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Females Paired with More Attractive Males Show Reduced Oxidative Damage: Possible Direct Benefits of Mate Choice in Pied Flycatchers

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Direct benefits of female mate choice may concern female fertility and fecundity but also physiological status. In birds with biparental care, males may contribute to improve the condition and health of their pair-mates through help in constructing nests, incubation or incubation feeding and nestling provisioning. They may also reduce harassment of females by non-pair males. A consequence of these male activities could be expressed in terms of oxidative damage, which may depend on metabolic effort and social stress. Here, we have related male contribution to parental and territorial duties to female oxidative status in the pied flycatcher Ficedula hypoleuca, a species where preferred males present darker dorsal plumage and, in Iberian populations, a large white forehead patch. Darker males were paired with females with high incubation attendance and reduced nestling provisioning rates, which may lead to reduced female exertion. These males owned nest boxes at which there were fewer visits by non-pair males. Although females paired with dark mates worked less hard, they were able to raise more fledglings. Female oxidative damage measured as malondialdehyde (MDA) level in plasma declined with increasing incubation attendance and male incubation feeding. Moreover, levels of MDA in females declined with both darkness of male dorsal plumage and male forehead patch size when controlling for female forehead patch size and male age. The effect of male plumage darkness was especially strong. Females paired with middle-aged males (2–3 yr) showed reduced levels of MDA compared with those paired with 1-yr-old and more than 3-yr-old males. Male age could not explain the effects of male attractiveness. Females paired with attractive males were more successful in reproduction while suffering reduced oxidative damage, possibly mediated by help during incubation and nestling rearing from their pair-mates. Although correlative, the evidence suggests direct benefits of females paired with more attractive males.
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RESEARCH PAPER
Females Paired with More Attractive Males Show Reduced
Oxidative Damage: Possible Direct Benefits of Mate Choice in
Pied Flycatchers
Juan Moreno*, Alberto Velando, Sonia Gonz
alez-Braojos*, Rafael Ruiz-de-Casta~
neda* &
Alejandro Cantarero*
* Departamento de Ecolog
ıa Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, Madrid, Spain
Departamento de Ecolox
ıa y Biolox
ıa Animal, Universidade de Vigo, Vigo, Spain
Correspondence
Juan Moreno, Departamento de Ecolog
ıa
Evolutiva, Museo Nacional de Ciencias
Naturales-CSIC, J. Guti
errez Abascal 2,
E-28006 Madrid, Spain.
E-mail: jmoreno@mncn.csic.es
Received: February 20, 2013
Initial acceptance: April 19, 2013
Final acceptance: May 31, 2013
(T. Tregenza)
doi: 10.1111/eth.12112
Abstract
Direct benefits of female mate choice may concern female fertility and
fecundity but also physiological status. In birds with biparental care, males
may contribute to improve the condition and health of their pair-mates
through help in constructing nests, incubation or incubation feeding and
nestling provisioning. They may also reduce harassment of females by
non-pair males. A consequence of these male activities could be expressed
in terms of oxidative damage, which may depend on metabolic effort and
social stress. Here, we have related male contribution to parental and ter-
ritorial duties to female oxidative status in the pied flycatcher Ficedula hyp-
oleuca, a species where preferred males present darker dorsal plumage
and, in Iberian populations, a large white forehead patch. Darker males
were paired with females with high incubation attendance and reduced
nestling provisioning rates, which may lead to reduced female exertion.
These males owned nest boxes at which there were fewer visits by non-
pair males. Although females paired with dark mates worked less hard,
they were able to raise more fledglings. Female oxidative damage mea-
sured as malondialdehyde (MDA) level in plasma declined with increasing
incubation attendance and male incubation feeding. Moreover, levels of
MDA in females declined with both darkness of male dorsal plumage and
male forehead patch size when controlling for female forehead patch size
and male age. The effect of male plumage darkness was especially strong.
Females paired with middle-aged males (23 yr) showed reduced levels of
MDA compared with those paired with 1-yr-old and more than 3-yr-old
males. Male age could not explain the effects of male attractiveness.
Females paired with attractive males were more successful in reproduc-
tion while suffering reduced oxidative damage, possibly mediated by help
during incubation and nestling rearing from their pair-mates. Although
correlative, the evidence suggests direct benefits of females paired with
more attractive males.
Introduction
Sexual selection theory posits that individuals can
obtain fitness benefits through their mate choice
(Darwin 1871). Choosy females may obtain benefits
derived from offspring genetic quality or directly
improved fertility, fecundity or survival. These last are
called ‘direct benefits’ in the literature and offer a the-
oretically plausible avenue for reducing the costs of
mate selection (Andersson 1994; Wolf et al. 1997;
Kokko 1998). Direct benefits are usually measured
during one breeding season in terms of fecundity or
fertility (Buchanan & Catchpole 2000; Voltura et al.
2002; Hadfield et al. 2006; Kleindorfer 2007) and
more rarely consider delayed benefits that affect the
whole life history (but see Wagner & Harper 2003).
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH 1
Ethology
However, females paired with preferred males may
gain in terms of increased survival through improved
nutrition (Bussiere 2002), reduced infection risk
(Mart
ınez-Padilla et al. 2012), reduced predation risk
(Pizzari 2003; Kleindorfer 2007; Cothran et al. 2012)
or higher assistance by mates in avoiding or resisting
harassment by other males (Low 2005). All these fac-
tors could affect female survival chances. In species
with biparental care, male assistance may be crucial
for ensuring female post-breeding survival probability
and thereby future reproductive value. Thus, males
could contribute in terms of defence of territories nec-
essary to raise their young (Calsbeek & Sinervo 2002)
or through increased assistance in parental care (Hoel-
zer 1989; Griffith 2000; Voltura et al. 2002). Preferred
males would be those improving physiological corre-
lates of female survival probability in terms of nutri-
tion, health and reduced stress.
Some male activities could contribute to reduce
their partners’ metabolic exertion, improve their con-
dition and mitigate social stress imposed by prospect-
ing males or rival females (Rosvall 2008; Moreno et al.
2013). Oxidative stress has received increasing atten-
tion in recent times as a potential index of the deleteri-
ous consequences of reproductive effort (Alonso-
Alvarez et al. 2004, 2006; Wiersma et al. 2004; Met-
calfe & Alonso-Alvarez 2010). Oxidative stress may
also constrain reproduction (Bize et al. 2008; Kim
et al. 2010) and reduce survival probability (Bize et al.
2008; Noguera et al. 2011; Saino et al. 2011). Thus,
female mate choice could focus on males that contrib-
ute to alleviate the oxidative damage implied by repro-
duction and thereby improve survival prospects.
Pied flycatcher Ficedula hypoleuca males exhibit a
melanin-based dorsal coloration (head and back),
which varies completely from brown to black (Lund-
berg & Alatalo 1992) and has been assumed to be
associated with sexual selection for conspicuous color-
ation. Thus, the extension of black plumage on the
back has shown associations with timing of breeding,
mate reproductive investment and reproductive suc-
cess (Saetre et al. 1995, 1997a; Grinkov & Kerimov
1998; Galv
an & Moreno 2009; Sirki
a et al. 2010);
mate choice (R
oskaft & J
arvi 1983; Potti & Montalvo
1991; Saetre et al. 1994; Sirki
a & Laaksonen 2009);
malemale interactions (Huhta & Alatalo 1993); prob-
ability of being cuckolded (Canal et al. 2011; but see
Lehtonen et al. 2009; Moreno et al. 2010, 2013); sur-
vival (Belskii & Lvakhov 2004); predation risk (Sla-
gsvold et al. 1995); energy cost of mate attraction
(Ilina 2004); stress levels (Lobato et al. 2010); and
condition (Slagsvold & Lifjeld 1992; Dale et al. 1999).
The black/brown melanin coloration is connected to
various other functions via the pleiotropic POMC
gene (Moreno & Møller 2010). These functions may
help explain the behavioural differences between
males, as well as the genetic benefits the females
might gain for their offspring. Males also exhibit a
contrasting white forehead patch (Lundberg & Alatalo
1992). Sexual selection has been found to act on fore-
head patch size in Spain (Potti & Montalvo 1991; Os-
orno et al. 2006; Canal et al. 2011), but not
elsewhere (Dale et al. 1999; Lehtonen et al. 2009;
Sirki
a & Laaksonen 2009). We assume henceforth
that males with darker dorsal plumage and larger
white forehead patches are preferred by females in
our study population (Galv
an & Moreno 2009). The
two male plumage traits are not correlated in our
population.
Male pied flycatchers have been shown to contrib-
ute directly to mate well-being through participation
in nest construction (Mart
ınez-de la Puente et al.
2009), through incubation feeding (Moreno et al.
2011) and by contributing to nestling provisioning
(Moreno et al. 1995, 2006). Darker males have been
shown to provision nestlings at higher rates (Saetre
et al. 1995, 1997a), while this has not been shown for
the forehead patch in northern populations (Dale
et al. 1999). For Iberian populations, there is no pub-
lished information regarding associations of male
plumage traits with paternal effort. Increased female
absence from the nest during incubation is positively
related to oxidative damage (Moreno et al. 2013),
which suggests that males may contribute to raise
female nest attendance at this stage, leading to reduced
oxidative damage. Dominant males may contribute to
increase female incubation attendance through feed-
ing their mates (Moreno et al. 2011) or by reducing
the incidence of social interactions around the nest
box or during female recesses (Moreno et al. 2013).
In the present study, we test whether male attrac-
tiveness is linked to female behaviour during incuba-
tion and nestling rearing given the results presented
by Moreno et al. (2013). Moreover, we test whether
female oxidative damage is associated with female
parental effort and with male plumage traits. Some
females in Iberian populations also present a white
forehead patch (Potti 1993; Potti & Merino 1996;
Morales et al. 2007; Potti & Canal 2011). In a previous
experimental study, we obtained evidence that female
ornamentation in the form of forehead patch presence
is associated with increased oxidative damage
(Moreno et al. 2013). We have only included in the
present study the unmanipulated females considered
by Moreno et al. (2013) given the effects of female
forehead patch manipulation on female oxidative
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH2
Benefits of Mate Choice in Pied Flycatchers J. Moreno et al.
damage. Thus, we have controlled in analyses of
female oxidative damage for female forehead patch.
We have also controlled for male age as it may inter-
act with attractiveness in affecting female oxidative
damage. Male age has been shown to correlate with
ornamentation (Budden & Dickinson 2009), paternal
effort (Laaksonen et al. 2011), reproductive success
(Mitrus 2006) and social dominance (Collis & Borgia
1992). Supposing that increased exertion in reproduc-
tive activities may imply higher oxidative damage for
females and that females may obtain direct benefits
through mate choice, we have established the follow-
ing predictions:
1. More ornamented males should be associated with
reduced female activity during incubation and/or
nestling provisioning.
2. Females paired with more ornamented males
should attain a higher reproductive success.
3. Female oxidative damage should increase with
measures of female parental exertion.
4. Female oxidative damage should decrease with
degree of male ornamentation.
Methods
Study Areas
The study was conducted in 2011 in two montane
deciduous oak Quercus pyrenaica forests in central
Spain, namely at Valsa
ın (40°54N, 4°01W, 1200 m
altitude) and at Lozoya (40°58N, 3°48W, 1400 m
altitude) where pied flycatchers breeding in nest
boxes have been studied since 1991 and 2001, respec-
tively (see Appendix in Lambrechts et al. 2011 for
description of design, measurements, position and set-
up of nest boxes in our study areas). Breeding activi-
ties are followed routinely every year, and laying and
hatching dates and brood sizes at hatching and fledg-
ing are determined. Basic breeding and reproductive
success data were collected at both study areas as no
differences between areas were found (all p >0.10).
Females in both study areas were included as no dif-
ferences between areas in any measurement were
found (all p >0.10). Behavioural measures of repro-
ductive effort were taken only at Lozoya.
Males and females were captured in their nest
boxes with traps while feeding nestlings of 78 d (nes-
tlings fledge 1617 d after hatching). They were
ringed if necessary and identified if ringed. In females,
the presence of a white forehead patch was deter-
mined. In both sexes, measures of width and height of
the patch, if present, were taken with a digital calliper
to the nearest 0.01 mm. Blackness of male dorsal
plumage was calculated as percentage black feathers
on back and head on a 0100 scale with 10% interval
scores. This scale is strongly correlated with the Drost
scale used by other authors (see Galv
an & Moreno
2009). Male age could be accurately estimated for
male recruits of known age and for males breeding in
their first year of life (Galv
an & Moreno 2009). Males
captured for the first time after the first year were
assumed to be 2 yr old on first capture, and their age
was estimated as a minimum age based on the year of
first capture as an adult (>1 yr). We assume that esti-
mated minimum ages approximate real ages in such
short-lived birds.
In females, a brachial vein was punctured at cap-
ture, and a sample of approximately 100 ll of blood
was collected in heparinised microtubes and stored in
locked Eppendorf tubes in an ice box until returning
to the laboratory in the same day where they were
centrifuged at 1310 9gRCF for 2 min. Plasma was
then separated with capillary tubes, collected in
Eppendorf microtubes and frozen at 80°C until anal-
ysis. At 13 d of age (hatching day =day 1), nestlings
were counted and ringed.
Parental Care
Ten days after clutch completion, we filmed nest
boxes in Lozoya for 90 min (87.55 1.70 min, range
73104 min, n =24) with digital video cameras
placed at least 10 m from the nest and covering the
front of the nest box and its immediate surroundings.
On films, we counted the number of male visits with
food and estimated the duration of female incubation
sessions and recesses (absences) and the percentage of
time spent by the female inside the nest box. Nests
were again filmed 3 d after hatching of the young
(86.80 3.09 min, range 49121, n =24). The num-
ber of visits with food by males and females was
recorded, and the percentage of time spent brooding
by the female was estimated (brooding activity was
defined as periods spent by the female inside the nest
box longer than 3 min). Unfortunately, some filmed
males were not captured so only 12 films recording
captured males for each period could be used. From
films, we could not detect any obvious bias in capture
success with respect to male plumage traits. All films
were recorded at 11:0015:00 h, so no time of day
effects were noted (effect of time of day p >0.50).
We also recorded during incubation the frequency
of appearance of non-pair males near the nest box.
Non-pair males were distinguished from mates feed-
ing females in the nest box by their behaviour: they
hovered in front of the nest box entrance, often
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH 3
J. Moreno et al. Benefits of Mate Choice in Pied Flycatchers
repeatedly, without entering. In some cases, the film
recorded an attack and a chase by another male, sup-
posedly the mate of the incubating female. The fre-
quency of appearance of these males was interpreted
as male harassment intensity.
Marker of Oxidative Damage
Analyses were performed blind with respect to female
identity. Plasma lipid peroxidation, a major indicator of
oxidative damage, was assessed per triplicate by quan-
tifying malondialdehydes (MDA) by high-performance
liquid chromatography (Karatas et al. 2002), but
modifying sample volume and reagents (Noguera
et al. 2011). Previous to HPLC analysis, plasmatic pro-
teins and other amino compounds were precipitated
by adding perchloric acid. The absorbance of the
eluent was monitored at 254 nm and quantified by
the use of MDA standards (correlation of calibration
curves r
2
>0.99, see Moreno et al. 2013 for an exam-
ple). MDA standards were daily prepared from 1,1,3,3-
tetraethoxypropane (TEP; SIGMA) as described by
Karatas et al. (2002). Samples were analysed within
3 d (interday CV =5.23). Data were expressed as
micrograms of MDA per millilitre of plasma in loga-
rithmic scale (within-day repeatability: r=0.97,
p<0.001), henceforth MDA. We obtained MDA for
48 females, of which we captured the male in 29
cases. Given that we have only used a single oxidative
damage marker, we will use MDA or ‘oxidative dam-
age marker’ alternatively and not the general term
‘oxidative damage’.
Statistical Analyses
No effect of study area on any variable was detected,
so samples from both areas have been pooled for anal-
yses. We explored associations of male ornamentation
with female incubation behaviour in the restricted
Lozoya subsample (12 nests with films of captured
males). We considered as incubation variables the
percentage time spent inside the nest box (atten-
dance) and the mean incubation session (session).
Laying date and male blackness have been included as
explanatory variables for incubation variables, male
incubation feeding frequency and extra-pair male
harassment. For the nestling period, brooding atten-
dance (percentage observation time spent inside the
nest box) and hourly male and female provisioning
rate have been tested with brood size and male black-
ness as explanatory variables.
Including both male plumage and behavioural vari-
ables in the same analysis of MDA was precluded due
to the very limited sample of captured filmed males
available for which we had female MDA. However,
MDA could be associated with behavioural data in 17
nests. For this sample, we have conducted simple cor-
relations to detect direct associations of female paren-
tal behaviour with MDA.
To explain female MDA, we have used multiple
regression analyses. For the sample of pairs with cap-
tured males and female MDA (n =29), we have
tested male blackness score and male forehead patch
height (the more variable of forehead patch mea-
sures) separately as explanatory variables while con-
trolling for male estimated age and female forehead
patch height. Models with all effects being significant
are presented. There is no correlation between the
male traits (r
34
=0.07, p =0.70) in the population.
Effect sizes and power estimates are presented
throughout.
Results
Male Plumage Traits and Behavioural Variables
Incubation attendance increased with laying date and
male blackness (Table 1). The model was highly
significant (F
2,9
=9.17, p =0.007) and explained
60% of variation in attendance. Session duration also
increased with laying date and male blackness
(Table 1). The model was highly significant (F
2,9
=
8.40, p =0.009) and explained 57% of variation in
session duration. Male incubation feeding frequency
was not associated with laying date or male plumage
(p >0.10). Male harassment during incubation
decreased with male blackness (Table 1), and this trait
explained 34% of variation in male harassment fre-
quency (F
1,10
=6.58, p =0.0280).
Brooding attendance showed no association with
any tested variable (all p >0.10), while female provi-
sioning rate was positively related to brood size and
negatively to male blackness (Table 1). Females provi-
sioned more at nests with large broods and less when
paired with darker males. The model was significant
(F
2,9
=5.13, p =0.032) and explained 43% of the vari-
ation in provisioning rates. For male provisioning
rate, no variable showed significant effects (all
p>0.10).
Male estimated age showed no association with any
behavioural variable (all p >0.20).
Male Plumage Traits and Breeding Success
Male dorsal blackness showed positive associations
with clutch size (r
35
=0.45, p =0.0061) and number
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH4
Benefits of Mate Choice in Pied Flycatchers J. Moreno et al.
of fledged young (Fig. 1) and marginally with mean
nestling wing length (r
33
=0.34, p =0.0533). No
such associations were found for male forehead patch
height or male age (all p >0.20).
Female MDA and Behavioural Variables
Female MDA decreased with incubation session dura-
tion (Fig. 2a). It also decreased with male incubation
feeding rate (Fig. 2b). There was also a marginally
significant negative association of MDA with the
proportion of observation time spent brooding small
nestlings (r
16
=0.45, p =0.0716). No other behavio-
ural variable was significant (all p >0.10).
20 30 40 50 60 70 80 90 100
Male % black dorsal plumage
0
1
2
3
4
5
6
7
8
Number of fledged young
1
2
3
4
Fig. 1: Association between number of fledged young and male per-
centage black dorsal plumage (r
36
=0.48, p =0.0032).
Table 1: GLM analyses of female incubation attendance and provisioning rate with different explanatory variables including effect size and power for
each variable (statistically significant p values are in bold)
df bSE Fp
Partial
Eta-squared Power (a=0.05)
Incubation stage
Attendance
Laying date 1, 9 0.69 0.19 12.82 0.0059 0.588 0.888
Male percentage dorsal blackness 1, 9 0.50 0.19 6.82 0.0282 0.431 0.644
Session duration
Laying date 1, 9 0.63 0.19 10.30 0.0107 0.534 0.814
Male percentage dorsal blackness 1, 9 0.55 0.19 7.756 0.0212 0.463 0.699
Male harassment
Laying date 1, 9 0.21 0.25 0.70 0.4235 0.072 0.117
Male percentage dorsal blackness 1, 9 0.65 0.25 6.67 0.0296 0.426 0.634
Nestling stage
Female provisioning rate
Brood size 1, 9 0.77 0.26 8.96 0.0151 0.499 0.759
Male percentage dorsal blackness 1, 9 0.61 0.26 5.74 0.0402 0.389 0.570
5 101520253035404550
Mean incubation session duration (min)
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Female log MDA (µg/ml)
(a)
1012345678
Male hourly incubation feeding
0.4
0.6
0.8
1.0
1.2
1.4
1.6
Female log MDA (µg/ml)
(b)
Fig. 2: Association between female MDA (log lg/ml) and (a) mean incu-
bation session duration during second observation period (r
16
=0.73,
p<0.001) and (b) male incubation feeding rate during second observa-
tion period (r
16
=0.51, p =0.037).
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH 5
J. Moreno et al. Benefits of Mate Choice in Pied Flycatchers
Female MDA and Male Plumage Traits
Female MDA decreased with male blackness when
controlling for male age and female patch height
(Table 2, Fig. 3). Female forehead patch height and
male age increased with female MDA (Table 2). The
model was highly significant and explained 47% of
the variation in female MDA (F
3,25
=9.43,
p<0.001). Female MDA decreased with male fore-
head patch height when controlling for male age,
female patch height turning non-significant in this
analysis (Table 2). Male age was positively associated
with female MDA in this analysis also (Table 2). This
model explained less variation in female MDA (adj.
r
2
=0.30, F
2,26
=6.91, p =0.003). Male age showed
a nonlinear association with female MDA, with
females paired with middle-aged males (2 and 3 yr)
having lower MDA than those paired with young
(1 yr) or old males (45 yr; Fig. 4). There was no
association between male age and male plumage traits
(p >0.20).
Discussion
Darker males were associated with higher female
incubation attendance and lower female provisioning
rates to small nestlings. They also seemed to affect
negatively the frequency of visits to incubating
females by non-pair males. However, reduced female
effort was not accompanied by reduced reproductive
success, but on the contrary, females paired with dar-
ker males showed improved reproductive success in
terms of number and size of young fledged. Female
MDA declined with increased incubation attendance
and male incubation feeding rate. Moreover, females
paired with darker males and to males with larger
forehead patches showed lower MDA during the
breeding season when correcting for their own orna-
mentation (forehead patch) and male age. Male age
showed a quadratic association with female MDA,
with females paired with middle-aged males having
the lowest MDA values. This is, to our knowledge, the
first time that such effects of partner attractiveness on
a female oxidative damage marker have been
reported.
Table 2: GLM analyses of associations of male plumage traits with female MDA including effect size and power (models with only significant effects
are presented)
df bSE Fp
Partial
Eta-squared Power (a=0.05)
Male dorsal blackness
Female forehead patch height (mm) 1, 25 0.36 0.14 6.61 0.0164 0.209 0.696
Male estimated age 1, 25 0.36 0.14 6.67 0.0160 0.211 0.699
Male percentage dorsal blackness 1, 25 0.49 0.14 12.35 0.0017 0.331 0.922
Male forehead patch
Male estimated age 1, 26 0.47 0.16 8.91 0.0061 0.255 0.819
Male forehead patch height (mm) 1, 26 0.37 0.16 5.41 0.0281 0.172 0.610
20 30 40 50 60 70 80 90 100
% Black on male dorsal plumage
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
2.0
2.2
2.4
Female log MDA (µg/ml)
Fig. 3: Association between female MDA (log lg/ml) and male percent-
age of dorsal black plumage (r
28
=0.47, p =0.009).
12345
Male estimated age (yr)
0.4
0.6
0.8
1.0
1.2
1.4
1.6
1.8
2.0
2.2
2.4
Female log MDA (µg/ml)
Fig. 4: Nonlinear association between female MDA (log lg/ml) and
male estimated age (y=1.660.64x+1.45x
2
,F
2,26
=13.16, p <0.001,
adj. r
2
=0.46).
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH6
Benefits of Mate Choice in Pied Flycatchers J. Moreno et al.
The study presents several limitations. First, the use
of only one marker of oxidative damage from only
one time point limits the generality of the results with
respect to oxidative stress. Unfortunately, we have
not been able to follow the recommendation by H~
orak
& Cohen (2010) to measure several markers of oxida-
tive damage at different time points to obtain a better
overview of organismal redox state. Second, the study
presents data from only 1 yr, which may limit its con-
clusiveness as Sirki
a et al. (2010) have shown that
male plumage traits may show different associations
with breeding success depending on climatic condi-
tions during the year of study. However, climatic con-
ditions during the year of study were average in the
study area, which suggests that results may not be
due to exceptional weather.
More attractive males are paired with females with
reduced MDA, the effect being stronger for dorsal
plumage darkness than for forehead patch size. In the
same population, male darkness has a stronger effect
than forehead patch size on mating success (Galv
an &
Moreno 2009). It suggests that females prefer darker
males and that successfully paired females obtain a
benefit in reduced oxidative damage. There is an
alternative explanation for the found association,
namely that females with reduced MDA are of higher
quality and are able to pair up with the most attractive
males, assuming that oxidative damage during the
nestling phase is positively correlated with oxidative
damage on arrival to the breeding grounds. However,
there is no reason to assume that oxidative damage
during the nestling phase would be positively corre-
lated with oxidative damage on arrival to the breeding
grounds as oxidative damage markers can change
rather fast (Sepp et al. 2012). It is also possible that
high-quality females are capable of supporting high
levels of oxidative damage. Moreover, our results con-
tradict this expectation as there is no association of
female MDA with laying date (p >0.40).
The negative associations of male plumage traits
with female MDA are not due to male age as male age
showed a positive quadratic association with female
MDA. Thus, females paired with both young (1 yr)
and old (45 yr) males show higher MDA values. The
first result agrees with Laaksonen et al. (2011), who
found that females paired with young males had
clearly higher provisioning rates than those paired
with older males. Here, we show that females paired
with presumably senescent males may also pay a cost
in terms of increased levels of an oxidative damage
marker. There was also a positive association of female
forehead patch size with MDA in the model including
male blackness. This confirms our experimental result
that females with forehead patches show higher MDA
(Moreno et al. 2013). The underlying cause remains
to be explored but may be related to the costs of bad-
ges of dominance in females.
The hypothesis that attractive males reduce the oxi-
dative damage of their partners requires the existence
of mechanistic links between male quality and female
metabolic exertion or social stress. We here suggest
two mechanisms to explain this strong association,
namely reduced parental effort by females due to
male help and reduced harassment by other males
during incubation. In the first case, darker males
apparently allowed females to reduce their time out-
side the nest during incubation and to reduce their
provisioning rates to small nestlings. These benefits in
terms of reduced maternal exertion were linked to
improved, not impaired, reproductive success.
Females spending more time on the nest during
incubation experience reduced levels of an oxidative
damage marker as shown previously by Moreno et al.
(2013). Here, we show a strong negative association
of female MDA with mean incubation session dura-
tion. Incubation has been shown in this species to be
energetically costly (Moreno & Sanz 1994). Moreover,
female MDA was reduced when males provisioned
them more frequently during incubation. Although
darker males did not provision females more often
during incubation, our measure of frequencies did not
consider the quality or prey size carried to the nest by
males. Males take a relatively more important role
than females in provisioning nestlings during the first
days after hatching (Moreno et al. 2006), so their con-
tribution may help to reduce female provisioning
effort at this stage. Provisioning rates have been
shown to be positively associated with daily energy
expenditure in female pied flycatchers (Moreno et al.
2001). The proportion of time spent brooding small
nestlings by females showed a weak negative ten-
dency with MDA, suggesting as in case of incubation
that female inactivity on the nest has positive effects
on their oxidative status. Here again, we did not
detect any association of male plumage traits with
their own provisioning effort, but unfortunately,
information on prey size or prey quality is absent.
However, dark males have been suggested to be more
efficient in bringing food to the brood (Saetre et al.
1997a), which may explain female reduced effort in
our study. Degree of male plumage melanisation has
been related to reproductive success in northern pied
flycatcher populations (Sirki
a et al. 2010). Some of
these associations may in fact be related to effects of
male reproductive effort on female oxidative status.
The associations between male plumage traits and
Ethology 119 (2013) 1–11 ©2013 Blackwell Verlag GmbH 7
J. Moreno et al. Benefits of Mate Choice in Pied Flycatchers
female parental effort found here with a reduced sam-
ple should be confirmed with a larger data set but
offer a possible explanation for the correlations with
female MDA. Another tentative explanation may be
related to the reduced frequency of visits by extra-pair
males to nest boxes defended by darker males. Harass-
ment by males prospecting for extra-pair mates (Moreno
et al. 2010, 2013) may contribute to female metabolic
exertion during incubation recesses and correspond-
ingly to female oxidative damage. Although it is possi-
ble that the correlative relationships between female
MDA and male plumage are due to territory/home
range quality (more ornamented males defending bet-
ter territories), which allows females to exert them-
selves less or males to help them more, this does not
detract from the fact that females may gain direct ben-
efits when pairing with ornamented males.
To conclude, we show here that females may obtain
direct benefits by pairing with darker, presumably
more dominant males, in terms of reduced levels of
an oxidative damage marker. This may improve the
chances for females to moult and migrate successfully
after breeding in these long-distance migrants. We
also offer some tentative explanations for these bene-
fits in terms of reduced female exertion during incu-
bation and nestling provisioning and possibly of
reduced harassment by extra-pair males. This suggests
that male help may alleviate increased oxidative stress
induced by reproduction (Alonso-Alvarez et al. 2004;
Wiersma et al. 2004). Carry-over effects with respect
to oxidative damage have been suggested (Harrison
et al. 2011) and cannot be excluded in our case,
although larger samples would be necessary to
explore them. However, there is evidence that oxida-
tive damage is associated with survival between
breeding seasons in nestlings (Noguera et al. 2011)
and that antioxidant capacity is related to survival in
adult long-distance migrants (Saino et al. 2011). The
relative importance of direct benefits with respect to
female residual reproductive value compared with
indirect genetic benefits in terms of improved off-
spring quality (Møller & Jennions 2001) remains to be
elucidated. As the present study is correlational and
performed in only 1 yr, experimental and multiyear
studies are needed to confirm these results. Direct
benefits of mate choice in terms of improved female
oxidative status should be explored in other species.
Acknowledgements
The study has received financial support from project
CGL2010-19233-C03-02 to JM and CGL2009-10883-
C02-01 to AV (DGI-Ministerio de Ciencia e Innovac-
i
on). We are grateful to A. Tato for helping with labo-
ratory analyses. At the time of the field study, RRdC
was supported by a grant from CSIC, and SGB and AC
were supported by contract grants from Ministerio de
Ciencia e Innovaci
on and Ministerio de Educaci
on,
Cultura y Deporte. We were authorised by Javier
Don
es, Director of the ‘Montes de Valsa
ın’ nature
reserve, to work in Valsa
ın and by Consejer
ıa de
Medio Ambiente-Comunidad de Madrid to work in
Lozoya. This manuscript is a contribution from the ‘El
Ventorrillo’ field station. The regional wildlife author-
ities of Castilla-Le
on and Madrid authorised the cap-
ture, ringing and blood sampling of birds. The field
methods comply with current Spanish laws. We
declare that we have no conflict of interests.
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J. Moreno et al. Benefits of Mate Choice in Pied Flycatchers
... Plumage characteristics, such as brightness and badge size, have also been associated with reproductive success and females may use ornaments displayed by males to select higher quality mates that provide better parental care (the good parent hypothesis; Hoelzer 1989). In support, plumage ornamentation of male birds has been positively correlated with male feeding rate (e.g., Siefferman and Hill 2003;Silva et al. 2008) and the number of young fledged (e.g., Silva et al. 2008;Moreno et al. 2013). Females can also display variation in plumage ornamentation. ...
... As male Tree Swallows do not brood the nestlings, this better care would have to be provided as improved provisioning or acquisition of higher quality territory. Plumage ornamentation of male birds has been positively associated with feeding rate (e.g., Pagani-Núñez and Senar 2014), the number of young fledged (Silva et al. 2008;Moreno et al. 2013), brood mass (Saetre et al. 1995), and mass of young at fledging (Siefferman and Hill 2003). Specifically, in our population, older male Tree Swallows were found to be bluer and brighter than younger males . ...
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... Kingma et al. 2012) and obtain direct benefits, which increase their fitness (e.g. Moreno et al. 2013). A possible condition-signalling function of grey plumage coloration in sexual selection is suggested by earlier studies, where relationships between individual health and rearing conditions with grey coloration were found (Parejo & Silva 2009, Parejo et al. 2011). ...
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Melanin is the most common pigment in avian plumage and has various functions including: signalling individual condition, social status, aiding in camouflage and/or strengthening feathers. To date, most research focusing on melanin‐based colours has focused on eumelanin black and pheomelanin rusty traits. The occurrence and function of grey melanin‐based coloration, however, remains largely unstudied. Using colour plates from a bird identification guide and a phylogenetic comparative approach, we analysed the occurrence and relative patch size of grey plumage regions in 239 passerine species belonging to 36 families occurring in Western Palearctic. We proposed four hypotheses to explain the evolution of grey plumage: 1) protection from visually oriented predators, 2) badges of social information, 3) sexually selected ornaments, 4) visual enhancement of badges and ornamental colour patches via high between‐colour contrast. We tested these hypotheses by analysing the occurrence and relative size of grey patches in relation to ecological and life history traits and the occurrence of other colours. Moreover, we surveyed the distribution of grey over avian body regions and its adjacency to other plumage colours. Grey coloration was present in 97 species from 25 families (40.5% of all species, and 69.4% of all families sampled, respectively). Our results support the idea that grey plumage evolved to provide cryptic coloration and/or as a sexual signal used in female mate choice. Grey colour occurrence was associated with less concealed nest structure and open habitats, and this effect was especially pronounced in species in which males incubate. In both sexes, grey was more abundant on the head and back regions, which are the most visible body parts during incubation. The occurrence of grey was related to a greater dichromatism and was slightly higher in males compared to females, which suggests that it could have evolved in response to female mate choice. No evidence suggests that grey plumage enhances ornamental colours or act as a competitive signal. The study provided the first insight in potential functions of grey plumage in birds. Further studies at species level are needed to test our findings.
... This increase in EPP frequency is compatible with a scenario in which the levels of EPP are influenced by male pursuit instead of female choice, and is backed up by previously published descriptive data from the same population [26]. This effect was robust after controlling for the possible influence of additional factors in EPP [47,48]. However, alternative explanations cannot be ruled out if we assume that the manipulation could lead to reduced female attractiveness. ...
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There is no consensus yet on the reasons why females engage in extra-pair copulations (EPC). In some species, females have been shown to accrue some indirect benefits, but these effects are not consistent across species and studies. The sexual conflict hypothesis posits that extra-pair paternity (EPP) is the result of strong selection for male pursuit of EPC without real benefits for females. In order to test this hypothesis, we experimentally reduced wing area (reversibly tying together some primary feathers), in a group of pied flycatcher females (Ficedula hypoleuca). The manipulation increases wing loading (body mass/wing area), which is negatively associated with flying ability, and thus with the capacity to escape from unwanted copulations. We compared the levels of EPP in this experimental group with those of a group of un-manipulated females. Experimental females almost doubled the proportion of extra-pair young (EPY) with respect to control females. In addition, more males sired EPY in experimental than in control broods containing EPY. These results suggest that in our study population, EPP could be partially a product of female capacity to avoid EPCs. We also discuss the alternative hypothesis that results might be due to an eventual reduction of female attractiveness.
Chapter
The process of sexual selection results from mating advantages gained when members of one sex, usually males, compete for access to the other sex, and when competitors in better condition or bearing more extravagant ornaments are selected by individuals of the opposite sex, usually females. These ideas, published in detail by Darwin in 1871, led to the foundation of modern theory describing animal breeding systems, and are still instigating numerous researchers in ongoing studies that seek to understand reproductive phenomena in animals. Sexual selection promotes adaptations in behavior, morphology, and physiology, and also is an agent of speciation. In the first part of this chapter, we present an overview of sexual selection theory and some of the major advances in the last few decades. We then present work that we have developed within the scope of sexual selection theory, using as a model a small Neotropical passerine, the blue-black grassquit (Volatinia jacarina). We describe general parameters of this species and why it is an ideal model to study sexual selection. We follow this with a summary of field and laboratory methods we have used, and then address conceptual topics subdivided into four major categories: (1) parasite-mediated sexual selection; (2) social and sexual mating systems; (3) female choice; and (4) the evolution of sexual ornamentation.
Article
Adaptive phenotypic plasticity may respond to present ambient conditions. Sexual and social signals in both sexes may express phenotype performance. Plumage signals that change discontinuously allow relating discrete variation to previous performance. Both sexes of the Pied flycatcher Ficedula hypoleuca present white patches on the wings and on the forehead, which constitute sexual and social signals. Forehead patches are moulted together with body plumage in Africa, while wing patches are partly moulted in Africa and partly in the breeding area soon after breeding. We studied individual inter‐year changes (corrected for regression to the mean) in the size of forehead and wing patches of both sexes in 7 years for females or 6 years for males in two nearby study areas in central Spain. We found that initial signal extent strongly delimits the possible subsequent changes negatively. There is a negative association of male age with forehead patch changes. Cold and rainy springs are associated in females with decreases in both patch areas and vice versa, while no association with climate is observed in male wing patch changes. Cold pre‐breeding conditions predict positive changes in female wing and male forehead patches. Breeding success is positively associated with forehead patch changes in females. Late‐breeding males experience more positive changes in forehead patch size than early‐breeding males. Some of these trends can be explained by variable costs of breeding in certain conditions for subsequent signal production and/or maintenance, while absence of trends in some cases may be explained by sex differences in costs of breeding and interactions with phenotypic quality of breeders. This article is protected by copyright. All rights reserved.
Article
Sexual selection, as a form of social selection based on reproductive resources, is a crucial driver of evolutionary change. Many studies on sexual selection identify potential targets only within the reproductive fraction of populations. Floaters constitute the non-territorial fraction of the population, according to the usual definitions. Floaters have been identified through exhaustive capture and marking programmes, removal and nest-box addition experiments, extra-pair paternity studies, acoustic marking and genetic studies. The literature shows that floaters may represent a considerable fraction of populations, especially among males. There is no clear evidence that size, condition or testosterone level is necessary for explaining floater status generally. However, the literature suggests that ornament size and expression are involved in territorial exclusion and may be either its cause or one of its consequences. There is some evidence that floaters survive and reproduce less well than territorials, and that changes from floater to territorial status are accompanied by changes in survival and reproductive rates. However, certain male floaters may obtain some reproductive success through extra-pair copulations. The possibility that floating constitutes a successful alternative strategy in some species cannot be excluded, although the current preliminary consensus is that floaters are 'making the best of a bad job'. Floater status may be imposed by limitations in the availability of mates or breeding space resulting in skewed population sex ratios, polygamous mating systems, high population densities and increased demand for specific breeding requirements such as space in colonies or adequate nesting cavities. Predictions concerning the effects of these factors have not been conducted to date. Few studies have been able to clarify the duration of floater status in any population. For short-lived species, floater status in a single breeding season may in fact imply zero lifetime reproductive success. In males, the existence of a considerable fraction of floaters attempting to breed may select for intense territorial behaviour and competitive mate guarding tactics in territory holders and in aggressive extrapair copulation and territory acquisition tactics in floaters. Interference competition from floaters may lead to density-dependent declines in reproductive success. In females, the attempts by floaters to attain breeding opportunities may have contributed to the observed propensities for female prospecting and for female-female aggression and the signalling of female dominance towards other females. Moreover, there may exist selection in females for signalling quality to mates in order to avoid being evicted by rivals. Excluding floaters from the analysis of sexually selected traits may severely affect sexual selection estimates because of biased sampling for large or more intensely expressed ornamentation. The importance of sexual selection may be negated or underestimated when in fact its action on floaters could be maintaining current levels of expression in the territorial fraction. Existing phenotypes should express, in their morphology, physiology and behaviour, the relentless drive through evolutionary time to avoid becoming a floater.
Chapter
Scientists have long been fascinated by the evolution of body colourations and, in particular, of sexually selected ornaments. Males may develop carotenoid- and melanin-based ornaments or achromatic morphological sexual signals. Females may also produce pigmented or non-pigmented patches that are important in social competition with females and in the context of sexual selection. The development of these signals may impose costs to both males and females, but the underlying physiological mechanisms are not well understood yet. The development of colour signals can also be costly in contexts beyond that of mate choice, such as in the case of quality signalling in young or in warning signalling (e.g., Batesian and Müllerian mimicry). Recent research has focussed on how the building up of body colourations induces oxidative stress and how oxidative stress itself may constrain investment in signalling. This chapter examines the many hypotheses that link carotenoid- and melanin-based colourations to the capacity of the bearer to withstand oxidative stress. It also examines the role of oxidative stress in the development of colour signals in young and of conspicuous body colourations that are used by some species to signal their unprofitability to predators.
Article
If offspring develop in adverse conditions, the maternal component of their phenotypic variation might increase due to the stronger dependence of offspring traits on parental investment. This should result in increased parental investment to individual offspring, as assumed by the model of optimal egg size. The opposite pattern, i.e., stronger dependence of offspring fitness on parental investment and consequently larger parental investment under good conditions is assumed by both the theory of differential allocation if attractive males provide material benefits, and reproductive compensation if they invest less into paternal care. Another influential idea is the Trivers-Willard model, which assumes sexspecific dependence of offspring fitness on parental investment. Here we tested these ideas by examining the effects of egg size on offspring fitness across many postnatal contexts in the Collared Flycatcher Ficedula albicollis. We employed a cross-fostering design that generated variation in egg size within nests and used brood means of fledgling mass as a functional measure of the quality of rearing conditions. Effects of egg size on three offspring traits, including lifetime reproductive success of recruits, were more pronounced in low-quality broods. These results support the assumption of the model of optimal egg size. Based on female preference for males providing material benefits, this pattern could support differential allocation, if attractive males invest less in paternal care, or reproductive compensation, if they invest more. By comparison, we did not find any evidence for sex specificity of fitness returns that might explain sex monomorphism of egg size in this species. The challenge for future studies will be the integration of components of parental investment and offspring fitness into their global measures and testing how the former affects the latter across gradients of postnatal conditions.
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Clutch destruction and replacement are sometimes observed during studies of cavitynesting birds. This could be due to abandonment by the first female to lay, with subsequent replacement by another female, or to male infanticide. Clutch replacement is accompanied in some cases by evidence of aggressive competition between females and of destruction of eggs/hatchlings immediately prior to a new clutch being laid. This may indicate that clutch replacements are in fact nest take-overs by females after eviction of incumbent females. In the course of long-term studies of pied flycatchers Ficedula hypoleuca iberiae in central Spain, I have found evidence of clutch destruction through egg burial and ejection and replacement during laying or incubation, as well as of female-female aggression. No male involvement has been detected. Clutch replacements occur with a frequency that depends on the density of available nest-boxes and is positively associated with the rate of nest-box occupation by the same or other species. Moreover, clutch replacements can be accompanied by female wounds or death and involve clutch destruction in all cases. Putative replacers within the area of highest occupation frequently display the white forehead patch that is more typical of males, which may thus be associated with social dominance in females in Iberian populations. Clutch replacements in cavity-nesters should be studied in detail to confirm whether they represent cases of nest take-overs by competing females.
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The study was conducted on Ladoga Lake Coast in Nijnesvirskiy Reserve (61 degrees N 33 degrees E) during 1994-1995 years on polymorphic population of the pied flycatcher Ficedula hypoleuca Pall. Influence of the male plumage colour on male fitness components (reproduction time, clutch size and it's efficiency, sizes, weight, fat content and condition of the parents in different stages of a breeding cycle, and nestlings before fledging) was estimated.; Indexes of 93 males, 78 females and 369 nestlings from 71 nests have been analyzed. A mean value of male plumage coloration, assessed by Drost's scale (Drost, 1936) made 3.42 in 1994 and 3.98 in 1995. In both young and old males the type of coloration was connected with the breeding status. Males, taking part in reproduction, on average had brighter coloration, than those which mate. Bright males were characterized by earlier reproduction time and it's smaller variation. The fecundity parameters were not connected with the coloration type. Zn the whole sample bright males (1-2 type of Drost's score) exceeded intermediate (3-4) and pale (5-7) colored ones in weight and condition of their females and nestlings. Nevertheless bright and pale colored males had similar high fitness parameters of their females and descendants whereas males of intermediate colour remained on a low level in these fitness characters. The fitness components of light birds in a considerably greater degree are controlled be environmental factors. It is supposed, that preservation of light males in populations results from disruptive selection in combination with migrations between different populations in spite of weak sexual selection favoring bright males.
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In animals with internal fertilization, sperm competition among males can favor the evolution of male ejaculate traits that are detrimental to females. Female mating preferences, in contrast, often favor traits in males that are beneficial to females, yet little is known about the effect of these preferences on the evolution of male ejaculates. A necessary condition for female preferences to affect the evolution of male ejaculate characteristics is that females select mates based on a trait correlated with ejaculate quality. Previous work has shown that females of the variable field cricket, Gryllus lineaticeps, prefer males that produce calling songs containing faster and longer chirps. In this study, we tested the hypothesis that females receive more beneficial ejaculates from preferred males. Females were placed on either a high- or a reduced-nutrition diet then mated twice to a male of known song phenotype. Females received only sperm and seminal fluid from males during these matings. There was no effect of male song phenotype on any fitness component for females on the high-nutrition diet. Reduced-nutrition females mated to males that produced preferred song types, however, lived longer, produced more eggs, produced more fertile eggs, and had a higher proportion of their eggs fertilized than those mated to other males. The life-span benefit was positively associated with male chirp duration, and the reproductive benefits were positively associated with male chirp rate. We explored two possible mechanisms for the life span and reproductive benefits. First, a path analysis suggested that part of the effect of male chirp duration on female life span may have been indirect; females mated to males that produced longer chirps showed delayed oviposition, and females that delayed oviposition lived longer. Males that produce longer chirps may thus transfer fewer or less potent oviposition stimulants to females in their seminal fluid. Second, there was a positive correlation between male chirp rate and the number of sperm transferred to females. The fertility benefit may thus have resulted from females receiving more sperm from males that produce faster chirps. Finally, there was a negative phenotypic correlation between male chirp rate and chirp duration, suggesting that females may have to trade off the life span and reproduction benefits when selecting a mate.
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Male arrival and female mate choice are documented for a montane Spanish population of Pied Flycatchers. Early arriving males were older and defended a higher number of nestboxes than males arriving later. A first analysis of female mate choice in the entire population detected significant differences between mated and unmated males only in their respective arrival dates. This type of analysis may be unrealistic, owing to the operation of female searching costs. A second test based on the between-year dispersal tendencies of adult females and their presumed mating 'decisions' revealed a central role of site-tenacity in female choice, with variation in a secondary sexual character, the male's white patch in the forehead, also being important for pairing success.
Article
Females may benefit from expending more resources in care of offspring sired by sexually attractive males than by those of unattractive males in species with biparental care. Attractive males may therefore reduce their share of parental expenditure to increase own survivorship and to further mating success. On the other hand, if direct benefits through male care are important for female mate choice, sexually attractive males may be expected to have a higher parental expenditure than unattractive males. We measured daily energy expenditure of attractive and unattractive (i.e. brightly and dull coloured) male Pied Flycatchers Ficedula hypoleuca during a period of intensive parental care applying the doubly-labelled water technique. We did not find any consistent differences in energy expenditure between bright and dull males, lending little direct support to either hypotheses. Combined with previous studies of the same species, we suggest that bright males are more efficient in bringing food to the brood per unit of energy spent. Polygamously mated males divide their feeding effort among the primary and secondary brood(s), although most care is given to the primary brood. We found that bigamous males had higher daily energy expenditures than monogamous males. This result suggests that polygamy is associated with energetic costs to males, possibly related to the need of travel between nests but perhaps also to an overall higher parental investment. We argue that costs to males should be incorporated in discussions on the evolution of polygamy.
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Color morphs of breeding Ficedula hypoleuca males were studied in the Middle Urals (56°49′ N, 59°34′ E) in 1997-2002. No males of the 1st and 2nd morphs (according to the Drost's scale, 1936) were registered in the study area. Males of the 3rd, 4 th, 5th, and 6th morphs accounted for 12.0, 15.7, 30.6, and 11.1% of the total number of the birds studied (n = 376), respectively. The mean plumage color (+SE) is 5.13 ± 0.06. The differences between years were insignificant. The length of wings in males averaged 81.82 + 0.09 mm (n = 371), the coefficient correlation between the length and color type was - 0.26. The body mass averaged 12.61 ± 0.03 g (n = 352) and was not related to coloration. Male return rates averaged 26.3%. The maximal rate was in the 5th morph (33.0%), the minimal one, in 7th morph (14.6%). The phenotypic structure of the population was similar in optimal habitats (coniferous and small-leaved forests). In biotopes damaged by industrial emissions, the share of the 3rd morph decreased, that of the 7th one, increased.
Article
The average level of singing activity in males of different Ficedula hypoleuca phenotypes (n = 101) was similar. At the same time, their behavioral pattern was different. The metronome timing of 56 bachelor males (178 hours) was carried out. The average level of energy expenditures for each male in the daytime (without cost of thermoregulation) was calculated from the time budget using converting coefficients (Dolnik, 1980). The rate of energy expenditure was found to be higher in cryptically colored males (V-VII grades by Drost's scale) than in conspicuous ones (II-III grades) (2.5 x BMR and 2.1 x BMR, correspondingly) mainly due to the heavier time expenses for flight activities (12% against 7.8% in conspicuous males). The pattern of behavior in males with the color type IV was intermediate. The more expensive style of advertising behavior in cryptically colored birds compensate their less attractive appearance than that in dark-colored males.
Article
Models of sexual selection suggest that populations may easily diverge in male secondary sexual characters. Studies of a Spanish population of the pied flycatcher, Ficedula hypoleuca, and a Swedish population of the closely related collared flycatcher, F. albicollis, have indicated that the white forehead patch of males is a sexually selected trait. We studied the white forehead patch of male pied flycatchers (n = 487) in a Norwegian population over seven years. Males with large forehead patches were in general more brightly colored, but patch height was not correlated to body mass, body size, or parasite loads. Conditions during the nestling period did not seem to influence patch height as an adult. Patch height increased slightly from the first to the second year as adults, but then remained relatively constant at higher ages. Patch height was not related to survival. Year-to-year changes showed that males who increased in patch height also increased in body mass, suggesting that expression of the forehead patch may be partly condition dependent. However, changes in body mass explained only a small proportion of the variance in patch height between males. Thus, patch height would not be a good indicator of male quality. Furthermore, patch size was also not related to male ability to feed nestlings, indicating that females would not obtain direct benefits by choosing males with large patches. However, patch height could be a Fisher trait, but this requires heritability and there was no significant father-son resemblance in patch height. Comparisons of the males visited by each female during the mate sampling period indicated that chosen males did not have larger forehead patches than rejected males. Experimental manipulation of patch height did not affect male mating success. These results indicate that females do not use patch size as a mate choice cue. Finally, patch height did not predict the outcome of male contests for nestboxes, suggesting that the forehead patch is not an intrasexually selected cue of status. Norwegian pied flycatchers have smaller forehead patches than both Spanish pied flycatchers and Swedish collared flycatchers. We suggest that this pattern may be explained by the lack of sexual selection on the forehead patch in the Norwegian population as compared to the other populations, where the patch is apparently sexually selected. We discuss possible reasons for these population divergences, such as female choice on an alternative secondary sexual character (general plumage color) and speciation among Ficedula flycatchers.