Yolk testosterone, postnatal growth and song in male canaries

Department of Biology-Ethology, University of Antwerp, Antwerp, Wilrijk, Belgium.
Hormones and Behavior (Impact Factor: 4.63). 07/2008; 54(1):125-33. DOI: 10.1016/j.yhbeh.2008.02.005
Source: PubMed
ABSTRACT
Avian eggs contain substantial amounts of maternal yolk androgens, which have been shown to modulate offspring phenotype. The first studies on the functional consequences of maternal yolk androgens have focused on early life stages and their role in sibling competition. However, recent longitudinal studies reported long-lasting effects of maternal yolk androgens on offspring phenotype, mostly concerning traits that are sensitive to androgens. This suggests that maternal yolk androgens could play an important role in sexual selection, since the expression of many male sexual characters is testosterone-dependent. Using male canaries as a model, we examined the consequences of an experimental elevation of yolk testosterone concentrations on early development as well as long-lasting effects particularly on song, which is one of the most important sexual characters in male songbirds. Elevated yolk testosterone concentrations inhibited male growth, possibly in interaction with an existent ectoparasite exposure. Males hatched from testosterone-treated eggs (T-males) did not have enhanced competitive skills, in contrast to previous studies. The elevation of yolk testosterone concentrations delayed song development but did not affect adult song phenotype. This is intriguing, as yolk testosterone possibly induced developmental stress, which is known to reduce song quality. We hypothesize that yolk testosterone has either no direct effect on adult song phenotype, or that positive effects are merged by the negative effects of developmental stress. Finally, females mated with T-males invested more in their clutch indicating that females either assess T-males as more attractive (differential allocation hypothesis) or compensated for lower offspring viability (compensation hypothesis).

Full-text

Available from: Marcel Eens, May 02, 2016
Yolk testosterone, postnatal growth and song in male canaries
Wendt Müller
, Jonas Vergauwen, Marcel Eens
Department of BiologyEthology, University of Antwerp, Belgium
Received 31 October 2007; revised 7 February 2008; accepted 8 February 2008
Available online 10 March 2008
Abstract
Avian eggs contain substantial amounts of maternal yolk androgens, which have been shown to modulate offspring phenotype. The first studies
on the functional consequences of maternal yolk androgens have focused on early life stages and their role in sibling competition. However, recent
longitudinal studies reported long-lasting effects of maternal yolk androgens on offspring phenotype, mostly concerning traits that are sensitiveto
androgens. This suggests that maternal yolk androgens could play an important role in sexual selection, since the expression of many male sexual
characters is testosterone-dependent. Using male canaries as a model, we examined the consequences of an experimental elevation of yolk
testosterone concentrations on early development as well as long-lasting effects particularly on song, which is one of the most important sexual
characters in male songbirds. Elevated yolk testosterone concentrations inhibited male growth, possibly in interaction with an existent ectoparasite
exposure. Males hatched from testosterone-treated eggs (T-males) did not have enhanced competitive skills, in contrast to previous studies. The
elevation of yolk testosterone concentrations delayed song development but did not affect adult song phenotype. This is intriguing, as yolk
testosterone possibly induced developmental stress, which is known to reduce song quality. We hypothesize that yolk testosterone has either no
direct effect on adult song phenotype, or that positive effects are merged by the negative effects of developmental stress. Finally, females mated
with T-males invested more in their clutch indicating that females either assess T-males as more attractive (differential allocation hypothesis) or
compensated for lower offspring viability (compensation hypothesis).
© 2008 Elsevier Inc. All rights reserved.
Keywords: Maternal effects; Sexual selection; Developmental stress; Bird song; Mate choice; Signal evolution; Differential allocation; Catch-up growth; Early
nutrition
Introduction
Sex steroids play an important role in the process of sexual
differentiation, translating offspring genotype into sexual
phenotype (Moore et al., 1998; Balthazart and Adkins-Regan,
2003). However, sex steroids are not only responsible for the
expression of sexually dimorphic traits, but differences in
exposure to sex steroids during critical periods of development
can also lead to variation in sexually dimorphic traits among
individuals within the same sex (Crews, 1998; Moore et al.,
1998). Such differences in steroid exposure can be due to
individual differences in steroid secretion following gonadal
differentiation, but also relate to external sources of steroid
hormones in the embryonic environment of the offspring (Crews,
1998). In birds, the embryonic environment is largely shaped by
the characteristics of the egg. The avian egg contains not only all
nutrients necessary for offspring development, but also a number
of specific components among which steroid hormones of
maternal origin, in particular maternal androgens (Schwabl,
1993). These m ater nal yolk androgens may represent an
important pathway along which offspring phenotype is shaped.
Variation in maternal yolk androgen concentrations across
the laying sequence was one of the first patterns that has been
described (Schwabl, 1993; Schwabl et al., 1997). This has been
interpreted as a maternal strategy modifying offspring pheno-
type in order to mitigate or enhance the consequences of
hatching asynchrony (Schwabl, 1993; Groothuis et al., 2005a).
Studies dealing with the functional consequences of embryonic
exposure to maternal yolk androgens have therefore primarily
A
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Hormones and Behavior 54 (2008) 125 133
www.elsevier.com/locate/yhbeh
Corresponding author. Department of BiologyEthology, University of
Antwerp, Campus Drie Eiken C-1.27, Universiteitsplein 1, 2610 Antwerp
(Wilrijk), Belgium. Fax +32 38202271.
E-mail address: Wendt.Muller@ua.ac.be (W. Müller).
0018-506X/$ - see front matter © 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2008.02.005
Page 1
focused on the effects on early life stages (e.g. Schwabl, 1996;
Sockman and Schwabl, 2000; Eising et al., 2001). These studies
revealed that maternal androgens affect numerous phenotypic
traits during early development, most of which play an
important role in the context of sibling competition (Gil,
2003; Groothuis et al., 2005a). Besides their role as mediators of
sibling competition, yolk androgens may also allow to translate
the general environmental conditions experienced by the female
into adaptive phenoty pic variation of the offspring. This
hypothesis is supported by the observed systematic between-
clutch variation, which is among others modulated by the
maternal environment (Gil, 2003; Groothuis et al., 2005a).
However, so far studies dealing with the functional conse-
quences of between-clutch variation in relation to offspring
environment during the early development al period have not yet
been able to support this hypothesis (Tschirren et al., 2005;
Müller et al., 2007). But recently it could be shown that
maternal yolk androgens modified offspring's dispe rsal beha-
vior post-fledging, providing a functional explanation for the
observed between-clutch variation in yolk androgens in relation
to maternal ectoparasite exposure (Tschirren et al., 2004, 2007).
This study adds to the growing number of recent studies
reporting long-lasting effects of embryonic exposure to maternal
yolk androgens on offspring behavior (Schwabl, 1993; Strasser
and Schwabl, 2004; Eising et al., 2006; Tobler and Sandell,
2007), fecundity (Uller et al., 2005; Rubolini et al., 2007; but see
von Engelhardt et al., 2004; Rutkowska et al., 2007), sexual
characters (Strasser and Schwabl, 2004; Eising et al., 2006; but
see Uller et al., 2005; Rubolini et al., 2006; von Engelhardt et al.,
2004) and attractiveness (von Engelhardt et al., 2004, but see
Rutkowska et al., 2007). A number of effects concern traits, of
which the expression or development is modulated by andro-
gens. This suggests that the nature of these effects may be
organizational: embryonic exposur e to maternal androgens may
have changed either endogenous androgen production or the
sensitivity towards exposure to androgens at later life stages
(Groothuis et al., 2005a; Carere and Balthazart, 2007). However,
the long-lasting effects observed may also be a (indirect)
consequence of activational effects at an earlier time (Carere and
Balthazart, 2007). The expression of speci fic behaviors during
early development may have priming effects on other behaviors
at later life stages (e.g. Groothuis and Meeuwissen, 1992). For
instance, a positive effect of maternal yolk androgens on begging
(e.g. Schwabl, 1996; Eising and Groothuis, 2003) may increase
the probability that a chick becomes dominant in sibling
competition, and could enable those individuals to dominate
other individuals at later life stages more easily. Such positive
long-lasting effect on dominance status has been shown
previously (Schwabl, 1993; Strasser and Schwabl, 2004; Eising
et al., 2006). Furthermore, yolk androgen mediated changes in
competitiveness likely affect the nutritional conditions during
early development with consequences for later life stages.
Independent of the proximate mechanism, the fact that long-
lasting effects concern traits that are often modulated by
androgens, suggests that maternal yolk androgens could play an
important role in sexual selection, since the expression of many
male sexual characters is testosterone-dependent. In songbirds,
one of the most important sexual characters is song, and the
quality of song has a strong effect on reproductive success, both
through mate choice and malemale competition (Catchpole
and Slater, 1995). The development and the expression of the
adult song phenotype is dependent on steroid hormones (e.g.
Gahr, 2004), and it is there fore likely that yolk androgens could
have a positive effect on adult song phenotype, given that most
of the previous studies have reported enhancing effects on
androgen-dependent traits. Furthermore, adult song phenotype
is affected by the early developmental conditions (e.g. Nowicki
et al., 2002) so that yolk androgen may also have an indirect
positive effect on adult song phenotype through an improve-
ment of the early growth conditions (Gil, 2003; Groothuis et al.,
2005a). However, in a recent comparative analysis it was shown
that song duration and syllable repertoire size were negatively
related to yolk testosterone concentrations (Garamszegi et al.,
2007). Yet experi mental studies investigating the relationship
between yolk androgens and adult song phenotype are missing.
Here we investigate consequences of maternal yolk test oster-
one on offspring phenotype in mal e canaries (Serinus canaria).
We chose for a between-clutch treatment (all eggs within a clutch
were either injected with testosterone diss olved in sesame oil, or
with sesame oil only {control}) to avoid direct contact/com-
petition between chicks of different treatments, as this may have
a long-lasting effect on other behaviors ( see above). We
investigated the effects of elevated yolk testosterone concentra-
tions on growth during the early developmental period, since
growth conditions will be important for the interpretation of any
observed long-lasting effect. We analysed possible long-lasting
effects on social dominance, a trait that previously has been
shown to be modulated by yolk androgens in several species
including the canary (Schwabl, 1993; Strasser and Schwabl,
2004; Eising et al., 2 006) and bird song. Bird song is a highly
important sexual character in songbi rds, which is both during
development and adult life sensiti ve to testosterone (Gil and
Gahr, 2002). Finally, we mated all males and measured the
female's investment in her clutch in order to obtain an estimate
of a male's reproductive success.
Materials and methods
(a) Testosterone injections
Five Canaries were obtained from local suppliers mid January 2006 and
housed under a L:D regime of 14:10. Throughout the experiments, if not stated
otherwise, birds were provided with canary seed mixture (van Camp, Belgium),
water, shell grit, and cuttlefish bone ad libitum and egg food mixture (van Camp,
Belgium) twice weekly. After five weeks, all birds were randomly paired and
housed in separate breeding cages equipped with nest boxes and nesting
material. Nests were checked daily for new eggs, and two days after the first egg
was laid all eggs present were weighed and injected, all subsequent eggs were
injected and weighed as they were laid. Yolk hormone concentrations have
been shown to be highly repeatable within species across different studies
[Gil et al., 2007, e.g. range of yolk testosterone concentrations in canaries:
10160 pg/mg in waterslager canaries (Schwabl, 1993); 17142 pg/mg in
domestic canaries (Gil et al., 2004)]. In order to allow a close comparison with
the study by Schwabl (1996), we used the injection protocol and concentrations
for canaries as described therein. Briefly, all eggs within a clutch were injected
either with 100 ng testosterone dissolved in 5 μl sesame oil, or 5 μl sesame oil
only as control treatment. The type of treatment was inverted with every new
126 W. Müller et al. / Hormones and Behavior 54 (2008) 125133
Page 2
clutch. The injection elevated yolk testosterone concentrations to levels in the
upper range of maternal testosterone in canary eggs (Schwabl, 1993; Gil et al.,
2004; Tanvez et al., 2004; Marshall et al., 2005). Two months later (begin May,
L:D regime 15:9), all pairs were allowed to lay a second clutch with inversion of
the treatment. The experiment was performed under proper legislation by the
Flemish and Belgian law and approved by the animal experimentation
committee of the University of Antwerp.
(b) Early development
At the time of expected hatching, we controlled nests twice daily and if
possible, identified from which egg a hatchling hatched. Hatchlings were
weighed to the nearest 0.01 g and marked with a non-toxic pen for individual
recognition until numbered plastic bands were given. During the period of
parental care we provided the birds with fresh egg food daily. Body mass was
measured early in the morning every day until fledging. Survival to fledging was
recorded. Molecular sex determination was used to determine offspring sex
using either a blood sample taken around fledging or tissue samples of dead
chicks (first clutch only)(Griffiths et al., 1998).
(c) Song development
All fledglings were separated from their parents when about 30d old. All
male (N = 40 from 23 different families) offspring were kept together in one
room under natural light regime in groups of four individuals per cage, within
each group, both treatments being present. As tutors, five adult canary males
were housed in separate cages with visual and acoustic contact to all juvenile
males.
Birds were observed several times a day until singing for the first time was
recorded for all individuals. Furthermore, twice a week we measured the time an
individual spent singing for a period of more than 3 months (Sept.Dec.). In the
course of this experiment, all birds were moved to separate cages within the
same room 48 h in advance of the registration procedure. Birds were observed
for half an hour in the morning and half an hour in the afternoon, and every
minute it was recorded whether a bird was singing or not.
(d) Behavioral measures
At 3 and 6 months of age, we investigated treatment effects on social
dominance following a slightly modified protocol published by Strasser and
Schwabl (2004). Briefly, we established pairs of birds of similar body mass,
same age, not related and that had never interacted with one another before.
Since dominance was measured at two different age classes, nearly all birds were
tested twice, but with a different opponent. After a period of food deprivation
(one night and additional 6 h), a feeder with seeds was given and the behavior of
the birds was videotaped for 10 min. The behavior of the birds was analyzed
from videotapes while unaware of the treatments. We measured the latency to
gain access to the feeder for the first time, the time spent at the feeder and the
number of wins (the number of wins corresponds to the sum of (a) the number
of successful defenses of the food source when the other bird tried to gain access,
(b) the number of successful takeovers of the food source and (c) the number of
times winning in overt conflicts).
(e) Adult song
Mid January 2007, all males were separated and the light regime was
changed to 14:10 L:D. Five weeks after the change in light regime, we started
with song recordings using a Monacor ECM-2005 microphone and a Marantz
PMD 660 solid state recorder. To this end, males were individually placed in a
cage in a sound attenuated room along with a single female in the adjacent cage
with visual and acoustic contact. Song recordings were made for 1 h, after which
the female was placed in a cage on the opposite side of the room, still allowing
visual and acoustic contact. Recordings were restarted for another 1 h. This
procedure was repeated until at least 300 s of song had been recorded (Spencer
et al., 2005). We estimated the repertoire size of each male by determining the
total number of different syllable types within the first 300 s of recorded song
using Avisoft SAS-Lab Pro (Specht, Germany). We noted the number of A
syllables according to Vallet and Kreutzer (1998). Body mass and length of the
tarsus were measured for each male at the beginning of the song recordings.
(f) Reproduction
Thirty males (excluding same treatment brothers) were randomly mated with
untreated females (females mated with T-males weighed: 19.95± 0.43 g; females
mated with C-males weighed 20.27±0.44 g, t-test, p= 0.61). All pairs were
housed in separate breeding cages equipped with nest boxes and supplied with
nesting material. Nests were checked daily for new eggs and eggs were replaced
by dummy eggs as they were laid. Eggs were weighed to the nearest 0.01 g and the
number of eggs laid was recorded. After clutch completion, we also calculated the
total clutch mass as indicator of the total investment of a given female.
(g) Statistical analyses
Data were analysed in MLwiN 1.10.0006 by hierarchical linear models
(Bryk and Raudenbush, 1993). These models accommodate unbalanced data
and allow analyses of variances and co-variances, while taking the nested
relationships of related offspring into account. Parameters were removed
successively from the full model, starting with the least significant highest
interactions while the amount of data used in the compared models remained the
same. Only variables that contributed significantly (α 0.05) to the model were
retained. Significance was tested using the increase in deviance (Δdeviance)
when a factor was removed from the model, which follows a χ
2
-distribution.
Body mass during the nestling period was analyzed in a four-level model:
(i) pair (ij) clutch identity (ijk) individual offspring (ijkl) repeated measure. We
included age, the square of age and the cube of age as predictors in the model to
model the sigmoidal growth curve (see Eising et al., 2001; von Engelhardt et al.,
2006). Furthermore, the following variables/interactions were included: sex,
treatment, hatching order, hatching date (of the first chick), brood size, 1st/2nd,
age×treatment, age × sex, treatment × sex, age×treatment × sex. In all statistical
analyses presented below age, the square of age and the cube of age revealed
significant effects reflecting growth and therefore these statistics are not
presented. Singing activity was analyzed in a four-level model: (i) pair (ij) clutch
identity (ijk) individual offspring (ijkl) repeated measure. The following
variables/interactions were included: age, treatment, hatching order, hatching
date (of the first chick), brood size, 1st/2nd clutch, age × treatment. All other data
were analyzed in a three-level model: (i) pair (ij) clutch identity (ijk) individual
offspring/egg identity. Depending on the model different variables were
included. Models concerning asymptotic mass/tarsus length/male body mass
at later life stages: treatment, hatching order, hatching date (of the first chick),
brood size, 1st/2nd clutch. Models concerning age of first song/repertoire size/
song production rate/song bout duration: treatment, hatching order, hatching
date (of the first chick), brood size, 1st/2nd clutch, male body mass. Models
concerning egg mass/clutch size/clutch mass: treatment, hatching order,
hatching date (of the first chick), brood size, 1st/2nd clutch, female body
mass, repertoire size and song bout length.
Logistic growth curves were fitted individually for all males that survived till
fledging by least squares regression (SPSS 14.0) using the model: W =A / (1 +
e
k (t ti)
), in which W is body mass at a given age, A is asymptotic body mass
[g], k [d
1
] is the logistic growth constant, and t
i
is the point of inflection [d]
(Ricklefs, 1968).
Survival data were analyzed in a life-tables analysis using the Wilcoxon
(Gehan) test. Behavioral data had a cross-classified structure (related individuals
were tested in different paired dominance tests). These data were analysed using
paired statistics (SPSS 14.0), since multi-level logistic model analyses revealed
that there was no evidence that variance in any of the behavioral traits at the
family level was significantly different from zero.
The sex of chicks that did not fledge was only determined for chicks of the
first clutch. Therefore, all subsequent analyses including sex do not include
chicks of the second clutch that did not survive until fledging. Post-fledging,
sample sizes may vary due to mortality and are therefore indicated for each
measure.
We indicate below when we transformed data [log (Y + 1)] to obtain a
normal distribution or homogeneity of variance. Data are shown as mean± se of
the mean unless stated otherwise.
127W. Müller et al. / Hormones and Behavior 54 (2008) 125133
Page 3
Results
(a) Early growth and survival
There were no differences in clutch size (control 3.97 ± 0,16,
testosterone: 3.93 ± 0,14), egg mass (control: 1.72± 0.03,
testosterone: 1.75 ± 0.03) or hatching success between testoster-
one and control clutches (control: 56%, testosterone: 62%)
( p N 0.2 in all cases). Due to a strong infection with ectoparasitic
mites (Dermanyssus gallinae) that could not be eliminated
before the end of the breeding cycle, overall breeding success
was low (56% of all hatchlings survived until fledging).
Chicks of the second clutch grew better than chicks of the
first clutch (1st/2nd clutch: estimate = 0.57, error = 0.24, Δde-
viance = 5.48, p = 0.02). The re was a highly significant effect of
the three-way interaction betw een treatment, sex and age
(estimate 1.33, error 0.02, Δdeviance = 47.80, p b 0.0001),
indicating that the effects of elevated yolk testosterone were
different for the two sexes. In females, testosterone had a
positive e ffect on growth (treat ment × age: estimate = 0.04,
error = 0.01, Δdeviance = 7.06, pb 0. 01, 1st/2nd clutch: esti-
mate= 0.69, error= 0.34, Δdeviance= 3.43, p =0.06), while
testosterone had a significant negative effect on growth in
males (estimate 0.10, error 0.01, Δdeviance = 65.69,
p b 0.0001, 1st/2nd clutch: estimate = 0.82, error= 0.34, Δde-
viance = 5.61, p = 0.02) (Fig. 1). Since the focus of the following
experiments is on male offspring, we will henceforth focus on
males, while the data on females form part of a separate project
and will be discussed elsewhere (Müller et al. unpublished).
There was no difference in the survival pattern between
offspring from testosterone-treated eggs (henceforth T-birds,
T-males) and offspring from control-treated eggs (henceforth
C-birds, C-males) neither in the first (Wilcoxon (Gehan) statistic
1.55, p = 0.21) or second clutch (Wilcoxon (Gehan) statistic
0.46, p = 0.50). When considering only male offspring in the
survival analysis of the first clutch, testosterone did not affect the
pattern of male survival (Wilcoxon (Gehan) statistic 0.08,
p = 0.78).
(b) Asymptotic mass, body mass at later stages and tarsus length
Testosterone reduced growth (see above) and T-males
consequently reached a significant lower asymptotic body
mass (N = 39, T-males 17.89 ± 0.32 g, C-males 19.50± 0.25 g,
estimate = 1.59, error = 0.42, Δ deviance= 10.90, pb 0.001).
Body mass of all males was measured again in course of the
dominance tests (see below). T-males had not yet completely
caught up in terms of body mass when 3 months old (N = 38,
T-males 20.45 ± 0.55 g, C-males 21.17 ± 0.66 g, estimat e =
0.87, error = 0.46, Δdeviance = 3.01, p = 0.09), but there were
no more differences in body mass any more at 6 months of
age (N= 38, T-males 21.89 ± 0.55 g, C-males 22.55 ± 0.66 g,
estimate = 1.04, error= 0.84, Δdeviance = 1.19, p= 0.28).
At the start of the song recordings (N
=38), T- and C-
males s ignificantly differed in tarsus length (T-males: 17.81 ±
0.15 mm, C-males 18.36 ± 0.1 1 mm, estimate = 0.59, error = 0.19,
Δ deviance = 7.71, p = 0.005), but not in body mass (C-males
19.17 ± 0.41 g, T-males: 19.12 ± 0.47 g, estimate = 0.10, error = 0.66,
Δ deviance = 0.04, p= 0.84).
(c) Behavioral measures
There were no significant differences in body mass within the
pairs [paired t-test, 3 months (N=26): t=0.93, p= 0.37; 6 months
(N = 28): t =0.10, p = 0.92], because males were matched for
weight. At both time points there were no differences in the latency
to gain access to the feeder for the first time (3 months: T-males
48.54±39.24 s, C-males 75.08±34.74 s, Wilcoxon Signed Ranks
test, z =0.64, p=0.53; 6 months: T-males 63.15± 30.14 s, C-males
25.08 ± 15.15 s, log transformed, paired t-test, t = 0.29, p=0.78),
the time spent at the feeder (3 months: T-males 231.92 ± 44.32 s,
C-males 170.69± 45.70 s, 6 months: T-males 152.93±29.38 s,
C-males 137.29±30.70 s; paired t-test, p b 0.40 in both cases) or
the number of wins (3 months: T-males 12.23 ± 3.18, C-males
5.23±1.84, 6 months: T-males 9.36 ± 2.44, C-males 7.43±2.63,
log transformed, paired t-test, pN 0.35 in both cases; Fig. 2).
There were no significant differences in any of the traits
investigated if the analysis was restricted in a way that only one
member of each family was included (3 months: N = 16,
p N 0.17 in all cases, 6 months: N = 12, p N 0.20 in all cases).
(c) Song development
There was a significant difference in the age at whi ch the
juveniles started singing for the first time. T-males (75.30 ±
2.84 days) were on average later to start singing than C- males
(64.41 ± 2.11) (estimate = 10.89, error = 3.68, Δ deviance = 7.93,
p = 0.005). The time spent singing increased with age (age:
estimate = 0.10, error = 0.02, Δdeviance= 36.94, p b 0.001).
However this change in the time spent singing was different
for T-males compared to C-males (treatment × age: estimate =
0.56, error = 0 .02, Δdeviance = 6.85, p b 0.01). We subse-
quently subdivided the data into two age equal classes
[young juveniles: 125191 days old (first two month of
recordings) vs. old juveniles: 192258 days old (second two
month of recordings). There was a significant difference in the
Fig. 1. Testosterone significantly reduced male growth s.e) [filled circles:
control-eggs (injected with sesame oil); open circles: testosterone-eggs (injected
with testosterone dissolved in sesame oil)].
128 W. Müller et al. / Hormones and Behavior 54 (2008) 125133
Page 4
time spent singing between T- and C-birds when they were
young juveniles (treatment: estimate = 2.78, error = 0.74,
Δdeviance = 13.93, pb 0.001), but no difference in the time
spent singing could be observed between T- and C-birds when
they were old juveniles (treatment: estimate = 1.43,
error = 1.55, Δdeviance = 0.89, p = 0.35; Fig. 3).
(d) Adult song
Testosterone treatment did not affect repertoire size (C-males
21.33 ± 1.55 syllables, T-males 18.50 ± 1.10 syllables, esti-
mate = 2.47, error = 1.49, Δdeviance = 2.55, p = 0.11; Fig. 4).
There was a significant effect of the group an individual was
belonging to during the post-fledging period on the repert oire
size (Δdf = 9, Δdeviance = 19.92, p = 0.02).
The average length of a song bout did not differ between T-
and C-males (T-males 8.11 ± 0.89 s, C-males 7.97± 0.59 s,
estimate= 0.13; error=0.99, Δdeviance=0.01, p= 0.92). There
was also no difference in the time that was necessary to record
300 s of song, which may serve as a measure of song production
rate (T-males 7443.32±943.39 s, C-males 10620.87±2649.20 s,
log transformed, estimate = 0.10, error= 0.08, Δdeviance =
0.24, p = 0.62).
The incidence of A syllables was low (5 T-males and 4
C-males), and was therefore not further analyz ed.
(e) Reproduction
There was no difference in egg mass between females mated
with T-males compared to females mated with C-males (females
mated with T-males: 1.74± 0.04 g; females mated with C-males:
1.73±0.04 g; estimate= 0.04, error= 0.05, Δdeviance=0.55,
p = 0.46). Females mated with T-males laid larger clutches than
females mated with C-males (females mated with T-males: 4.50±
0.18; females mated with C-males: 3.77±0.20; log transformed,
estimate= 0.07, error = 0.02, Δdeviance=7.20, p = 0.01). Heavier
females laid larger clutches (log transformed, estimate=0.02,
error=0.01, Δdeviance = 5.79, p=0.02). The total clutch mass of
females mated with T-males was larger than the total clutch mass
of females mated with C-males (females mated with T-males:
7.87 ± 0.38 g; females mated with C-males: 6.90 ± 0.50 g;
estimate= 1.09, error= 0.33, Δdeviance=7.52, pb 0.01). The
total clutch mass was positively affected by female body mass
(estimate = 0.64, error = 0.15, Δdeviance= 10.98, p b 0.001).
There was no effect of repertoire size or song bout length on
any of the parameters (p N 0.20 in all cases).
Discussion
Early development
In several specie s including the canary it has been shown that
yolk testosterone enhances post natal growth (Schwabl, 1996,
reviewed by Gil, 2003; Groothuis et al., 2005a). We therefore
Fig. 3. The time spent singing (min, mean ± s.e) within 30 min of observation
was significantly lower in T-males during the first but not second age class.
Statistical tests were carried out on individual data points. Open circles male
offspring hatched from control-eggs (injected with sesame oil), filled circles
male offspring hatched from testosterone-treated eggs (injected with testoster-
one dissolved in sesame oil).
Fig. 4. Total syllable repertoire size for males hatched from control-eggs and
males hatched from eggs with elevated yolk testosterone concentrations. The
open circles show the mean ±s.e.
Fig. 2. The number of wins (sum of the number of successful defenses of the
food source, the number of successful takeovers of the food source and the
number wins in overt conflicts) during 10 min of observation. The birds were 3
and 6 months old. Test pairs are connected by lines.
129W. Müller et al. / Hormones and Behavior 54 (2008) 125133
Page 5
expected that our experimental elevation of yolk testosterone
levels would benefit growth of male offspring, the focus of this
study. However, we found that T-males grew slower, reached a
lower asymptotic body mass and had shorter tarsi as adult in
comparison to C-males (Fig. 1).
Since the consequences of maternal yolk androgens are
thought to depend on the post-hatching environment, differ-
ences in the environmental conditions, particularly the reported
infestation with ectoparasitic mites (D. gallinae) in our study,
may account for the different findings. T-males in our study may
have suffered more strongly from the ectoparasites, because
yolk androgens have been shown to reduce the chicks immune
response (e.g. Groothuis et al., 2005b; Müller et al., 2005a, but
see Tschirren et al., 2005). However, we did not find an overall
negative effect, but the elevation of the yolk testosterone
concentrations did have a sex-specific effect on growth. Male
offspring may have a lower immunocompetence as has been
shown for some bird species (e.g. Fargallo et al., 2002;
Tschirren et al., 2003), which could have rendered males more
vulnerable to any further reduction of the immune system by
yolk testosterone (e.g. Groothuis et al., 2005b, Müller et al.,
2005a, but see Tschirren et al., 2005). However, this remains
speculative since we did not measure any component of the
immune system. Alternatively, yolk testosterone may have sex-
specific effects in general, which is supported by a growing
number of recent studies showing that yolk androgens elevate
growth of female nestlings while inhibiting growth of male
nestlings (Müller et al., 2005b; von Engelhardt et al., 2006;
Rutkowska et al., 2007; Sockman et al., 2007, but see Saino
et al., 2006 for negative effects on growth of female offspring).
The proximate mechanism of male sensitivity towards high yolk
androgen concentrations is yet unknown (Sockman et al.,
2007). Independent of the proximate mechanism(s), the
negative effects of elevated yolk testosterone on growth are
likely relevant for the interpretation of long-lasting effects
mediated by yolk testosterone.
Long-lasting effects on male behavior
Previous studies have shown that maternal yolk androgens
correlate with the social rank of juvenile canaries (Schwabl,
1993), improve the success rate in a competition for a food
source (Strasser and Schwabl, 2 004) and enhance the frequency
of aggressive displays (Eising et al., 2006). There is thus
consistent evidence that yolk androgens modulate aggressive
behavior at different age classes post-fledging (between 1.5 and
10 months of age). However, here we did not find evidence for
improved competitive skills of T-males in an experimental
setting comparable to the study by Strasser and Schwabl (2004),
neither when meas ured at 3 or 6 months of age. T-males tended
to be lighter at 3 months of age, but it is unlikely that body mass
differences itself affected the outcome of the first behavioral
testing, since we matched opponents for body mass. Though,
T-males were still in a period of catch-up growth, and we cannot
exclude that associated physiological processes could have
affected the competitive skills. However, there were no dif-
ferences in body mass anymore when the birds were 6 months
old (second behavioral testing), indicating that by that time
catch-up growth was terminated. This render s the previous
explanation unlikely, since the outcome of the staged encounters
was similar at both times. Still, although of similar body mass,
T-males were skeletally smaller at both behavioral tests, which
may have hampered T-males to dominate the food source. Fur-
thermore, it is possible that T-males behaved differently under
developmental stress, with different priming effects on adult
behavior, if the long-lasting behavioral changes are a conse-
quence of activational effects at earlier age (Carere and
Balthazart, 2007).
Song development and adult song phenotype
T-males were on average about 10 days older when they were
observed singing for the first time. Initially they spent less time
singing, but within about 3 months time they had made up for
this difference ( Fig. 3). By the time that the birds were matured
and had crystallized their songs, there were no differences in
repertoire size (Fig. 4), song bout duration or singing activity
between T- and C-males.
Thus, while we did find long-lasting effects of yolk
testosterone on (the timing of) song development, we could
not find any evidence that yolk testosterone modified adult song
phenotype. As pointed out above, any long-lasting effect of yolk
testosterone is likely affected by the yolk testosterone mediated
growth inhibition during early development. Early develop-
mental stress as reflected e.g. in retarded growth has been
shown to negatively affect adult song phenotype and male
singing behavior (e.g. Nowicki et al., 2002; Buchanan et al.,
2003; Spencer et al., 2003 ; but see Gil et al., 2006). Adult song
phenotype has therefore been hypothesized to serve as an honest
indicator of male quality, in particular of the early develop-
mental history of an individual (the developmental stress
hypothesis, Nowicki et al., 1998). The delayed song develop-
ment in T-males may thus be interpreted as a consequence of the
yolk testosterone related growth retardation. However, the only
study investigating the effects of developmental stress on song
development reported an earlier onset of subsong of birds that
experienced a period of undernutrition (Nowicki et al., 2002).
As already indicated by the catch-up effect in singing
activity, T-males apparently compensated for initial differences
in song performance and we did not find differences in adult
song phenotype between T- and C-males, despite the negative
consequences of elevated yolk testosterone on growth. This
finding is intriguing and in contradiction with the develop-
mental stress hypothesis.
At the moment, we can only speculate
about the reason of our findings.
First, the developmental stress hypothesis may not apply,
which is unlikely given the number of studies finding such an
effect in a variety of species including canaries (e.g. Nowicki
et al., 2002; Buchanan et al., 2003, Spencer et al., 2003; Spencer
et al., 2005, but see Birkhead et al., 1999, Gil et al., 2006). Vocal
development actually continues during the juvenile period
including growth of brain structures underlying bird song (e.g.
Nottebohm, 1984; Bottjer, 2002) and is affected by the envi-
ronmental conditions (Spencer et al., 2003, 2004; Buchanan
130 W. Müller et al. / Hormones and Behavior 54 (2008) 125133
Page 6
et al., 2003). There is thus potential for modification of the adult
song phenotype during the juvenile perio d, and T-males may
have compensated during this period when conditions were
more favorable. However, if yolk testosterone reduces male
growth in general (see above), this would not necessarily mean
that these individuals suffered from developmental stress.
Second, it is unlikely that yolk testosterone in itself has a
negative effect on song phenotype (Garamszegi et al., 2007),
since a negative effect of yolk testosterone would have
reinforced possible effects of developmental stress. Such a
negative effect of yolk testosterone might be expected if yolk
testosterone increases adult testosterone production or sensitiv-
ity (Groothuis et al., 2005a; Carere and Balthazart, 2007), which
could then again cause a premature crystallization (Whaling
et al., 1995; Titus et al., 1997). However, canaries were an
outlier in the analysis by Garamszegi and colleagues (2007).
This suggests that canaries are able to maintai n a high repertoire
size although being exposed to high yolk androgen concentra-
tions in contrast to all other bird species. Further studies on the
effects of yolk androgens on adult song phenotype on other bird
species are therefore needed.
Third, it is possible that yolk testosterone in itself may have
positive effects on adult song phenotype, but that those effects
are offset by the negative effects of early developmental stress.
The consequences of yolk testosterone would then depend on
the environmental conditions post-hatching or the (genetic)
quality of the offspring. In case of the latter, only offspring of
attractive males that are inheriting good paternal genes would be
able to withstand high yolk testosterone concentrations (Gil
et al., 1999). This would explain as to why females deposit
higher concentrations of yolk androgens if mated with attractive
males (e.g. Gil et al., 1999, 2004 but see also Marshall et al.,
2005). Studies simultaneously manipulating yolk testosterone
exposure and genetic/en vironmental quality are necessary in
order to test this hypothesis.
Long-lasting effects on reproductive success
Females should adjust the level of investment to the expected
reproductive value of their offspring, since any parental
investment to increase the fitness of current offspring evokes
costs in terms of parental future survival and reproduction
(Trivers, 1972; Stearns, 1992). One potential indicator for
offspring quality is the attractiveness of the mate (Andersson,
1994) and females mated to attractive males might increase their
parental effort either to improve the chances of retaining the mate
or because the young are more valuable (the differential
allocation hypothesis, Burley, 1986; Sheldon, 2000). Thus our
finding suggests that females mated with T-males invest relatively
more in their clutch indicates that females assess T-males as more
attractive than C-males. The reproductive decisions of the females
also indicate that T-males were not disadvantaged by the
developmental stress they experienced (Blount et al., 2003 but
see De Kogel and Prijs, 1996). T-males were apparently able to
compensate for developmental stress, although such compensa-
tion may come at a cost (Birkhead et al., 1999; Blount et al.,
2003). However, the fact that females invested relatively more
when mated with T-males may also be interpreted as maternal
compensation for a lower mate quality and thus offspring viability
(e.g. Bluhm and Gowaty, 2004; Gowaty et al., 2007), since
females were not allowed to choose their mates. In that case,
females may have based their decision e.g. on the structural size as
a possible indicator of the developmental stress their mate has
experienced.
Besides that, we do not have any information about the
decisive modification of a (sexual) character b y yolk testoster-
one that determined the female's investment. Previous studies
have shown that song stimulates female nesting and egg laying
in canaries (Kroodsma, 1976) and that females exposed to
specific features (A syllables) of canary song produce larger
eggs (Leitner et al., 2006). We therefore hypothesized that any
changes in male reproductive success would be mediated by the
effects of yolk testosterone on male song quality, which was not
the case.
Acknowledgments
We thank Peter Scheys and Geert Eens for their assistance
with taking care of the animals. This study was supported by a
postdoctoral grant (1.5.033.07 to WM) and a research project
(G.0130.07 to ME) from FWO Flanders Belgium. We thank
Nikolaus von Engelhardt and the referees for their suggestions.
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  • Source
    • "Quails selected for a higher maternal testosterone deposition therefore appear to have an advantage of an increased growth rate, with no effect seen for unfavourable environmental conditions. Growth effects of experimentally elevated egg testosterone were repeatedly demonstrated in birds (Schwabl, 1996; Pilz et al., 2004; Müller et al., 2008; Muriel et al., 2013), but these studies provide ambiguous results and only a few of them were performed under suboptimal environmental conditions. Quail from the HET line displayed higher body weight than the LET line in an age-dependent manner. "
    [Show abstract] [Hide abstract] ABSTRACT: Yolk testosterone concentrations vary in response to environmental conditions and different testosterone contents can subsequently modify the phenotypic traits of offspring. Apart from effects on growth, proactive behaviour and secondary sexual characteristics, possible negative impacts of maternal testosterone on the immune system are often considered a limitation for its deposition. Effects of maternal testosterone can be modulated by postnatal environmental conditions, such as the availability of food resources. However, the majority of studies considering the effects of maternal testosterone on the immune system have been conducted under optimum conditions. In our study we evaluated the influence of genetic selection for high (HET) and low (LET) egg testosterone content in Japanese quail on immune responsiveness of offspring to phytohaemagglutinin (PHA) and lipopolysaccharide (LPS) stimulation under severe protein restriction. Protein restriction negatively influenced body weight and performance in the PHA-test. We observed an increase in Cort (corticosterone) and He/Ly (heterophil/lymphocyte ratio) after LPS, while no changes occurred in total IgY levels in the protein-restricted group. HET quails showed higher body mass and total IgY levels and lower He/Ly ratio than LET quails, while the PHA index and Cort concentration did not differ between lines. No interactions were found between protein restriction and genetic line. In conclusion, the immune response was not compromised under conditions of severe protein restriction in the faster growing HET line compared with the LET line. We hypothesise that the immune responsiveness of birds with higher yolk testosterone may be linked with other maternally-derived substances in a context-dependent manner.
    Full-text · Article · Nov 2014 · Comparative Biochemistry and Physiology - Part A Molecular & Integrative Physiology
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    • "However, the only two experimental studies examining the effect of maternally derived testosterone on the development of their offspring song in canaries and starlings provided complex and nonsignificant results (Müller et al. 2008; Müller and Eens 2009). In the blood, circulating egg hormone concentrations, moreover, did not seem to pass to the egg yolk (Marshall et al. "
    [Show abstract] [Hide abstract] ABSTRACT: Maternal investment can play an important role for offspring fitness, especially in birds, as females have to provide their eggs with all the necessary nutrients for the development of the embryo. It is known that this type of maternal investment can be influenced by the quality of the male partner. In this study, we first verify that male song is important in the mate choice of female Eurasian reed warblers, as males mate faster when their singing is more complex. Furthermore, female egg investment varies in relation to male song characteristics. Interestingly, clutch size, egg weight, or size, which can be considered as an high-cost investment, is not influenced by male song characteristics, whereas comparably low-cost investment types like investment into diverse egg components are adjusted to male song characteristics. In line with this, our results suggest that female allocation rules depend on investment type as well as song characteristics. For example, egg white lysozyme is positively correlated with male song complexity. In contrast, a negative correlation exists between-song speed and syllable repetitiveness and egg yolk weight as well as egg yolk testosterone concentration. Thus, our results suggest that female egg investment is related to male song performance in several aspects, but female investment patterns regarding various egg compounds are not simply correlated.
    Full-text · Article · Apr 2014 · Ecology and Evolution
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    • "Indeed, long-term studies showed that egg androgens affected male morphological and secondary sexual traits (Strasser & Schwabl 2004; Eising et al. 2006; Rubolini et al. 2006; Riedstra et al. 2013), female reproduction (Rubolini et al. 2007), as well as socio-sexual behaviour (Strasser & Schwabl 2004; Eising et al. 2006; Partecke & Schwabl 2008; Bonisoli- Alquati et al. 2011a; Schweitzer et al. 2013) and personality traits (Tobler & Sandell 2007; Ruuskanen & Laaksonen 2010). These effects, however, were often inconsistent across studies and species (M€ uller et al. 2008; M€ uller & Eens 2009; Bonisoli-Alquati et al. 2011b; Ruuskanen et al. 2012). "
    [Show abstract] [Hide abstract] ABSTRACT: Studies of avian species have shown that maternal effects mediated by the transfer of egg hormones can profoundly affect offspring phenotype and fitness. We previously demonstrated that the injection of a physiological amount of testosterone (T) in the eggs of ring-necked pheasants (Phasianus colchicus) disrupted the covariation among male morphological traits at sexual maturity and positively affected male mating success. Here, we investigate whether egg T exposure affected adult male circulating T levels at the onset of the breeding season (reflecting gonadal maturation), and the relationship between circulating T and male traits. Egg T exposure did not affect pre-mating plasma T. T levels were not associated with the expression of secondary sexual and non-sexual traits or socio-sexual behaviour (social rank, overall fighting ability and mating success). However, wattle brightness decreased with increasing circulating T in males hatched from T-eggs (T-males) but not among control males. In dyadic encounters during the peak mating period, control males with higher pre-mating T levels had higher chances of being dominant over other control males. However, higher pre-mating T levels did not predict success in male-male competition in encounters involving T-males. We suggest that the long-term effects of egg T on male phenotype do not originate from differential gonadal maturation according to egg T treatment. Rather, prenatal androgens may have priming effects on functioning of target tissues, translating into differential phenotypic effects according to androgen exposure during embryonic development.
    Full-text · Article · Jan 2014 · Ethology
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