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Maternal testosterone influences a begging component that makes fathers work harder in chick provisioning

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Abstract

In species with biparental care, parents disagree evolutionarily over the amount of care that each of them is willing to provide to offspring. It has recently been hypothesised that females may try to manipulate their mates by modifying offspring begging behaviour through yolk hormone deposition, shifting the division of labour in their own favour. To test this hypothesis we first investigated how yellow-legged gull (Larus michaellis) parents feed offspring in relation to each component of complex begging behaviour and if feeding behaviour vary between sexes. Then we investigated the effect of yolk testosterone on chicks' begging by experimentally increasing yolk testosterone levels. Our results revealed that yolk testosterone has a component-specific effect on chicks' begging, specifically increasing the number of chatter calls. Parental feeding effort was influenced by the number of chatter calls emitted by chicks, but most importantly, the influence was stronger in male than in female parents. Moreover, chick body mass increased with the number of paternal feeds. In conclusion, these results show that female gulls may use yolk testosterone deposition to exploit their partners as predicted by the 'Manipulating Androgen Hypothesis (MAH)'.
Maternal testosterone inuences a begging component that makes
fathers work harder in chick provisioning
José C. Noguera
a,b,
, Sin-Yeon Kim
b
, Alberto Velando
b
a
Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UK
b
Dpto. Ecoloxia e Bioloxía Animal, Edicio de Ciencias Experimentales, Universidade de Vigo, 36310 Vigo, Spain
abstractarticle info
Article history:
Received 22 February 2013
Revised 21 April 2013
Accepted 24 April 2013
Available online 4 May 2013
Keywords:
Birds
Maternal effects
Manipulation
Sexual conict
Hormones
Begging
Parental care
In species with biparental care, parents disagree evolutionarily over the amount of care that each of them is
willing to provide to offspring. It has recently been hypothesised that females may try to manipulate their
mates by modifying offspring begging behaviour through yolk hormone deposition, shifting the division of
labour in their own favour. To test this hypothesis we rst investigated how yellow-legged gull (Larus
michaellis) parents feed offspring in relation to each component of complex begging behaviour and if feeding
behaviour varies between sexes. Then we investigated the effect of yolk testosterone on chicks' begging by
experimentally increasing yolk testosterone levels. Our results revealed that yolk testosterone has a
component-specic effect on chicks' begging, specically increasing the number of chatter calls. Parental
feeding effort was inuenced by the number of chatter calls emitted by chicks, but most importantly, the in-
uence was stronger in male than in female parents. Moreover, chick body mass increased with the number
of paternal feeds. In conclusion, these results show that female gulls may use yolk testosterone deposition to
exploit their partners as predicted by the Manipulating Androgen Hypothesis (MAH).
© 2013 Elsevier Inc. All rights reserved.
Introduction
A family is a small society in which family members have shared
but not identical interests (Lessells, 1999; Trivers, 1974). These evolu-
tionary conicts of interest are of special importance in the evolution
of parental care (Parker et al., 2002). For instance, a conict between
parents occurs because both benet from care provided by either of
the parents but the cost for each parent depends only on its own ef-
fort (sexual conict; Lessells, 1999). Thus, each parent has increased
tness if the other gives more care. How these conicts of interest
among family members are resolved is a current issue in evolutionary
biology (Royle et al., 2012).
In a number of bird species, allocation of maternal hormones to
egg yolks varies within and between clutches (review in Gil, 2008;
Groothuis et al., 2005; Smiseth et al., 2011). This variation may be a
strategy mediating adaptive transgenerational phenotypic plasticity
(Groothuis et al., 2005; Mousseau and Fox, 1998) in which molecular
(neuroendocrine) signals promote programmed responses in physi-
ology and behaviour that favour the young during development
(Alonso-Alvarez and Velando, 2012; Lessells, 2008). However, it has
recently been hypothesised that such hormonal variation may also
be a female strategy to manipulate the male's contribution to parental
care (Manipulating Androgens Hypothesis; MAH:Groothuis et al.,
2005; Lessells, 2006; Moreno-Rueda, 2007; Müller et al., 2007).
This hypothesis is based on the effects that yolk hormones exert on
offspring signals (i.e. begging behaviour; reviewed in Smiseth et al.,
2011) that are used by the partner to adjust their level of parental
care (Kilner and Johnstone, 1997 and references therein). A key
assumption and prediction of this hypothesis is that maternal hormones
increase offspring begging and that the male parent responds to offspring
begging affected by maternally-derived hormones (Moreno-Rueda,
2007). Although this hypothesis seems theoretically plausible, yet there
is no empirical evidence supporting this hypothesis (but see Barnett et
al., 2011; Laaksonen et al., 2011; Ruuskanen et al., 2009; Tschirren and
Richner, 2008 for similar experiments).
The yellow-legged gull (Larus michaellis)isasuitablemodeltostudy
the effects of maternal hormones on complex begging displays and the
assumptions and predictions of the MAH. In this species, parental care is
provided by both parents over a long period (more than three months),
so there is potentially severe sexual conict over parental care. Nes-
tlings perform complex begging displays involving calls (chatter calls)
and pecking at the parents' bills. Although chatter calls and pecks may
function collectively, the two begging components not only appear to
have evolved through different evolutionary-pathways but alsoencode
different information during parentoffspring communication (Kim et
al., 2011; Noguera et al., 2010). Importantly, maternal hormones may
differentially affect different components involved in complex begging
displays (Smiseth et al., 2011 and references therein). Moreover, analy-
ses of within-clutch variation of yolk testosterone have revealed that in
Hormones and Behavior 64 (2013) 1925
Corresponding author at: Division of Environmental and Evolutionary Biology,
Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow,
Glasgow G12 8QQ, UK.
E-mail address: jose.noguera@glasgow.ac.uk (J.C. Noguera).
0018-506X/$ see front matter © 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.yhbeh.2013.04.008
Contents lists available at SciVerse ScienceDirect
Hormones and Behavior
journal homepage: www.elsevier.com/locate/yhbeh
the yellow-legged gull and other closely related gull species mothers
may allocate a higher level of testosterone to the third egg (Royle et
al., 2001; Rubolini et al., 2011), the chicks from which also appear to
show a higher rate of chatter calls after hatching (Kim et al., 2011).
Another important aspect of this species is that both sexes have a
conspicuous carotenoid-based sexual signal during adulthood, the
red-spot on the lower mandible. This trait depends on carotenoid de-
position and reliably reects the bearer's antioxidant status, body
condition and health (Pérez et al., 2008, 2010, 2012). Furthermore,
the red spot in gulls has been a classic model in the study of signalling
between parents and young because it elicits begging responses in
hatchlings (i.e. Tinbergen and Perdeck, 1950; Velando et al., 2013).
A recent study indicates that this trait is used by both sexes to adjust
their level of parental care during the chick rearing period (Morales et
al., 2009). Thus, all members in a gull family use this signal to adjust
their behavioural strategies during conict.
It has been suggested that carotenoid-based signals, such as the
red spot on the lower mandible of the yellow-legged gull, may mirror
the provisioning ability of the signallers (Endler, 1980; Hill, 1991;
McGraw et al., 2003; Velando et al., 2005). In this case, it would be ad-
vantageous for both parents and offspring to utilize this information
in their own favour. For instance, gull mothers and offspring would
benet if yolk testosterone particularly promotes begging behaviour
toward better caregivers. Although several studies have shown that
females allocated more testosterone to eggs when mated with more
attractive or colourful males (Gil, 2003; Groothuis et al., 2005 and ref-
erence therein), how maternal testosterone and sexual signals may
interact and affect offspring begging behaviour and tness-related
traits is unknown.
In the present study, we rst observed whether parents adjust food
provisioning according to the begging behaviour of their offspring. Then
we performed an experiment to investigate whether maternal testos-
terone and the sexual signals exhibited by parents inuence the inten-
sity of complex begging displays. We experimentally manipulated the
testosterone level in the last laid egg of three-egg clutches and also
the size of the red spot on a dummy head used to elicit begging re-
sponses in the gull chicks. If females can manipulate male contribution
to parental care through testosterone deposition into the eggs, we ex-
pect that, (1) chicks hatched from testosterone-treated eggs will per-
form more intense begging behaviour and (2) in our observational
study, males but not females will increase their feeding effort according
to chick's begging. Additionally, if sexual signals displayed by adult par-
ents encode reliable information about their provisioning capacity, we
expect an interactive effect of yolk testosterone and red spot size on
begging intensity.
Materials and methods
All eld procedures used in this study were performed with
permission by the Xunta de Galicia, permit numbers 2008/190 and
2009/232.
Field procedures
The study was conducted during the breeding season of 2008 and
2009 in a large yellow-legged gull colony at Sálvora Island (Parque
Nacional das illas Atlanticas de Galicia, NW Spain). Yellow-legged
gulls generally lay clutches of three eggs at one to three day intervals
(modal clutch size; 85% of breeding pairs lay a clutch of three eggs in
the study population; our unpublished data), and incubation and pa-
rental care of the chicks are shared by both parents. They are socially
monogamous colonial breeders that defend a small breeding territory
(Alonso-Alvarez and Velando, 2001) where chicks are fed. The semi-
precocial young hatch asynchronously, with the third chick hatching
normally one to three days after the other two chicks (Hillström
et al., 2000).
Observational study of begging behaviour and parental feeding
In MayJune 2008, we conducted an observational study to see how
parents respond to chick begging. We searched for nests with three
eggs close to hatching, which is usually detectable by a small hole in
the shell. We captured one adult per nest with nest traps (TRB60-tent
string trap; www.moundry.cz). Captured birds were marked with a
numbered coloured PVC ring and a black spot on the neck to facilitate
identication from distance. All captured birds (n = 14) were sexed by
means of the following discriminant function (Bosch, 1996): D =
1.430 HL + 5.135 BD + 0.114 W+0.262T366.988, where
HLis head length, BDis bill depth, Wwing length and Tis tarsus
length. By using this function, values under zero correspond to females
and over zero to males. Sexes determined by using this function
are known to be 100% consistent with sex determined by copulatory
behaviour (Alonso-Alvarez and Velando, 2003). On the day of hatching,
all chicks within a clutch were individually marked with a small
coloured spot on the head (black, blue or green) and leg ags made
with Velcro strip. Different colour marks did not inuence feeding by ei-
ther parental sex (generalized linear mixed model; sex: F
1,35
=0.68,
p = 0.42; chick's colour: F
2,36
= 1.82, p = 0.18; sex × chick's colour:
F
2,33
= 0.43, p = 0.65). Two days after the rst chick hatched, we con-
tinuously observed each pair from 09.00 to 13.00 h. Each observer simul-
taneously recorded the behaviour of two to three focal pairs from a hide
that had been put in place the previous day. During the 4 h of observa-
tion, we recorded the number of chatter calls and pecks to the parents'
bill performed by each individual chick and the number of regurgitates
that each chick received from each parent (male and female). During
the rst days after hatching parents often feed the chicks one by one
and therefore, sibling competition for regurgitates among siblings rarely
occurs. All chicks were weighed immediately before and after the obser-
vation period.
Testosterone experiment
From May to June 2009, we performed an experiment where tes-
tosterone levels were increased in the last laid eggs and the begging
behaviour of chicks measured after hatching. We visited each nest
in the study area daily during the egg laying period until clutch com-
pletion to mark eggs and register laying dates. The third eggs from 92
three-egg clutches were randomly assigned to either the testosterone
or control treatment. Only the third eggs were used for the experi-
ment because we expected that female manipulation would have
stronger effects on the third chicks due to their initial disadvantages
in sibling competition (Kim et al., 2011).
Eggs were collected from the nest and weighed (± 0.01 g) on the day
of laying and immediately transported to a hide located outside the col-
ony (within 10 min walking distance from all the study areas). Egg mass
and laying date did not differ between experimental treatments (General
Lineal Model, GLM; egg mass: F
1,90
= 0.348, p = 0.56; laying date:
F
1,90
= 0.239, p = 0.63). The eggshell over the acute pole of the egg
was carefully cleaned, sterilized with ethanol and the egg left in a vertical
position (acute pole upward) for 30 min until the egg yolk stabilized. A
hole was then drilled close to the acute pole with a sterilized needle of
the same diameter as the needle used for injection. In the testosterone-
injected group (T), the egg yolk was injected with 261 ng of testosterone
(Sigma, Germany) dissolved in 20 μl of sterile sesame oil, using a 100 μl
Hamilton syringe mounting 23-gauge needle (51 mm-long). The same
amount of testosterone was previously used in other studies on the
same species (Boncoraglio et al., 2006; Rubolini et al., 2006), which
reported an increase of the total content of the hormone equal
(12.6 ng/g yolk ± 5.44 SD in 38 freshly laid eggs) to two standard devi-
ations of the population mean (see details in Rubolini et al., 2006). Con-
trol eggs (C) were injected with 20 μl of sterile sesame oil using the same
procedureasforTeggs.Theholeintheshellwassealedwithapatchof
previously-sterilized hen eggshell. The path was glued with a very small
20 J.C. Noguera et al. / Hormones and Behavior 64 (2013) 1925
amount of cyanocrylate placed around of the drilled hole, paying special
attention that cyanocrylate glue was never in direct contact with the
hole.
Nests were checked daily beginning two days before the estimat-
ed hatching date. In the experiment, 52 eggs (23 T and 29 C) did not
develop successfully and 17 eggs (8 T and 9 C) developed but died
during hatching. A total of 22 chicks [14 T (30.4%) and 8 C (17.4%)]
hatched and were used for the experiment (a detailed description of
the effect of testosterone treatment on sex ratio, egg development,
hatching success and survival in this experiment can be found in
Noguera et al., 2011a). At hatching, all chicks were marked with num-
bered leg ags made of Velcro. Gull chicks were weighed (±0.1 g) at
1 (one day after hatching), 5 and 9 days of age. A blood sample was
also taken at 1 day of age. Blood samples were kept cool until the
plasma was separated from blood cells (within 8 h after collection)
and then stored in liquid nitrogen. Red blood cells from day 1 were
used for molecular sexing of the chicks following Grifths et al.
(1996). Chick body mass at day 1 of age did not differed between ex-
perimental groups (GLM: F
1,20
= 0.135, p > 0.717).
The frequency of begging behaviours was estimated in all study
chicks (T- and C-chicks) at age 2 days (third chicks, n = 22). Multi-
components of their begging display were measured using the
standard protocol of Tinbergen and Perdeck (1950) with minor mod-
ications described by Noguera et al. (2010). Begging tests were
performed for each chick individually (in the absence of sibling com-
petition) in a hide placed outside the gull colony to avoid any effect of
adult gull alarm calls on chick behaviour. The chicks were transported
from their nests to the hide in textile bags. Each chick was placed on
the ground and covered with a cloth until it was calm and quiet. The
chick was then exposed to playback of three mew calls, which had
been previously recorded at the same colony, to simulate a natural
feeding event (see Kim et al., 2011; Noguera et al., 2010 for details).
Immediately after removing the cloth, a dummy mimicking a natural
sized parent head was presented to the chick, which was allowed to
move freely on the ground. The dummy was made of white plaster
and the bill was painted in yellow and equipped with an interchange-
able red spot on the lower mandible. Two different sizes of red spot
were used during begging tests; one with the minimum area (hereaf-
ter small) and the other with the maximum area (hereafter large)
of red spots found in the colony (see Morales et al., 2009 for details
on red-spot size in this population). Thus, each chick was subjected
to two consecutive begging tests that only differed in the size of the
red spot in the dummy head. The order of presentation of dummy
head with the small or large red spot was alternated between consec-
utive chicks to control for any effect of presentation order. In all beg-
ging tests, visual stimulation was performed by nodding the dummy
head once every 2 s for a minute (for more details see Kim et al.,
2011). The number of distinct pecks delivered to the red spot during
the dummy presentation was recorded. The total number of chatter
calls(an easily discernible call), was also recorded during the entire
begging test (i.e. from mew-call playback to the end)(Impekoven,
1971; Noguera et al., 2010; Tinbergen and Perdeck, 1950).
All chicks wereweighed (± 0.1 g) immediately after the begging be-
haviour test (before being returned to their nests). Chick body mass on
the day of the begging test did not differ between experimental groups
(GLM: F
1,20
= 0.839, p = 0.373). Chicks were usually returned to their
nests of origin within 45 min of being collected. Each chick was
protected from wind and strong sunlight by keeping it inside a textile
bag placed under thick vegetation while away from the nest and not
being tested (Kim and Monaghan, 2006). Begging tests were not
performed during unfavourable weather conditions.
Statistical analysis
We used SAS software (SAS Institute, 2001) for all statistical anal-
yses. In the observational study, we tted a generalized linear mixed
model (GLIMMIX procedure in SAS) with Poisson errors to examine
the effect of begging (number of pecks and chatter calls) on feedings
(number of regurgitates) that each individual chick received from
each parent. In this model, the sex of the adult and the chick order
were included as xed factors. Nest identity was included as a ran-
dom term to control for non-independence of chicks from the same
brood and individual chick as a repeated measure subject (Littell et
al., 2006). The number of chatter calls showed a marginally signicant
positive correlation with the number of pecks (Pearson correlation
tests; r = 0.232, p = 0.05), so to avoid colinearity problems, we ran
two separate models for the number of regurgitates, including either
the number of chatter calls or pecks, and its interaction with sex as a
covariates. Additionally, to explore a possible sex-related effect of the
parental feedings on chick condition, we tted a general mixed model
(MIXED procedure in SAS) with the change in body mass of the chicks
during the observation period as the response variable. Chick order
was included as a xed factor, the number of feedings of male and fe-
male adults during the observation period as covariates and nest
identity as a random term.
The effects of testosterone treatment and red spot size on begging
behaviour (number of pecks and chatter calls) were analysed using
generalized linear mixed models with a Poisson error distribution
(GLIMMIX procedure in SAS), including chick identity as a repeated
measures subject, to account for nonindependence of two successive
begging tests from the same chick. Testosterone treatment, red spot
size, the order of red spot size presentation and sex were included
in the models as xed factors. Chick body mass and hatching date
(Julian date) were included as covariates. All two-way interactions
between xed factors were also tested.
Finally, we explored the effect of testosterone treatment
(T-treatment) on chick growth (body mass at 5 and 9 days of age).
We tted a repeated-measures models (MIXED procedure in SAS), in-
cluding age as a repeated-measure factor and chick identity as a subject
term (REPEATED statement). Sex and treatment were included in the
models as xed factors. Age was included as a within-group xed factor,
and hatching date and brood size as covariates. Begging behaviour may
affect chick growth (Noguera et al., 2010). Thus, additionally, we test
whether the relationship between body mass growth and begging
differed according to testosterone treatment. We re-ran the above
full model but including each component of begging behaviour sepa-
rately (log-transformed; i.e. the total number of pecks or chatter calls
performed during the two consecutive begging behaviour tests) and
their interactions with treatment as covariates. In the nal model (see
Results section) the quadratic term for the number of chatter calls
was also tested to explore a possible non-linear trend, and the partial
regression coefcients and p-values for each experimental group calcu-
lated (see Results).
All models were simplied by removing non-signicant terms (in
a backward deletion procedure), starting from two-way interactions;
signicance was tested when terms were dropped from the model. In
the models testing the effect of testosterone treatment and begging
behaviour on body mass growth, Satterthwaite's approximation for
degrees of freedom was used, and the best covariance structure was
selected in accordance with t statistics (Littell et al., 2006). Data
are presented as means ± standard error, and the signicance level
was set at α= 05.
Results
Feeding rate and begging behaviour
Parental feeding was related to the number of chatter calls
performed by the chicks, but this relationship varied between sexes
(Table 1); male parents were signicantly more responsive than
females to chatter calls (Fig. 1). Parental feeding also varied with
chick order when controlling for chatter calls (Table 1); the third
21J.C. Noguera et al. / Hormones and Behavior 64 (2013) 1925
chicks receiving a lower number of feedings than the rst and second
ones. Moreover, the number of parental feedings increased with the
number of pecks performed by the chicks (Table 1;Fig. 2) but in
this case the relationship was similar in the two sexes (parental sex:
F
1,34
= 2.55, p = 0.12; number of pecks × parental sex = F
1,33
=
0.01, p = 0.98). Results did not change after removing an outlier from
the data set (number of pecks: F
1,33
=62.96,pb0.001; Fig. 2,indicated
by an asterisk). In the model including pecking rate as a covariate, chick
order was not signicant (F
2,35
= 2.34, p = 0.11).
Interestingly, chick body mass increased with the number of feedings
providedbythemaleparent(F
1,21
= 7.67, p = 0.011; estimate =
0.779 ± 0.281 se; Fig. 3a) but not those by the female parent (F
1,20
=
0.02, p = 0.89; estimate = 0.143 ± 0.460 se; Fig. 3b). Chick body
mass change did not vary among chick orders (F
2,18
= 1.53, p = 0.24).
Effect of experimental yolk testosterone and red spot size on complex
begging behaviour
Testosterone treatment had a signicant effect on the frequency of
chatter calls during the begging test (estimate = 1.048 ± 0.480 se;
F
1,22
= 4.76, p = 0.040). Thus, chicks hatched from eggs with exper-
imentally elevated yolk testosterone produced more chatter calls
than control chicks (Fig. 4). Red spot size (F
1,20
= 0.83, p = 0.374),
the order of red spot presentation (F
1,21
= 3.07, p = 0.094), chick
sex (F
1,19
= 0.10, p = 0.750), chick body mass (F
1,21
= 1.5, p =
0.234), hatching date (F
1,19
= 0.33, p = 0.572) and two-way
interactions between xed factors (all p > 0.08) did not have a signif-
icant effect on chatter calls.
Red spot size in the lower mandible of dummy head had a sig-
nicant effect on the number of pecks performed by gull chicks
(estimate = 0.267 ± 0.112; F
1,21
= 5.69, p = 0.026); chicks pecked
more frequently to the dummy head when they were stimulated with
a large red spot than with a small one. Testosterone treatment
(F
1,20
= 0.14, p = 0.716), chick sex (F
1,21
= 0.74, p = 0.400), the
order of red spot presentation (F
1,20
= 0.67, 0.423), hatching date
(F
1,19
= 0.03, p = 0.858) and body mass (F
1,21
= 0.61, p = 0.445)
did not have a signicant effect on the number of pecks. Two-way
interactions between xed factors were also non-signicant (all
p > 0.72).
Effects of testosterone on chick growth
Chick body mass increased with age (F
1,15
= 26.34, p b0.001), but it
was not affected by testosterone treatment (F
1,16
= 0.06, p = 0.808).
Chick sex (F
1,14.2
= 0.01, p = 0.994), brood size (F
1,18.3
=0.01,p=
0.921), hatching date (F
1,16.9
= 0.18, p = 0.678) and the rest of two
way interactions between xedfactorsdidnothaveasignicant effect
on body mass (all p > 0.097). These results did not change when total
number of pecks and its interaction with testosterone treatment were
included into the full model (T-treatment: F
1,14.3
= 0.06, p = 0.806;
number of pecks: F =
1,17
= 1.51, p = 0.236; T-treatment × number
Table 1
Summary of nal generalized lineal mixed models (GLMMs) with a Poisson error distribution and a log link for the number of parental feedings received by gull chicks (2 days old)
during the observational period (4 h). The minimal adequate models are shown when (a) the number of chatter calls and (b) number of pecks were included into the model.
Dependent variable Source of variation Estimate ± se Fdfp
(a) Number of feedings Intercept 0.912 ± 0.364
Chick order
(First) 0.640 ± 0.640 4.96 2,33 0.013
(Second) 0.875 ± 0.875
Adult sex (female) 0.378 ± 0.288 1.72 1,33 0.198
Number of chatter calls 0.369 ± 0.076 24.05 1,33 b0.001
Adult sex × number of chatter calls 0.256 ± 0.107 5.66 1,33 0.023
(b) Number of feedings Intercept 0.280 ± 0.190
Number of pecks 0.210 ± 0.029 51.79 1,35 b0.001
Full model: (a) chick order + adult sex + number of chatter calls + adult sex × number of chatter calls. (b) Chick order + adult sex + number pecks + adult sex × number of
pecks.
6
8
4
2
0
0
246810
Number of chatter calls
Number of feedings
Fig. 1. Relationship between the number of feedings delivered by the female (white
triangles and dashed line; r = 0.161, p = 0.35) and the male parent (black dots and
solid line; r = 0.55, p b0.001) during the observational period (4 h) and the number
of chatter calls emitted by yellow-legged gull chicks to each parent (n = 36 chicks
from 14 broods). The size of the symbols correspond to sample sizes (range 18).
8
6
4
2
0
02468
*
10 12
Number of pecks
Number of feedings
Fig. 2. Relationship between the number of feedings delivered by the female (white
triangles) and the male parent (black dots) during the observational period (4 h)
and the number of pecks performed by yellow-legged gull chicks to each parent
(n = 36 chicks from 14 broods). The size of the symbols correspond to sample sizes
(range 120). A possible outlier (Cook's D = 1.7) in the dataset is indicated by an as-
terisk (see Results).
22 J.C. Noguera et al. / Hormones and Behavior 64 (2013) 1925
of pecks: F
1,11.5
= 1.68, p = 0.219). When the total number of chatter
calls was included in the full model, testosterone treatment × number
of chatter calls had a signicant effect on chick body mass until day 9
of age (F
1,14.9
= 10.72, p = 0.005; Fig. 5). This model was improved
when the interaction between the quadratic term for the number of
chatter calls and testosterone was included (F
1,13.6
= 5.06, p = 0.041).
Thus, chick body mass increased with the number of chatter calls in
C-chicks (partial regression coefcient: r = 0.734, p = 0.016, n = 10)
but not in T-chicks (partial regression coefcient: r = 0.207, p =
0.619, n = 25).
Discussion
In this study we investigated sex differences in parental respon-
siveness to chick begging and the inuence that yolk testosterone ex-
erts on complex begging behaviour. Three lines of evidence indicate
that maternally-derived testosterone in the egg yolk may be a female
strategy to manipulate the male's contribution to parental care in the
yellow-legged gull. First, chicks hatched from eggs with elevated level
of yolk testosterone performed more chatter calls than control chicks.
Second, the parental feeding effort was related to the number of chat-
ter calls given by gull chicks but importantly, this relationship was
stronger in male parents than in the female parents. Third, chick
body mass increased only with the number of feeds received from
the male parent during our observation period. As far as we are
aware, this is the rst study providing empirical support for the Ma-
nipulating Androgen Hypothesis. Although maternal testosterone
can inuence chick begging, our results suggest that an elevated
amount of this hormone may lead to a reduction of growth, possibly
through excessive begging behaviour, which could hamper the evolu-
tion of female manipulation.
A subtle implicit assumption of the MAHis that male parents
should be particularly responsive to those begging components affected
by yolk hormones. In our observational study we found that males,
more than females, allocated food according to the number of chatter
calls, which was the only begging component affected by testosterone
treatment in our experimental study. Such component-speciceffects
of testosterone on begging behaviour may explain, at least partially,
why previous studies on MAH did not nd conclusive results (Barnett
Fig. 3. Changein body mass ofyellow-legged gull chicksin relationto the number feedings
delivered by (a) the male and (b) the female parent during the 4 h of observational period
(n = 36 chicks from 14 broods). The tted line shows the adjusted linear regression.
3.0
2.5
2.0
1.5
1.0
0.5
0
Control Testosterone
Fig. 4. Effects of experimental testosterone treatment on the totalnumber of chatter calls
(least square mean ± standard error from the nal model) in yellow-legged gull chicks.
Fig. 5. Body mass in relation to the intensity of begging behaviour (total number of
chatter calls) performed by T-chick (full dots and solid line) or C-chick (open dots
and dashed line). Fitted lines show the adjusted linear (C-chicks) and quadratic
(T-chicks) regression lines. In T-chicks, the quadratic regression line showed the best
t to data points. Body mass values at 5 and 9 days of age for each chick are shown.
23J.C. Noguera et al. / Hormones and Behavior 64 (2013) 1925
et al., 2011; Laaksonen et al., 2011; Ruuskanen et al., 2009; Tschirren
and Richner, 2008). In addition, we cannot discard the possibility that
in other species females may use hormones to compensate the poten-
tially lower genetic quality of the offspring rather than to manipulate
the males (see Laaksonen et al., 2011 for discussion). Yolk hormones
rarely affect all components involved in begging behaviour (for review
see Smiseth et al., 2011). Interestingly, unlike chatter calls, response to
pecking behaviour was similar in the two parents, and this begging
component was not affected by our testosterone manipulation (but
see Eising and Groothuis, 2003). Thus, by being sensitive to pecking be-
haviour but less so to chatter calls, females may allocate food according
to the chicks' need (Noguera et al., 2010) and avoid their maternal ef-
fects on chatter calls. On the other hand, it is interesting to note that
for the evolution of hormone deposition mothers should have tness
benets (in the current or future reproduction) as result of increased
male parental investment. Parental care is almost always costly, but it
has a strong inuence on chick tness (Alonso-Alvarez and Velando,
2012). Interestingly, in our study, chick body mass increased with
the number of feeds provided by the father but not by the mother,
suggesting that maternal effects could have important benets for
chick tness.
The positive effect that yolk testosterone had on the number of
chatter calls supports the inuence of maternal hormones in shaping
offspring phenotype (Gil, 2003; Groothuis and Schwabl, 2008;
Smiseth et al., 2011). In particular, yolk testosterone could have in-
duced an early stimulation in some brain regions involved in calling
behaviour of gulls, such as the nucleus itercollicularis (ICo; Delius,
1971). For instance, testosterone positively affects cell size and thick-
ening of the external membranes of ICo which are important traits in-
volved in the production of sound in birds (review in Panzica et al.,
1995). Thus, the promoting effect that testosterone had on chatter
calls may be based on the activation of neuroendocrine pathways
governing begging calls. Testosterone also seems to promote com-
pensatory responses that prevent the accumulation of oxidative dam-
age during the early development of chicks (Noguera et al., 2011a).
Therefore, it is possible that testosterone might allow the chicks to
increase the frequency of chatter calls at the expense of the loss of
some antioxidant capacity. Alternatively, testosterone treatment
could have produced an indirect effect on begging, for instance, via
improved growth (Schwabl, 1996) or hatching muscle (musculus
conplexus)(Lipar and Ketterson, 2000). Nevertheless, we did not
nd any effect of our testosterone treatment on chick growth before
two days of age.
Our results conrm the previous results that gull chicks make
more pecks at large red spots (Velando et al., 2013). Although red
spots are costly to produce for parents and reect their current condi-
tion and health (Pérez et al., 2008, 2010, 2012), red spot size presum-
ably also provides information about their ability as caregivers (Hill,
1991). Nevertheless, we found no evidence that testosterone promot-
ed pecking or that T-chicks were particularly biased towards pecking
and/or calling at large red spots. Therefore, although maternal manip-
ulation seems plausible in yellow-legged gulls, such manipulation did
not affect the begging component inuenced by the phenotypic cues
encoded in sexual signals (Morales et al., 2009).
The existence of costs associated with begging behaviour is essential
to explain how begging behaviour has evolved under different theoret-
ical models (Godfray, 1995; Harper, 1986; Kilner and Johnstone, 1997;
MacNair and Parker, 1979; but see Bergstrom and Lachmann, 1998 for
cost-free models). In the present study T-chicks experienced a reduc-
tion of growth particularly when they performed an excessive number
of chatter calls, which would support previous studies showing that
nestlings may suffer a marginal cost of excessive begging through im-
paired growth (Kilner, 2001; Rodríguez-Girones et al., 2001). Chatter
calls couldhave impaired growthas a consequence of limiting the avail-
ability of energy (Chappell and Buchman, 2002) or antioxidant re-
sources (Noguera et al., 2010) needed for chick growth (De Ayala et
al., 2006; Drent et al., 1992; Noguera et al., 2011b). Additionally, the re-
duction of growth could have arisen as a consequence of parents feed-
ing less to those chicks that beg excessively (Hendersson, 1975;
Morales et al., 2009). Irrespective of the mechanism, an elevated
level of maternal testosterone could negatively affect chick's tness
(Gebhardt-Henrich and Richner, 1998) which would explain why fe-
males do not maximise the androgen deposition within a clutch
(Moreno-Rueda, 2007). Furthermore, this result also suggests that the
evolution of female manipulation may be constrained by the negative
effects of yolk hormones on chicks' growth. Thus, the benets of manip-
ulation may only occur below a threshold, which may explain the con-
troversial evidences in favour of MAH (i.e. Barnett et al., 2011;
Laaksonen et al., 2011; Ruuskanen et al., 2009; Tschirren and Richner,
2008).
In conclusion, our results suggest that in yellow-legged gull yolk
testosterone could mediate the resolution of sexual conict over pa-
rental care. Maternal testosterone allocated into the eggs promotes
an increase in chatter calls and only male parents increase their in-
vestment in parental care according to intensity of chatter calls.
Such results highlight the importance of identifying those chick char-
acteristics that differentially affect the effort of parents to improve
our understanding about the role that maternal effects mediated by
hormones may have in the resolution of sexual conict (Ruuskanen
et al., 2009).
Acknowledgments
We thank Kate Lessells and two anonymous reviewers for their very
constructive comments. We also thank C. Perez and J. Morales for their
help during eld work and particularly to J.M. and K. Herborn for their
very constructive comments on the manuscript. We specially thank
the staff of the P. N. Illas Atlánticas at Salvora (Pablo, Marcos, Jacinto,
Gema y Andrés) and the lighthouse keepers Pepe and Julio for their
generous support. We thank the J.A. Fernandez Bouzas (P. N. Illas
Atlánticas) for the permissions and for facilities on Sálvora Island.
Finance wasprovided by the Spanish Ministerio de Ciencia e Innovación
(CGL2012-40229-C02-02). J.C.N. began this study supported by a grant
from MICINN (BES-2007-16432) and completed it through the support
from Marie Curie Intra European Fellowship within the 7th European
Framework Program (PIEF-GA-2011-301093). S.Y.K. was supported by
an Isidro Parga Pondal fellowship (Xunta de Galicia).
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... If, for example, mothers produce offspring phenotypes that demand more parental care, this action would be costly for the mother if she, along with her partner, must increase her parental investment in these demanding offspring. If, in contrast, the mother can produce an offspring phenotype that only exerts extra care from the father (for example, by dampening her own response to offspring begging), there is no cost to her of exaggerating the signal to produce a highly demanding offspring phenotype as only her partner will bear the costs of increased care (as seems to be the case in yellow-legged gulls Larus michaellis; Noguera, Kim & Velando, 2013). In the latter case, selection should favour fathers who express a reduced response to offspring phenotypes to compensate for maternally induced exaggeration of offspring solicitation behaviourand the parental arms race begins. ...
... Such experiments are designed to test the 'differential allocation' (females invest more in offspring of desirable males; Sheldon, 2000) and 'manipulating androgens' (females use hormones to elicit extra parental care from the father; Moreno-Rueda, 2007) hypotheses. The results are mixed; in one study, fathers seem to blindly follow the instructions provided by maternal hormones (providing more care to more demanding offspring, for example; Noguera et al., 2013) whereas in others, paternal strategy appears to be completely independent of maternal hormone allocation (Ruuskanen et al., 2009;Barnett et al., 2011). In the context of intrafamilial conflict, we can make clear predictions about this variation: fathers should respond positively to maternal hormone allocation if they lack sufficient information about the environment to reliably exert their own optimum offspring phenotype. ...
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... For example, in yellow-legged gulls, Larus michahellis, males are more responsive to one component of begging (i.e. chatter calls) than females, and experimentally elevated levels of yolk testosterone specifically stimulate this component of begging (Noguera, Kim, & Velando, 2013). Thus, there is now a need for more experimental work investigating (1) offspring preferences for begging towards and associating with male and female parents, (2) whether such preferences are innate or based on familiarity with the two parents, and (3) whether females use prenatal maternal effects to alter such preferences to their advantage. ...
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In species with biparental care, begging offspring may preferentially associate with or beg more towards one of their parents. Such preferences may reflect that the benefits of begging vary with the parent's sex given that females and males often differ in the amount of care they provide and/or in their responsiveness to begging levels. Alternatively, they may reflect the outcome of sexual conflict over care as females may deposit compounds into eggs tha talter offspring begging behaviour such that it increases male contributions towards care. For example, females might use male presence during egg laying as a cue for whether they might receive male assistance in care. Here, we studied offspring begging behaviour towards male and female parents in the burying beetle Nicrophorus vespilloides by manipulating male presence or absence during egg laying and providing larvae with a simultaneous choice between an unfamiliar female and male adult beetle. We then recorded begging behaviour of (1) naïve newly hatched larvae that had no prior experience of a parent and (2) larvae after 24 h of care by foster parents. Larvae showed a clear preference for associating with and begging towards females both when naïve and after 24 h of care. We found no evidence for prenatal maternal effects on larval begging behaviour. Our study reveals that offspring are predisposed to preferentially beg towards females independently of prior experiences with parents and highlights the importance of considering responses of begging offspring to parental attributes, such as the parent's sex, for our understanding of family conflicts.
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En las especies con múltiples reproducciones, la inversión en reproducción a menudo disminuye el mantenimiento somático y la supervivencia, generando así un compromiso entre la reproducción actual y las oportunidades para reproducirse en el futuro. En esta pequeña reseña de nuestros estudios mostramos cómo este compromiso modula los conflictos de familia y las estrategias de inversión parental a lo largo de la vida, y puede ser determinado por las presiones de selección durante el desarrollo. Estudiamos cómo las señales sociales, incluidas las sexuales, afectan a las decisiones de inversión parental y pueden ser usadas por todos los miembros de la familia para ajustar su comportamiento, lo que provoca una coevolución social compleja. Nuestros estudios de seguimiento a largo plazo señalan que las estrategias de inversión cambian a lo largo de la vida y están afectadas por el valor de la presente reproducción y por las expectativas futuras. Diversos estudios indican que las trayectorias vitales pueden depender de las presiones selectivas a edades muy tempranas sobre un conjunto de rasgos, y el ambiente social puede ser determinante en su desarrollo. En las últimas décadas, el estudio de los rasgos de comportamiento ha ido cambiado; de examinar cada rasgo de forma independiente a estudiar las relaciones complejas entre rasgos o la coevolución con los rasgos de otros individuos en el entorno social. Quedan muchas preguntas por abordar y para resolverlas se necesitan nuevos estudios y modelos teóricos que recojan la complejidad de factores que afectan a los rasgos de comportamiento.
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Tinbergen’s classic “On Aims and Methods of Ethology” (Zeitschrift für Tierpsychologie, 20, 1963) proposed four levels of explanation of behavior, which he thought would soon apply to humans. This paper discusses the need for multilevel explanation; Huxley and Mayr’s prior models, and others that followed; Tinbergen’s differences with Lorenz on “the innate”; and Mayr’s ultimate/proximate distinction. It synthesizes these approaches with nine levels of explanation in three categories: phylogeny, natural selection, and genomics (ultimate causes); maturation, sensitive period effects, and routine environmental effects (intermediate causes); and hormonal/metabolic processes, neural circuitry, and eliciting stimuli (proximate causes), as a respectful extension of Tinbergen’s levels. The proposed classification supports and builds on Tinbergen’s multilevel model and Mayr’s ultimate/proximate continuum, adding intermediate causes in accord with Tinbergen’s emphasis on ontogeny. It requires no modification of Standard Evolutionary Theory or The Modern Synthesis, but shows that much that critics claim was missing was in fact part of Neo-Darwinian theory (so named by J. Mark Baldwin in The American Naturalist in 1896) all along, notably reciprocal causation in ontogeny, niche construction, cultural evolution, and multilevel selection. Updates of classical examples in ethology are offered at each of the nine levels, including the neuroethological and genomic findings Tinbergen foresaw. Finally, human examples are supplied at each level, fulfilling his hope of human applications as part of the biology of behavior. This broad ethological framework empowers us to explain human behavior—eventually completely—and vindicates the idea of human nature, and of humans as a part of nature.
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Mothers, fathers, and offspring regularly clash over how much care offspring receive. Offspring beg to solicit for more resources--but how much begging is rewarded can depend on who is listening. While both parents benefit from provisioning offspring, each would benefit from their partner shouldering more of the burden of care, leading to sexual conflict. Additionally, if the costs and benefits of provisioning differ by sex, parent-offspring conflict should vary by sex. How these evolutionary conflicts influence sex differences in parent-offspring communication is unknown. To determine whether the sexes differ in their response to offspring signals, we conducted a meta-analysis on 30 bird species, comparing responsiveness to social and physiological traits affecting conflict. We found that a species' typical pair bond strength predicts whether males or females respond more to offspring begging. In species with stable and/or monogamous bonds, and thus lower sexual and paternal-offspring conflict, males' provisioning effort is more strongly correlated with offspring begging than females'. The opposite holds for species with weak pair bonds: females respond more to begging, perhaps compensating for males' lower responsiveness. These results demonstrate that sex differences in parental care can arise via sex differences in parent-offspring communication, driven by evolutionary conflicts.
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Prenatal maternal effects are increasingly recognized as important mediators in the development of individual differences during early sensitive or even critical periods. Hormone-mediated maternal effects in egg-laying species are a frequently used model to study such effects, mostly to test whether these increase maternal fitness. However, experimental evidence is inconsistent. This has led researchers to divert to other topics. In this review, we argue that from a Darwinian perspective one should however expect strong interactions between effects of maternal hormones with contextual cues, including environmental factors, embryonic modulation of maternal signals, offspring age and sex, and fathers’ influence. Taking these into account may explain the inconsistencies and new experiments should reveal how the benefits and costs of maternal hormones and prenatal maternal effects in general play out in different contexts.
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This paper evaluates sexual size dimorphism in the Yellow-legged Gull (Larus carhinnans) from a colony in northeast Spain and provides a reliable method for predicting the sex of measured individuals. Males were significantly larger than females in all body measurements. Predictive functions using two to four measurements correctly sexed 100% of the sampled individuals, although one measurement (head length) was almost as accurate (99.4%). Other authors reported no differences between the measurements taken from gulls in this colony and those taken from gulls in colonies as far away as the Moroccan coast. Thus, the discriminant functions described in this paper might be applicable to other colonies of Yellow-legged Gulls.
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In order to explain the huge variation in parental behaviour, evolutionary biologists have tradition-ally used a cost–benefit approach, which enables them to analyse behavioural traits in terms of the positive and negative effects on the transmission of parental genes to the next generation. Empir-ical evidence supports the presence of a number of different trade-offs between the costs and ben-efits associated with parental care (Stearns 1992; Harshman and Zera 2007), although the mecha-nisms they are governed by are still the object of debate. In fact, Clutton-Brock's (1991) seminal book did not address the mechanistic bases of parental care and most work in this field has been conducted over the last 20 years. Research on mechanisms has revealed that to understand parental care behaviour we need to move away from traditional models based exclusively on currencies of energy or time. Despite repeated claims, the integration of proxi-mate mechanisms into ultimate explanations is cur-rently far from successful (e.g. Barnes and Partridge 2003; McNamara and Houston 2009). In this chapter we aim to describe the most relevant advances in this field. In this chapter, we employ Clutton-Brock's (1991) definitions of the costs and benefits of parental care. Costs imply a reduction in the number of off-spring other than those that are currently receiv-ing care (i.e. parental investment, Trivers 1972), whereas benefits are increased fitness in the off-spring currently being cared for (see also Chapter 1). Benefits may be derived directly from resources allocated to the offspring (e.g. food, temperature), indirectly from protection against predators, or from the modification of the environment in which the offspring are developing (Chapter 1). We begin this chapter by reviewing the traditional idea of resource allocation trade-offs, and also explore how trade-offs need not be based on resources, and the relevance of cost-free resources. We then analyse in more detail studies of the benefits and costs of parental behaviour and, above all, work that combines mechanistic and functional explanations. Finally, we address the control systems that trans-late cues perceived by the organism about costs and benefits allowing individuals to take decisions. 3.2 Trade-offs and the nature of the parental resources
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Introduction, In many bird species, young beg for care from their parents. A parent arriving at the nest with food is met by begging nestlings, which are waving their wings, calling and stretching to expose brightly coloured gapes, all within the confines of a nest that may contain several other begging nestlings. This mode of parent–offspring communication has become a model for the study of the evolution of biological signalling. Hungrier nestlings beg more intensely, so the parent can use the display to decide which nestling to feed and to decide how soon it should return to the nest with food (reviewed by Budden & Wright, 2001). The fact that the parent can extract information on nestling hunger from such a confusing burst of signalling raises numerous questions. How does each nestling ensure that its own signal of need is received above the din of its nestmates' displays? How do parents differentiate among these displays to choose which nestling to feed? How much do the displays, as opposed to the physical jostling toward the parent that also goes on in the nest, determine which nestlings are fed? To answer such questions we need to understand how the begging behaviours of whole broods function together. Concepts derived from the new field of communication networks seem well suited to this task but have not yet been explicitly applied to begging. As currently defined (McGregor & Dabelsteen, 1996; McGregor & Peake, 2000), a communication network forms whenever several individuals communicate within transmission range of each other's signals.
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Interacting phenotypes are traits whose expression is affected by interactions with conspecifics. Commonly-studied interacting phenotypes include aggression, courtship, and communication. More extreme examples of interacting phenotypes-traits that exist exclusively as a product of interactions-include social dominance, intraspecific competitive ability, and mating systems. We adopt a quantitative genetic approach to assess genetic influences on interacting phenotypes. We partition genetic and environmental effects so that traits in conspecifics that influence the expression of interacting phenotypes are a component of the environment. When the trait having the effect is heritable, the environmental influence arising from the interaction has a genetic basis and can be incorporated as an indirect genetic effect. However, because it has a genetic basis, this environmental component can evolve. Therefore, to consider the evolution of interacting phenotypes we simultaneously consider changes in the direct genetic contributions to a trait (as a standard quantitative genetic approach would evaluate) as well as changes in the environmental (indirect genetic) contribution to the phenotype. We then explore the ramifications of this model of inheritance on the evolution of interacting phenotypes. The relative rate of evolution in interacting phenotypes can be quite different from that predicted by a standard quantitative genetic analysis. Phenotypic evolution is greatly enhanced or inhibited depending on the nature of the direct and indirect genetic effects. Further, unlike most models of phenotypic evolution, a lack of variation in direct genetic effects does not preclude evolution if there is genetic variance in the indirect genetic contributions. The available empirical evidence regarding the evolution of behavior expressed in interactions, although limited, supports the predictions of our model.