Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae)

Molecular Ecology (2006) 15, 551–558
doi: 10.1111/j.1365-294X.2005.02822.x
Blackwell Publishing Ltd
Polymorphism of visual pigment genes in the muriqui
(Primates, Atelidae)
M . G . T A L E B I ,* T . R . P O P E ,† E . R . V O G E L ,‡ M . N E I T Z § and N . J . D O M I N Y ‡
*Department of Biological Anthropology, University of Cambridge, Downing Street, Cambridge CB2 3DZ, UK, †Department of
Biological Anthropology and Anatomy, Box 90383, Biological Sciences Building, Duke University, Durham, North Carolina 27708,
USA, ‡Department of Anthropology, 1156 High Street, University of California, Santa Cruz, California 95064, USA, §Medical College
of Wisconsin, Department of Cell Biology, Neurobiology and Anatomy, 8701 Watertown Plank Road, Milwaukee, Wisconsin 53226,
USA
Abstract
Colour vision varies within the family Atelidae (Primates, Platyrrhini), which consists of
four genera with the following cladistic relationship: {Alouatta [Ateles (Lagothrix and
Brachyteles)]}. Spider monkeys (Ateles) and woolly monkeys (Lagothrix) are characteristic
of platyrrhine monkeys in possessing a colour vision polymorphism. The polymorphism
results from allelic variation of the single-locus middle-to-long wavelength (M/L) cone
opsin gene on the X-chromosome. The presence in the population of alleles coding for
different M/L photopigments results in a variety of colour vision phenotypes. Such a poly-
morphism is absent in howling monkeys (Alouatta), which, alone among platyrrhines,
acquired uniform trichromatic vision similar to that of Old World monkeys, apes, and
humans through opsin gene duplication. Dietary and morphological similarities between
howling monkeys and muriquis (Brachyteles) raise the possibility that the two genera share
a similar form of colour vision, uniform trichromacy. Yet parsimony predicts that the colour
vision of Brachyteles will resemble the polymorphism present in Lagothrix and Ateles.
Here we test this assumption. We obtained DNA from the blood or faeces of 18 muriquis and
sequenced exons 3 and 5 of the M/L opsin gene. Our results affirm the existence of a single
M/L cone opsin gene in the genus Brachyteles. We detected three alleles with predicted λmax
values of 530, 550, and 562 nm. Two females were heterozygous and are thus predicted to
have different types of M/L cone pigment. We discuss the implication of this result towards
understanding the evolutionary ecology of trichromatic vision.
Keywords: Brachyteles, opsin, primates, trichromatic vision, woolly spider monkey
Received 7 August 2005; revision accepted 31 October 2005
The genus is placed in the family Atelidae, along with
Introduction
howling monkeys (Alouatta), spider monkeys (Ateles), and
The muriqui, or woolly spider monkey, is an endangered
woolly monkeys (Lagothrix).
primate endemic to the Atlantic Forest of Brazil. Fewer
Cladistic relationships within the Atelidae have been
than 700 individuals survive in 15 remnant, geographically
debated. Morphological studies provide conflicting results
isolated populations (Mittermeier et al. 1987; Martuscelli
on the sister-group relationships among the four genera.
et al. 1994). On the basis of recent morphological assess-
Rosenberger (1984) used an unspecified number of mor-
ments, two former subspecies of muriqui, Brachyteles arach-
phological characters to group Ateles and Brachyteles clos-
noides arachnoides and B. arachnoides hypoxanthus, are now
est to each other, followed by Lagothrix and Alouatta. Ford
recognized as species, Brachyteles arachnoides (southern
(1986) used 205 dental and postcranial characters to group
muriqui) and Brachyteles hypoxanthus (northern muriqui).
Ateles, Brachyteles, and Lagothrix into an unresolved tri-
tomy, with Alouatta as sister to this clade. Kay (1990) used
Correspondence: Nathaniel J. Dominy, Fax: 1-831-459-5900; E-
117 dental characteristics to produce two sister subclades,
mail: njdominy@ucsc.edu
one grouping Alouatta with Brachyteles and the other
© 2006 Blackwell Publishing Ltd

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552 M . G . T A L E B I E T A L .
grouping Ateles with Lagothrix. In contrast to these results,
The foraging ecology of the muriquis
studies using DNA sequences have yielded congruent
sister-group relationships: Brachyteles sister groups with
The Alouatta-Brachyteles subclade of Kay (1990) reflects
Lagothrix followed by Ateles and the basal Alouatta (Harada
dental similarities between the two genera; both possess
et al. 1995; Schneider et al. 1996; Porter et al. 1997; Horovitz
relatively small lower incisors and molars with well-
et al. 1998; Hugot 1998; Meireles et al. 1999; Cortès-Ortiz et al.
developed shearing crests (Zingeser 1973; Anthony & Kay
2003; Fig. 1).
1993). The dentition of Brachyteles, together with its gnathic
and digestive system characteristics, has been viewed as an
adaptation to a folivorous diet (Hill 1962; Zingeser 1973;
Anthony & Kay 1993). Yet muriquis travel by means of sus-
pensory locomotion, a trait that has been associated with
specialized frugivory in the closely related Ateles and
Lagothrix (Cant 1986). Behavioural observations of muriquis
confirm that young leaves and fruits are important food
items, but they are consumed to different extents in differ-
ent populations (Milton 1984; Strier 1991; de Carvalho et al.
2004; Talebi et al. 2005). Importantly, Brachyteles tends
to rely on young leaves more than Lagothrix and Ateles
(Table 1). This tendency, coupled with the morphological
traits that muriquis share with Alouatta, raises questions
regarding the evolution of their colour vision.
Colour vision in the Atelidae
Variation exists in the photopigments and colour vision of
atelid monkeys. Like most platyrrhine monkeys, Ateles and
Lagothrix possess a colour vision polymorphism (Jacobs &
Deegan 2001). The polymorphism results from allelic vari-
ation of the single-locus middle-to-long wavelength (M/L)
cone opsin gene on the X-chromosome (Mollon et al. 1984;
Jacobs et al. 1993). The presence in the population of two
alleles coding for different M/L photopigments results in
a variety of colour vision phenotypes. Females that are
heterozygous for the M/L opsin gene possess trichromatic
vision. All other individuals possess dichromatic vision.
Such a colour vision polymorphism is absent among how-
ling monkeys. Alone among known platyrrhines, Alouatta
acquired uniform trichromatic vision similar to that of Old
World monkeys and apes (including humans) through
opsin gene duplication (Jacobs et al. 1996; Boissinot et al.
1997; Hunt et al. 1998; Kainz et al. 1998).
The selective factors that favoured the evolution of uni-
form trichromatic vision have been debated. Authors have
stressed the importance of detecting food targets against a
Fig. 1 Phyletic relationships of the Atelidae. The cranial and
background of mature foliage, but there has been disagree-
postcranial morphologies of each genus are depicted. The skulls of
Ateles and Lagothrix are similar: the braincase is globular, the
ment concerning the importance of particular foods. Some
mandible is relatively shallow, and the face is relatively ortho-
authors have argued that ripe fruits are critical, whereas
gonal. The skulls of Alouatta and Brachyteles are distinguished by
others have emphasized the importance of detecting ten-
their relatively small cranial capacity and lack of cranial flexion.
der young leaves (Surridge et al. 2003). Understanding the
Compared to Ateles and Lagothrix, the faces of Alouatta and
colour vision of muriquis may help refine these hypotheses.
Brachyteles are more prognathic and the mandibular rami are
Ecological and morphological similarities between Brach-
expanded and deep (Zingeser 1973). The traits that distinguish
yteles and Alouatta raise the possibility that the two genera
Ateles and Lagothrix from Alouatta and Brachyteles have been
associated with adaptations to frugivory and folivory, respect-
share a similar form of colour vision, uniform trichromacy.
ively (Anthony & Kay 1993). Drawn by C. Underwood.
Yet parsimony predicts that the colour vision of muriquis
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M / L C O N E O P S I N P O L Y M O R P H I S M O F M U R I Q U I S 553
Table 1 Summary of dietary behaviour in Brazilian howling monkeys and other atelid monkeys

Feeding records (%)
Fruit
Leaves
Flowers
Other
Reference
Howling monkeys
Alouatta belzebul
59.0
13.3
27.6
0.0
Bonvicino (1989)
43.1
45.6
10.8
0.5
Pinto et al. (2003)
A. caraya
28.9
60.9
2.7
0.0
Bicca-Marques & Calegaro-Marques (1994)
A. fusca
13.9
71.5
8.6
6.0
Mendes (1989)
5.0
73.0
12.0
0.0
Chiarello (1994)
12.0
72.0
10.0
0.0
Limeira (1997)
A. seniculus
47.3
45.5
1.5
5.7
Queiroz (1995)
Mean = 29.9
54.4
10.5
1.7
Spider monkeys
Ateles belzebuth
83.0
7.0
< 0.1
10.0
Klein & Klein (1977)
88.5
8.3
0.0
3.2
Nunes (1998)
72.0
12.0
5.0
11.0
Stevenson et al. (2000)
A. geoffroyi
77.7
11.1
9.8
1.3
Chapman (1988)
A. paniscus
82.9
7.9
6.4
2.8
van Roosmalen (1985)
85.4
9.5
2.5
2.6
Simmen & Sabatier (1996)
Mean = 81.6
9.3
4.7
5.2
Woolly monkeys
Lagothrix lagothrica
74.5
16.2
0.5
8.8
Peres (1994)
55.0
16.0
1.0
29.0
Stevenson et al. (2000)
83.2
11.4
0.1
5.3
Defler & Defler (1996)
Mean = 70.9
14.5
0.5
14.4
Muriquis
Brachyteles arachnoides
21.0
67.0
12.0
0.0
Milton (1984)
59.2
33.2
4.1
3.6
de Carvalho et al. (2004)
73.2
21.7
1.7
3.1
Talebi et al. (2005)
B. hypoxanthus
32.0
51.0
11.0
6.0
Strier (1991)
32.9
60.0
4.5
2.6
Rìmoli & Ades (1997)
Mean = 43.7
46.6
6.7
3.1

will resemble that of Lagothrix and Ateles; that is, muriquis
eastern São Paulo State, one of us, M.G.T., collected 5–
are predicted to possess a colour vision polymorphism.
10 g of faeces from seven free-ranging individuals of B.
Here we evaluate this prediction.
arachnoides (Talebi 2005). M.G.T. collected three additional
faecal samples of B. arachnoides from the semicaptive
environment of Curitiba Zoological Park, Curitiba, Paraná,
Methods
Brazil. The samples were stored in 5–10 mL 92% ethanol in
the field at 4 °C for up to 3 months and transported to the
Study populations and sample collection
University of California, Santa Cruz, under CITES permit
Four populations of Brachyteles were sampled. They rep-
no. 02001.006912/2002. The Institutional Animal Care and
resent the extremes in geographic range and visible pheno-
Use Committee of Duke University and the Chancellor’s
type for the genus (Aguirre 1971). At Fazenda Esmeralda,
Animal Research Committee of UC Santa Cruz approved
eastern Minas Gerais, Brazil, Lemos de Sá & Glander (1993)
the sampling protocols. Lastly, a sample of B. arachnoides
captured and anaesthetized five individuals of Brachyteles
genomic DNA was obtained from the laboratory of M.
hypoxanthus. At Fazenda Barreiro Rico, eastern São Paulo
Goodman, Wayne State University (Meireles et al. 1999).
State, Lemos de Sá & Glander (1993) captured and ana-
Genomic DNA was obtained from blood or faeces using
esthetized two individuals of B. arachnoides. One of us,
a phenol–chloroform extraction or QIAamp DNA Stool
T.R.P., collected blood from the anaesthetized animals. The
Mini Kit per manufacturer instructions (QIAGEN).
blood was separated by centrifugation and frozen in liquid
Faecal samples were placed in a fume hood overnight to
nitrogen. The samples remained frozen until analysis at
evaporate the ethanol prior to DNA extraction (Surridge
Duke University (Pope 1998). At Carlos Botelho State Park,
et al. 2002). Amplification and sequencing of the M/L
© 2006 Blackwell Publishing Ltd, Molecular Ecology, 15, 551–558

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554 M . G . T A L E B I E T A L .
cone opsin genes was performed at the Medical College of
277, 14 animals had Tyr and 2 had Phe. The remaining two
Wisconsin.
animals, MTG3 and MTG6, had both residues. At position
285, 16 animals had Thr and 2 animals had Ala. Variation
at these positions predicts corresponding pigment vari-
Amplification and sequencing of the M/L cone opsin genes
ation. Those predictions are also listed in Table 2. Two
The genes encoding the opsins of M/L photopigments
female subjects, MTG3 and MTG6, were heterozygous and
consist of six exons. Of these, exons 2 to 5 specify the
are thus predicted to have different types of M/L cone
membrane spanning regions of the opsin (Nathans et al.
pigment. Table 3 summarizes the distribution of M/L
1986). Peak absorption spectra (λ
) of the M/L pigment
opsin alleles among ateline X-chromosomes.
max
can be predicted from the amino acid composition of
three sites: site 180 encoded on exon 3 and sites 277 and
Discussion
285 encoded on exon 5 (Neitz & Neitz 1998). Amino acid
changes from Ser to Ala at site 180 (denoted Ser180Ala),
Here we report the existence of a single M/L cone opsin
Tyr277Phe, and Thr285Ala shift the λ
values by −7, −8,
gene in the genus Brachyteles. The result is consistent with
max
and −15 nm, respectively, although estimates of spectral
genetic examinations of Ateles and Lagothrix (Hagstrom
positioning may vary somewhat depending on the measure-
et al. 1993; Boissinot et al. 1997; Hiramatsu et al. 2005). We
ment methodology employed (Neitz et al. 1991; Merbs &
detected varying residues at positions 180, 277, and 285 of
Nathans 1992; Asenjo et al. 1994; Yokoyama & Radlwimmer
the M/L cone opsin gene that are predicted to yield
2001).
pigments with λ
values of 530, 550, and 562 nm. Two of
max
Polymerase chain reaction (PCR) was used to amplify
11 female subjects were heterozygous for the M/L cone
exons 3 and 5 of the M/L opsin gene (Neitz & Neitz 1995).
opsin gene and are predicted to possess allelic trichromatic
Exons 3 and 5 were amplified separately using the
vision. The spectral separation of the 550 and 562 nm
AmpliTaq Gold PCR kit per manufacturer instructions
pigments is equivalent to human anomalous trichromacy
(ABI). Each 50-µL reaction contained a final concentration
(Neitz et al. 1991), and is consistent with the performance
of 1× Buffer, 1 mm MgCl , 600 nm of each primer, 50 µm
of female Ateles in colour-discrimination tasks (Grether
2
each of dATP, dCTP, dTTP, and dGTP, and 1.25 U of
1939; Blakeslee & Jacobs 1982).
AmpliTaq Gold (ABI). Exon 3 was amplified using the
The spectral positions of the M/L opsin pigments in
forward primer 5′-CGTCTGTCTGCTCTCCCCTA, and the
Ateles and Lagothrix has been determined with electro-
reverse primer 5′-TTGCCTCAGGGTCACAGAGT. One or
retinogram (ERG) flicker photometry. In contrast to other
two rounds of PCR were done in an ABI 2700 thermal cycler
platyrrhine species, which possess three types of M/L pig-
using cycling conditions of 94 °C for 9 min for one cycle,
ment, evidence exists for only two pigment types in Ateles
followed by 37 cycles of 94 °C for 45 s, 61 °C for 45 s, 72 °C
and Lagothrix (Jacobs & Deegan 2001). Among 47 spider
for 45 s. Reactions were then incubated at 72 °C for 7 min
monkeys, the pigments had a λ
value of 550 and 562 nm;
max
and stored at 4 °C. Exon 5 was amplified using the forward
among 9 woolly monkeys, the pigments had a λ
value
max
primer 5′-GTGGCAAAGCAGCAGAAAG and the reverse
of 548 and 563 nm. These differences in spectral tuning
primer 5′-CTGCCGGTTCATAAAGACATAG; or using the
could reflect opsin sequence variation at one of the tuning
forward primer 5′-TCCACCCCCCGACTCACTATCC and
sites known to yield small shifts in the spectral positioning
the reverse primer 5′-ACGGTATTTTGAGTGGGATCTGCT.
of primate M/L cone photopigments (Shyue et al. 1998).
The thermal cycling conditions were the same as those
The absence of a third pigment type in Ateles and Lagothrix
used to amplify exon 3 except that the 61 °C step was done
is a potentially important distinction between atelines and
at 59 °C. PCR products were directly sequenced using the
other platyrrhines. Jacobs & Deegan (2001) suggested that
same primers that were used to amplify the exons and the
a third pigment likely exists, but that the allele specifying
BigDye Terminator 3.1 kit (ABI). Sequencing reactions were
the pigment is rare in ateline populations. Recently, Riba-
analysed on an ABI 3100 Avante.
Hernández et al. (2004) reported unpublished sequence
data for the 530 nm allele in a population of Ateles. Here we
confirm the existence of a 530 nm allele in Brachyteles.
Results
Although sample sizes are relatively small, the infre-
quency (1.3%) of the allele across ateline X-chromosomes
Variation in muriqui M/L opsin genes
indicates that it is in fact rare (Table 3).
A total of 18 muriquis served as subjects for this analysis.
Under the Hardy–Weinberg equilibrium, the existence
Table 2 shows the variation in the residues detected at
of two alleles in population should result in a 50% fre-
positions 180, 277, and 285 for these animals. At position
quency of heterozygous females, whereas the existence of
180, 12 animals had Ser, 2 had Ala, and 4 could not be
three alleles should result in a 67% frequency. The rarity
determined because exon 3 failed to amplify. At position
of the 530 nm allele among atelines has a major practical
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M / L C O N E O P S I N P O L Y M O R P H I S M O F M U R I Q U I S 555
Table 2 Variation in residues detected at positions 180, 277, and 285 of the M/L opsin gene and the predicted pigment absorbances for
Brachyteles arachnoides and Brachyteles hypoxanthus*

Exon 3
Exon 5
Residue at
Residue at
Residue at
λ
(nm) genotype
max
monkey ID
Sex
position 180
position 277
position 285
prediction
B. arachnoides
Carlos Botelho
MGT1
Male
Ser
Tyr
Thr
562
MGT2
Female
Ser
Tyr
Thr
562
MGT3
Female
Ser
Tyr/Phe
Thr
550/562
MGT5
Female
Ser
Tyr
Thr
562
MGT6
Female
Ser
Tyr/Phe
Thr
550/562
MGT8
Male
Ser
Tyr
Thr
562
GIGI
Female
Ser
Tyr
Thr
562
Curitiba Zoological Park
MGT7
Female
Ser
Tyr
Thr
562
MGT9
Female
Ser
Tyr
Thr
562
MGT10
Female
Ser
Tyr
Thr
562
Fazenda Barreiro Rico
TRP10
Female
—
Tyr
Thr
562†
TRP11
Male
Ser
Tyr
Thr
562
Goodman Laboratory
No identification
—
—
Phe
Thr
550
B. hypoxanthus
Fazenda Esmeralda
TRP2
Male
Ala
Phe
Ala
530
TRP3
Male
Ser
Tyr
Thr
562
TRP5
Female
—
Tyr
Thr
562†
TRP6
Male
Ala
Phe
Ala
530
TRP7
Female
—
Tyr
Thr
562†
*GenBank (www.ncbi.nlm.nih.gov/GenBank/) Accession numbers for the nucleotide sequences generated for this paper are DQ218051–
DQ218055.
†The failed amplification of exon 3 leaves the spectral tuning of this pigment in some doubt. The detection of Ala at position 180 would
yield a photopigment with a predicted λ
of c. 555 nm. Although the pigment exists in the family Cebidae, which includes squirrel
max
monkeys, capuchin monkeys, and owl monkeys, it has yet to be found in an atelid monkey. Accordingly, we infer that these three animals
possess an M/L pigment with λ
of 562 nm, although such an assumption should be treated with caution.
max

Table 3 Distribution of M/L opsin alleles
M/L alleles (nm)
among ateline X-chromosomes
Genus
N individuals X-chromosomes ∼530 ∼550 ∼562 Reference
Ateles
47
76
0
26
50
Jacobs & Deegan (2001)
20
37
0
15
22
Hiramatsu et al. (2005)
Brachyteles 18
27
2
2
23
This study*
Lagothrix
9
9
0
5
4
Jacobs & Deegan (2001)
Totals
94
149
2
48
99
*The animal of unknown sex presented in Table 2 is not included in this summary.

implication: the number of heterozygous females (and,
observed: 18% (2 of 11) of the female Brachyteles examined
hence, the number of trichromats in the population) will be
here and 52% (24 of 46) of female Ateles possess, or are pre-
relatively low compared to species that maintain three
dicted to possess, two M/L pigments (Jacobs & Deegan
allelic versions of the gene. This difference has been
2001; Hiramatsu et al. 2005). In contrast, c. 63% of female
© 2006 Blackwell Publishing Ltd, Molecular Ecology, 15, 551–558

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556 M . G . T A L E B I E T A L .
squirrel monkeys (Saimiri) have been found to possess two
et al. 2002; Surridge et al. 2005). Instead, trichromatic colour
M/L pigments (Jacobs et al. 1993). Even more strikingly,
vision may allow for a range of visual advantages that could
the proportion of heterozygous females can reach 83%
potentially serve to maintain the adaptation.
among titi monkeys (Callicebus moloch), a species that main-
tains five alleles (Jacobs & Deegan 2005).
Acknowledgements
This result demonstrates the difficulty of linking the
photopigments of primates, particularly those of atelid
We are grateful for the intellectual and material contributions of A.
monkeys, with aspects of their foraging ecology. Both
Almquist, A. Bastos, D. Conklyn, M. Goodman, S. Roy-Choudari,
Ateles and Lagothrix are specialized frugivores, with fruits
K. B. Strier, P. C. Lee, W.-H. Li, P. W. Lucas, B. L. W. Miller, V.
Pessa, D. M. Snodderly P. P. Soares, J. N. Thompson, R. H. Tuttle,
comprising 55–89% of their annual diet (Table 1). Colour
D. E. Wildman, S. Yi, and the UC-Santa Cruz Molecular Ecology
vision would appear to be an intuitive sensory modality
and Evolutionary Genetics Facility. We received permission to
for guiding fruit selection. Accordingly, fruits have figured
conduct this study from the Forestry Institute of Sao Paulo State,
prominently in discussions of primate trichromacy. It has
CNPq (CITES permit no. 02001.006912/2002), and the US Fish and
long been an article of faith that the detection and discrim-
Wildlife Service. The Institutional Animal Care and Use Committee
ination of ripe fruit against a foliage background favoured
of Duke University and the Chancellor’s Animal Research Com-
the evolution of allelic and uniform trichromatic vision
mittee of UC–Santa Cruz approved our sampling protocols. We
received funding from Conservation International USA, the
(Smith et al. 2003; Surridge et al. 2003). On the surface, this
Leakey Foundation, the Margot Marsh Biodiversity Foundation, a
hypothesis might suggest that Ateles and Lagothrix would
Ruth L. Kirchenstein NIGMS National Service Research Award,
be best served by possessing uniform trichromatic vision,
and the World Wildlife Fund–Brazil.
rather than Alouatta, the atelid genus with the lowest
annual consumption of fruit (Table 1). The fruit-selection
hypothesis also predicts that the 530 nm allele should exist
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