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Environment Modifies the Testosterone Levels of a
Female Bird and Its Eggs
Rockefeller University, Field Research Center for Ecology and Ethology,
Millbrook, New York 12545
Past studies have shown that the yolk of the canary (Serinus canaria) egg contains maternal testosterone, that its concentrations increase in the subsequently formed eggs of a
clutch, and that testosterone influences development. The present study investigated 1)if the
testosterone levels vary in the female during yolk formation; 2) how such putative variations may
be related to the concentrations of maternal testosterone in the yolk; and 3) if environmental
factors, such as day length, can modify the testosterone levels in the mother and her eggs. Maternal testosterone levels, measured in the females' feces, increased during yolk formation and egg
laying, and decreased during incubation. This pattern was modified by day length. In a photoperiod of 12 h of light and 12 h of darkness (12L 12D), female testosterone levels decreased after the
last egg of the clutch was laid while in a photoperiod of 16L 8D, they decreased after the first egg
was laid. These different patterns were reflected in the testosterone concentrations in the egg
yolk. Further, the eggs of subsequent clutches that were produced under a naturally changing
photoperiod differed significantly in their testosterone concentrations. Finally, the doses of testosterone in the yolk of individual eggs were positively correlated with the concentrations of testosterone in the female during the yolk phase of each egg. I conclude that here we have a mechanism
which communicates environmental conditions from the mother to the offspring, and that this
mechanism serves to optimize reproduction andor modify offspring traits. @ 1996 Wiley-Liss, Inc.
The yolk of vertebrate eggs contains maternal
hormones and growth factors which influence development (e.g., de Pablo et al., '82; Brown et al.,
'88; Scavo et al., '89; Dickhoff et al., '90; Schreck
et al., '91; Sechman and Bobek, '88; Adkins-Regan
et al., '95). The yolk of the canary contains the
ovarian sex steroid hormone testosterone in increasing doses in each subsequently laid egg of a
clutch (Schwabl, '93). These differential doses of
maternal testosterone in the eggs of a clutch influence the growth of the hatchlings (Schwabl,
'96). Moreover, the aggressiveness of the fully
grown offspring is positively correlated with the
doses of maternal testosterone in the eggs (Schwabl,
'93; unpublished results). Two hypotheses emerged
from these observations: 1) female birds can enhance their reproductive fitness by hormonal influences on sibling competition and growth (Winckler,
'93; Schwabl, '96); and 2) the maternal hormones
of birds can permanently alter the phenotype of
the offspring (Schwabl, '93, '96) in a way that is
analogous to how hormones transferred in utero
between littermates in mammals affect development (Clark and Galef, '95). The functions for optimal reproduction and adaptation to a stochastic
environment imply that the contents of maternal
hormones in the eggs vary with maternal and/or
environmental conditions. The present study
probed for such environmental influences on the
testosterone levels in the mother and the egg yolk.
The major sources of sex steroid hormones, including testosterone, in female birds are the theca and granulosa cell layers that surround the
ovarian follicles. The production of testosterone
by these cells changes as follicles are recruited
into the follicular hierarchy and sequester yolk
(e.g., Bahr et al., '83; Etches and Duke, '84;Porter et al., '89) and this is reflected in the circulating levels of ovarian hormones in the blood (e.g.,
Shahabi et al., '75; Johnson and van Tienhoven,
'SO). While the secretion of ovarian steroid hormones is well studied with regard to the regulation of vitellogenesis, ovulation, egg laying, and
behavior (e.g., Gilbert, '71; Schwabl, '921, it has
not been studied with regard t o the possibility of
transfer of these hormones to the egg. The different doses of testosterone in the yolk of the eggs
may reflect either the androgenic activity of all
Received March 4, 1996; accepted May 3, 1996.
Address reprint requests to Hubert Schwabl, Department of Zoology, Washington State University, Pullman, WA 99164-4236.
ovarian follicles or the androgenic activity of each
individual follicle. To partly differentiate between
these possibilities and to test the prediction derived from the above-presented hypotheses the
present study investig,ated 1)how the testosterone levels of female canaries change during the
yolk phases of the subsequently formed eggs of a
clutch; 2) if such changes are reflected in the concentrations of testosterone in the yolk; and 3) if
the testosterone levels in the female and her eggs
are influenced by environmental conditions, in this
case photoperiod.
Answering these questions required daily measurements of the hormone concentrations in the
same female during egg formation and laying.
Therefore, I monitored female testosterone levels
non-invasively by the analysis of the concentrations in their feces. Previous studies with Japanese
quail Coturnixjaponzca (Bishop and Hall, '91) and
domestic fowl Gallus domesticus (Cockrem and
Rounce, '94) have showin that the testosterone concentrations in the feces correlate with the concentrations in the blood.
Birds and breeding conditions
Subjects were Water xhlager canaries from the
stock at the Rockefeller University Field Research
Breeding under constant photoperiodic
The breeding pairs used in this study had
hatched in spring 1993. They had experienced the
photoperiod of Millbrook, NY (42"N), until the beginning of the experiment. In October 1994 these
birds were transferred t o a day length of 8 h of
light and 16 h of darkness (8L 16D). Females were
individually housed in breeding cages (46 x 26 x
23 cm), while males were kept in groups of 6 in
flight cages (62 x 38 x 52 cm). After 6 weeks pairs
were formed by introducing a male t o each female.
Twelve pairs were then exposed to a photoperiod
of 12L 12D and 12 pairs to one of 16L 8D. Birds
were provided with fresh food and water daily as
described previously (Schwabl, '93).
Breeding under natural photoperiodic
Here birds experienced the naturally changing
day length of Millbrook, NY,and were paired in
March, Housing conditions were as described earlier (Schwabl, '96).
Collection and preparation of fecal samples
After exposure to long days droppings were collected daily from each female 1-2 h after the lights
were turned on. For collection of fecal material
the male and the female of a pair were separated
by the insertion of a wire partitioning into the
cage for 10-30 min. One to three droppings were
then scraped from clean paper at the bottom of
the cage that had been placed there after separation of the pair partners. Droppings were dried at
room temperature for 24 h and weighed. The remaining procedure of measuring the concentrations of "free," unconjugated testosterone in the
feces followed the protocol of Bishop and Hall ('91).
Validation of testosterone
measurements in feces
The validation of this protocol for measurements
of free testosterone in the feces of female canaries included the following steps.
Three fecal samples (diluted 1:60 with phosphate-buffered saline, w:v) that were serially diluted with phosphate-buffered saline yielded
displacement curves that were parallel t o the
serial dilution of the testosterone standard (Fig.
1). The antiserum (Wien Laboratories, Inc.,
Succa-Sunna, New Jersey) that was used in the
radioimmunoassays cross-reacts to 55% with 5adihydrotestosterone and may also cross-react with
other steroid hormone metabolites in the feces.
To test if the testosterone immunoreactivity that
is measured in a buffer solution of feces without
extraction and purification of steroids reflects testosterone, 12 fecal samples were treated as follows: 20 pl of fecal buffer solution was subjected
to hydrolysis following the protocol of Payne and
Talahay ('86). After hydrolysis with a mixture
of P-glucuronidase and sulfatase from Helix
pomatia (Boehringer-Mannheim Biochemicals,
Indianapolis, IN) for 18 h steroids were extracted with 3 x 3 ml of diethylether-petroleum
ether (1:l) using Extrelut minicolumns. Extracts were dried under a stream of nitrogen
and steroids were separated and partially purified on diatomaceous earth chromatographic
columns a s described earlier for blood samples
(Schwabl, '92, '93). The fraction containing testosterone was then subjected t o a testosterone
radioimmunoassay. The concentrations of immunoreactive testosterone that were measured in
the unextracted fecal buffer solutions were
Sample volume (PI)
80 -
B/Bo (“A)
Testosterone (pgltube)
Fig. 1. Displacement curves of serially diluted fecal samples from three female canaries
and testosterone standard in the testosterone radioimmunoassay.
is present in the feces in “free” form 100 pl of
fecal buffer solutions of the same samples was
extracted with 3 x 3 ml of diethylethedpetroleum ether (1:l).The dried organic extracts
were purified on diatomaceous earth chromatographic columns and subjected to testosterone
assay. The remaining buffer solution from which
steroids had been extracted was then hy5000
drolyzed, extracted as described above, the expco.01
tract purified, and assayed for testosterone. The
comparison of the concentrations measured before and after hydrolysis showed that 95% of
the testosterone is present in the buffer solution in conjugated form. “Free” and conjugated
testosterone concentrations were positively correlated (r = 0.70, n = 13, P < 0.01). The concentrations of testosterone in the buffer solution
were positively correlated with the concentrations
of conjugated (r = 0.79, n = 13, P < 0.01; data not
shown) and free testosterone (r = 0.56, n = 13, P
c 0.05; data not shown). Thus the concentrations
7500 of testosterone that are measured in unextracted
Total testosterone (pglml)
feces provide a good estimate of the total test(hydrolysis-extraction-chromatography)
osterone levels in the female.
strongly correlated with the concentrations of testosterone measured after hydrolysis, organic extraction, and chromatographic separation from
5a-dihydrotestosterone and other metabolites
(Fig. 2).
To investigate the fraction of testosterone that
. e/l
Fig. 2. Correlation of the immunoreactive (ir) testosterone concentrations measured in a phosphate buffer extract
of the feces with the testosterone concentrations measured
after hydrolysis, organic extraction, and separation of steroids by chromatography.
All samples were measured in a single assay
and the intra-assay variation was 7%.
lkstosterone concentrations in the egg yolk
Constant photoperiods
Eggs were collected and replaced with dummy
eggs at the day they were laid. The yolk was separated from the albumin, weighed, and frozen at 20°C. The testosterone concentrations in the yolk
were assayed in 10-20 mg of yolk. All samples
were analyzed in a single assay.
A) 12L 12D (n=5)
Natural photoperiod
Yolk samples were obtained by biopsy from
freshly laid eggs of first clutches (laid in March
1994) and third or fourth clutches (laid in May)
as described earlier (Schwabl, '93). The yolk
samples were weighed, suspended in 0.5 ml distilled water, and frozen at -20°C.
The extraction and measurement of testosterone followed the previously published protocol
(Schwabl, '93).
8 ) 16L 8D (n=5)
Data were analyzed by analysis of variance
(ANOVA)for repeated rneasurements with the levels of significance for posthoc pair comparisons
set a t P = 0.05.
Maternal testosterone levels
during yolk formation
In both photoperiodic regimens female testosterone levels varied significantly during vitellogenesis, egg laying, and inleubation [12L 12D: F(7,28)
= 2.82, P = 0.024; 16Li 8D: F(7,26) = 13.32, P <
0.00011. In 12L 12D female testosterone levels increased significantly 1day before the first egg was
laid. These levels were about twice as high as 4
days before the onset of laying. Levels remained
high until the third of four eggs was laid and incubation started. During incubation testosterone
levels declined to levels that were lower than those
prior t o the laying (Fig. 3A). This pattern was different in females which laid in a photoperiod of
16L 8D. Here there waij a single peak of testosterone on the day when tbe first egg was laid. Testosterone levels dropped sharply with the second
laid egg and continued t o decrease during incubation which began with the second egg. Levels
during incubation were significantly lower than
during the prelaying phase (Fig. 3B).
Days from first laid egg
Fig. 3. Changes of immunoreactive (ir) testosterone concentrations (means with 1 S.E.M.) in female canaries during
egg formation, laying (day 0 = first egg laid), and incubation.
A: Females kept in a photoperiod of 12L 12D. B: Females
kept in a photoperiod of 16L 8D. Four growing follicles (FlF4) are sketched into each graph t o indicate the phases of
yolk deposition and ovulation. Asterisks indicate significant
differences between two adjacent values (P< 0.05, two-tailed
paired t-tests).
quently laid eggs of a clutch contained increasing
doses of maternal testosterone (Fig. 4A). The dosages of testosterone and the pattern of increase
from egg to egg appeared to be influenced by photoperiod although the differences were not significantly different, probably due to the small sample
sizes. First eggs of clutches that were produced
in 12L 12D seemed t o contain more testosterone
than first eggs that were produced in 16L 8D.
Moreover, in 12L 12D the yolk testosterone contents tended to continue to increase up to the
fourth egg, while in 16L 8D there appeared to be
Yolk testosterone concentrations
no further increase from the third to the fourth
As reported earlier for eggs that were laid in a egg. These overall patterns of the testosterone conphotoperiod of 14L 101) (Schwabl, '93) the subse- tents of subsequently laid eggs reflect the differ-
T i
Correlation of the yolk testosterone
concentrations with the testosterone levels in
the female during vitellogenesis
The relationship between the testosterone levels in the mother and in the eggs was further
explored by correlating the concentrations in individual yolks with the levels of the female during vitellogenesis of each egg. It was assumed 1)
that the major portion of the yolk of each egg was
sequestered during the last 72 h before the egg
was ovulated (Romanoff and Romanoff, '49; Warren and Conrad, '39) and 2) that ovulation occurred 24 h before the egg was laid (Warren and
Scott, '34). Pilot work (Schwabl, unpublished results) investigating "yolk rings," which can be used
t o estimate the duration of yolk deposition in an
egg (Grau, '76; Meathrel, '91), supports the former
assumption. The results show that the testosterone concentrations in the yolk are positively correlated with the mean testosterone levels in the
female during yolk deposition (Fig. 5).
Laying order
Fig. 4. Testosterone concentrations (means with 1S.E.M.)
in the yolk of eggs that were produced (A) in constant photoperiods of 12L 12D or 16L 8D and (B) during different times
of the year in a naturally changing photoperiod of 42"N. Asterisks indicate significant differences in the testosterone contents among the eggs of a clutch (P< 0.05, two-tailed paired
This study reports four major findings: 1)The
testosterone levels of female canaries increase during vitellogenesis and egg laying and decrease during incubation. 2) This pattern is influenced by
photoperiod. 3) The Concentrations of testosterone
in the eggs vary also with photoperiod and change
with the progress of the breeding season. 4) The
testosterone concentrations in the egg yolk are
16L 8D(n=4)
140- 0 12L12D(n=3)
.. .
100ent duration of elevated female testosterone levels in the two photoperiodic conditions.
80 In naturally changing photoperiod conditions
the eggs of first clutches, laid in March when phoa
60 0
toperiod was approximately 12L 12D, had significantly higher testosterone contents than the eggs
of third or fourth clutches, laid in May when photoperiod was approximately 15L 9D [F(1,21) =
8.36, P = 0.0231. While there was variation among
0 . 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0
the eggs of the March clutches [F(3,16) = 2.79, P
= 0.0741, there was no indication for variation in
Maternal irTestosterone 1 :60 (ng/ml)
the May clutches [F(3,12) = 1.023, P = 0.4171.
Third and fourth eggs of the March clutches had
5. Correlation of the testosterone concentrations in
significantly higher testosterone levels than first theFig.
yolk of individual eggs with the levels of testosterone in
egg. Such an increase was absent in the May the female during the putative yolk phase of each egg. rs:
clutches (Fig. 4B).
Spearman rank correlation coefficient.
positively correlated with the testosterone concentrations in the female during vitellogenesis. These
results clearly show that environmental factors
influence the testosterone levels of the egg-laying
female and her eggs.
As four to five follicles are recruited into the
follicular hierarchy and they grow by the incorporation of yolk the testlosterone production of the
steroidogenic cells of tlhe follicular walls changes
(e.g., Bahr et al., '83; Etches and Duke, '84). These
changes in steroidogenic activity of the ovary
which are reflected in the blood levels of the hormones have been studied extensively with regard
to the control of the follicular hierarchy, vitellogenesis, ovulation, egg laying, and behavior (Gilbert, '71). The results presented here show that
the production of testosterone is modified by photoperiod. Apparently vi tellogenesis, ovulation, and
laying can successfully proceed despite such differences in the testostei~onelevels, suggesting that
testosterone is only loosely associated with the control of these processes. The differences in female
plasma levels of testosterone during egg formation
among avian species (e.g., Hector et al., '86a,b;
Donham, '79; Fowler et al., '94; Hannon and
Wingfield, '90; Johnson and Van Tienhoven, '801,
and more importantly, within species when they produce multiple clutches in a season (e.g., Hegner and
Wingfield, '86; Windield, '85; Schwabl et al., '80;
Licht et al., '79; McPheieson et al., ,821, suggest the
same. One conclusion tlhat emerges from these observations is that, instead of being intimately involved in the control of reproductive functions,
testosterone may be associated with behavioral responses to variable environmental conditions. This
could be similar to the social control of the testosterone levels in males (Wingfield et al., '90).
The results presented here, together with the previously published work (Schwabl, '93, '961, suggest,
however, yet another, new possibility: testosterone
and other hormones may convey to the offspring
information that is perceived by the mother. The
results of the present study are consistent with two
predictions from this hypothesis: 1) the maternal
testosterone levels vary with environmental conditions; and 2) this varia1;ion is reflected in the testosterone contents of the eggs. This new fundion of
maternal steroid hormones as communicators between the mother and the egg is not at odds with
their well-known roles in ovarian physiology. In fact,
the dissociation of steroid production by the two steroidogenic cell layers which compose the follicular
walls during follicular growth may reflect these different functions (e.g., Nitta et al., '93; Etches and
Duke, '84). The outer theca cells, which are in intimate contact with the mother's bloodstream, might
be the principal source of steroids that affect the
mother, while the inner granulosa cells, which are
not vascularized and are closer to the yolk, might
be the source of steroids, which via the yolk affect
the offspring. Further experiments are necessary
to test this idea.
The adaptive significance of environmentally
modified transmission of maternal hormones to the
offspring may come &om two mutually not exclusive effects. First, seasonal differences of the concentrations of maternal hormones in the eggs,
caused by changing day length, may influence developmental rates in offspring born at various times
during the breeding season. Moreover, they may
cause individual differences in life history strategies (e.g., Adriaensen, '86; Smith and Nilsson, '87;
Clark and Galef, '95; Gross, '96). Whether other
environmental factors, such as population density,
degree of competition for resources, and male courtship behavior can also influence the transmission
of maternal hormones into the egg is currently under study. Second, the variation among clutches in
the doses and pattern of testosterone may allow females to optimize reproduction by favoring individual offspring in a brood (Schwabl, '96; Schwabl
et al., manuscript submitted).
In summary, I conclude that testosterone is produced by females to modify, in an epigenetic way,
offspring characteristics in response to environmental conditions. Further studies, ideally with
animals in their natural environment, are necessary to probe the proposed adaptive functions and
evolutionary significance of such a new role of hormones (Bern, '90; Schreck et al., '91), in this case
ovarian sex steroids, as communicators between
This work was supported by NIMH grant MH
49877 and a grant from the Harry Frank Guggenheim Foundation. I thank Fernando Nottebohm
for his support during this study.
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