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Biol. Lett. (2006) 2, 217–221
doi:10.1098/rsbl.2006.0440
Published online 7 February 2006
Bare skin, blood and the
evolution of primate
colour vision
Mark A. Changizi
1,
*, Qiong Zhang
2
and Shinsuke Shimojo
2,3
1
Sloan-Swartz Center for Theoretical Neurobiology, California Institute
of Biology, MC 139-74, Caltech, Pasadena CA 91125, USA
2
Division of Biology, Computation and Neural Systems, MC 139-74,
Caltech, Pasadena CA 91125, USA
3
JST ERATO Shimojo Implicit Brain Function Project, California
Institute of Technology, MC 139-75, Pasadena CA 91125, USA
*Author for correspondence (changizi@caltech.edu).
We investigate the hypothesis that colour vision
in primates was selected for discriminating the
spectral modulations on the skin of conspecifics,
presumably for the purpose of discriminating
emotional states, socio-sexual signals and threat
displays. Here we show that, consistent with this
hypothesis, there are two dimensions of skin
spectral modulations, and trichromats but not
dichromats are sensitive to each. Furthermore,
the M and L cone maximum sensitivities for
routine trichromats are optimized for discrimi-
nating variations in blood oxygen saturation,
one of the two blood-related dimensions deter-
mining skin reflectance. We also show that,
consistent with the hypothesis, trichromat pri-
mates tend to be bare faced.
Keywords: colour; primate; evolution; skin; blood;
vision
1. INTRODUCTION
The primate face and rump undergo colour modu-
lations (such as blushing or blanching on the human
face, or socio-sexual signalling on the chimpanzee
rump), some which may be selected for signalling and
some which may be an inevitable consequence of
underlying physiological modulations. Because for
highly social animals like most primates, one of the
most important kinds of object to be competent at
perceiving and discriminating is other members of
one’s own species, we investigated the hypothesis that
primate colour vision has been selected for discrimi-
nating the spectral modulations on the skin of
conspecifics, these modulations providing useful
information about the current state or mood of
another conspecific.
A first prediction of our hypothesis is that the
space of skin colour modulations should be ade-
quately spanned by the two chromatic mechanisms
available to trichromats, but not to the single chro-
matic mechanism available to dichromats. This is
indeed the case, as we now explain. The reflectance
spectra for human skin possess a characteristic signa-
ture (figure 1a), including a ‘W’ feature near 550 nm
(see electronic supplementary material, figure 2).
This feature is due to the absorption spectrum of
oxygenated haemoglobin in the blood (figure 1b), and
is found in spectra of primate skin as well (figure 1a).
What is important for our hypothesis is not the
baseline reflectance spectrum of skin, which will differ
across human phenotypes ( Jablonski & Chaplin
2000) and across primates (Sumner & Mollon 2003),
but the manner in which the skin reflectance is
modulated in the short term, something that is
universal across primates. There are two dimensions
of skin reflectance modulation, (i) haemoglobin oxy-
gen saturation and (ii) haemoglobin skin concen-
tration (Zonios et al. 2001). Changes in these two
parameters lead to predictable changes in the reflec-
tance of skin (figure 1c). Greater oxygen saturation
leads to a more-defined ‘W’ feature with a larger
difference between its troughs and centre peak, raising
the L cone activation (which is at the peak of the ‘W’)
relative to the M cone (which is near the first trough
of the ‘W’), leading to redder; lower oxygen saturation
does the opposite, leading to greener (figure 1d). For
example, skin with veins underlying it, possesses a
high concentration of deoxygenated blood and is
greenish blue (Kienle et al. 1996), and skin with
blood accumulation after administering a tourniquet
possesses a high concentration of relatively oxyge-
nated blood and is reddish-blue (i.e. purplish); these
two skin conditions differ primarily in regards to
oxygen saturation (because they both have high-
haemoglobin concentration), and their colour differ-
ence is primarily a red–green one (figure 1e). Greater
haemoglobin concentration in the skin, on the other
hand, leads to an overall lowering of the entire ‘W’
feature in the filtered spectrum (but not much change
in the difference between the troughs and the peak of
the ‘W’), lowering the M/L activation relative to the S
activation, which leads to bluer; lower haemoglobin
concentration does the opposite, leading to yellower
(figure 1d). For example, bloodless skin is relatively
yellow, whereas skin with greater amounts of blood is
bluer, e.g. green-blue for veins and reddish-blue
after application of a tourniquet (figure 1e). Dichro-
mat primates have only one chromatic dimension, not
two, and will be able to capture only one of the two
blood-related dimensions of skin colour variation,
namely the haemoglobin concentration dimension.
If trichromacy was selected for discerning the
colour modulations in skin, then trichromats should
not merely be sensitive to the oxygen saturation
dimension. Rather, the hypothesis predicts that the M
and L maximum wavelength sensitivities should be
near optimal for discriminating this dimension. To
see that this is the case, note first that varying the
oxygen saturation of haemoglobin in the skin modu-
lates the ‘W’ feature, turning it from a ‘W’ when
oxygen saturation is high to a ‘U’ when oxygen
saturation is low (figure 1band c). Supposing that the
M and L sensitivities must jointly serve the ancestral
role of the single M/L cone in dichromatic primates
(which has maximal sensitivity at 543 nm), it follows
that the maximal sensitivities for M, L and their sum
must be near 543 nm. With this constraint, M and L
wavelength sensitivities would be optimized for
detecting oxygenation variation if they were at
approximately 540 and 560 nm, respectively
(figure 2a). This prediction fairs well among the
The electronic supplementary material is available at http://dx.doi.
org/10.1098/rsbl.2006.0440 or via http://www.journals.royalsoc.ac.
uk.
Received 5 December 2005
Accepted 3 January 2006
217 q2006 The Royal Society
bluer
redder
yellower
greener
0
0.25
0.5
0.75
(a)(b)
(c)(d)
(e)
400 450 500 550 600 650 700
wavelength (nm)
reflectance
Caucasion (dark)
Caucasion (light)
African American
East Indian (light)
Asian
East Indian (dark)
M L
mandrill (red nose)
mandrill (purple rump)
–0.1
0.15
–0.1 0.04
(L–M)
norm
S–(M+L)
norm
–0.2
0.2
–0.1 0.1
(R-G)norm
B-(R+G)norm
0.1
1
10
100
1000
400 450 500 550 600 650 700
wavelength (nm)
molar extinction coeff. e (l cm–1 mmol–1)
He02
He
M L
tourniquetveins
bloodless
baseline
oxy
high blood
deoxy
low blood
blood space
Figure 1. (a) Reflectance spectra from a variety of human skin (data from NCSU spectral database), and from one male
primate, namely Mandrillus sphinx (Sumner & Mollon 2003). Also shown here and in (b) are the maximal sensitivities for the
M and L cones for routine trichromats. (b) Absorption spectrum for oxygenated and deoxygenated haemoglobin (from Scott
Prahl, Oregon Medical Laser Center, http://omlc.ogi.edu). (c) Blood space for skin spectral modulation, showing the two
principle variables that affect skin colour in the short term: haemoglobin oxygen saturation (x-axis), and haemoglobin skin
concentration (y-axis). ‘High’, ‘baseline’ and ‘low’ values for these two variables were chosen, and the figure shows the nine
skin spectra for all pairs of these parameter settings. Colours code the approximate direction of colour shift from baseline
(centre). (d) Relative change from baseline for LKM and SK(LCM) for the nine model skin spectra varying over blood
space from (c). Shown now are the filtered skin spectra actually reaching the retina. (e) Example skin colour modulations
from modulations of blood variables. Data points show positions in this colour space for RGB values of skin under these
conditions, along with the average values. See electronic supplementary material for the extended legend for this figure.
218 M. A. Changizi and others Evolution of primate colour vision
Biol. Lett. (2006)
routine trichromats, who have M and L maximal
sensitivities (Jacobs & Deegan 1999) of approximately
535 and 562 nm, respectively (figure 2a), providing
near-optimal sensitivity to oxygenation modulation
(figure 2b). Among polymorphic trichromats, most of
the Cebid (e.g. Callicebus,Ateles,Lagothrix,Cebus and
Saimiri ) trichromat phenotypes possess significant
sensitivity to oxygen saturation, although not all
phenotypes are near-optimal (figure 2b). Among the
Callitrichidae (e.g. Saguinus,Leontopithecus,Callimico,
Cebuella and Callithrix) trichromat phenotypes, two of
the three possess near optimal sensitivity to oxygen
saturation, and the third (approximately 556/562)
possesses little or no sensitivity (figure 2b). It is
interesting to note in this regard that the M/L cone
with maximal sensitivity at 556 nm occurs dispropor-
tionately rarely in the population (Rowe & Jacobs
2004), only 19.7%, perhaps because the 556/562
phenotype is insensitive to oxygen saturation vari-
ation. Our hypothesis predicts sensitivity to skin
colour variation not just for the early visual mechan-
isms (i.e., cone sensitivities and opponency), but in
–25
0
25
500 510 520 530 540 550 560 570 580 590 600
wavelength (nm)
routine trichromatic
polymorphic trichromatic
dichromatic
monochromatic
(a) (b)
sensitivity to
oxygenation
variation
100%
50%
0%
Gorilla
Homo
Pan
Pongo
Hylobates
Presbytis
Colobus
Miopithecus
Cercopithecus
Macaca
Callicebus
Ateles
Lagothrix
Alouatta
Cebus
Saimiri
Aotus
Saguinus
Leontopithecus
Callimico
Cebuella
Callithrix
Tarsius
Perodicticus
Nycticebus
Loris
Otolemur
Galago
Daubentonia
Cheirogaleus
Microcebus
Propithecus
Varecia
Hapalemur
Lemur
Eulemur
Catarrhines…Platyrrhines…
Prosimians…
difference between He and HeO2
molor extinction coefficient (liters/cm/mole)
Figure 2. (a) The curve shows the difference between the absorption spectrum for oxygenated and deoxygenated
haemoglobin. The difference between oxygenated and deoxygenated skin spectra lead to qualitatively identical curves, no
matter the specific skin constants (i.e. same peak and valley wavelengths). Shown also are peak M/L cone sensitivities for the
primate genera shown (reviewed in Surridge et al. (2003)). (Height in the plot for these is only to separate the data.) The
vertical lines are at wavelengths where we would expect the maximal sensitivities of M and L cones to be, respectively, if they
are optimally sensitive for oxygenation variation, and subject to the constraint that M and L jointly function as the single
dichromat M/L cone. For Tarsius,Surridge et al. (2003) give two different values for the single M/L cone, and an ‘x’ point is
shown for the longer wavelength one. For Cebuella, an allele at 543 nm has been added because Surridge & Mundy (2002,
p. 2164) believe it probably exists but was not measured due to low sample size. (b) A plot of sensitivity of M/L cones to
oxygenation variation, for each primate genus, where 100% would occur if the maximal sensitivities of M and L occurred at
the optimum for oxygenation sensitivity. For polymorphic trichromatic primates, points are placed for each of the possible
pairs of M/L cones. In several cases, Surridge et al. (2003) do not mention all three M/L cones, and we utilized the value
from other genera in the same family. The line shows the average sensitivity for all M and L pairs centred around 543 nm
(the typical dichromat maximal sensitivity wavelength), where M ranges as low as 500 nm.
Evolution of primate colour vision M. A. Changizi and others 219
Biol. Lett. (2006)
perception as well, and evidence supports this (see
electronic supplementary material, §2). And related
to this, our hypothesis predicts that dichromats
should be perceptually handicapped at discriminating
skin colour modulations, and they are, as predicted,
notoriously poor at such discriminations (see elec-
tronic supplementary material, table 1).
Because skin spectral variations cannot be per-
ceived on a face without bare skin, the hypothesis
predicts that trichromatic primates should have
bare faces (or at least some other body region with
bare skin, such as a bare rump, something widely
known to be true among Old World Primates,
Wickler (1967)). A cursory look at photographs of
97 species from 35 primate genera demonstrates
that this is a strong regularity (see electronic
supplementary material, figure 1). Estimates of the
average bareness on the face are shown in elec-
tronic supplementary material, figure 1e, and one
can see that monochromats and dichromats tend to
have furry faces, whereas polymorphic and routine
trichromats tend to have bare faces. Note that
among the polymorphic trichromats are two prosi-
mians (prosimians who in other known cases are
monochromatic or dichromatic), Varecia and Pro-
pithecus (the top two photographs in electronic
supplementary material, figure 1efor the poly-
morphic trichromats), and they each have substan-
tial bare spots on their face. This connection
betweenbareskinandcolourvisionmaybe
important in understanding why humans are the
‘naked ape’: for primates with colour vision, skin
modulations may serve as signalling on any body
part that can be seen (e.g. a chimpanzee rump),
and for apes that walk upright, more parts of the
body are potentially visible and amenable to colour
signalling. (See §3 of the electronic supplementary
material for further discussion of face bareness and
also see §4 and figures 2 and 3, for a discussion of
evidence of the visibility of skin colour
modulations.)
We should emphasize that the idea that colour
vision is important for colour signalling is not new
(e.g. Hingston 1933;Wickler 1967;Regan et al.
2001;Liman & Innan 2003;Waitt et al. 2003;
Zhang & Webb 2003), except that typically it is
assumed that colour vision was originally selected for
some other reason. One of the main contributions
we make here is the argument that colour vision is
near-optimal for discriminating skin colour modu-
lations, something that increases the prima facie
plausibility of the hypothesis that trichromacy was
originally selected for the perception of skin colour
signalling. Other adaptive explanations have been put
forth to explain primate colour vision, including
advantages for frugivory (Allen 1879;Mollon 1989;
Osorio & Vorobyev 1996;Regan et al.2001;
Surridge & Mundy 2002), and for folivory (Lucas
et al. 2003). Our discussion here provides no answer
as to which of these may more likely have been the
original selection pressure for trichromacy, or
whether all these hypotheses may be important
contributors (Regan et al. 2001). One advantage of
the skin colour-signalling hypothesis is that, whereas
there is a wide variety of trichromat frugivory and
folivory behaviour, skin colour modulation is due to
fundamental properties of blood shared by all pri-
mates, and this could be key in understanding the
universal M and L cone sensitivities of routine
trichromats. There are other phenomena that colour
signalling can explain but these others cannot,
including the high degree of perceptual discrimin-
ability and colour-uncategorizability of skin tones
(see electronic supplementary material, §2), the bare-
ness of trichromat faces, and the close affinity of
colour to blood, skin colour and emotional
states (see electronic supplementary material, §5and
figures 4, 5 and 6).
We wish to thank two helpful referees for their comments.
Support for this research was given by 5F32EY015370-02,
NIH (to M.A.C) and JST.ERATO, Japan (to S.S.).
Allen, G. 1879 The colour-sense: its origin and development.
London, UK: Trubner & Co.
Hingston, R. W. G. 1933 The meaning of animal colour and
adornment. London, UK: Edward Arnold.
Jablonski, N. G. & Chaplin, G. 2000 The evolution of
human skin coloration. J. Hum. Evol. 39, 57–106.
(doi:10.1006/jhev.2000.0403)
Jacobs, G. H. & Deegan, J. F. 1999 Uniformity of colour
vision in Old World monkeys. Proc. R. Soc. B 266,
2023–2028. (doi:10.1098/rspb.1999.0881)
Kienle, A., Lilge, L., Vitkin, A., Patterson, M. S., Wilson,
B. C., Hibst, R. & Steiner, R. 1996 Why do veins appear
blue? A new look at an old question. Appl. Opt. 35,
1151–1160.
Liman, E. R. & Innan, H. 2003 Relaxed selective
pressure on an essential component of pheromone trans-
duction in primate evolution. Proc. Natl Acad. Sci. USA
100, 3328–3332. (doi:10.1073/pnas.0636123100)
Lucas, P. W. et al. 2003 Evolution and function of routine
trichromatic vision in primates. Evolution 57,
2636–2643.
Mollon, J. D. 1989 “Tho she kneel’d in that place where
they grew.”. J. Exp. Biol. 146, 21–38.
Osorio, D. & Vorobyev, M. 1996 Colour vision as an
adaptation to frugivory in primates. Proc. R. Soc. B 263,
593–599.
Regan, B. C., Julliot, C., Simmen, B., Vienot, F.,
Charles-Dominque, P. & Mollon, J. D. 2001 Fruits,
foliage and the evolution of primate colour vision. Phil.
Trans. R. Soc. B 356, 229–283. (doi:10.1098/rstb.2000.
0773)
Rowe, M. P. & Jacobs, G. H. 2004 Cone pigment
polymorphism in New World monkeys: are all pigments
created equal? Visual Neurosci. 21, 217–222.
Sumner, P. & Mollon, J. D. 2003 Colors of primate
pelage and skin: objective assessment of conspicuous-
ness. Am. J. Primatol. 59, 67–91. (doi:10.1002/ajp.
10066)
Surridge, A. K. & Mundy, N. I. 2002 Trans-specific
evolution of opsin alleles and the maintenance of
trichromatic colour vision in Callitrichine primates. Mol.
Ecol. 11, 2157–2169. (doi:10.1046/j.1365-294X.2002.
01597.x)
Surridge, A. K., Osorio, D. & Mundy, N. I. 2003 Evolution
and selection of trichromatic vision in primates. Trends
Ecol. Evol. 18, 198–205. (doi:10.1016/S0169-5347(03)
00012-0)
220 M. A. Changizi and others Evolution of primate colour vision
Biol. Lett. (2006)
Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown,
A. P., Buchanan-Smith, H. M. & Perrett, D. I. 2003
Evidence from rhesus macaques suggests that male
coloration plays a role in female primate choice. Proc. R.
Soc. B 270(Suppl), S144–S146.
Wickler, W. 1967 Socio-sexual signals and their intra-
specific imitation among primates. In Primate ethology
(ed. D. Morris), pp. 69–147. London, UK: Weidenfeld
and Nicolson.
Zhang, J. & Webb, D. M. 2003 Evolutionary deterioration
of the vomeronasal pheromone transduction pathway in
catarrhine primates. Proc. Natl Acad. Sci. USA 100,
8337–8341. (doi:10.1073/pnas.1331721100)
Zonios, G., Bykowski, J. & Kollias, N. 2001 Skin melanin,
hemoglobin, and light scattering properties can be
quantitatively assessed in vivo using diffuse reflectance
spectroscopy. J. Invest. Dermatol. 117, 1452–1457.
(doi:10.1046/j.0022-202x.2001.01577.x)
Evolution of primate colour vision M. A. Changizi and others 221
Biol. Lett. (2006)
