ANIMAL BEHAVIOUR, 2004, 67, 69e83
doi:10.1016/j.anbehav.2003.02.004
Female colour and male choice in sockeye salmon:
implications for the phenotypic convergence of
anadromous and nonanadromous morphs
CHRI S J. F OOTE*, GA Y LE S. BR OWN † & C RAIG W. HAWRYSHYN‡
*Department of Fisheries and Aquaculture, Malaspina University-College
yPacific Biological Station, Canadian Department of Fisheries and Oceans
zDepartment of Biology, University of Victoria
(Received 6 March 2002; initial acceptance 29 April 2002;
final acceptance 22 February 2003; MS. number: A9300R)
Divergent mate choice patterns between populations may lead to premating isolation and speciation.
However, similar or identical mate choice patterns may also constrain phenotypic divergence, although
not necessarily genetic divergence, across populations. We examined spectral characteristics necessary for
male mate choice of abstract female models in sockeye salmon, Oncorhynchus nerka, in experiments
conducted on the breeding grounds and under controlled conditions in the wild. Males preferentially
selected and spawned with models with a red hue, the predominant colour of females. Small changes in
wavelength, saturation and brightness affected preference. Sexually naı̈ve males showed the same
preference as experienced males, suggesting that a preference for red hue might be innate. We discuss these
results in relation to female colour, the transmission environment and the visual physiology of salmon to
evaluate further the possible role of a pre-existing bias for red in the evolution of red breeding colour in
nonanadromous (kokanee) salmon. Our results suggest that a sensory bias can account for the reemergence of red in kokanee, after its loss during the initial development of a freshwater morph.
Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
The importance of colour in mate choice has been
recognized in diverse taxa, typically in the form of female
choice. In fish, studies of mate choice based on colour
have been used to address hypotheses relating to the
evolution of elaborate secondary sexual traits, including
run-away selection (e.g. Houde 1988), phylogeny (e.g.
McLennan 1991), selection for good genes (e.g. KodricBrown & Brown 1984; Milinski & Bakker 1990; Houde &
Torio 1992; Berglund & Rosenqvist 2001), the evolution of
signals and signal recognition (e.g. Ryan 1990; Endler
1992; McDonald et al. 1995; Boughman 2001) and the
interaction between natural and sexual selection (e.g.
Endler & Houde 1995). Endler & Houde (1995) described
the clear link between sexual selection promoting population divergence within species and the evolution of
premating isolation between species (see Ryan & Rand
1993; Boake et al. 1997; Panhuis et al. 2001). Strong
Correspondence: C. J. Foote, Department of Fisheries and Aquaculture,
Malaspina University-College, 900 Fifth Street, Nanaimo, BC V9R
5S5, Canada (email: [email protected]). G. S. Brown is at the Pacific
Biological Station, Canadian Department of Fisheries and Oceans,
Nanaimo, BC V9T 6N7, Canada. C. W. Hawryshyn is at the
Department of Biology, University of Victoria, Victoria, BC V8W
3N5 Canada.
0003e3472/03/$30.00/0
supporting evidence has been provided from studies on
cichlid fish that link the role of colour in mate choice to
the rapid divergence of sympatric species (Knight &
Turner 1999; Seehausen & van Alphen 1999).
Pacific salmon species (genus Oncorhynchus) display
a variety of striking species-specific breeding colours (Scott
& Crossman 1973). However, we know little about the role
of colour in the breeding behaviour of any salmonid, or
about the factors promoting the evolution of these traits
(Schroder 1981; Satou et al. 1987; Takeuchi et al. 1987;
Fleming & Gross 1989; Craig & Foote 2001). Oncorhynchus
nerka displays the most extreme colours of all, with both
sexes developing olive-green heads and bright carotenoidbased red bodies (males are brighter red than females;
Craig & Foote 2001). The story is complicated by the fact
that O. nerka occurs as two genetically distinct and
reproductively isolated life-history morphs, the large
anadromous sockeye and the small nonanadromous
kokanee (Wood & Foote 1996). While both morphs
display the same breeding colours, they do so by very
different physiological means. Sockeye inhabiting a productive marine environment in which carotenoids are
readily available in their krill-dominated diet are much
less efficient in utilizing carotenoids than are kokanee,
69
Ó 2004 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
70
ANIMAL BEHAVIOUR, 67, 1
which inhabit relatively unproductive, and possibly
carotenoid-limited, freshwater lakes (Craig & Foote
2001). Indeed, sockeye, which spend their whole lives in
lakes, cannot turn red at maturity due to this limited
utilization ability, rather they turn green (Ricker 1940,
1959; Krogius 1981; Scott 1984; Quinn et al. 1998). Craig
& Foote (2001) postulated that sexual selection promoted
genetic divergence in the ability to utilize carotenoids
between the morphs to compensate for environmental
differences in their availability. That is, the phenotypic
convergence of the morphs in colour is the result of the
interaction of sexual selection and countergradient variation (see Conover & Schultz 1995).
Specifically, Craig & Foote (2001) hypothesized that
some aspect of sensory drive (see Endler & Basalo 1998)
probably accounted for kokanee reacquiring the ability to
turn red as they diverged from their sockeye ancestors on
numerous independent occasions over the last 10 000
years. If this is so, then we expect the colour red to play
a very important role in the sexual behaviour of sockeye,
the ancestral form of the species, to account for its
independent re-emergence in kokanee throughout their
range. Furthermore, such a preference would have to be
inherited, so that the preference would persist in lakedwelling sockeye even if the initial ability to produce a red
breeding colour were lost.
In this paper we address the question of what, if any,
spectral traits are involved in mate choice in sockeye
salmon. First, we tested the ability of sockeye to
discriminate between two colours (red and yellow) independent of brightness of the red model (e.g. Birgersson
et al. 2001). The capacity for a colour vision system to
discriminate a broad range of targets without the confounding variable of brightness is central to the issue of
demonstrating colour vision (Hawryshyn 1998). Second,
we tested whether males discriminate between models
based on variation in brightness (light intensity) alone.
Third, we examined mate choice where red colour
saturation was varied by the addition of incremental
aliquots of white. Inhibition with decreased saturation,
probably resulting from some form of opponency across
different cone pigments, would indicate that the response
was not simply wavelength specific (McFarland & Munz
1975; Marshall et al. 1996; McDonald & Hawryshyn
1999). Finally, we examined directional fine-scale wavelength acuity by testing the preference of males when
given the choice of models ranging from yellow to red.
Preference for more spectrally pure red models would
support the potential for strong directional sexual selection for red in the species.
We were also interested in whether the responses to
colour that we observed were the product of learning on
the breeding grounds. Oncorhynchus nerka are semelparous
and as such all arrive on their breeding grounds with no
previous sexual experience. If the response to colour was
learned through association of breeding and colour, we
would not expect sexually naı̈ve sockeye to express any
clear colour preferences. The demonstration that sexually
naı̈ve fish display the same colour preference as experienced fish would be consistent with the hypothesis that
the response to colour was innate, although it would not
rule out the possibility that they may have all acquired
this preference through some association prior to maturity.
We examined male choice, as it is more direct and easier
to document than female choice in salmon (Schroder
1981; Foote 1988, 1989; Blanchfield & Ridgway 1999;
Berejikian et al. 2000). In Pacific salmon, females are the
territorial sex, selecting, preparing and defending a nest
site until death or displacement. In contrast, males provide no parental care and move between females after egg
deposition is complete (Foote 1990; Fleming & Gross
1992; Quinn & Foote 1994). Males select (move to)
females based on their readiness to spawn (Schroder
1981; Berejikian et al. 2000) and on their large relative
size compared with the male, presumably to maximize
their breeding opportunities and the number of eggs sired
per breeding (Foote 1988). Females affect an indirect
choice by varying their rate of breeding dependent on the
size of the courting male, breeding more rapidly with
larger males (Schroder 1981; Foote 1989; Berejikian et al.
2000). Such delays increase the chances that larger males
will ultimately displace attending males (Blanchfield &
Ridgway 1999).
METHODS
Experiments were conducted using sockeye salmon in
Iliamna Lake, Alaska, U.S.A. (59(30#N, 155(00#W) during
the month of August 1995e1997. Iliamna Lake is a clear
oligotrophic lake that is situated adjacent to the Bering
refugium from whence sockeye dispersed following the
last ice age (McPhail & Lindsey 1970). Kokanee do not
occur in the drainage and are rare in Alaska in general
(McPhail & Lindsey 1970). Without the opportunity for
gene flow between morphs, we assume sockeye choice in
Iliamna to be representative of the ancestral morph.
We conducted tests with free-ranging sockeye salmon
on their island beach breeding grounds (wild experiments)
and with individual sockeye in enclosed arenas on the
breeding grounds (arena experiments). Wild experiments
allowed us to gauge the importance of colour to sockeye
under natural conditions (Bakker & Mundwiler 1994).
Arena experiments allowed us to examine specific behaviours while controlling for environmental variables such
as competition for, and availability of, potential mates
(Hamon et al. 1999). We used abstract female models,
thereby eliminating confounding of colour with other
condition and behavioural indices (Barlow & Siri 1994).
Models were painted with Sherwin-Williams house paints,
most of which were Krylon oil-based spray paints. The
models were made with 4-mm-thick Plexiglas. The base
was 30 cm long and 23 cm wide with a 11.5-cm-high perpendicular (upright) rib running lengthways along the
centre of the base. Steel bolts held the model in place.
We limited our study to wavelength variation greater
than 400 nm because, until recently, salmon UV detectors
were thought to be forever lost in juveniles. However,
Novales Flamarique (2000) showed that these receptors
are reacquired in adults. Hence, we cannot rule out that
variation in the ultraviolet spectrum is also important in
sockeye male choice, as has recently been shown in
guppies, Poecilia reticulata (Kodric-Brown & Johnson
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
this was the clearest measure of choice. Between trials,
models were switched between quadrats to control for side
and observer biases. Within experiments, we completed
each set of comparisons before commencing the next
replicate to control for temporal variation in light. A small
proportion of males (7 of 184; 3.8%) did not clearly
respond to any model. To minimize variance, we excluded
from the analyses the seven males that spent less than 30 s
(5% of their time), in total, within the two 1-m2 quadrats.
At the end of a trial, males were released to the wild or, in
two cases, returned to a separate cage for testing in an
independent experiment before release the next day.
Experiment 1: Spectrally Neutral
and Unique Models
In the wild we compared the reactions of males to six
different coloured models (experiment 1a). The six colours
consisted of four spectrally unique models (‘banner’ red
cwa-1261, ‘chrome’ yellow cwa-1259, ‘azure’ green cwa1258, ‘true’ blue 1910; the colour ‘descriptor’ and Krylon
number code are hereafter provided for each model) and
two spectrally neutral models (‘glossy’ white 1501 and
‘glossy’ black 1601; Fig. 1). Six divers conducted 72 trials
in total.
In the arena, we tested sexually naı̈ve fish to determine
whether preference for spectral models existed before the
fish had the opportunity to associate colour with breeding
behaviour (experiment 1b). To collect sexually naı̈ve
males, we surveyed a spawning beach each day before
commencement of sockeye settlement and breeding (see
Foote & Brown 1998). On the morning of the first day of
settlement, we collected 40 males that showed no signs
of intrasexual conflict (scrapes), which indicated that
they had not commenced breeding. The near-complete
absence of breeding activity was verified by examining the
120
100
Relative reflectance (%)
2002). Nevertheless, our tested models displayed little
reflection in the spectrum less than 400 nm. Hence, any
UV spectral properties that may be important in sockeye
mate choice are in addition to those shown here.
In wild experiments, divers (black dry-suits, mask and
snorkel) placed a model in the centre of a 1-m2, 2-cm
diameter white PVC quadrat on the spawning grounds in
measured depths between 0.5 and 3.0 m (X G SE ¼
1:58 G 0:4 m, N ¼ 258) and recorded male behaviour
for 5 min. No acclimation period was used as males
appeared undisturbed by our presence (see Results).
Between observations, divers moved at least 3e4 m in
a systematic fashion before starting another trial, while
remaining within their own delineated section of the
beach. Males generally move very little on these spawning
grounds (Quinn & Foote 1994) and new males were tested
in each trial. We controlled for differences among sections
and divers by testing each model an equal number of
times in each section. We recorded the maximum number
of males with their heads (measured at the eye) inside the
quadrat at any one time (number of males attracted), total
number of times the model was physically contacted by
males (contacts with model), number of quivers performed and number of spawning events. Quivers are
discrete behaviours where males move parallel to a female
and vibrate their body at high frequency. A spawning
event occurred when sperm release was observed and
could involve up to 15 males. A spawning event continued as long as there was no clear break in the release of
sperm across males. For analyses, we summed quivers and
spawnings into total sexual behaviour.
In arena experiments, a single male was introduced into
an enclosed arena that contained two different coloured
models. Males in good physical condition were captured
by beach seine 1e3 days before testing and held in pens
(1:5 ! 1:5 ! 2:1 m) made of fine-mesh, sealed-nylon
netting and secured in 1.5 m of water 10 m adjacent to
the arena. Arenas were constructed of 2-cm mesh chickenwire fencing, with an inner coating of fine (1 mm) silver
(1995) or black (1996e1997) screening to eliminate
interactions with the fish on the natural spawning
grounds. In 1995 the arena measured 14 m long and
extended 6 m from shore. In 1996e1997 the size was
reduced to 5:5 ! 5 m. Before each trial, the models were
placed in about 0.75 m of water in the centre of 1-m2
quadrats with the centre rib perpendicular to the
shoreline. The two quadrats were set in the same plane
(square to shore) with the nearest edge of each 2.0 m apart
(measured in a line parallel to the shoreline), in the
offshore centre of the arena. In 1995, the outer edges of
the quadrats were 0.5 m from the side of the arena, and in
1996e1997, they were 0.75 m.
In each trial, a male was transported from the holding
pen in a 40-litre container of water and released into the
near-shore centre of the arena about 3 m from each
model. After 2 min of acclimation, fish behaviour was
recorded for 10 min by two observers (one per model). We
recorded the time near each model (head, measured at the
eye, within the quadrat) and the number of contacts,
quivers and spawnings that occurred with it. Spawnings
observed during the acclimation period were included, as
W
80
60
Y
40
20
0
350
R
BU
BK
420
G
490
560
Wavelength (nm)
630
700
Figure 1. Relative reflectance of light from two spectrally neutral (W:
white; BK: black) and four spectrally unique (BU: blue; G: green; Y:
yellow; R: red) abstract sockeye salmon female models.
71
ANIMAL BEHAVIOUR, 67, 1
reproductive state of 100 females collected in the seine
hauls (see Foote 1989). Only four were judged to have
spawned at all, and none had completed spawning (4e5
spawnings per female). The males were held in two groups
of 20 in fine-mesh, sealed-nylon cages (1:5 ! 1:5 ! 2:1 m)
anchored on the bottom at 20-m depth, about 75 m
offshore and 65 m away from the nearest spawning fish,
for 12 days before testing to limit their interaction with
females and exposure to red light. Long-wavelength
radiation (red light) attenuates rapidly in water and 20-m
depths are virtually devoid of red light, even in clear water
(Lythgoe 1979). Within 24 h of bringing the fish to the
surface, we tested their preference when given a choice of
red versus yellow, green, blue or black models. Red versus
white was not tested due to the limited number of males
available. All but five males were in good condition. Three
had died and two were near moribund (note that O90%
of their natural spawning cohort were already dead at this
time; the absence of spawning activity prolonged the life
of captive males). We first tested 14 males with a red and
green choice. We considered this test paramount as it best
mimicked the colour difference between nonanadromous
sockeye and anadromous sockeye females (see Introduction). We then tested 21 males with red and one of the other
colours. Five males did not respond to the models (see
above).
Experiment 2: Spectral Purity of Red Model
To examine further the discriminatory ability of sockeye
males relative to different coloured models, we presented
males with a series of four models of more limited spectral
range (‘safety’ yellow 1813, ‘John Deere’ yellow 1804,
hereafter referred to as ‘yellow-orange’, ‘popsicle’ orange
2410 and ‘banner’ red; Fig. 2). The models differed in the
initial point of increase of reflection of longer wavelengths and in the intensity of light reflected. The rate of
increase in light reflection with wavelength was similar.
Forty trials were conducted in the wild (experiment 2a)
and 39 trials were conducted in the arena, where the
red model was paired with each of the other models
(experiment 2b). In experiment 2c, we presented 10 males
with the choice of the yellow and yellow-orange models
to determine whether they preferred one to the other.
Males used in these experiments had been tested previously in experiment 4b. One male failed to respond
(experiment 2c).
Experiments to Test Whether Spectral Purity of
Red Model was Key to Selection
Experiment 3: spectrally perceived differences
We created four reds of differing brightness by applying
coatings of 3M film of different thickness (Scotchtint
RE70NEARL, RE50NEARL and RE35NEARL) to three of
four red models (‘cherry’ red 2101). These coatings are
designed to reject the transmission of solar energy on
windows by 34%, 43% and 56% of light, respectively
(Fig. 3). A greater decrease in light occurred, presumably
because light transmission was restricted as it initially
passed through the film and again as it reflected off the
model. In the wild, we recorded the behaviour of males to
each of the four red brightness models (experiment 3a;
N ¼ 40). In the arena, we conducted two separate experiments. In experiment 3b, we gave 20 males a choice
between a yellow model and one of the four red brightness models to test whether males could distinguish
between colours, independent of variation in red brightness. One male failed to respond. Using the same males,
we compared the choice of 10 males to each of a pair of
red-0% and red-43% light-rejected models (R1 versus R3)
or red-34% and red-56% light-rejected models (R2 versus
R4; experiment 3c).
100
100
Y-O
Y
O
R
80
60
40
60
40
20
20
0
350
Y
R1
R2
R3
R4
80
Relative reflectance (%)
Relative reflectance (%)
72
420
490
560
Wavelength (nm)
630
700
Figure 2. Relative reflectance of light from four abstract sockeye
salmon female models that ranged incrementally in colour: yellow
(Y); yellow-orange (Y-O); orange (O); red (R).
0
350
420
490
560
Wavelength (nm)
630
700
Figure 3. Relative reflectance of light from a yellow (Y) model and
four red abstract female models that varied in brightness (R1eR4
were progressively darker).
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
Experiment 4: colour saturation
We used mixtures of red and white paint to produce
one pure red model (100% ‘red’ paint: S1) and four reds
of varying saturation with white (S2eS5; Fig. 4). The
addition of white paint increased light reflection (and
hence the colour value in addition to saturation) across
the range of 400e700 nm and created a series of increasingly lighter pink models. In the wild, five divers
tested the five models (N ¼ 50; experiment 4a). In the
arena, we compared the behaviour of 40 males when
given a choice of pure red (S1) and one of each of the four
red-white mixtures (S2eS5; experiment 4b). We also tested
10 males with a choice of a pure white model (W) versus
the lightest pink model (S5) to see whether the model
with the lowest red spectral purity would be selected over
an unattractive white model by males (experiment 4c).
Experiment 5: Model Characteristics and
Male Attraction
We ran an experiment in the wild to determine whether
reflectance from any particular part of a ‘cherry’ red model
was responsible for the strong sexual attraction observed.
Four models were tested: (1) an all red model (R-R,); (2)
a model in which only the central vertical rib was painted
red (R-C, the base was clear); (3) a model in which only the
base was painted (C-R); and (4) an all clear model (C-C),
which acted as a control. Four divers carried out the
experiment over two beach-spawning sites (N ¼ 56).
Underwater Light Measurements
All field measurements were obtained with an underwater spectroradiometer (model LI1800-UW, LiCor instruments, Lincoln, Nebraska, U.S.A.) interfaced to a computer
terminal operated from a boat. The spectroradiometer was
120
W
Relative reflectance (%)
100
80
60
S5
S4
set to measure photon flux (log10 photon/m2/s/nm) at
5-nm intervals from 300 to 850 nm. The spectroradiometer
was calibrated using a LiCor optical radiation calibrator as
a standard light source (LiCor model LI1800-02). The
calibration took place in air, and field measurements were
corrected for the difference in refractive index between air
and water at the collector interface (immersion effect).
Specifically, the absolute calibration in air was multiplied
by standard immersion effect corrections (wavelengthspecific) provided by LiCor, to generate an underwater
calibration. Field measurements were divided by the underwater calibration to generate absolute values of underwater
spectral irradiance. To do this, the spectroradiometer was
attached to a system of ropes and lowered into the water 1 m
away from the side of the boat that faced the sun. Spectral
irradiance was measured at the centre of the sockeye
breeding area on Woody Island beach. Downwelling, sidewelling (horizontal) and upwelling light were measured by
adjusting the orientation of the sensor in the water column
(see Barry & Hawryshyn 1999).
Spectral Measurements of Sockeye Salmon and
Female Models
Three male and female sockeye salmon were caught with
a beach seine. The fish were anaesthetized with 0.5 g/litre of
MS-222 (methanetricaine sulfonate), with no effect on
dermal colour. The fish’s gills were irrigated throughout and
all were released after recovery in a net pen. Reflectance
from colour patches was measured with an attachment to
the cosine collector of the spectroradiometer, consisting of
a tube with a 7( collection angle held 3 cm from the patch to
be measured. Each patch was scanned three times, with the
mean used. Following Craig & Foote (2001), we measured
the head region (top of the skull, between the eyes), middorsal region (midway between the origin of dorsal fin and
lateral line) and caudal peduncle (below adipose fin on
lateral line). Measurements took place outside, between
1200 and 1700 hours, under sunny conditions. Reflectance
spectra for the live fish and models (see below) were
expressed relative to a barium sulphate standard (Wyszecki
& Stiles 1982).
Spectral reflectance measurements on female models
were performed in the laboratory using an USB2000-UV-VIS
Ocean Optics Spectrometer, with a reflectance fibre optic
probe (R400-7-UV-VIS) consisting of six outer illumination
fibres (using a Thermo Oriel 150 W Xenon light source) and
an inner read fibre. The end of the probe was held 22.8 mm
above the (horizontal) reflecting surface at 45(.
40
20
S3
Statistical Analyses
S2
Data were analysed using SYSTAT version 9 (Wilkinson
1999) for KruskaleWallis, ManneWhitney U tests and for
Wilcoxon matched-pairs signed-ranks tests where N O15.
For sample sizes less than 15, Wilcoxon tests were performed according to Sokal & Rohlf (1995, pp. 440e444).
The test statistic, T, is the smaller of the absolute value of
the sums of positive or negative ranks. Within arena experiments, difference scores were used as the independent
S1
0
350
420
490
560
Wavelength (nm)
630
700
Figure 4. Relative reflectance of light from a white (W) abstract
female model and five different models that varied in red saturation
(S1 = red; S2eS5 were progressively lighter).
73
ANIMAL BEHAVIOUR, 67, 1
downwelling light from 350 to 700 nm, with maximum
transparency in the range of 460e570 nm (Fig. 6). While
there was an expected reduction in intensity and a spectral
narrowing of downwelling light with depth, there was
still a broad transmission of light up to 700 nm at 2 m.
Sidewelling light at 2-m depth was an order of magnitude
less than downwelling irradiance, with a greater attenuation of long-wavelength light. The intensity of sidewelling light coming from off the beach was slightly greater
than that recorded coming from the beach, probably
because of light absorption by the grey rock substrate.
Nevertheless, the spectra were similar. Upwelling light,
light reflected off the substrate, showed the greatest attenuation and loss of irradiance because of absorption by
the substrate and the greater path length of light on route
to the spectroradiometer.
variable in comparisons across groups (see Foote & Larkin
1988). Difference scores were obtained by subtracting the
total scores of a particular behaviour (time near model,
number of contacts, number of spawnings) performed
with one model (e.g. for experiment 1, those with the
yellow, green, blue and black models) from those performed with the model that was used across comparisons
(red model). All tests were two tailed. Values presented in
the text are means G SE.
RESULTS AND DISCUSSION
Fish Colour
For both males and females, all individuals measured
showed the same general colour patterns, with the mean
colour values for the head, mid-dorsal and caudal peduncle
measures presented in Fig. 5. To the human eye, both sexes
display an olive-green head colour. Spectrally, this is
composed of broad reflectance from short (400 nm) to long
(700 nm) wavelengths with an area of some dominance in
middle (525e550 nm, green) wavelengths. The bodies and
caudal peduncles of males are more intensely red than those
of females. The mid-dorsal regions on both sexes reflected
similar intensities of red light (O600 nm). However, females
displayed relatively greater reflectance of shorter (bluegreen) wavelengths, which accounts for why they appear as
a slightly duller red than males. While both sexes showed
the greatest reflectance of red on the caudal peduncle, the
greatest intensity (brightness) of red reflectance was about
25% higher in males.
General Description of Male Behaviour
Towards Models
In arenas, reaction to models took the form of tight
circling around the model (within the 1-m2 quadrat),
frequent physical contacts with it (body rubs, fin touches
or head butts), and direct sexual displays (quivers) and
spawnings (Fig. 7). Quivers and spawnings are unequivocal sexual behaviours (Foote 1990); their display by males
clearly shows that males perceived the models as females.
The quickest spawning occurred within 5 s of a male’s
release into the arena. In the wild, reaction to an attractive
model usually consisted of multiple males rapidly entering
the quadrat, swimming vigorously around the model, and
making multiple contacts with it (up to 200 in 5 min).
Numerous spawning events were observed (maximum Z
12 within one trial), involving 1e15 males at a time.
Activity surrounding spawning events was intense, making the recording of contacts with the model difficult.
Numbers of recorded contacts greater than 50 in 5 min
should be treated as conservative.
Underwater Light Environment
Iliamna is a clear oligotrophic lake, which results in
a spectrally rich environment on the shallow island beach
breeding grounds. There is a broad transmission of
1
(a)
0.8
Relative reflectance
74
Males
(b)
Females
Head
Body
0.6
Caudal
0.4
0.2
0
400
500
600
700
400
500
600
700
Wavelength (nm)
Figure 5. Mean relative reflectance from three different areas (head, main body and caudal peduncle) of sexually mature (a) male (N ¼ 3) and
(b) female (N ¼ 3) sockeye salmon from Iliamna Lake, Alaska.
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
14
Log photon irradiance
Surface
1-m d
12
2-m so
2-m d
2-m sb
2-m u
10
8
350
450
550
650
Wavelength (nm)
750
Figure 6. Spectral irradiance measures (log10 photons/m2/s/nm) of:
downwelling light at the surface, and at 1 m (1-m d) and 2 m (2-m
d) from the surface; sidewelling light with the collector pointing off
(2-m so) and onto (2-m sb) a sockeye salmon spawning beach at
2 m from the surface; and upwelling light at 2 m from the surface
(2-m u) measured over a 3.25-m-deep spot on Woody Island beach,
Iliamna Lake, Alaska.
Experiments with Spectrally Neutral and
Coloured Models
Experiment 1: tests with virgin and experienced males
In the wild (experiment 1a), there were significant
differences in male behaviour towards the six differently
coloured models in maximum number of males attracted,
total contacts and total sexual behaviours (KruskaleWallis
test: H5 ¼ 14:7, 28.5 and 53.9, respectively, N ¼ 72,
P ! 0:05; Fig. 8a). The red model received by far the most
attention on all scores followed distantly by the black
model. Sexual behaviours by males were observed in all 12
trials involving the red model (82 in total, including 37
spawning events). Twenty-two sexual behaviours were
observed in three of 12 trials involving the black model,
including the four spawning events that all occurred
within one trial. The yellow model received one spawning
from a near-senescent male but no other sexual behaviours. The green, blue and white models elicited no sexual
behaviours, and no apparent interest from males.
In the arena (experiment 1b), virgin males reacted very
strongly to the red model and overall showed little
attraction to the paired yellow, green, blue and black
models (Table 1). There were no significant differences
across model pairs in difference scores for time near
model, total contacts and total sexual behaviours (H4 ¼
0:33, 0.87 and 3.08, respectively, N ¼ 35, all NS). Overall,
males spent 60:7 G 5:1% of their time near the red model
versus only 2:8 G 1:1% with the other model in the 84-m2
arena. Similarly, males were nearly 15 times more likely to
make contact with the red model than with the other
model (20:4 G 1:8 versus 1:3 G 0:6). Males displayed
sexual behaviours towards the red model in 25 of 30
(83%) trials, spawning with it 29 times in 17 trials. In
contrast, no males spawned with nonred models, and
Figure 7. Underwater photograph (1.5-m depth) of sockeye salmon
males clustering around and spawning with a red abstract female
model on the substrate of sockeye breeding grounds on an island
beach in Iliamna Lake, Alaska.
only one male directed any sexual behaviour (three
quivers) towards another (black) model.
In individual comparisons, males spent more time and
made more contacts with the red model regardless of
whether it was paired with the yellow, green, blue or black
model (Wilcoxon matched-pairs signed-ranks test: all
P%0:05 except for both cases with the blue model and
contacts with the black model where P%0:1; Table 1).
Similarly, males directed more sexual behaviours (spawnings + quivers) to the red model in all four comparisons,
with the result significant in individual comparisons of
red to the yellow, green and black models (all P%0:05).
Experiment 2: spectral purity of red model
In the wild (experiment 2a), male response was by far
the greatest with the red model, with a rapid decline in
response from the orange to the yellow model (Kruskale
Wallis test: H3 ¼ 17:87, 24.98 and 33.28, for maximum
number of males attracted, total contacts and total
spawnings, respectively, N ¼ 40, P ! 0:001; Fig. 8b). Males
displayed sexual behaviours only to the red model (90% of
trials), including 11 spawning events.
75
76
ANIMAL BEHAVIOUR, 67, 1
In the arena (experiment 2b), males spent 72:6 G 3:5%
(N ¼ 38) of their time near the models (Table 2). The
reaction to the red model depended on what model it was
paired with. Variation in the difference scores for time
spent near the model and total contacts with the model
were significant across comparisons (KruskaleWallis test:
H2 ¼ 18:86 and 7.68, respectively, N ¼ 38, P ! 0:05).
Within comparisons, males made no clear distinction
between the red and orange models, in either total time
near the model or total contacts with the model
(Wilcoxon matched-pairs signed-ranks test: T ¼ 38,
N ¼ 13 and T ¼ 16, N ¼ 10, NS). In contrast, scores for
both variables were greater with the red model when
paired with the yellow-orange (T ¼ 1 and 8.5, N ¼ 12,
P ! 0:05) and yellow models (T ¼ 1 and 2.5, N ¼ 13,
P ! 0:005). Males displayed sexual behaviour to the red
model during 28.9% of the trials (11 of 38) including one
spawning, but did so only 2.6% of the time with the other
models (1 of 38; to the orange model).
The results of experiments 2a and 2b suggested increasing discrimination by males with increasing red
spectral purity of the model. To examine this further, we
gave 10 males a choice between the yellow-orange and
yellow models (experiment 2c; Table 2). Males spent
nearly 2.5 times more time near the yellow-orange model
but the difference was not significant (Wilcoxon matchedpairs signed-ranks test: T ¼ 15, N ¼ 9, NS). Contacts with
the yellow-orange model totalled 52 versus only four with
the yellow model, but the difference was not significant
(T ¼ 1, N ¼ 5, NS). Sexual behaviour was observed in only
one trial, in which a male quivered four times to the
yellow-orange model, indicating that this model had
limited sexual attraction to males. The most striking
difference from experiment 2a was in the percentage of
time that males stayed near the models. Males spent
38:4 G 9:7% of their time near either model in this test
(27:7 G 0:9 and 10:7 G 3:7%, respectively, for the yelloworange and yellow models).
Experiments to Test Whether Spectral Purity of
Red Model was Key to Selection
Figure 8. Results from experiments 1e5 showing the responses of
free-ranging sockeye salmon males towards abstract female models
that varied in spectral properties. MM: maximum number of males
attracted; TC: total number of contacts with model, divided by 10;
TS: total sexual behaviours (spawnings + quivers). (a) Experiment 1:
six models of a wide spectral range (R: red; Y: yellow; G, green; BU:
blue; BK: black; W: white; see Fig. 1). (b) Experiment 2: four models
that ranged from red to yellow (R: red; O: orange; Y-O: yelloworange; Y: yellow; see Fig. 2). (c) Experiment 3: four red models of
decreasing brightness (R1eR4; see Fig. 3). (d) Experiment 4: five
models with decreasing red saturation (S1eS5; see Fig. 4). (e)
Experiment 5: four models that varied in the extent and placement
(rib and/or base) of red paint (R-R: red rib, red base; R-C: red rib,
clear base; C-R: clear rib, red base; C-C: all clear). In each case, the
purest, brightest and/or most extensively painted red model is
shown at the left with, in general, models of declining red
reflectance shown to the right. yP ! 0:10; *P ! 0:05; **P ! 0:01;
***P ! 0:001.
Experiment 3: is choice dependent on spectral or
brightness characters?
In the wild (experiment 3a), males responded vigorously
to all four red models independent of varying brightness.
Contacts averaged over 60 with each model, and all models
elicited at least eight spawning events in 10 trials (Fig. 8c).
Nevertheless, there was a general decline in response for
all variables with decreasing brightness (R1eR4), but only
the decline in the maximum number of males attracted
was even marginally significant (KruskaleWallis test:
H3 ¼ 6:79, N ¼ 40, P ¼ 0:08).
In the arena (experiment 3b), males spent 65:1 G 5:7%
of their time with the red models compared with only
1:2 G 0:4% with the yellow model (Table 3). Across treatments, there were no significant differences in difference
scores for total time near model, total contacts or total
sexual behaviours (KruskaleWallis test: H3 ¼ 0:84, 0.82
and 1.02, respectively, N ¼ 19, NS). Furthermore, 94
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
Table 1. Responses (X G SE) by individual male sockeye salmon over 10 min of observation in a test arena on the natural breeding ground to
two abstract female models, one red and one of another colour (blue, green, yellow or black)
Time near model*
Other model
Blue
Green
Yellow
Black
Contacts with modely
Spawningsz
Sexual behaviourx
Red
Other
Red
Other
Red
Other
Red
Other
N
379.7 G 87.4
353.8 G 50.0
344.7 G 50.6
390.0 G 72.0
32.2 G 28.9
9.1 G 3.1
14.3 G 6.8
20.5 G 17.3
23.0 G 5.5
19.1 G 2.6
24.2 G 4.7
16.7 G 3.2
2.3 G 2.1
0.7 G 0.3
1.3 G 0.8
1.7 G 1.2
0.5 G 0.3
1.0 G 0.3
1.7 G 0.7
0.7 G 0.3
0G0
0G0
0G0
0G0
4.2 G 2.3
6.8 G 1.8
8.3 G 1.5
4.7 G 2.0
0G0
0G0
0G0
0.5 G 0.5
6
12
6
6
Red: responses to the red model; other: responses to blue, green, yellow or black models.
*Total time spent inside the 1-m2 quadrat within which each model (‘red’ or ‘other’) was centred.
yTotal number of individual physical contacts by males with the model.
zTotal number of spawnings involving sperm release; totals for this behaviour alone included a 2-min acclimation period.
xTotal numbers of spawnings and quivers combined.
sexual behaviours (including 23 spawnings) occurred with
the red models, whereas none occurred with the yellow
model. Unfortunately, the sample sizes were too small
within treatments for statistical comparisons (N%5).
However, when the data were pooled across treatments,
preference for the reds of varying brightness over the yellow
model in time near the model, contacts with the model and
sexual behaviour were clear (Wilcoxon matched-pairs
signed-ranks test: Z !3:5, N ¼ 19, P ! 0:001 for all
variables). The ability of males to distinguish between the
yellow (and undoubtedly other colours; see experiment 1)
and reds, independent of their brightness, shows that males
use colour vision in mate choice (McFarland & Munz 1975;
Lythgoe 1979; Birgersson et al. 2001).
When presented with a choice of reds of different
brightness (R1 versus R3, and R2 versus R4; experiment
3c), males spent 61:4 G 6:7% of their time near the
brightest model (R1 and R2) versus 19:6 G 6:5% of their
time with the duller model (R3 and R4; Table 4). Similarly,
total contacts with the brighter model were triple that
with the duller model (14:7 G 1:8 versus 4:0 G 1:4,
N ¼ 20). Males spawned with the brighter models 20
times versus only twice with duller models. There were no
differences between treatments in the difference scores for
any of these variables (ManneWhitney U test: U ¼ 59:0,
62.5 and 66.0, N1 ¼ N2 ¼ 10, NS, respectively, for differences in time near model, total contacts and total sexual
behaviours). Analyses of the pooled data set showed
a strong male preference for the brighter model on all of
these scores (Wilcoxon matched-pairs signed-ranks test:
Z ¼ 2:43, 2.74 and 3.25, N ¼ 20, P ! 0:05). However,
within treatments, differences in time spent near model,
total contacts with the model and total sexual behaviours
performed were only significant in the comparison of R2
and R4 (T ¼ 0, 0 and 0, N ¼ 10, 9 and 9, respectively,
P ! 0:05 using the Bonferroni method for multiple
comparisons).
Experiment 4: colour saturation
In the wild (experiment 4a), males reacted differently to
the individual presentation of red (S1: saturated red) and
progressively pinker models (S2eS5; KruskaleWallis test:
H4 ¼ 11:94, 26.41 and 19.74, respectively, for number of
males attracted, contacts with the model and sexual
behaviours performed, N ¼ 50, P ! 0:05; Fig. 8d). S1
received the most attention in all measures, with a decline
in male response with decreasing red saturation. S4 and S5
received little attention (scores for number of males
attracted and number of contacts with the model were
low). Nevertheless, males displayed sexual behaviours
(including at least one spawning) to all but S4. It seems
likely that the reception of shorter wavelength light, most
likely by middle wavelength (green) cone receptors,
increasingly inhibits behavioural response to red light
Table 2. Responses (X G SE) by individual male sockeye salmon over 10 min of observation in a test arena on the natural breeding grounds to
two abstract female models: one red and another from a series that varied progressively from yellow (Y), through yellow-orange (Y-O), to
orange (O)
Time near model
Other model
O
Y-O
Y
Contacts with model
Spawnings
Sexual behaviours
Red
Other
Red
Other
Red
Other
Red
Other
N
190.5 G 43.0
360.3 G 38.8
468.3 G 46.3
228.2 G 46.8
44.7 G 15.7
11.9 G 9.2
6.6 G 1.4
9.1 G 1.6
8.0 G 1.5
5.5 G 1.3
2.9 G 1.1
0.4 G 0.3
0.1 G 0.1
0G0
0G0
0G0
0G0
0G0
0.2 G 0.1
0.3 G 0.1
0.4 G 0.1
0.1 G 0.1
0G0
0G0
13
13
13
Y-O
165.9 G 65.4
Y
64.4 G 22.3
Y-O
0.4 G 0.2
Y
5.8 G 2.6
Y-O
0G0
Y
0G0
Y-O
0G0
Y
0.4 G 0.4
9
See Table 1 for a description of the behavioural response categories.
77
78
ANIMAL BEHAVIOUR, 67, 1
Table 3. Responses (X G SE) by individual male sockeye salmon over 10 min of observation in a test arena on the natural breeding grounds to
two abstract female models, one yellow and one of four red models of decreasing brightness (R1eR4)
Time near model
Other model
R1
R2
R3
R4
Contacts with model
Spawnings
Sexual behaviours
Yellow
Other
Yellow
Other
Yellow
Other
Yellow
Other
N
6.8 G 5.9
7.8 G 4.8
7.6 G 7.4
5.5 G 1.9
389.0 G 76.2
353.8 G 57.9
422.2 G 97.8
399.8 G 25.4
0.2 G 0.2
0.6 G 0.6
0.8 G 0.8
0G0
18.6 G 2.2
20.0 G 3.7
22.2 G 2.1
19.3 G 1.5
0G0
0G0
0G0
0G0
1.6 G 0.7
1.6 G 0.6
0.8 G 0.6
0.8 G 0.5
0G0
0G0
0G0
0G0
5.0 G 1.9
3.4 G 0.9
5.2 G 1.6
6.5 G 2.4
5
5
5
4
See Table 1 for a description of the behavioural response categories.
from long-wavelength receptors (McFarland & Munz
1975; McDonald & Hawryshyn 1999).
In the arena (experiment 4b), males reacted very
strongly to at least one of the pair of S1 and S2eS5
models, spending 86:4 G 3:2% of their time near both
models (Table 5). In general, males showed no clear
preference for S1 versus S2 or S3 (time near model and
contacts with model did not differ), but showed increasingly greater attraction to S1 when it was paired
with either S4 or S5. The difference in time near model
across pairs was not significant (KruskaleWallis test:
H3 ¼ 4:42, N ¼ 40, NS) but the differences in total
contacts with model and total sexual behaviours performed were (H3 ¼ 10:86 and 9.77, N ¼ 40, P ! 0:05).
Males performed sexual behaviours with all but S4, and
spawned with S1, S2 and S3. Within choices, the pattern
was less clear. There were no significant differences
within the comparisons of S1 and S2, S1 and S3 or S1
and S4 in either total time spent near model or total
contacts with model (Wilcoxon matched-pairs signedranks test: time near model: T ¼ 23, 27.5 and 14, N ¼ 10,
NS; contacts with model: T ¼ 27:5, 21 and 16, N ¼ 10,
NS). Males strongly preferred S1 to S5 (time near model
and contacts with model: T ¼ 0, N ¼ 10, P ! 0:01).
Indeed, they spent only 1:1 G 0:5% of their time near
S5 when S1 was present. In contrast, S5 elicited strong
sexual reaction from males when paired with a white
model (T ¼ 1:5 and 0, N ¼ 10 and 9, P ! 0:01, for time
near model and contacts with model, respectively; Table
5). Three males spawned a total of 11 times with S5.
Nevertheless, the percentage of time that each male
spent near the model (53:3 G 9:8%) was much lower
than the lowest score observed in experiment 4b
(77:3 G 9:8% for the comparison of S1 and S4).
Experiment 5: Paint Distribution Characteristics
and Male Attraction
Males reacted sexually to the three differently painted
red models but not to the all clear model (Fig. 8e). Scores
for number of males attracted, number of contacts with
model and number of sexual behaviours performed were
highest for the fully painted model (R-R), lowest for the all
clear (C-C) model and intermediate for the red-rib (R-C)
and red-base models (C-R; KruskaleWallis test:
H3 ¼ 12:02, 18.04 and 12.44, N ¼ 56, P ! 0:01). Males
spawned with R-R (12 times), R-C (three times) and C-R
(seven times) but not with C-C. Males appeared not to
perceive the all clear model; contacts with it appeared to
be inadvertent collisions rather than directed movements.
In summary, because the response to red models did not
appear to depend on a single particular coloured shape,
the position of the colour (red) directly on the substrate
(like the body position of an egg-depositing female)
probably accounts for the strong male sexual response
(see Newcombe & Hartman 1980).
GENERAL DISCUSSION
The Role of Female Colour in Male Choice
Male sockeye salmon discriminated between abstract
female models that varied in their spectral qualities,
spawning almost exclusively with models that had maximum reflection in long (red) wavelengths and a general red
hue. The results were consistent over years (1995e1997),
over the course of the day including dusk, over variable
weather conditions (sunny and calm to overcast, windy
and raining), between sexually naı̈ve and experienced
Table 4. Responses (X G SE) by individual male sockeye salmon over 10 min of observation in a test arena on their natural breeding grounds to
two abstract red female models of varying brightness (one bright: R1, R2; one dull: R3, R4)
Time near model
Models
R1 versus R3
R2 versus R4
Contacts with model
Spawnings
Sexual behaviours
HB
LB
HB
LB
HB
LB
HB
LB
N
339.7 G 72.0
396.6 G 38.1
185.3 G 68.0
120.4 G 27.4
13.1 G 3.3
16.2 G 1.7
5.8 G 2.4
2.2 G 1.3
1.2 G 0.8
0.8 G 0.3
0.2 G 0.2
0G0
2.8 G 1.2
4.1 G 0.9
0.3 G 0.2
0.4 G 0.3
10
10
See Table 1 for a description of the behavioural response categories. HB: higher brightness (R1, R2); LB: less bright (R3, R4).
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
Table 5. Responses (X G SE) by individual male sockeye salmon over 10 min of observation when tested in an arena on the natural breeding
grounds to two abstract female models: one red (S1) and another from a series of models of decreasing red saturation (S2eS5); and one white
model and one light pink (S5) model
Time near model
Other model
S2
S3
S4
S5
Contacts with model
Spawnings
Sexual behaviour
S1
Other
S1
Other
S1
Other
S1
Other
N
323.0 G 86.8
276.4 G 86.0
300.4 G 70.4
473.3 G 39.7
244.4 G 79.7
291.0 G 86.9
163.1 G 60.1
6.6 G 3.1
12.1 G 3.6
9.7 G 2.9
13.0 G 2.7
19.8 G 2.2
12.4 G 3.6
13.4 G 3.8
7.8 G 2.1
0.1 G 0.1
0G0
0G0
0.1 G 0.1
0.4 G 0.4
0.2 G 0.2
0G0
0G0
0G0
0G0
0.2 G 0.2
0.7 G 0.6
1.7 G 1.5
0.5 G 0.2
0.2 G 0.2
0G0
0G0
10
10
10
10
S5
305.7 G 63.6
White
13.9 G 6.2
S5
14.2 G 3.4
White
0.4 G 0.2
S5
1.1 G 0.7
White
0G0
S5
1.4 G 1.0
White
0G0
10
See Table 1 for a description of the behavioural response categories.
males and between arena and wild experiments. The
strength and consistency of these results indicate that male
choice based on female spectral characteristics is a significant evolutionary force in this species.
There is a very close correspondence between female
trait expression and male preference in sockeye as has
been observed in other fish (Houde & Endler 1990;
McDonald et al. 1995; Berglund & Rosenqvist 2001;
Boughman 2001). Of particular interest here is the
demonstration of the broad range of spectral characteristics that are important in male choice. The bodies of
female sockeye show a rapid increase in reflectance
starting at about 570 nm, with the measured maximum
at about 700 nm (Fig. 5b). Males showed the greatest
attraction to models of similar reflectance patterns
(Fig. 8a). Indeed, even relatively slight decreases in the
initial point of increase of long-wavelength light (with
an incremental shift in hue from red to yellow) resulted in
a sharp decrease in male attraction in the wild (Fig. 8b).
While males preferred brighter red models (Table 4), they
still showed strong attraction over a wide range in
brightness, from bright red to near black-red (Fig. 8c).
This is consistent with marked variation in red brightness on the female body (Fig. 5b; Craig & Foote 2001), and
with the fact that female brightness will vary over the
day, with weather conditions, and with their distance
from the surface (Fig. 6). Similarly, while males preferred
the purest reds over unsaturated reds, they still showed
a broad range of attraction to unsaturated reds. This is
consistent with variation in red saturation that occurs
over a female’s body (Fig. 5b). Females can vary the
intensity of black on their lower flanks (from white to
black) and in a lateral band on their sides (from present to
absent) within minutes (Schroder 1981; C. J. Foote,
unpublished data). The limited but repeated sexual
attraction observed towards black models (Table 1, Fig.
8a) indicates that such achromatic characters are important in mate choice in sockeye as previously demonstrated
by Takeuchi et al. (1987; see also Baube et al. 1995; Endler
& Houde 1995; McDonald et al. 1995; Berglund &
Rosenqvist 2001).
Green models were not attractive to males (Fig. 8a,
Table 1), which suggests that the olive-green head colour
of sockeye is not a sexually attractive trait on its own.
However, this conclusion must remain tentative because
the tested green showed only little of the long-wavelength
reflectance present in the green heads of females (Figs 1,
5). Nevertheless, the results of experiment 2 indicate that
the predominant short- and medium-wavelength reflectance from a female’s green head would inhibit any male
sexual response to the reflected red light.
Males discriminated between relatively unattractive
models as well as between attractive models. For example,
males marginally preferred the yellow-orange to the
yellow model, even though both were largely unattractive
(Table 2, Fig. 8b). Similarly, males strongly preferred the
least saturated red model (S5) over a white model, even
though the former was almost totally ignored when paired
with a saturated red model (S1; Table 5). At the other end
of the attraction spectrum, males preferred bright over
dull reds, even though both were highly attractive on
their own (Table 4, Fig. 8c). This fine-scale, broad-range
comparative differentiation of models indicates that
sockeye males use variation in female spectral characters
(see Craig & Foote 2001) in mate choice and not simply
for species recognition. In the latter case, one would
expect an all-or-none response, not such a finely textured
comparative approach using both chromatic and achromatic cues.
Male Colour Preference and Sexual Dimorphism
There are a number of interrelated hypotheses that
account for the evolution of carotenoid-based red secondary sexual colours in fish (Endler & Houde 1995; Grether
2000). Carotenoids have received much attention with
regard to their beneficial roles as antioxidants and in the
immune system (Chew 1993; Olson & Owens 1998;
Møller et al. 2000). By displaying carotenoid-based traits,
fish may advertise their ability to sequester this often
limited and important resource (Endler 1980; KodricBrown & Brown 1984; Kodric-Brown 1989; Grether et al.
1999). In fish, including salmonids, there is a positive
relationship between condition and carotenoid expression
(Torrissen 1984; Milinski & Bakker 1990; Nicoletto 1991;
Houde & Torio 1992; Skarstein & Folstad 1996; but see
Candolin 1999). For example, Fleming & Gross (1989)
showed that in coho salmon, O. kisutch, there is a positive
79
80
ANIMAL BEHAVIOUR, 67, 1
relationship between the intensity of red carotenoid-based
coloration in females across populations and a female
competition (parental care) index. In sockeye, the more
carotenoids a fish sequesters from its diet, the redder it
becomes at maturity, with the ability to acquire carotenoids a heritable trait (Craig & Foote 2001; see KodricBrown 1989; Hill 1992). Hence, the possibility exists that
by selecting redder females, sockeye males may benefit
immediately through the increased quality of parental
care provided by the female and later through the genetic
benefits of greater carotenoid utilization abilities of their
young. Note, however, that in a closely related species,
chinook salmon, O. tshawytscha, ‘white-fleshed’ fish exist
that are genetically limited in their ability to store
carotenoids in their muscle (Withler 1986; Ando et al.
1994). Given that they appear to suffer no obvious fitness
disadvantage, the postulated critical role of carotenoids
remains in question.
Independent of their potential physiological benefits, it
is clear that red carotenoid-based colours are very conspicuous when contrasted against the green dominated
background light of freshwater environments, including
Iliamna Lake (Figs 5, 6; Lythgoe 1979; Sigmund 1983;
McDonald & Hawryshyn 1995). Sockeye females have
only a single short breeding life span on the island
beaches (an average of 8 days; Quinn & Foote 1994) and
their conspicuousness probably decreases the time it takes
to attract a suitable mate and spawn (Endler 1992;
Johnstone 1997; Hamon et al. 1999). Furthermore, the
conspicuousness of red against the background light and
the contrasting green head colour may act to amplify
a male’s perception of female body size (Hasson 1997),
which is another important criterion in male choice
(Foote 1988; Blanchfield & Ridgway 1999; Berglund 2000).
Sockeye salmon are sexually dimorphic in physical
dimensions and colour (Fig. 5). The exaggerated traits of
males (e.g. snout length, hump size, colour) are consistent
with the greater variance in reproductive success observed
in that sex (Quinn & Foote 1994; Foote et al. 1997).
However, Blount et al. (2000) provided another explanation for sexual dimorphism in carotenoid-based colours.
Females may be limited in their ability to express carotenoid-based sexual traits because of a strong natural selection pressure to store large amounts of carotenoids in
their eggs. In sockeye, both sexes store equal amounts of
carotenoids in their flesh and both fully utilize these stores
during maturation (Craig & Foote 2001). However,
females deposit upwards of 85% of their carotenoids in
their eggs (Crozier 1970). Therefore, the brighter and
purer reds of sockeye males may not reflect differences in
the intensity of sexual selection but rather a difference in
the trade-off between the sexes between natural and
sexual selection. We saw no sign of decrease in male
attraction towards increasingly brighter red models within
or across experiments to indicate that male preference for
brighter reds has an upper limit (Fig. 8), yet females are
duller red than males (Fig. 5).
The expression of sexual colours in both sexes, and in
particular the less intense colours of females, leaves open
the possibility that female colour has evolved as a correlated trait resulting from female selection for male
colour. Skarstein & Folstad (1996) rejected this in their
study of carotenoid-based sexual dimorphism in the
closely related Arctic charr, Salvelinus alpinus, arguing that
such traits would be expected to uncouple given the costs
of carotenoid expression. The direct link shown here
between male choice and female colour adds support to
their argument.
Sensory Bias and the Evolution of Red Secondary
Sexual Colour in Kokanee
The results of this study support Craig & Foote’s (2001)
contention that a pre-existing bias towards red in sockeye
was an evolutionary force behind the re-emergence of red
in kokanee, the nonanadromous morph of the species (see
Endler & Basalo 1998). We know that salmon detect light
from a broad spectrum with four different cones (ultraviolet to red), and that this system is ideally suited to
detect red in freshwater environments (Beatty 1966;
Novales Flamarique et al. 1992; Hawryshyn & Harosi
1994; Novales Flamarique 2000; Hawryshyn et al. 2001).
Here, we have shown that sockeye, the recent progenitor
of kokanee (Foote et al. 1989; Wood 1995; Taylor et al.
1996), have a strong sexual preference for the colour red.
It seems likely that this preference is innate, as would be
expected in a semelparous species, but we do not have
conclusive evidence for this. Nevertheless, the supporting
evidence is strong. Sexually naı̈ve sockeye, those without
opportunity to associate red directly with breeding
behaviour, showed the same strong colour preferences as
experienced males did (Table 1). Furthermore, sockeye
reared to maturity in a freshwater hatchery under limited
light conditions in the absence of red stimuli (including
themselves; they were green at maturity) also preferred red
models (C. J. Foote, G. S. Brown, J. S. Drake & R. D. Ball,
unpublished data). Clearly, it seems highly unlikely that
the preference for red is environmentally induced. A
genetic basis for mate choice based on colour has been
shown repeatedly in fish (see Houde 1997 for review).
Over the last 10 000 years, as anadromous sockeye
invaded lakes that were previously glaciated and gave rise
to nonanadromous populations, they probably passed on
to those populations the strong preference for red, but not
the ability to turn red in carotenoid-limited freshwater
environments. This potentially inherited preference for
red has apparently resulted in the evolution of the
increased genetic ability (three times) of kokanee to utilize
carotenoids and ultimately to express red colour at
maturity, just like their sockeye ancestors (Drake 1999;
Craig & Foote 2001). Therefore, while sexual selection and
sensory drive are considered driving forces behind the
phenotypic and genetic differentiation of populations
(Lande 1981; Endler & Basalo 1998; Boughman 2001;
Panhuis et al. 2001), the results of this study and those of
Craig & Foote (2001) point out the constraints that these
selective forces can impose on phenotypic differentiation.
None the less, these phenotypic constraints do not negate
genetic differentiation in processes involved in the production of similar phenotypes. Indeed, such constraints
may play an important role in population genetic
FOOTE ET AL.: MALE MATE CHOICE AND COLOUR IN SALMON
differentiation and even speciation in situations where
resources necessary to produce the sexual traits in question vary in availability across environments (Conover &
Shultz 1995; Craig & Foote 2001).
Acknowledgments
All experiments were performed under the conditions and
guidelines of the University of Washington Animal Care
Committee (Bristol Bay Salmon, 1992e1997, IACUC No.
2584-01). We are indebted to W. N. McFarland for his
advice on experimental design and help in technical
aspects of our study. We thank J. K. Craig, G. Grether, A.
Kodric-Brown, I. Novales Flamarique, N. R. Liley, C. C.
Wood and two anonymous referees for their valuable
input. We thank R. Garcia, T. Hamon, B. Horan, M.
Kinneson, L. Lehmann, F. Leonetti, N. R. Liley, J. Miller, D.
Peterson, A. Reischauer, R. Steen and R. Tabor for help
in conducting the experiments. We thank the Pacific Seafood Processor’s Association and independent seafood processing companies for funding this work. We thank the
School of Fisheries, University of Washington, for permission to use their field facilities and the Alaska Department
of Fish and Game for their permission to conduct research
on sockeye salmon in Iliamna Lake. NSERC provided an
equipment grant for the underwater spectroradiometer.
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