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Color vision pigment frequencies in wild tamarins (Saguinus spp.)

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American Journal of Primatology 67:463–470 (2005)
Color Vision Pigment Frequencies in Wild Tamarins
(Saguinus spp.)
School of Biological Sciences, University of East Anglia, Norwich, England
Department of Anthropology, New York University and the New York Consortium in
Evolutionary Primatology (NYCEP), New York, New York
Scottish Primate Research Group, Department of Psychology, University of Stirling,
Stirling, Scotland
Department of Life Sciences, Anglia Polytechnic University, Cambridge, England
Department of Zoology, University of Cambridge, Cambridge, England
The adaptive importance of polymorphic color vision found in many New
World and some prosimian primates has been discussed for many years.
Polymorphism is probably maintained in part through a heterozygote
advantage for trichromatic females, as such individuals are observed to
have greater foraging success when selecting ripe fruits against a
background of forest leaves. However, recent work also suggests there
are some situations in which dichromatic individuals may have an
advantage, and that variation in color vision among individuals
possessing different alleles may also be significant. Alleles that confer a
selective advantage to individuals are expected to occur at a higher
frequency in populations than those that do not. Therefore, analyzing the
frequencies of color vision alleles in wild populations can add to our
understanding of the selective advantages of some color vision phenotypes over others. With this aim, we used molecular techniques to
determine the frequencies of color vision alleles in 12 wild tamarin groups
representing three species of the genus Saguinus. Our results show that
allele frequencies are not equal, possibly reflecting different selective
regimes operating on different color vision phenotypes. Am. J. Primatol.
67:463–470, 2005. c 2005 Wiley-Liss, Inc.
Key words: balancing selection; color vision; photopigment; polymorphism; tamarin
Contract grant sponsor: BBSRC; Contract grant number: 98/S11498; Contract grant sponsor: J.
William Fulbright Foreign Scholarship Board; Contract grant number: 1999/2000; Contract grant
sponsor: Wenner-Gren Foundation; Contract grant number: Gr. 6560; Contract grant sponsor:
L.S.B. Leakey Foundation; Contract grant sponsor: American Society of Primatologists.
Correspondence to: A.K. Surridge, School of Biological Sciences, University of East Anglia,
Norwich NR4 7TJ, England. E-mail:
Received 27 October 2004; revised 18 February 2005; revision accepted 10 March 2005
DOI 10.1002/ajp.20200
Published online in Wiley InterScience (
r 2005 Wiley-Liss, Inc.
464 / Surridge et al.
Eutherian mammals have a poor color sense compared to many birds and
reptiles. This is probably due to a loss of photopigments during the nocturnal
phase of their evolution. Primates, however, have uniquely re-evolved a form of
color vision. We have a good understanding of how this trichromatic color vision
has evolved in primates, as many of the molecular and physiological adaptations
accompanying this change are known (for a recent review see Jacobs and Rowe
[2004]). What is less well understood are the selective processes that led to the
evolution of color vision, and the reasons why primates alone evolved this sense.
The advantages offered by red-green color vision may involve a superior foraging
ability, as it appears that primate photopigments are optimized for detecting both
ripe fruit and young leaves against a dappled background of mature leaves
[Dominy & Lucas, 2001; Lucas et al., 1998; Osorio & Vorobyev, 1996; Regan et al.,
2001; Sumner & Mollon, 2000a,b].
Color vision in different primate species is remarkably variable. Primates
with three different opsin proteins (one short-wavelength sensitive (SWS) and
two middle- to long-wavelength sensitive (M- to LWS)) expressed in separate
classes of cone photoreceptors in the retina have trichromatic vision. Those with
two different opsin proteins (one SWS and one M- to LWS) have dichromatic
vision. Trichromacy has been achieved in two ways. In Old World primates (OWP)
and howler monkeys (Alouatta spp.), a gene duplication of the X-linked M- to LWS
locus has occurred. In most New World primates (NWP) and some prosimians, a
single X-linked M- to LWS locus has two or more alleles, giving heterozygous
females trichromacy [Jacobs, 1984; Mollon et al., 1984]. However, in these species
all males and homozygous females have dichromatic vision. This polymorphism
within species allows us to test hypotheses regarding the selective advantages of
color vision in primates by comparing the foraging abilities of individuals with
different vision phenotypes.
Experiments on captive marmosets have revealed a foraging advantage for
trichromatic individuals based on food color [Caine & Mundy, 2000; Caine et al.,
2003]. The same result was observed in a study of captive tamarins that used
naturalized color stimuli based on those encountered in the wild [Smith et al.,
2003a]. These studies reiterate the advantages of trichromacy over dichromacy
for finding food, and provide support for hypotheses evoking a role for
heterozygote advantage, as a form of balancing selection, in maintaining the
polymorphic color vision system in platyrrhines [Mollon et al., 1984].
However, this polymorphic color vision system found in some primates still
represents a puzzle [Surridge et al., 2003]. Opsin protein alleles have remained
unchanged, in both function and number, over long periods of evolutionary time
in the face of both selection and genetic drift [Surridge & Mundy, 2002]. An
inevitable conclusion from this is that photopigments, finely tuned by selection,
represent some form of adaptive peak that maintains a population containing
both dichromats and trichromats. This notion is difficult to reconcile with
the hypothesis that trichromacy is generally better than dichromacy. An
alternative (but not mutually exclusive) explanation for the stability of
the polymorphism is that frequency-dependent selection operates on different
color vision phenotypes in NWP [Mollon et al., 1984; Osorio et al., 2004]. Under
this model, allele frequencies could change over space and time, depending
on the availability of different food resources. Alleles that confer a selective
advantage to individuals are expected to occur at a higher frequency than those
that do not.
Am. J. Primatol. DOI 10.1002/ajp
Opsin Allele Frequencies in Wild Tamarins / 465
There is some preliminary evidence that allele frequencies are not equal in
callitrichid primates (marmosets and tamarins). In these species, three opsin
alleles are observed, with the intermediate allele (with lmax 5 556 nm) being
found at a lower frequency than the two extreme alleles (543 and 563 nm) in
previous studies [Rowe & Jacobs, 2004; Surridge & Mundy, 2002]. However,
many of the individuals used in those studies were housed in captive populations,
and small initial population sizes and inbreeding may result in allele frequencies
that do not resemble those found in wild populations. In the present study we
determined opsin allele frequencies in wild callitrichids (taxonomy following
Rylands et al. [2000]) to obtain deeper insights into the fascinating color vision
polymorphism of NWP.
Two mixed-species groups of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax) were observed for 164 full days (1,612 hr) from
January 2000 until December 2000 at the Estación Biológica Quebrada Blanco II
in northeastern Peru (41210 S, 731090 W). During this time fecal samples were
collected from individually identifiable animals for DNA extraction (for further
details see Smith et al. [2003b]). The samples were stored in 100% ethanol at
ambient temperature. Eight neighboring groups of red-bellied moustached
tamarins (S. labiatus) were live-trapped and sedated for genetic sample collection
between the months of April and June 2000 as part of a larger, 18-month
behavioral field study at the Tahuamanu Biological Station located in the
Department of Pando, northwestern Bolivia (111240 S, 69110 W). Hair samples were
tweezed from each animal and stored at ambient temperature until DNA was
DNA Analysis and Determination of Color-Vision Genotype
DNA was extracted from fecal samples with the use of a QIAamp DNA Stool
Kit (Qiagen, Crawley, UK), and from hair samples with a QIAamp DNA Minikit
(Qiagen, Crawley, UK) following the manufacturer’s recommended protocol. In
callitrichids, differences in spectral tuning among the three functional alleles
(543, 556, and 563 nm) have been attributed to substitutions at four amino acid
positions: position 180 in exon 3, positions 229 and 233 in exon 4, and position 285
in exon 5 [Shyue et al., 1998]. Although a recent report showed that positions in
exon 4 do not contribute significantly to functional changes in spectral alleles
[Hiramatsu et al., 2004], this exon was included in our typing process for
thoroughness. The combinations of amino acids at each of these respective sites
for each allele are as follows: 543 nm 5 Ala Ile Ser Ala; 556 nm 5 Ala Phe Ser Thr;
and 563 nm 5 Ser Phe Gly Thr. Color-vision status was determined for each
individual by polymerase chain reaction (PCR) and sequencing of exons 3, 4, and
5 of the X-linked opsin gene. The nucleotide substitutions that code for each
amino acid as described above were determined directly from DNA sequence
traces. Because the material used for DNA extraction (feces and hair) yield low
concentrations of genomic DNA, each of the three exons were amplified
individually, with the combination of nucleotides of all three used to determine
the genotype. All three exons were amplified in order to obtain three independent
amplifications (and therefore three replicates) per individual to eliminate
spurious results due to genotyping errors. The entire procedure (extraction,
Am. J. Primatol. DOI 10.1002/ajp
466 / Surridge et al.
amplification, and sequencing) was performed twice for fecal samples (on two
separately collected samples) to provide six replicates per individual and to
eliminate the chance of individuals being incorrectly assigned as homozygotes due
to allelic dropout (for further details see Surridge et al. [2002]). PCR and
sequencing were performed as described previously [Surridge & Mundy, 2002;
Surridge et al., 2002].
The observed allele frequencies were compared with those expected
(assuming that the frequency of each allele was equal in each population) by
means of Chi-square goodness-of-fit tests.
Color vision genotypes were obtained for 71 individuals (49 males and 22
females), yielding a total of 93 X chromosomes examined. The frequency of each
allele for each species is shown in Fig. 1. For S. mystax (15 X chromosomes in 12
individuals) the 543 nm allele is the most common in our sample, with the 556 nm
allele being absent. The numbers of each allele detected differ significantly from
that expected if the allele frequencies had been equal (w2 5 6.23, Po0.05). For
S. fuscicollis (17 X chromosomes in 12 individuals) the 556 nm allele is the most
common allele; however, the numbers of each allele detected do not differ from
the values expected with equal allele frequencies. For S. labiatus (61 X
chromosomes in 47 individuals) the 543 nm allele is again the most common
allele, with the 556 nm allele being the least common, and allele counts show a
significant deviation from equal-frequency expectations (w2 5 9.40, Po0.01). We
found no evidence for recombinant alleles in our sample of homozygous
individuals, in agreement with previous data for callitrichids [Surridge & Mundy,
2002]. However, because exons are amplified individually in the typing process,
haplotypes cannot be determined in heterozygous individuals. Putative recombinant alleles have been detected in capuchins [Boissinot et al., 1998] and squirrel
monkeys [Cropp et al., 2002].
S. mystax (n=15)
Saguinus labiatus (n=61)
S. fuscicollis (n=17)
Fig. 1. Frequencies of the three opsin alleles (with lmax at 543, 556, and 563 nm) in three species of
wild tamarins (Saguinus spp.). N 5 number of X-chromosomes examined.
Am. J. Primatol. DOI 10.1002/ajp
Opsin Allele Frequencies in Wild Tamarins / 467
Saguinus spp. (n=137)
Callithrix spp. (n=25)
Leontopithecus spp. (n=32)
Callimico goeldii (n=39)
Saimiri spp. (n=261)
Fig. 2. Frequencies of opsin alleles determined in previous studies. Data for Saguinus, Callithrix,
Callimico, and Leontopithecus are taken from Surridge and Mundy [2002]. Data for Saimiri are
from Cropp et al. [2002]. N 5 number of X-chromosomes examined.
For comparison, the allele frequencies for each genus of callitrichid sampled
in our previous study [Surridge & Mundy, 2002], together with those from a study
of squirrel monkeys (Saimiri spp. [Cropp et al., 2002]), are given in Fig. 2. For
Saguinus, Leontopithecus, and Callimico the observed number of each allele
differs significantly from that expected for equal frequency alleles, with the
556 nm allele being the rarest allele (the 556 nm allele was completely absent from
our sample of 39 Callimico X chromosomes) in all cases. In contrast, the 556 nm
allele was the most common allele in Callithrix; however, the number of observed
alleles did not differ from that expected for equal allele frequencies for either
Callithrix or Saimiri.
Allele Frequencies in Wild Tamarins Are Not Equal
Our sample of 93 wild tamarin X-chromosomes indicates that the frequencies
of opsin alleles are not equal. Some variation in allele frequencies across the three
species was observed, and notably the rarest allele (556 nm) in S. labiatus and
Am. J. Primatol. DOI 10.1002/ajp
468 / Surridge et al.
S. mystax was the most common allele in S. fuscicollis. S. fuscicollis and S. mystax
form mixed-species troops, with each species foraging preferentially in different
strata in the tropical rain-forests (S. fuscicollis is found at lower heights than its
congeners [Heymann & Buchanan-Smith, 2000]). This may account, in part, for
the differences in allele frequencies between the two species (illustrated in Fig. 1).
However, because of the relatively small number of chromosomes examined in
S. mystax and S. fuscicollis, together with the limited range of geographical
sampling, these results should be interpreted with some caution. Nevertheless,
when all three species are combined, our data from wild tamarins are in
agreement with that of our previous study of captive tamarins in revealing the
556 nm allele to be the rarest allele. In our sample of wild tamarins, the
frequencies of each allele were as follows: 543 nm 0.53, 556 nm 0.17, and 563 nm
0.30. The allele frequencies of the tamarin species in our previous study were
0.30, 0.15, and 0.55, respectively [Surridge & Mundy, 2002]. Over all callitrichid
primates analyzed to date, the average allele frequencies are 0.39, 0.17, and 0.44
(for 326 X-chromosomes).
Do Some Photopigments Have a Selective Advantage Over Others?
Our finding that the intermediate 556 nm allele is the least common allele in
wild tamarins provides some evidence that it may also be the allele that is least
favored by selection. This is in agreement with a study showing that the 543/
563 nm trichromat is expected to outperform either of the intermediate
trichromats (543/556 nm or 556/563 nm) at fruit detection, irrespective of the
effects of variable illumination [Osorio et al., 2004]. This effect was demonstrated
in a study of human observers in which visual stimuli were chosen to simulate
cone excitations as observed in the cones of callitrichids viewing fruit [Rowe &
Jacobs, 2004]. Similarly, in spider monkeys (in which alleles are of slightly
different lmax), modeling of fruit detection by different color-vision phenotypes
has shown that the 535/562 nm trichromat performs better than the intermediate
535/550 nm and 550/562 nm trichromats [Riba-Hernández et al., 2004].
Despite this apparent selective disadvantage for the intermediate opsin allele,
it has been maintained for several millions of years in callitrichids (with the
possible exception of Callimico, for which more data are needed to confirm
the presence or absence of this allele in the wild [Surridge & Mundy, 2002]).
There are two possible explanations for this. First, if trichromats always have an
advantage over dichromats, this allele would be maintained through a heterozygote advantage for trichromats carrying the allele (even though it may not be
favored among trichromats). Second, there may be an advantage for longerwavelength alleles in dichromats [Osorio et al., 2004]. Therefore, dichromats
carrying the 556 nm allele could be favored over those carrying the 543 nm allele.
Hence, this system with three alleles is balanced by selection for widely spaced
photopigments in trichromats and longer wavelength pigments in dichromats.
Furthermore, the presence of three alleles may represent a compromise between
a selective advantage of polymorphism whereby more alleles result in more
heterozygous individuals that are fitter, and a functional constraint on the opsin
Frequency-Dependent Selection and the Importance of Trichromacy to
If different color vision phenotypes have different levels of foraging fitness
depending on subtle differences in color and light [Osorio et al., 2004; Regan
Am. J. Primatol. DOI 10.1002/ajp
Opsin Allele Frequencies in Wild Tamarins / 469
et al., 2001], then individuals may forage within visually distinct niches [Tovée
et al., 1992], reducing competition from conspecifics. In this situation, allelic
polymorphism would be maintained by frequency-dependent selection, such that
alleles are most beneficial when they are rare. It is interesting to note that such
selection may operate above the species level. When allele frequencies of species
that form polyspecific associations (in this case S. fuscicollis and S. mystax) are
combined, they do not differ significantly from equal-frequency expectations
(w2 5 3.84; Pr0.20). Hence, alleles that might be favored in one species are
balanced by the favoring of different alleles in another species. Further support
for different roles for different phenotypes comes from the observation that
trichromatic marmosets perform poorly when faced with the task of detecting
camouflaged food items [Caine et al., 2003]. In the wild, cryptic food items (e.g.,
camouflaged insects) that are overlooked by trichromats may be detected by
conspecific dichromats [Mollon et al., 1984]. The role of cooperative behavior
within this system is obscure. To date there is no evidence to suggest that other
members of a group benefit from another individual’s trichromacy through social
foraging. In a study of foraging behavior of tamarins, trichromatic females did not
consistently lead the group to fruiting trees [Smith et al., 2003b].
In summary, while frequency-dependent selection would act to maintain
opsin polymorphism through long periods of time, differing opsin allele
frequencies support lines of evidence that suggest that some color vision alleles
have a selective advantage over others at this present point in evolutionary time
[Osorio et al., 2004]. Subtle differences in a species’ ecology might shift these
selective advantages, with a corresponding shift in allele frequencies. Further
studies on larger spatial and temporal scales are required to test this. Notably, no
correlates between opsin allele frequencies and biogeography or behavior were
detected in a study of squirrel monkeys [Cropp et al., 2002]. In addition, genetic
drift, migration, and social group composition (including mate choice and
inbreeding avoidance) may have important influences on allele frequencies. This
may be deduced from fine-scale analyses of wild primate groups. A comparative
study of foraging ecology across different platyrrhine genera (such as tamarins
and squirrel monkeys) with opsin alleles of different spectral sensitivities could
provide further insight into this fascinating color vision system.
We thank two anonymous reviewers for their comments on the manuscript.
This work was funded by the BBSRC (98/S11498 to H.M.B.-S. and N.I.M.).
Funding for fieldwork on Saguinus labiatus was provided by the J. William
Fulbright Foreign Scholarship Board (1999/2000), the Wenner-Gren Foundation
(grant no. Gr. 6560, 1999/2000), the L.S.B. Leakey Foundation (1999/2000), and
the American Society of Primatologists (Conservation Small Grant, 1999/2000).
Special thanks go to field assistants Stephanie Dammermann, Leeann Haggerty,
Rina Aviram, Laura Miller, Edilio Nacimiento, and Rafael Suárez. We are grateful
to Dr. E. Montoya of the Proyecto Peruano de Primatologia and Biologo R. Pezo of
the Universidad Nacional de la Amazonia Peruana (UNAP), Iquitos, Peru, for
help and support with logistical matters. Particular thanks are due to Ney
Shahuano, who provided unflagging assistance in the field.
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color, frequencies, pigment, saguinus, spp, vision, wild, tamarins
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