Behavioral Ecology Vol. 15 No. 4: 543–548
DOI: 10.1093/beheco/arh043
Female collared flycatchers learn to prefer
males with an artificial novel ornament
Anna Qvarnström, Veronica Blomgren, Chris Wiley, and Nina Svedin
Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University,
Norbyvägen 18D, SE-752 36 Uppsala, Sweden
We experimentally investigated whether learning from previous experiences can lead to the establishment of a new mate
preference in a wild population of birds. During year one (2001), 63 female collared flycatchers (Ficedula albicollis) bred together
with males that we had provided with a novel trait, a red stripe on their white forehead patch (a sexually selected trait). Some
color patterns of birds are largely determined by a few genes, and this experiment was designed to mimic the occurrence of
mutations in such genes. In the subsequent year (2002), we found that females with previous experience with red-striped males
were more likely to pair with red-striped males (76%) than with control males. By contrast, naı̈ve females (i.e., with no previous
experience with red-striped males) were not more likely to pair with red-striped males (44%) than with control males. Females
paired with red-striped males produced more offspring than females paired with control males, suggesting that males with the
novel trait had become favored by selection. Thus, female collared flycatchers appear to quickly learn to associate a novel trait
with a suitable mate that, in turn, leads to assortative mating between local mates (i.e., males with the new trait and females with
previous experience of the new trait). Our results provide support for the notion that learning may play an important role when
the co-evolution of preferences and preferred traits takes different routes in different populations of the same bird species. Key
words: assortative mating, imprinting, learning, mate choice, novel ornament, population divergence, preference. [Behav Ecol
15:543–548 (2004)]
heoretical models of speciation show that sexual selection
can generate rapid divergence between populations
(Lande, 1981, 1982; Pomiankowski and Iwasa, 1998; Schluter
and Price, 1993), and these models are well supported by
patterns in nature. For example, closely related species
generally differ markedly in sexually selected traits (reviewed
by West-Eberhard, 1983; Price, 1998; Panhuis et al., 2001).
Thus, sexual selection seems to play a central role in the
evolution of pre-zygotic isolation.
In this study we investigated the plausibility of one
suggested route to new directions of sexual selection. Some
color patterns of birds are largely affected by a small number
of genes (Grant and Grant, 1997), and mutations in such
genes may frequently provide potential new targets of sexual
selection (Price, 2002). A novel color pattern may become
favored by female choice either because females have a preexisting bias in their sensory system in favor of the novel trait
(Kirkpatrick, 1987) or because they learn to associate the trait
with a suitable mate (Price, 2002; Weary et al., 1993). Preexisting biases in the sensory system and learning are not
likely to act as two mutually exclusive mechanisms by which
new preferences may become established in a population.
They are, by contrast, likely to interact. For example, the male
trait that females are able to perceive and remember depends
on the females’ sensory system.
Mate preferences are often viewed as static traits, but some
recent studies have demonstrated adaptive plasticity in mate
preferences (Badyaev and Hill, 2002; Lesna and Sabelis, 1999;
Qvarnström et al., 2000). There are at least two possible
proximate explanations for plasticity in a mate preference;
females may either use a genetically determined choice
strategy or modify their mate preference as they learn from
past experiences. Empirical studies on the role of learning in
T
Address correspondence to A. Qvarnström. E-mail: anna.
[email protected]
Received 29 January 2003; revised 3 August 2003; accepted 18
August 2003.
mate choice are mainly restricted to sexual imprinting (i.e., it
is investigated whether offspring learn to prefer mates similar
to their parents; Freeberg et al., 1999; Riebel, 2000; Slagsvold
et al., 2002). It is debated whether sexual imprinting could
lead to preferences for extreme traits (e.g., Laland, 1994; ten
Cate and Vos, 1999; Weary et al., 1993; Witte and Sawka, 2003).
Female mate preferences may not only be influenced by
their parents but also by experiences with both conspecific and
heterospecific individuals later in life (Domjan, 1992; Irwin
and Price, 1999). The aim of this study was to investigate
whether learning from previous experiences can lead to the
establishment of a new mate preference in a wild population of
birds. We artificially simulated the occurrence of a mutation
affecting coloration of male collared flycatchers breeding on
an island. Male collared flycatchers are black and white and
possess a conspicuous white forehead patch that functions as
a signal, both in male-male competition over suitable nest sites
(Pärt and Qvarnström, 1997; Qvarnström, 1997) and in female
choice (Qvarnström et al., 2000; Sheldon et al., 1997). In
sympatry with the pied flycatcher (Ficedula hypoleuca), female
preference for this trait has been suggested to reinforce
reproductive isolation (Sætre et al., 1997). In this study we
introduced a red stripe on the base of the forehead patch of
males and investigated its effect on assortative mating between
‘‘local’’ males (i.e., red-striped) and local females (i.e., with
previous experience of red-striped males) in the subsequent
year.
METHODS
The study was performed in 2001 and 2002 in three study plots
on the southern part of the island of Gotland (57 109 N, 18
209 E), Sweden. The study site consists of several separated
nest-box plots that were established in 1980 and are inhabited
by a population of collared flycatchers displaying a high
annual rate of return of both adults and juveniles (Gustafsson,
1989; Pärt and Gustafsson, 1989). The mean reproductive
success differs between plots, and female collared flycatchers
Behavioral Ecology vol. 15 no. 4 International Society for Behavioral Ecology 2004; all rights reserved.
Behavioral Ecology Vol. 15 No. 4
544
Table 1
Results from a multiple logistic regression showing the influences
of male experimental treatment (painted with either a red or
a transparent 4 mm stripe on the forehead patch) and arrival date
on male likelihood to be found breeding after treatment in the
collared flycatchers (Ficedula albicollis)
Variable
df
L-R v2
p
Treatment (A)
Arrival date (B)
A*B
1
1
1
2.002
4.702
4.460
.16
.03
.03
Model: v2 ¼ 8.88, p ¼ .03, n ¼ 90.
are known to base their decision to return to the same study
plot the subsequent year on the reproductive success
experienced by them (Pärt and Gustafsson, 1989) and by
their neighbors (Doligez et al., 2002). To increase the
likelihood that experimental females would return to the
same study plot on two consecutive years (a prerequisite for
our experiment), we selected three plots within prime habitat.
From early May to early June in year one (2001) we searched
two of the selected plots for male collared flycatchers that had
newly arrived after their migration from the African winter
quarters. All observed males (n ¼ 57) were caught, ringed, and
measured using standard procedures (Gustafsson, 1989; Pärt
and Gustafsson, 1989). Afterwards, they were painted with a 4
mm red stripe (using a permanent marker pen) on the base of
their white forehead patch. The two study plots were checked
regularly to determine date of egg laying, clutch size, hatching
date, and number of fledged young. Breeding red-striped
males (n ¼ 32) were caught again, weighed, and measured
when feeding 7-day-old offspring. In addition, the breeding
males (n ¼ 31) within the third study plot (which had not been
caught on arrival) were painted with a red stripe on the base of
their forehead patch when feeding 7-day-old offspring. Adult
females were mostly caught when incubating. Females not
ringed as nestlings were classified either as yearlings or older
based on the shape of their primary coverts and the color of
the inside of their upper mandible (Karlsson et al., 1986). A
similar classification of previously unmarked males was based
on the color of their remiges (Svensson, 1992). Nestlings were
ringed, measured, and weighed when 13 days old. Judging
from recaptured birds and from observations of males feeding
offspring, the red stripe slowly faded after exposure to various
weather conditions during the breeding season and finally
disappeared when the birds molted before their autumn
migration.
During the subsequent year (2002), from early May to early
June, we searched the same three study plots for newly arrived
males. All observed males (n ¼ 90) were caught, ringed, and
measured using standard procedures (Gustafsson, 1989; Pärt
and Gustafsson, 1989) and they were divided into two
treatment groups. Every second male was provided with a 4
mm red stripe (using a permanent marker pen) on the base of
the white forehead patch (n ¼ 46, red-striped). Remaining
males (n ¼ 44, control) were painted with a transparent
marker. Female collared flycatchers, which arrive a few days
after the males, were thereby given a choice to settle either
with red-striped males or with control males. Local females
that had bred with red-striped males the previous year (2001)
and their daughters were classified as ‘experienced.’ Pairing
speed was estimated as the number of days passing between the
release of a male and the onset of nest building. Data on adult
morphology and breeding performance were collected following the same procedure as the previous year (see above).
RESULTS
Female experiences of breeding with males possessing
the novel trait in year 1
In year 1 (2001), female collared flycatchers breeding in the
study plots where we introduced the novel male trait (a red
stripe on the forehead patch) had no choice but to breed with
males possessing the novel trait. We compared the reproductive success of these females with the reproductive success of
females breeding with males in other study plots. Because the
estimate of reproductive success, the number of fledged
young, was not normally distributed, we used ordinal logistic regression (see Thompson et al., 1998). Females paired with redstriped males produced relatively more fledged young (n ¼
202, v2 ¼ 14.10, p ¼ .0002, means 5.00 and 3.81 for females
paired with red-striped and to normal males, respectively). The
main reason for this difference is probably that we painted the
males exclusively in study plots within prime habitat (see
Methods).
Does the novel trait influence male success in
competition over mates in year 2?
Male collared flycatchers that we found breeding after the
treatment in year 2 had successfully passed two episodes of
sexual selection. First, these males had regained their
territories (i.e., an episode of male-male competition, see Pärt
and Qvarnström, 1997, Qvarnström, 1997) and then attracted
a female (i.e., an episode of mate choice). To test whether
a male’s probability of breeding was influenced by the
experimental treatment we performed a multiple logistic
regression. The arrival date of males was included in the model
because arrival date is likely to influence the intensity of
competition over mates. Competition over mates is likely to
increase as the number of available breeding sites and
unpaired females declines during the course of the season.
We found that a male’s probability to breed after treatment was
influenced by an interaction between treatment and arrival
date (Table 1). To visualize this interaction we divided males
into two groups based on their arrival date (early , mean
arrival date , late). Among early males, there was no
significant difference between males belonging to the two
different treatment groups in their probability of breeding
(n ¼ 44, v2 ¼ 1.69, p ¼ .19). However, among late males, redstriped ones were more likely to breed (n ¼ 46, v2 ¼ 4.60, p ¼
.03; Figure 1). How quickly a male paired was also jointly
determined by experimental treatment and arrival date (Table
2), such that red-striped males experienced a relative mating
advantage late in the season (Figure 2).
Do females with experience of the novel trait
prefer such males in the subsequent year?
We investigated whether the re-introduction of the novel trait
in year 2 resulted in assortative mating between males
possessing the trait and females with previous experience with
the trait. We included female age (yearling or older) in the
model because age may influence mate choice (Kodrick-Brown
and Nicoletto, 2001). Females with previous experience with
red-striped males were more likely to pair with red-striped
males than with control males, but naı̈ve females (i.e., with no
previous experience with red-striped males) were not more
likely to pair with red-striped males than with control males
(Figure 3). This pattern remains significant also if ‘experienced’ females that paired with males after they were painted
with the red-stripe in year 1 are excluded from the analysis (L-R
v2 ¼ 4.041, p ¼ .04, n ¼ 43). Males paired with ‘experienced’
Qvarnström et al.
•
Learned origin of mate preference
545
Figure 1
The influence of experimental treatment (painted with either a red
or transparent 4 mm stripe on the base of the white forehead patch)
and arrival date on the likelihood that a male was found breeding
after treatment. Arrival date was divided into two categories for
the illustration purpose early , mean arrival date , late.
females on average had arrived two days earlier than males
paired with naı̈ve females (Table 3, means 6 May, 8 May for
experienced and naı̈ve females, respectively). Most females
classified as experienced were older than 1 year (88%),
whereas no such difference was found among females classified
as naı̈ve (50%, Table 3). There was no case of the same pair
breeding together on both of these two consecutive years.
The reproductive success (number of fledged offspring) of
each breeding pair was influenced by male treatment, by
females’ previous experience of the novel trait, and by male
arrival date (Table 4, Figure 4). Females paired with red-striped
males enjoyed a higher reproductive success compared to
females paired with control males (means 5.35 and 4.68 for
females paired with red-striped and control males, respectively),
but females with previous experience of the novel trait were on
average less successful than naı̈ve females (means 4.41 and 5.39
for experienced and naı̈ve females, respectively).
The higher reproductive success experienced by females
paired with red-striped males cannot be explained by
a corresponding difference in female age (n ¼ 49, v2 ¼ 1.31,
p ¼ .25) or by the laying date between the two male treatment
groups (F1,48 ¼ 0.04, p ¼ .84).
Figure 2
The influence of experimental treatment (painted with either a red
or transparent 4 mm stripe on the base of the white forehead patch)
and arrival date on residual pairing speed (i.e., number of days
passing between the release of a male and the onset of nest
building, corrected for date of release). Arrival date was divided
into two categories for the illustration purpose early , mean
arrival date , late.
stripe on the base of the white forehead patch) were more
likely to pair with males with the novel ornament than with
control males. Our experiment demonstrates that females can
learn to recognize small, conspicuous changes in color
pattern of males and that this may result in assortative mating
between local individuals in a wild population. The most
commonly suggested adaptive function of experience-related
mate choice is the facilitation of selecting genetically
compatible mates; by preferring mates that are rather similar
to their parents, females can avoid costs resulting from either
inbreeding or outbreeding (Bateson, 1978, 1980, 1982).
Moreover, females may be able to track local changes in the
relationship between male ornaments and direct benefits
DISCUSSION
Female collared flycatchers with previous experience of
breeding with males with an artificial novel ornament (red
Table 2
The effects of male experimental treatment (painted with either
a red or a transparent 4 mm stripe on the forehead patch) and arrival
date on days passing until pairing (i.e., onset of nest building) in
the collared flycatcher (Ficedula albicollis)
Variable
df
SS
F
p
Treatment (A)
Arrival date (B)
A*B
1
1
1
21.815
326.822
61.13
1.44
21.65
4.05
.24
,.0001
.05
Model: F ¼ 14.14, p , .0001, n ¼ 49.
Figure 3
The influence of male treatment (painted with new ornament or
control) on the likelihood to pair with ‘experienced’ females (i.e.,
females with previous experience of males with the new ornament) in
the collared flycatcher (Ficedula albicollis).
Behavioral Ecology Vol. 15 No. 4
546
Table 3
Results from a multiple logistic regression showing the influences of
a male’s experimental treatment (painted with either a red or
a transparent 4 mm stripe on the forehead patch) and arrival date
on his likelihood to be found breeding with an experienced female
(i.e., a female paired with a red-striped male in the previous year) in
the collared flycatcher (Ficedula albicollis)
Variable
df
L-R v2
p
Male treatment
Male arrival date
Female age
1
1
1
6.098
4.887
6.179
.01
.03
.01
Female age (yearling or older) is included in the model because age
may influence mate choice (Kodrick-Brown and Nicoletto, 2001).
Model: v2 ¼ 16.47, p ¼ 0.009, n ¼ 49. Interaction terms with p . .10
were deleted from the final model.
from mate choice by adjusting their preferences to past
experiences (e.g., Badyaev and Hill, 2002).
One may argue that we pre-selected for females with a bias
for preferring red-striped males by adding the novel trait
before pairing in year 1 in two of the three experimental plots
(see Methods). This is because females who dislike the trait
had the option to leave the experimental plot. However,
excluding females who had this option from the analyses did
not change our results, suggesting that such biases are
unlikely to provide an alternative explanation.
We found that among males that arrived late at the breeding
grounds, red-striped ones were more likely to be found
breeding after the treatment than were control birds. It may
appear contradictory that red-striped males enjoy a sexually
selected advantage late in the season when most females with
previous experience of such males have mated already. There
are at least two possible explanations for this result. First, male
collared flycatchers may have perceived the red stripe as an
aggressive signal, resulting in red-striped males experiencing
an increased ability to deter rivals and to re-establish and
maintain territories late in the season. Second, naı̈ve females
may have initially avoided males with the artificial novel trait
but preferred to breed with such males late in the season.
Because fewer territories are available late in the season, malemale competition should become fiercer as the breeding
season progresses. The social costs of cheating (signal too high
a status) are therefore likely to increase as the season
progresses, and we would instead expect cheaters to be less
successful late in the season (i.e., we would expect the opposite
pattern). Therefore we consider the second explanation more
likely, that is, a change in mate preference among naı̈ve
females. Furthermore, red-striped males paired relatively
faster late in the season, which also suggest that females found
them increasingly attractive. One reason for naı̈ve females to
Table 4
The effects of male treatment (i.e., painted with either a red or
a transparent 4 mm stripe on the forehead patch), female previous
experience of red-striped males, and male arrival date on number of
fledged offspring in the collared flycatcher (Ficedula ablicollis)
Variable
df
L-R v2
p
Male treatment
Female experience
Male arrival date
1
1
1
7.739
10.528
3.801
.005
.001
.05
Model: v2¼ 12.76, p ¼ 0.005, n ¼ 48. Interaction terms with p . .10
were deleted from the final model.
Figure 4
Comparison of reproductive success between breeding pairs including
males from the two treatment groups (painted with a novel ornament
or control). Females with previous experience of males with the novel
ornament are referred to as ‘experienced’ while females lacking
previous experience of the novel trait are referred to as ‘naı̈ve.’
change their mate preference during the course of the
breeding season could be that they are influenced by the
mate choice made by other females. In other words, redstriped males may have become attractive to naı̈ve females
once some of them established pair bonds with experienced
females. Mate choice copying occurs in many species (Brooks,
1998; Gibson and Höglund, 1992), and one suggested adaptive
explanation is that young females obtain benefits from
copying the mate choice made by experienced females (Stör,
1998). However, mate-choice copying alone cannot explain
the sexually selected advantage experienced by red-striped
males late in the season. This is because naı̈ve females should
be equally expected to copy the choice made by females that
paired with control males as by those with red-striped mates. A
potential bias in mate choice copying could arise if red-striped
males are easier to detect or remember compared to control
males. Thus, female collared flycatchers initially seem reluctant to pair with painted males, but this resistance was
strongly reduced by previous experience of breeding with
males possessing the novel trait and possibly also by simply
observing other females breeding with such males.
Females with a preference for a novel trait are probably
faced with several fitness costs. Such females may become
sexually under-stimulated by males lacking the novel trait,
spend more time and effort searching for a mate (if males with
the novel trait are rare), and they may be affected by potential
costs imposed on males with the novel trait. Possible costs
imposed on males with a novel ornament are increased time
and effort spent on attracting mates (because naı̈ve females
avoid mating with them), increased aggression from competitors (Butcher and Rohwer, 1989), and increased predation
pressure (Endler, 1978; but see also Götmark, 1994). We found
that female collared flycatchers with previous experience with
red-striped males had lower reproductive success than naı̈ve
females. Thus, it appears initially costly to possess a novel
preference. By contrast, females that actually paired with males
possessing the novel trait experienced higher reproductive
success when compared to females paired with control males.
Because we manipulated male appearance before pairing, we
cannot disentangle whether this difference in reproductive
success arises as a consequence of differences in female quality
Qvarnström et al.
•
Learned origin of mate preference
or motivation to invest in the current reproductive event.
Female age, one important determinant of reproductive
success in this species (Gustafsson and Pärt, 1990; Gustafsson
and Sutherland, 1988), did not differ significantly between the
two treatment groups. However, we cannot rule out the
possibility that there are other unmeasured differences in
female quality. That ‘experienced’ females suffered reduced
reproductive success in year two could imply that they are
paying a price for over-investing in reproduction when paired
with red-striped males in the previous year (despite the fact
that they were breeding in prime habitat). In any case, the
bearers of the novel trait appear to be favored by selection.
How may learning influence the genetic evolution of mate
preferences? As mentioned in the introduction, variation in
mate choice, caused by learning, is likely not only to depend on
past experiences but also on the sensory abilities of specific
females. Variation among females in their ability to perceive
and remember certain male traits partly has a genetic basis
which natural selection may act upon. More generally,
behavioral changes may influence the genetic evolution of
morphology and physiology by determining which peaks in the
‘adaptive surface’ form the realm of attraction for the
population (Price et al., 2003). Mate preferences may be
exposed to complicated selection pressures (Badyaev and
Qvarnström, 2002; Kokko et al., 2003), and whether females
will evolve stronger preferences for the novel trait or resistance
against it depends on the costs and benefits of choosing such
males.
Sexual imprinting has often been suggested to facilitate
speciation through sexual selection (e.g., Beach and Jaynes,
1954; Immelmann, 1975; Irwin and Price, 1999; ten Cate and
Bateson, 1988), but there are at least two main objections
against this idea. First, if daughters prefer mates exactly similar
to their fathers there will be no directional selection for
further exaggeration of ornaments. Second, assortative mating
results in frequency-dependent sexual selection such that the
most common male phenotype is favored (i.e., there is
selection against novel traits). These objections are lessened
if the imprinted preferences are asymmetrical (Laland, 1994;
ten Cate and Bateson, 1988; Weary et al., 1993). Indeed, aviary
studies on sexual imprinting in Japanese quails (Coturnix
coturnix, ten Cate and Bateson, 1989) and Javanese Mannikins
(Lonchura leucogastroides, Plenge et al., 2000; Witte et al., 2000)
have demonstrated that birds often prefer exaggerated
versions of the imprinted trait. In addition, when new
preferences can be learned later in life (as demonstrated in
this study) and possibly transmitted to others, the proportion
of individuals that prefer mates with the novel trait may rapidly
increase in the population.
One may argue that asymmetrical mate preferences that can
be learned from experiences late in life and socially transmitted to naı̈ve individuals would counteract rather than
preserve local genetic adaptations through pre-zygotic isolation. However, given that experience-related mate choice
facilitates the spread of novel ornaments in allopatric
populations, sexual selection could take completely different
routes and lead to rapid divergence in mate recognition
systems. Thus, learned mate preferences may play a central
role in the evolution of pre-zygotic isolation before genetic
incompatibility has evolved.
We thank Fredrik Broms, Annika Lydänge, and Martin Qvarnström
for excellent help in the field and Trevor Price and Tomas Pärt for
comments that greatly improved the manuscript. Two anonymous
reviewers also came up with useful suggestions. Thanks also to Lars
Gustafsson for help and discussions. Financial support was obtained
by A.Q. from Knut and Alice Wallenbergs Stiftelse, the Royal Swedish
Academy of Sciences, and the Swedish Natural Research Council.
547
REFERENCES
Badyaev AV, Hill GE, 2002. Parental care as a conditional strategy:
distinct reproductive tactics associated with elaboration of plumage
ornamentation in the house finch. Behav Ecol 13:591–597.
Badyaev AV, Qvarnström A, 2002. Putting sexual traits into the context
of an organism: a life history perspective in studies of sexual
selection. Auk 119:301–310.
Bateson PPG, 1978. Sexual imprinting and optimal outbreeding.
Nature 273:659–660.
Bateson PPG, 1980. Optimal outbreeding and the development of
sexual preferences in Japanese quail. Zeitschrift für Tierpsychologie
53:231–244.
Bateson PPG, 1982. Preferences for cousins in Japanese quail. Nature
295:236–237.
Beach FA, Jaynes J, 1954. Effects of early experiences on the behaviour
of animals. Psychological Bulletin 51:239–263.
Brooks R, 1998. The importance of mate copying and cultural
inheritance of mate preferences. Trends Ecol Evol 13:45–46.
Butcher GS, Rohwer S, 1989. The evolution of conspicuous and
distinctive coloration in birds. Curr Ornithol 6:51–108.
Doligez B, Danchine E, Clobert J, 2002. Public information and
habitat selection in a wild bird population. Science 297:1168–1170.
Domjan M, 1992. Adult learning and mate choice: possibilities and
experimental evidence. Am Zool 32:48–61.
Endler JA, 1978. A predator’s view of animal color patterns. Evol Biol
11:319–364.
Freeberg TM, Duncan SD, Kast TL, Engstrom DA, 1999. Cultural
influences on female mate choice: an experimental test in cowbirds,
Molothrus ater. Anim Behav 57:421–426.
Gibson RM, Höglund J, 1992. Copying and sexual selection. Trends
Ecol Evol 7:229–232.
Götmark F, 1994. Does a novel bright color patch increase or decrease
predation? Red wings reduce predation in European blackbirds.
Proc Roy Soc Lond B 256:83–87.
Grant PR, Grant BR, 1997. Genetics and the origin of bird species.
Proc Natl Acad Sci USA 94:7768–7775.
Gustafsson L, 1989. Collared flycatcher. In: Lifetime reproduction in
birds (Newton I, ed). London: Academic Press; 75–88.
Gustafsson L, Pärt T, 1990. Acceleration of senescence in the collared
flycatcher Ficedula albicollis by reproductive costs. Nature 374:
279–281.
Gustafsson L, Sutherland WJ, 1988. The costs of reproduction in the
collared flycatcher. Nature 335:813–815.
Immelmann K, 1975. Ecological significance of imprinting and early
learning. A Rev Ecol Syst 6:15–37.
Irwin DE, Price T, 1999. Sexual imprinting, learning and speciation.
Heredity 82:347–354.
Karlsson L, Petersson K, Wallinder G, 1986. Aging and sexing in the
pied flycatcher (Ficedula hypoleuca). Vår Fågelvärld 45:131–146.
Kirkpatrick M. 1987. Sexual selection by female choice in polygynous
animals. A Rev Ecol Syst 18:43–70.
Kodric-Brown A, Nicoletto PF, 2001. Age and experience affect female
choice in the guppy (Poecilia reticulata). Am Nat 157:316–323.
Kokko H, Brooks R, Jennions MD, Morley J, 2003. The evolution of
mate choice and mating biases. Proc Roy Soc Lond B 270:653–664.
Laland KN, 1994. On the evolutionary consequences of sexual
imprinting. Evolution 48:477–489.
Lande R, 1981. Models of speciation by sexual selection on
polygenetic traits. Proc Natl Acad Sci USA 78:3721–3725.
Lande R, 1982. Rapid origin of sexual isolation and character
divergence in a cline. Evolution 36:213–223.
Lesna I, Sabelis MW, 1999. Diet-dependent female choice for males
with ‘good genes’ in a soil predatory mite. Nature 401:581–584.
Panhuis TM, Butlin R, Zuk M, Tregenza T, 2001. Sexual selection and
speciation. Trend Ecol Evol 16:364–371.
Plenge M, Curio E, Witte K, 2000. Sexual imprinting supports the
evolution of novel male traits by transference of a preference for
the color red. Behaviour 137:741–758.
Pomiankowski A, Iwasa Y, 1998. Runaway ornament diversity caused by
Fisherian sexual selection. Proc Natl Acad Sci USA 96:5106–5111.
Price TD, 1998. Sexual selection and natural selection in bird
speciation. Phil Trans R Soc Lond B 353:251–260.
Price TD, 2002. Domesticated birds as a model for the genetics of
speciation by sexual selection. Genetica 116:311–327.
548
Price TD, Qvarnström A, Irwin DE, 2003. The role of phenotypic
plasticity in driving genetic evolution. Proc Roy Soc Lond B 270:
1433–1440.
Pärt T, Gustafsson L, 1989. Breeding dispersal in the collared
flycatcher (Ficeduala albicollis): possible causes and reproductive
consequences. J Anim Ecol 58:305–320.
Pärt T, Qvarnström A, 1997. Badge size in collared flycatchers predicts
outcome of male competition over territories. Anim Behav 54:
893–899.
Qvarnström A, 1997. Experimentally increased badge size increases
male competition and reduces male parental care in the collared
flycatcher. Proc Roy Soc Lond B 264:1225–1231.
Qvarnström A, Pärt T, Sheldon BC, 2000. Adaptive plasticity in mate
preference linked to differences in reproductive effort. Nature 405:
344–347.
Riebel K, 2000. Early exposure leads to repeatable preferences for
male song in female zebra finches. Proc Roy Soc Lond B 267:
2553–2558.
Sætre G-P, Moum T, Bures S, Král M, Adamjan M, Moreno J, 1997. A
sexually selected character displacement in flycatchers reinforces
premating isolation. Nature 387:589–592.
Schluter D, Price T, 1993. Honesty, perception and population
divergence in sexually selected traits. Proc Roy Soc Lond B 253:
117–122.
Sheldon BC, Merilä J, Qvarnström A, Gustafsson G, Ellegren H, 1997.
Paternal genetic contribution to offspring condition predicted
by size of secondary sexual character. Proc R Soc Lond B 264:297–
302.
Behavioral Ecology Vol. 15 No. 4
Slagsvold T, Hansen BT, Johannessen LE, Lifjeld JT, 2002. Mate choice
and imprinting in birds studied by cross-fostering in the wild. Proc
Roy Soc Lond B 269:1449–1455.
Stör S, 1998. Evolution of mate-choice copying: a dynamic model.
Anim Behav 55:893–903.
Svensson L, 1992. Identification guide to European passerines.
Stockholm: Märstatryck.
ten Cate C, Bateson PPG, 1988. Sexual selection: the evolution of
conspicuous characters in birds by means of imprinting. Evolution
42:1355–1358.
ten Cate C, Bateson PPG, 1989. Sexual imprinting and a preference
for ‘supernormal’ partners in Japanese quail. Anim Behav 38:
356–358.
ten Cate C, Vos DR, 1999. Sexual imprinting and evolutionary
processes in birds: a reassessment. Adv Study Behav 28:1–31.
Thompson DL, Furnes RW, Monaghan P, 1998. The analysis of ordinal
response data in the behavioural sciences. Anim Behav 56:
1041–1043.
Weary DM, Guilford TC, Weisman RC, 1993. A product of
discriminative learning may lead to female preferences for
elaborate males. Evolution 47:333–336.
West-Eberhard MJ, 1983. Sexual selection, social competition, and
speciation. Q Rev Biol 58:155–183.
Witte K, Hirschler U, Curio E, 2000. Sexual imprinting on a novel
adornment influences mate preferences in the Javanese Mannakin
Lonchura leucogastroides. Ethology 106:349–363.
Witte K, Sawka N, 2003. Sexual imprinting on a novel trait in the
dimorphic zebra finch: sexes differ. Anim Behav 65:195–203.