photometry, a noninvasive
electrophysiological procedure. Each of 12 animals studied
was found to have the same middle-wavelength cone pigment, with peak sensitivity at about 547 nm. In conjunction with earlier results, this implies that cone pigment
polymorphism is unlikely to exist in this species and that,
accordingly, such variation is not a consistently predictable feature of vision in diurnal strepsirrhines. Am J Phys
Anthropol 122:66 –72, 2003. © 2003 Wiley-Liss, Inc.
Many extant strepsirrhines are nocturnal. In accordance with this lifestyle, the retinas of these animals are heavily rod-dominated and lack foveas
(Rohen and Castenholtz, 1967), and their eyes also
typically contain a reflective tapetum (Wolin and
Massopust, 1970; Pariente, 1979). All these features
are characteristic of the adaptations for nocturnal
vision classically observed in many different mammals (Walls, 1942). A number of species from two
strepsirrhine families (Lemuridae and Indridae) depart from this pattern in having activity rhythms
that are described as either diurnal or crepuscular,
or in some cases, as cathemeral, i.e., including both
nocturnal and diurnal characteristics (Tattersall,
1987; van Schaik and Kappeler, 1996; Rowe, 1996;
Curtis and Rasmussen, 2002). Despite striking differences in their circadian behaviors, the eyes of
these latter species often (although not inevitably)
share a number of adaptational features found in
the eyes of nocturnal strepsirrhines including, for
example, tapeta and afoveate retinas. A conventional interpretation of these facts is that primitive
primates were nocturnal and that progression to the
more diurnal lifestyles has occurred secondarily in a
minority of strepsirrhine lines (Martin, 1990).
Studies of mammalian cone photopigments and
color vision conducted over the past 20 years seem
generally consistent with this view. The retinas of
most mammals either contain two classes of cone
that set the stage for dichromatic color vision, or
alternatively, in some species, a gene mutation has
reduced the cone pigment complement from two to
one, leaving such animals without color vision capacity (Jacobs, 1993, 1996). Among all eutherian
mammals, only primates have the three classes of
cone photopigment needed to support trichromatic
color vision, and even within the order, there is
considerable variation in the details of biology that
allow trichromacy. Specifically, catarrhine monkeys,
apes, and humans were found to have multiple Xchromosome opsin genes that specify spectrally distinct middle-wavelength-sensitive (M) and longwavelength-sensitive (L) cone pigments. In
conjunction with an autosomal gene that expresses
short-wavelength-sensitive (S) cone pigment, this
arrangement provides the photopigment basis for
©
2003 WILEY-LISS, INC.
Grant sponsor: National Eye Institute; Grant number: EY02052.
*Correspondence to: Gerald H. Jacobs, Neuroscience Research Institute, University of California, Santa Barbara, CA 93106.
E-mail: jacobs@psych.ucsb.edu
Received 17 December 2002; accepted 5 March 2003.
DOI 10.1002/ajpa.10309
STREPSIRRHINE DIURNALITY/PHOTOPIGMENT POLYMORPHISM
trichromatic color vision (Nathans et al., 1986). In
striking contrast, most platyrrhine monkeys are
polymorphic at a single X-chromosome opsin gene
site. This polymorphism allows females heterozygous at this gene site to produce two types of M/L
pigments and, with an S-cone photopigment that all
monkeys share in common, to achieve trichromatic
color vision (Jacobs, 1998a). Note that the nature of
this arrangement renders homozygous females and
all males as obligatory dichromats. Beyond this general pattern, across-species variations have also
been found, both in the spectral absorption properties of the M/L photopigments and in the number of
M/L gene alleles. Finally, members of two genera
(Aotus and Alouatta) have distinctly different arrangements from those of any other New World
monkeys. Aotus has only a single functional cone
pigment and thus lacks color vision capacity (Jacobs
et al., 1993), while members of Alouatta are like the
catarrhines in routinely having three types of cone
pigment and apparent trichromatic color vision (Jacobs et al., 1996b). The result of all this variation is
rich mixture of color vision phenotypes distributed
across the platyrrhines.
The photopigments and color vision of strepsirrhines have not received nearly as much attention
as that accorded the haplorrhines. Results from two
studies that assessed the cone photopigment complements in brown lemurs (Eulemur fulvus), ringtailed lemurs (Lemur catta) (Jacobs and Deegan,
1993), and greater bushbabies (Otolemur crassicaudatus) (Deegan and Jacobs, 1996) were taken to
suggest that color vision in strepsirrhines in general
might be most similar to that of nonprimate mammals. This conclusion was based on the findings that
each of these three species apparently had only a
single X-chromosome opsin gene site, while one of
them (the bushbaby) had additionally suffered loss
of function of its S-cone opsin gene as a result of
mutational changes (Jacobs et al., 1996c). Given this
understanding, it was a surprise when a recent
study involving a large-scale screening of M/L strepsirrhine opsin genes revealed the presence of polymorphic variation in 3 of 20 species examined: Coquerel’s sifaka (Propithecus verreauxi coquereli), the
red-ruffed lemur (Varecia variegata rubra), and the
greater dwarf lemur (Cheirogaleus major) (Tan and
Li, 1999). In each of these three species, two M/L
opsin gene alleles were detected, and further examination of the inferred amino-acid sequences of the
allelic versions of the opsin gene led to the prediction
that these specified two spectrally distinct M/L pigments. Subsequent analysis indicated that the claim
for polymorphism in the greater dwarf lemur was
probably based on a sample misidentification and is
therefore not correct (Y. Tan, personal communication). Measurements of photopigments documented
the variable presence of M/L cone photopigments in
the retinas of Coquerel’s sifaka and the black-andwhite-ruffed lemur (Varecia variegata variegata)
(Jacobs et al., 2002; Jacobs and Deegan, 2003b). In
67
each species, individual females were found that had
both classes of M/L pigment present in their retinas.
By analogy to the results from studies of platyrrhine
monkeys, this arrangement predicts the presence of
trichromatic color vision in some individual strepsirrhines, in addition to variant forms of dichromatic
color vision.
Based on their observations of cone opsin polymorphism in some strepsirrhines and on the phylogenetic distribution of the M and L opsin gene alleles
in this group, Tan and Li (1999) were led to suggest
that, counter to the traditional view, the common
ancestor of the strepsirrhines may have been
trichromatic. Since vertebrate trichromacy seems
inherently incompatible with nocturnality, this implied that these ancestral primates were also diurnal. This issue was recently analyzed by Heesy and
Ross (2001), who reconstructed the activity patterns
in fossil primates through an examination of the
evolution of a number of features of visual systems.
Their results reinforced the traditional view in implying that both nocturnality and dichromacy are
primitive traits for primates, and that shifts from
nocturnality have occurred only sporadically among
the strepsirrhines. This conclusion is also supported
by the results of a comparative analysis of orbit size
in fossil and extant primates (Kay and Kirk, 2000).
The three strepsirrhine species in which the biological basis for trichromatic color vision has so far
been shown to exist are all diurnal. That linkage
raises the question as to whether the acquisition of
an M/L opsin gene polymorphisms is a characteristic
of all diurnal strepsirrhines, or whether perhaps the
coexistence of diurnality and M/L polymorphism is
happenstance. A test case on this matter is offered
by the ring-tailed lemur, an animal judged diurnal
in most accounts (Sussman, 1999; Macdonald,
2001). The earlier pigment measurements made on
four members of this species revealed only a single
type of M/L photopigment (Jacobs and Deegan,
1993), and a later genetic examination of a single
member of this species supports that view (Tan and
Li, 1999). Although these results are consistent with
the conclusion that ring-tailed lemurs lack an M/L
cone pigment polymorphism, the number of animals
so far studied is too few to yield much confidence in
that conclusion. To provide further insight into this
issue, we used an electrophysiological technique,
electroretinogram (ERG) flicker photometry, to
study the cone photopigment complements of additional animals. Our results add support to the contention that this strepsirrhine does not have an M/L
cone photopigment polymorphism.
METHODS
ERG flicker photometry is a noninvasive procedure in which electrical signals evoked in the outer
retina by the presentation of stimulus lights are
sensed from a contact-lens electrode placed on the
corneal surface of the eye. We have frequently employed this technique to make spectral sensitivity
68
G.H. JACOBS AND J.F. DEEGAN
measurements and so draw inferences about photopigments in a range of different species. The physical features of the recording setup and details of
this procedure were fully described elsewhere (Jacobs et al., 1996a), so only a brief account is provided
here.
In this procedure, a train of temporally alternating flashes of light derived from two beams of an
optical system are imaged so that they fall in register onto the retina in Maxwellian view in the form of
a 59° circle. One of these lights originates from a
50-W tungsten-halide lamp and serves as a reference stimulus; the other, the test stimulus, comes
from a high-intensity grating monochromator
(10-nm half-bandwidth). A third beam of the optical
system, also originating from a tungsten-halide
lamp, is used as required to provide accessory adaptation. The ERGs generated by the test and reference lights are electronically compared and, over
presentations, the test light is adjusted in radiance
until the ERG it elicits is the same as that produced
by the reference light. Repeat equations made using
this procedure seldom vary by an amount greater
than 0.04 log units (Jacobs et al., 1996a). The intensity relationship between the two lights at the point
of equation defines one point on a spectral sensitivity function. Repetition of this procedure for a range
of different test wavelengths then permits the derivation of a complete spectral sensitivity function.
The ERGs are differentially recorded, and the amplified signals are windowed by a sinusoid that is set
to the frequency of the stimulus train. For each
experiment, the window position is initially adjusted
so as to maximize its correlation with the ERG signal. The comparison of the responses to test and
reference lights is based on the averages of the last
50 of 70 responses elicited from each source.
Two experiments were run on each animal. First,
complete spectral sensitivity functions were derived.
For this procedure, the stimulus rate was set to
31.25 Hz. The reference light was achromatic (2,450
K) and provided a retinal illuminance of 3.3 log td.
Photometric equations were made between the reference light and monochromatic test lights that
were successively varied in 10-nm steps from 450 to
640 nm. Two complete runs were made across this
spectral span, and the resulting pair of equations
was averaged. For any individual test wavelength
where the two equation values differed by more than
the 0.04 log unit, a third measurement was made,
and these results also contributed to the final mean
value. A second experiment provided an explicit test
of whether the eye contained more than one type of
M/L cone pigment. It followed a procedure first used
and validated on platyrrhine monkeys (Jacobs and
Neitz, 1987). For this test, ERG flicker photometric
equations were made between a 540-nm test light
and a 630-nm reference light (pulse rate ⫽ 31.25
Hz). These equations were obtained during a period
while the eye was being alternately adapted either
to bright 540-nm or 630-nm light. As for the spectral
sensitivity measurements, the photometric equations were made twice, and the resulting values
were then averaged. The adaptation lights were first
adjusted in intensity so that each produced the same
threshold elevation (0.5 log units) for a 560-nm test
light presented at 31.25 Hz. In this experiment, the
spectral properties of the reference and adaptation
lights were controlled by placing different interference filters (half-energy passband ⫽ 10 nm) into the
stimulus beams. Finally, a spectral sensitivity function was obtained for one animal under scotopic test
conditions. To accomplish this, the animal was initially dark-adapted for 15 min. Subsequently, spectral sensitivity measurements were carried out in a
darkened room, with the stimulus pulse rate reduced to 12.5 Hz and with the reference light
dimmed to yield a retinal illuminance of 1.5 log td.
In the fashion described above, wavelengths from
440 – 600 nm were then tested at 10-nm steps.
Recordings were obtained from 12 (10 male, 2
female) adult (age range, 12–20 years) ring-tailed
lemurs (Lemur catta). According to the American
Zoo and Aquarian Association (AZA) Studbook
records, two of these animals were siblings, but none
of the other subjects had a shared parentage. Recordings were made during the course of routine
physical examinations conducted on these animals
at the Santa Ana Zoo (Santa Ana, CA). Each animal
was initially anesthetized with isofluorane (5%) delivered through a mask. Subsequently, the animals
were intubated and maintained on 1.5–2% isofluorane for the duration of the recording session.
Heart rate, expired CO2, and body temperature were
monitored throughout the experiments. The cornea
of one eye was anesthetized by topical application of
proparacaine hydrochloride (0.5%), and the pupil
was dilated with mydriacyl (0.5% tropicamide). The
ERG electrode was installed and the animal was
positioned for recording with the aid of a specially
designed head holder that had no pressure points.
The recordings were conducted in a lighted room
that provided about 150 lux of ambient illumination
at the position of the test eye. All of the experimental procedures were conducted in accordance with
the National Institutes of Health guidelines on the
care and use of animals.
RESULTS
The flicker rate used in these experiments exceeded the 30-Hz photopic standard defined for human clinical ERG recording (Marmor and Zrenner,
1999), thus insuring that the signals recorded reflected cone activity. With these test conditions,
highly reliable signals were recorded from each of
the animals studied. The sensitivity functions obtained from members of this sample were remarkably consistent in their spectral shapes, as can be
seen in Figure 1, where we plotted mean spectral
sensitivity values (⫾1 SD) obtained from 12 ringtailed lemurs. That there are no obvious differences
among these animals can be inferred from the very
STREPSIRRHINE DIURNALITY/PHOTOPIGMENT POLYMORPHISM
69
Fig. 2. Results from a test of middle- to long-wavelength
response univariance in two species of strepsirrhine. Plotted are
differences (given in log units) in ERG photometric equations
obtained for a 540-nm test light and a 630-nm reference light
when eye was steadily exposed to either 540-nm or 630-nm adapting lights. Individual data points were for tests earlier run on
Coquerel’s sifakas (Jacobs et al., 2002). Shown are results for
animals having either one (triangles) or two (circles) types of M/L
photopigments. Equation values obtained for 12 ring-tailed lemurs are shown above, where horizontal line encompasses the
entire range of variation in equations measured for this group.
Fig. 1. Spectral sensitivity function for ring-tailed lemur.
Data points represent mean sensitivity values for 12 animals, as
derived from ERG flicker photometric measurements. Error bars
show ⫾ 1 SD. Continuous line is best-fit photopigment absorption
curve (␭max ⫽ 547.9 nm).
small variations in the sensitivity values recorded
across the spectrum: for a total of 20 test points, the
mean SD value was 0.036 log unit. The continuous
line drawn through the data points represents the
best-fitting single photopigment absorption function. To derive this fit, a visual pigment template
(Govardovskii et al., 2000) was progressively shifted
along the wavelength axis in steps of 0.1 nm to
determine the spectral location providing the best
least-squares fit to the entire data array. The values
of Figure 1 were not corrected for any possible intraocular filtering, and they thus reflect corneally
derived spectral sensitivity. With that restriction,
the best-fit template derived for this grouped data
has a spectral peak value (␭max) of 547.9 nm. An
additional indication of the small dispersion of spectral data across subjects is that individual spectral
fits made for the 12 subjects yielded a mean ␭max of
546.2 nm (SD ⫽ 1.26).
The second experiment was a test for spectral
response univariance, and it provided an explicit
means for assessing whether the retinas of these
ring-tailed lemurs contained more then a single type
of M/L photopigment. The assumption underlying
this test is that if there is only a single M/L pigment,
then the photometric match made between 540-nm
and 630-nm lights will remain invariant, irrespective of the nature of any chromatic adaptation. On
the other hand, if more than one type of M/L pigment is present, then the equation will change as a
function of the character of the chromatic adaptation, so that relatively more 540-nm light will be
required when the eye is exposed to 540-nm adap-
tation, and relatively less 540-nm light will be required when the adaptation is shifted to 630 nm.
Figure 2 illustrates results obtained from such tests.
Plotted for context are results of the identical test
obtained from an earlier experiment run on Propithecus verrauxi coquereli, a strepsirrhine that, as
noted above, has an M/L cone polymorphism (Jacobs
et al., 2002). Shown are the differences (expressed in
log units) in the 540/630-nm equations obtained for
the two adaptation conditions. The retinas of 7 of
these animals (triangles in Fig. 2) contained only a
single type of M/L pigment having a peak sensitivity
at either 545 nm or 558 nm. Note that there is no
significant change in the equation value recorded for
the two test conditions. The retinas of two other
female members of this species contained both of
these types of cone pigment and, as can be seen, they
(solid circles in Fig. 2) showed clear shifts in the
equation values obtained for the two chromatic adaptation conditions. As indicated by the full range of
equation values plotted in Figure 2, none of the
ring-tailed lemurs showed any hint of significant
differential adaptation, and so we conclude that
none of these animals had more than a single type of
M/L cone pigment.
In the earlier study of photopigments in lemurs, a
spectral sensitivity function was obtained from one
subject under test conditions expected to index rod
activity (Jacobs and Deegan, 1993). The resulting
function had a spectral peak slightly longer than
might seem typical for a mammalian rhodopsin. To
see if that result could be replicated, we measured a
spectral sensitivity function for one of the subjects of
this experiment under similar scotopic test conditions. The resulting spectral sensitivity function is
given in Figure 3 where, as in the fashion described
above, the data array (solid circles) was best fit to a
photopigment absorption template. The ␭max for the
best fit curve of Figure 3 is 509.5 nm.
70
G.H. JACOBS AND J.F. DEEGAN
Fig. 3. Scotopic spectral sensitivity function obtained from
ring-tailed lemurs, using ERG flicker photometric measurements. Circles represent values obtained from an animal examined in current experiments; those for another animal (triangles)
are from earlier published measurements (Jacobs and Deegan,
1993). Fitted photopigment absorption curve has a peak value of
509.5 nm.
DISCUSSION
Each of the 12 ring-tailed lemurs examined was
found to have only a single type of M/L cone photopigment, and analysis of the measured spectra
indicates (Fig. 1) that pigment was shared in common by each animal. These results are thus indistinguishable from what was found in 4 animals previously studied with ERG flicker photometry (Jacobs
and Deegan, 1993) and in a single subject whose M/L
cone opsin genes were recently examined (Tan and
Li, 1999). Of the total of 17 animals that have been
examined in the current study and the two previous
ones, 3 were female. Since these opsin genes are
X-chromosome-linked, this means that the 20 Xchromosomes sampled from ring-tailed lemurs were
all found to have the same M/L opsin gene. To examine the implications of this result, two-sided confidence intervals were computed based on this single
proportion (Newcombe, 1998). The results of this
test indicate that the true proportion of ring-tailed
lemur X-chromosomes harboring this same gene lies
somewhere in the range between 83.9 –100% (P ⫽
0.05). Our survey thus suggests that if a second M/L
pigment exists in ring-tailed lemurs, it must be
present only at quite a low proportion (⬍16%).
Obviously, the study of a very much larger sample
of animals would be required to achieve reasonable
certainty that Lemur catta formally lacks an M/L
cone pigment polymorphism. In the absence of such
an expanded sample, it is nevertheless useful to ask
how likely it is that a polymorphism exists at a
frequency as low as or lower than that implied by
the above analysis. One line of evidence that could
bear on the matter comes from studies of M/L cone
polymorphisms conducted in other nonhuman primates. Most of these studies necessarily involved
only relatively small numbers of subjects, but in
cases where the samples were more sizable, there
are reasons to believe that the polymorphic genes in
these species are represented at approximately
equal frequency. The evidence for this conclusion is
drawn most directly from the proportion of heterozygous females detected in these polymorphic species.
For example, the polymorphism of squirrel monkeys
(Saimiri) features three versions of the M/L pigment, and around two thirds of all females are found
to be heterozygous (Jacobs, 1998b), while in spider
monkeys (Ateles), where there appear to be only two
M/L alleles, roughly 50% of the females are heterozygous (Jacobs and Deegan, 2001). In both of
these cases, the incidence of female heterozygosity
(and thus predicted trichromacy) is close to what
would be expected if the allelic versions of the M/L
genes are equally frequent in the population. One
explanation for this correlation is that the polymorphism in these species is maintained by heterozygous advantage, thus ensuring relatively equal representation of the polymorphic genes. Making the
reasonable assumption that there may be similar
advantages for presence of trichromatic color vision
in other primates would in turn lead to the expectation that in strepsirrhines there should also be nearequal representation of any polymorphic M/L opsin
genes. Since the strepsirrhines known to be polymorphic have only two versions of the M/L opsin
gene (Tan and Li, 1999), this suggests that these two
versions should be about equally frequent in the
population. Given the number of animals tested to
date (see above), a calculation based on the binomial
sampling distribution shows the probability of there
being two equally frequent M/L alleles in L. catta to
be vanishingly low (9.5 ⫻ 10⫺7). Accordingly, we
suggest that ring-tailed lemurs probably do not have
some (as yet undetected) low-frequency M/L cone
polymorphism; rather, they probably lack such variation entirely.
The current results can also provide further insight into strepsirrhine photopigments. Our earlier
measurements of the spectral sensitivity of the M
cone of the ring-tailed lemur yielded an estimated
peak value of 546 nm (Jacobs and Deegan, 1993).
That location is extremely close to the one derived
from the current measurements (from Fig. 1, a value
of 547.9 nm) and, indeed, most of the residual difference between the results of the two experiments
reflects the fact that the photopigment template in
current use routinely predicts peak values slightly
longer than the metric we used a decade ago (Jacobs
and Deegan, 2003a). Although very consistent
across animals, these values do not necessarily give
an accurate account of the photopigment absorption
spectra. To properly infer those estimates requires
STREPSIRRHINE DIURNALITY/PHOTOPIGMENT POLYMORPHISM
knowledge about any spectral filtering within the
eye and of the pigment density in the cones of ringtailed lemurs. ERG spectral sensitivity measurements made at shorter wavelengths than those here
reported (unpublished) provided an indication that,
as in the eyes of many other diurnal animals (Douglas and Marshall, 1999), the lens of the ring-tailed
lemur provides some preferential absorption of
short-wavelength light. This could be particularly
relevant for the present sample, where many of the
subjects were quite old. One strategy that can be
used to minimize such influence is to truncate the
spectral sensitivity function so that it is based only
on those values for test locations of 520 nm and
longer, a portion of the spectrum that is relatively
immune to influence from any primate preretinal
filters (Sharpe et al., 1998). Following that procedure, and making the further assumption that the
cones of ring-tailed lemurs might have a pigment
optical density of 0.15, we refitted the averaged data
obtained from the 12 subjects. The result is an estimated M-cone peak value of 545.8 nm.
Spectral sensitivity measured under scotopic test
conditions for a single ring-tailed lemur yielded a
function (Fig. 3) quite similar to the one previously
obtained for this species (Jacobs and Deegan, 1993).
A template best fit to the averaged data from both
animals has a peak value of 509.4 nm. This scotopic
curve is thus shifted somewhat toward long wavelengths, relative to what might be expected for typical rod-based primate vision. Adding an assumption
about cone pigment density will shift the peak of
this function somewhat toward the shorter wavelengths (e.g., using a pigment density value of 0.3
moves the peak to 507 nm). Even this is long-wavelength-shifted relative to the peak value of 501 nm
reported for direct microspectrophotometric measurements made on rods in the retina of another
lemur, the black lemur (Eulemur macaco; Bowmaker, 1991). One possible explanation for this residual deviation is that tapetal reflection may have a
relatively greater impact on scotopic spectral sensitivity than it does on measurements made under
photopic conditions.
Following effectively identical procedures, we
measured M-cone spectral sensitivity in representatives of three genera of diurnal strepsirrhines (Lemur, Propithecus, and Varecia). If one uses the analysis assumptions described above, the spectral
properties of M-cone photopigments of these three
are quite similar, with derived M-cone peaks as follows: Lemur, 545.8 nm, n ⫽ 12; Propithecus, 545.3
nm, n ⫽ 3; and Varecia, 547.4 nm, n ⫽ 1. None of
these measurements take into account any potential
influence that tapetal reflection may have on spectral sensitivity measured in the intact eye. We suggest that any such effects are likely to be slight for
two reasons: (1) none of the spectral sensitivity functions show obvious departures from the pigment
templates, as one might expect if tapetal reflection
were significantly influencing spectral sensitivity;
71
and (2) there are striking differences in the prominence of the tapetal reflex among these species (for
instance, on gross examination, tapetal reflection is
much more obvious in Propithecus than in Varecia;
indeed, Wolin and Massopust (1970) suggest that
Varecia does not have a tapetum), but despite that,
the shapes of the M-cone spectra are very similar for
the three genera. Within measurement error, it
seems likely that these strepsirrhines share in common their M-cone pigments.
The available evidence suggests that M/L cone
pigment polymorphism (and thus potential withinspecies variations in color vision) is infrequent
among the strepsirrhines. The only genera in which
polymorphism has been clearly documented are diurnal. But while diurnality seems likely to be a
necessary condition for M/L pigment polymorphism
to emerge as an adaptive trait, the survey results
from Lemur catta suggest that diurnality, by itself,
is not sufficient to predict M/L pigment polymorphism.
The absence of a compelling linkage between diurnality and M/L cone pigment polymorphism could
reflect nothing other than the stochastic nature of
the alterations in opsin genes required to shift the
absorption spectra of the cone pigments they specify,
and thus initiate a polymorphic condition. In that
view, Lemur catta may just be unlucky. On the other
hand, it may be worth remembering that simply
describing different animals as diurnal does not
mean that they have identical visual adaptations.
For instance, although we are not aware of any
modern examinations of photoreceptor distribution
and density in the ring-tailed lemur, cone density in
the central retina of Propithecus is twice that seen in
an equivalent region in the retina of the brown lemur (Eulemur fulvus), and there are corresponding
differences in overall cone/rod ratios of these animals (Peichl et al., 2001). This difference is potentially important, since an increased cone density
seems likely to enhance the likelihood that signals
from two different cone types get processed in the
neural networks of the retina in a fashion needed to
support color vision (Dacey, 1999), and so one could
argue that the retina of Propithecus provides a more
favorable substrate for the emergence of cone pigment polymorphism as an adaptive trait than does
the retina of the brown lemur. Of course, the activity
patterns of the brown lemur are typically judged to
be cathemeral, so the reader may find tenuous any
implications of this argument to the ring-tailed lemur. Against that, we note two things: first, that
field observations often suggest that ring-tailed lemurs are less stringently diurnal than, say, Propithecus (Jolly, 1966), and an analysis of several
social and morphological features of the gregarious
lemurs concluded that Lemur catta is “mainly diurnal” and that they, along with Propithecus, are not
yet “fully adapted to a diurnal life style” (van Schaik
and Kappeler, 1996). A second observation is that in
the course of doing parallel ERG recordings on Pro-
72
G.H. JACOBS AND J.F. DEEGAN
pithecus, Varecia, and Lemur, we gained the impression that cone-based signals are typically larger in
the former two than in the latter. That fact could
have a number of interpretations, including the possibility that the retinal cone mosaic of these species,
all often considered diurnal, varies in the manner
just suggested. Whether that is true or not, our
examination of the cone pigments in Lemur catta
suggests that it is unwise to automatically assume
that all strepsirrhines with diurnal traits have M/L
cone pigment polymorphisms and thus the prospect
for within-species color vision variations, including
potential female trichromacy.
ACKNOWLEDGMENTS
We are indebted to the staff at the Santa Ana Zoo
(Santa Ana, CA) for their cooperation and enthusiastic help during the course of these experiments.
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