Top-down regression of the avian oviduct during late oviposition in a small passerine bird
Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, V5A 1S6, Canada
* Author for correspondence (e-mail: tdwillia{at}sfu.ca)
Accepted 3 October 2003
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Summary |
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Key words: cost of egg production, oviduct, organ size-function relationship, maternal effect, Taeniopygia guttata
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Introduction |
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Recent studies have suggested that the oviduct might have high energy costs
for growth and/or maintenance, contributing substantially to the energetic
cost of reproduction. For example, in breeding European starlings Sturnus
vulgaris egg production was associated with a 22% increase in resting
metabolic rate (RMR; Vézina and
Williams, 2002; see also
Nilsson and Raberg, 2001
), and
oviduct mass was the only organ that explained variation in RMR among laying
females (Vézina and Williams,
2003
). Similarly, in house sparrows Passer domesticus,
Chappell et al. (1999
) found
that basal metabolic rate (BMR) was positively correlated with combined dry
ovary and oviduct mass. While these studies suggest potential `costs' to
individuals with large oviducts, Christians and Williams
(1999
) reported a positive
relationship between albumen protein content of eggs and oviduct mass, i.e.
individuals with larger oviducts might benefit in being able to produce higher
quality eggs (Williams, 1994
).
Given these identifiable costs and benefits, this predicts that oviduct size
should be tightly coupled to the functional demands of this organ
(sensu Diamond and Hammond,
1992
). In support of this idea, Vézina and Williams
(2003
) found that total
oviduct mass decreased by 47% immediately following ovulation of the last
ovarian follicle even though an oviductal egg was still present at this point
(though they did not identify which component(s) of the oviduct accounted for
this decrease in mass).
The oviduct of oviparous vertebrates is a highly differentiated organ, with
five anatomically and functionally distinct regions
(King and McLelland, 1984;
Palmer and Guillette, 1988
).
In poultry, an egg takes approx. 25 h to pass down the entire length of the
oviduct, but spends most time (approx. 20 h) in the distal shell gland and
relatively little time in the proximal magnum and isthmus regions where
albumen and shell membrane formation occur
(Solomon, 1983
;
Bakst, 1998
). Here, in zebra
finches Taeniopygia guttata, we demonstrate that the oviduct does
have a highly regulated size-function relationship. Specifically, this linear
organ regresses very rapidly at the end of egg-laying from the top down as
soon as the more proximal regions have completed their function but while the
distal regions are still functional. This would minimize the time that the
different components of this organ are maintained in a functional state, and
thus reduce the energy cost of maintaining the complete oviduct.
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Materials and methods |
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Experimental treatments
Birds were assigned to breeding pairs randomly and all males and females
used in this experiment had bred previously. Nest boxes were checked daily
between 09:00 h and 11:00 h and any newly laid eggs were weighed
(±0.001 g) and numbered. Laying females were collected for body
composition analysis between 07:00 h and 07.15 h on the day after laying a
specific number of eggs. Laying females were killed by exsanguination under
anaesthetic (Rompun/Ketamine, 1:1 v/v), the oviduct was dissected out, and the
oviductal egg removed. We chose this collection time because 95% of eggs are
laid within 2 h of lights on in zebra finches
(Christians and Williams, 2001)
with ovulation occurring 30-45 min after oviposition
(Etches, 1996
). Thus, birds
ovipositing on the day of collection had an almost fully formed oviductal egg
in the distal shell gland region. This allowed us to dissect out the oviductal
egg without the risk of confounding oviduct mass by the presence of lumenal
albumen from developing eggs. Although intra-cellular albumen content in the
oviduct might have varied with time of day, since all birds were collected at
the same time, and given the short time window of oviposition, this would not
confound our subsequent analyses. Females were then categorized into different
stages of ovarian (follicle) development, based on the number of yolky
follicles in their ovary and the presence of an oviductal egg: (1) 1-egg birds
(N=10) that had laid only their first egg and had a full follicle
hierarchy of >3 follicles; (2) birds with 2-3 remaining yolky follicles
that had laid 3+ eggs (mean=3.8±0.8) and had an oviductal egg
(N=9); (3) birds with only one remaining yolky follicle that had laid
3+ eggs (mean=3.9±0.3) and had an oviductal egg (N=13); (4)
birds with no remaining yolky follicles that had laid 4+ eggs
(mean=4.3±0.5) and still had an oviductal egg (N=15); and (5)
birds at clutch completion with no yolky follicles and no oviductal egg
(N=8; mean clutch size 4.8±0.9). All females were weighed
(±0.1 g) at pairing, at the 1-egg stage and/or on the day they were
collected. In addition we collected the first and last egg that each female
laid for analysis of egg composition (first eggs were replaced with `dummy'
eggs to maintain clutch size). Eggs were boiled for 1-2 min and frozen at
-20°C until further analysis. Subsequently each egg was separated into
shell, albumen and yolk, each component was dried to constant weight at
60°C and weighed (±0.001 g).
Oviduct analysis
We divided the oviduct into three sections based on King and McLelland
(1984): (a)
infundibulum/magnum: we pooled these sections since the junction between the
infundibulum and magnum was not easily discernable, and the infundibulum on
average represented only 6.9±0.6% of the combined mass; (b) isthmus: we
separated the proximal end of the isthmus from the magnum at the sharply
distinguished translucent band of tissue, and the distal end of the isthmus
from the uterus at the `red region'; and (c) shell gland (uterus)/vagina. Each
section was subsequently dried to constant mass at 60°C and weighed again
(±0.001 g). We report data for dry oviduct mass throughout: we did not
lipid-extract oviduct tissue because this contains a negligible amount of
lipid (e.g. 3.9%, F. Vézina, unpublished data; see also Houston et al.,
1995).
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Results |
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Total dry oviduct mass varied with stage of ovarian development (F5,54=31.9, P<0.001, controlling for body mass; Fig. 1). Oviduct mass did not differ between birds at the 1-egg stage (with a full follicle hierarchy) and late-laying birds that had ovulated 3-5 follicles and had only one yolky follicle remaining (153±8 vs. 167±7 mg; P>0.90). However, oviduct mass then decreased by 44%, to 94±6 mg in birds with no remaining yolky follicles but still with an oviductal egg (P<0.001), and then decreased further to 55±10 mg in birds with no oviductal egg, i.e. in birds at clutch completion (P<0.01).
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This reduction in oviduct dry mass over the cycle of ovarian development occurred unequally among the different regions of the oviduct (Fig. 2). The mass of the proximal infundibulum/magnum regions and the isthmus region decreased by 56% and 38%, respectively, when birds with one yolky follicle were compared with those with no yolky follicles and only an oviductal egg (Fig. 2A,B; P<0.001 in both cases). In contrast, there was no change in mass of the shell gland/vagina at this stage (paired contrast, P>0.90). Rather, shell gland/vagina mass only decreased (by 34%) 24 h later, after the last egg had been laid, i.e. in birds at clutch completion with no oviductal egg (Fig. 2C; P0.001). Thus, regression of the oviduct was initiated first, and occurred most rapidly, in the proximal regions of the organ, but was delayed in the distal section until after the last oviposition. As a consequence, the relative morphology of this organ changed with stage of ovarian development. As laying progressed the relative contribution of the infundibulum/magnum regions decreased from 66.6±7.1% of total oviduct mass at the 1-egg stage to 52.5±3.6% in birds that had completed their last ovulation but still retained an oviductal egg. Conversely, the relative contribution of the shell gland/vagina regions increased from 21.7±4.5% to 34.2±2.9%, respectively.
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First-laid eggs were significantly lighter than last-laid eggs for females
laying 4 eggs (1.042±0.115 g vs. 1.093±0.083 g,
paired t-test, t23=2.85, P<0.01).
There was no difference in the absolute, or relative, dry mass of shell with
laying sequence, but late-laid eggs had higher absolute, and relative, albumen
content compared with first-laid eggs
(Table 1). In contrast, the
percentage dry yolk mass was lower in last laid eggs
(Table 1).
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Discussion |
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The pattern of oviduct regression in our study is very different from that
reported by Houston et al. (1995), also for the zebra finch. They suggested
that the oviduct reached peak mass at the 1-egg stage but then declined in
mass linearly through laying, decreasing from 120 mg to 40 mg (66%) between
the 1- and 4-egg stages. Houston et al. (1995) argued that this reflected
`release' of protein from the oviduct for egg formation, i.e. that the oviduct
acts as a storage organ. We disagree with this conclusion and suggest that the
result of Houston et al. (1995) was an artifact of (1) plotting oviduct mass
by egg number (laying sequence), rather than the actual stage of ovarian
development, (2) including birds at later stages of egg-laying that had
actually completed egg formation, and (3) not using mass-corrected oviduct
mass. Indeed, if we analyze our data this way, not accounting for these
confounding factors, we also find an apparent decrease in oviduct mass between
the 1- and 4-egg stage (data not shown). Although birds in the study by
Houston et al. (1995) were maintained on a low-quality seed diet (in contrast
to our study), our data show that diet per se does not explain the
difference in oviduct mass between studies. Even on a seed-only diet in our
study, birds late in laying had oviducts averaging 151 mg, which is much
larger than the mean of 30-50 mg reported by Houston et al. (1995). Thus, we
believe there is currently no evidence to support a protein storage function
for the avian oviduct in relation to egg production (cf. Houston et al., 1995;
see also Vézina and Williams,
2003).
The results of our study clearly show that total oviduct mass remains
constant during egg-laying as long as there is at least one remaining yolky
follicle still to be ovulated and to pass down the oviduct. However, once the
last ovulation has occurred there is rapid, and marked, regression of the
proximal regions of the oviduct (the infundibulum, magnum and isthmus) as soon
as the follicle has passed these regions (within 24 h post-ovulation), but
while the distal shell gland region is still processing the oviductal egg.
Part of this decrease might be explained by loss of stored secretory products
(albumen proteins) from oviductal tissue following the last ovulation. This
does not fully explain the differential pattern of oviduct regression we
report, but this source of mass loss would still be consistent with rapid
downregulation of oviduct function (although in the domestic hen, albumen
protein content of the magnum region does not decrease until after cessation
of laying; Yu and Marquardt,
1973). Our result is very similar to that reported for laying
female European starlings, where oviduct mass also remains constant up to the
last ovulation, but then decreases by 50% following this last ovulation in
birds with only one oviductal egg remaining
(Vézina and Williams,
2003
). Thus, in two small passerines, the avian oviduct has a
highly regulated size-function relationship consistent with a high energy cost
of maintenance for this organ (i.e. high levels of cellular secretory
activity). This interpretation is supported by the observation that individual
variation in residual RMR in European starlings during egg-laying is
positively related to oviduct mass but not to other organs
(Vézina and Williams,
2003
). There appears to be little known about the specific
mechanisms involved in oviduct regression, but our study suggests that these
mechanisms must be specific to each region of the oviduct (e.g. differential
timing of receptor expression) rather than involving a more generic, humoral
signal such as downregulation of plasma estrogen or progesterone levels
(Burley and Vadehra, 1989
).
Although we did not investigate the growth phase, Yu and Marquardt
(1973
) showed that the rate of
growth of the magnum during oviduct development is much greater than that of
more distal sections of the oviduct, i.e. the pattern of growth also closely
reflects functional demands.
Although maintenance of a large oviduct would appear to be costly, there
are likely advantages to having a large oviduct in terms of both the quantity,
and potentially the quality, of egg albumen. Albumen protein content of eggs
is positively related to oviduct mass
(Christians and Williams,
1999), and this might be important for offspring fitness in terms
of structural growth of the offspring
(Williams, 1994
;
Finkler et al., 1998
). In
addition, several recent studies have suggested that maternal effects might
include transfer of immunoglobulins and antibacterial factors from mother to
offspring in egg albumen (Saino et al.,
2001
,
2002
); thus, oviduct
size/function might play a role in mediating these maternal effects.
Nevertheless, we consider it unlikely that oviduct size determines egg size,
via albumen content, independently of ovarian factors that determine
yolk size (Williams et al.,
2001
). Rather, it seems more likely that high quality birds which
produce large yolks must also be able to sustain the high costs of oviduct
function to deposit the appropriate amount of albumen required by yolks of a
particular size. It is clear that animals possess considerable phenotypic
flexibility in body composition, undergoing reversible changes in organ size,
e.g. in relation to migration (Battley et
al., 2000
; Guglielmo and
Williams, 2003
) or reproduction
(Vézina and Willams,
2003
). However, in general these studies have focussed on
modulation at the whole-organ level. We suggest that the type of intra-organ
structure-function relationship documented here for the avian oviduct might
also occur in other linear organs with high maintenance energy costs where
there is temporal separation of function, e.g. in digestive tracts with
prolonged passage times (Secor and
Diamond, 1997
).
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Acknowledgments |
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