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First published online February 15, 2008
Journal of Experimental Biology 211, 654-660 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012344
Maternal antibodies reduce costs of an immune response during development
Indiana University, Department of Biology and Center for the Integrative Study of Animal Behavior, 1001 E. Third Street, Bloomington, IN 47405, USA
(e-mail: jen.grindstaff{at}okstate.edu)
Accepted 17 December 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: antibody transmission, maternal effects, growth, maternal antibodies, cost, immune response
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Solomon, 1971;
Lawrence et al., 1981).
Instead, maternally derived antibodies provide the primary form of humoral
(antibody-mediated) immune defense
(Brambell, 1970;
Grindstaff et al., 2003). The
diversity and quantity of specific antibodies transmitted to offspring have
been shown to reflect differences in the local disease environment experienced
by females prior to reproduction (Lemke
and Lange, 1999; Lundin et
al., 1999; Gasparini et al.,
2001). Collectively, these antibodies represent the cumulative
antigen exposure of females over their lifetime
(Lemke et al., 2003).
Conversely, those females not exposed to particular pathogens prior to yolk
deposition cannot transfer antibodies to those pathogens, leaving their
offspring susceptible to more severe infections
(Heller et al., 1990).
Furthermore, the strength of the female antibody response may partially
determine offspring susceptibility to disease. For example, offspring survival
after challenge with Escherichia coli is positively correlated with
the mother's antibody response during egg laying in the domestic hen
(Heller et al., 1990).
Offspring of hens with low antibody titers to E. coli are more likely
to die after immunization with E. coli than offspring of hens with
high antibody titers. Interestingly, maternal antibodies provide protection
only for homologous strains of E. coli, not heterologous strains
(Heller et al., 1990). Thus,
maternal antibodies seem to provide very specific resistance against the
pathogens encountered by mothers prior to reproduction.
As mothers and offspring are likely to be naturally infected with the same
pathogens, the antibodies to endemic pathogens that mothers have in
circulation, once transmitted to offspring, will also provide young with
protection against endemic pathogens. Moreover, maternal antibodies may
provide offspring with the benefits of immune defense without the growth
suppressive costs of generating an endogenous immune response. Several
previous studies have documented suppressive effects of natural infection or
experimental immunization on the growth of young animals
(Klasing et al., 1987;
Fair et al., 1999;
Soler et al., 2003;
Brommer, 2004). Because
differentiation of the specific immune response is largely determined by
exposure to antigens, it is poorly developed in neonatal vertebrates with
little previous antigenic exposure. Instead during development, the immune
response is biased towards production of non-specific, innate immune responses
rather than lymphocyte-mediated specific responses
(Seto, 1981;
Klasing and Leshchinsky,
1999). Although innate immune responses are more rapid than
specific responses, they are associated with suppression of growth and
reproduction through activation of the inflammatory response
(Klasing, 1997). Growth
suppression is primarily a result of the anorexia, fever, and changes in
nutrient use induced during the response
(Klasing and Leshchinsky,
1999).
Maternal antibodies should allow offspring to resist infection without
invoking the physiological and growth-retarding expense of an innate immune
response (Klasing et al.,
1987; Heeb et al.,
1998; Buechler et al.,
2002; Kristan,
2002). Therefore, young with high levels of maternally derived
antibodies would be predicted to have both elevated resistance against endemic
pathogens (Heller et al.,
1990; Goddard et al.,
1994) and higher growth rates than young with low maternal
antibody levels or young without maternal antibodies for the antigens they
encounter. This might be achieved either through the direct action of maternal
antibodies (Heeb et al., 1998)
or through a priming of the offspring's own antibody production
(Gasparini et al., 2006;
Grindstaff et al., 2006;
Reid et al., 2006). In both
cases, offspring could potentially reduce the energetically costly and
growth-retarding action of the innate immune system
(Klasing and Leschinsky,
1999).
In order to test whether the presence of specific maternal antibodies could ameliorate the growth suppressive effects of immunization during growth, I immunized adult female Japanese quail (Coturnix japonica) and then cross-fostered offspring across antigenic environments. I used three treatments (two antigens and one control), lipopolysaccharide (LPS) derived from Salmonella typhimurium, killed avian reovirus (AR) vaccine, and a control treatment of phosphate-buffered saline (PBS). Consequently, one group of offspring had experimentally induced maternal antibodies specific for the antigenic challenge they received, a second group of offspring possessed maternal antibodies specific for a different antigen than the one they were immunized with, and the third group of offspring did not have experimentally induced maternal antibodies.
LPS is the major component of the outer membranes of Gram-negative
bacteria. It induces fever, inflammation, and behavioral changes (e.g.
listlessness, anorexia) such that immunization entails energetic costs
(Johnson et al., 1993;
Koutsos and Klasing, 2001).
However, LPS is non-replicating so that only those individuals that are
immunized are affected. LPS also mimics the effects of antigenic exposure in
the wild because it is derived from pathogens that induce illness in natural
populations. More importantly, in birds it elicits an antibody response by the
immunized individual and these antibodies are transmitted to egg yolks
(Sunwoo et al., 1996). Avian
reovirus is a viral infection that affects captive poultry, as well as wild
populations of Galliformes (Magee et al.,
1993; Jones,
2000). Infection induces arthritis-like symptoms in the joints and
may lead to stunted growth and development
(Read-Connole, 2000). I used a
heat-killed avian reovirus vaccine to stimulate an antibody response without
inducing pathological symptoms or transmission to non-immunized individuals.
Use of the heat-killed virus does not adversely affect the transfer of
antibodies to egg yolks (Jones,
2000).
I predicted that offspring with maternal antibodies specific for the
immunization they received would maintain growth rates after immunization. By
contrast, offspring immunized with a novel antigen (defined as one their
mothers had not been exposed to) would have reduced growth. Offspring
immunized with a novel antigen were expected to have reduced growth because of
the growth suppressive effects associated with invoking an innate immune
response (Roura et al., 1992;
Dritz et al., 1996;
Klasing and Leshchinsky,
1999). Offspring immunized with the same antigen as their mother
would be predicted to possess maternally derived antigen specific antibodies
and, thus would not need to rely on innate immunity. As control offspring were
not immunized, their immune systems were not stimulated so growth should not
have been affected.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Maternal immunization
Pre-immunization blood samples (approximately 500 µl) were collected
from the brachial vein to assess previous exposure to LPS and AR. None of the
females had detectable levels of antibodies to LPS or AR prior to
immunization. Females were then randomly assigned to one of three experimental
groups: LPS immunized, avian reovirus immunized, or the control
phosphate-buffered saline (PBS) group. LPS females were immunized
intraperitoneally with LPS isolated from Salmonella typhimurium
(Sigma L-7261, St Louis, MO, USA) at a concentration of 1.5 mg LPS
kg–1 body mass suspended in 0.5 ml PBS (Sigma P-4417). This
dose has been shown to elicit both an antibody response and mild sickness
behaviors in Japanese quail (Koutsos and
Klasing, 2001). Avian reovirus females were subcutaneously
immunized with 0.05 ml inactivated AR vaccine (Lohmann Animal Health Intl.
1815, Dassel, MN, USA) according to the manufacturer's recommendations.
Control (PBS) females were injected intraperitoneally with 0.5 ml of PBS to
control for any effects of handling and immunization. All females were given a
secondary immunization 10 days after the primary immunization, at the same
concentration as the primary immunization to increase the magnitude of the
antibody response. Blood samples (approximately 500 µl) were collected 10
days after the secondary immunization to quantify antibody responses to LPS
and AR.
Egg and offspring measurements
Eggs were collected from females throughout the experiment. All eggs were
measured (length, width and mass) at the time of collection. Every third egg
laid by each female was frozen intact and reserved for antibody analyses. A
subset of eggs laid at least 12 days after the maternal secondary immunization
was incubated at 37.5°C in a commercial incubator (Stromberg's Chicks INC
1202; Pine River, MN, USA). Immediately prior to hatching, eggs were placed in
individually marked cups to ensure that parentage of chicks could be
determined accurately. Chicks were individually banded at hatching for
identification. All quail chicks were measured (mass, tarsus and wing length)
every other day from hatching to 2 weeks post-hatch, with the exception of day
6 post-hatch when blood samples were taken from the chicks and they were
immunized. At the completion of the experiment, chicks were sexed based on
plumage differences or internal anatomy for chicks with ambiguous plumage.
Offspring immunization
Offspring were randomly assigned to one of the three antigen treatments
(LPS, AR, control) 6 days post-hatch. Offspring within a family were divided
among treatments such that each female had at least one chick in each
treatment group. Offspring were immunized with the same antigen doses as
mothers, but were only immunized once. A blood sample (at least 50 µl) was
collected from all chicks immediately prior to immunization to quantify
maternal antibody transmission and a second blood sample was collected from a
subset of chicks 5 days post-immunization to assess changes in maternal
antibody levels and any potential endogenous antibody production by chicks.
Specific antibody responses to LPS and AR as well as total IgG concentrations
were quantified in all blood samples with sufficient amounts of plasma.
Total IgG enzyme-linked immunosorbent assay
Total IgG concentrations were quantified using an enzyme-linked
immunosorbent assay (ELISA) as described previously
(Grindstaff et al., 2005).
ELISA plates were coated with 100 µl of anti-chicken IgG (donkey
anti-chicken IgY; Jackson ImmunoResearch Labs, product no. 703-005-155, West
Grove, PA, USA) at a concentration of 3 µg ml–1 suspended
in carbonate buffer (0.15 mol l–1, pH 9.6). Plasma or egg
yolk samples were diluted 1:20 000 in diluent (1% milk powder, PBS–Tween
20). Egg yolks were prepared for ELISA as described previously
(Grindstaff et al., 2005).
After washing, diluted samples were added to the plate in duplicate. At least
two blank wells (containing diluent only) were included on each plate. The
labeling antibody (AP-conjugated rabbit, anti-chicken IgG; Sigma, catalogue
no. A-9171) was diluted 1:1000. Plates were read on a Bio-Rad (Hercules, CA,
USA) Benchmark microplate reader (catalogue no. 170-6850). All antibody
concentrations are reported as the slope of the substrate conversion [in
10–3x optical densities (OD); mod] over time
(mod min–1), with a steeper slope indicating a
higher concentration of antibodies in the sample.
To compute antibody concentration, the mean of the duplicate values for each sample was calculated. The mean value of the blanks was subtracted from the measured antibody concentration to account for non-specific binding. On each plate, a serial dilution of a chicken-IgY standard (chicken IgY, Promega, catalogue no. G116A, Madison, WI, USA) was included for a standard curve (0.1, 0.05, 0.025, 0.0125, 0.00625 and 0.003125 µg ml–1). The differences between the standard curves was used to account for between-plate variation.
LPS ELISA
Ninety-six well ELISA plates were coated with 100 µl of LPS at a
concentration of 5 µg ml–1 suspended in carbonate buffer
(0.15 mol l–1, pH 9.6). Plates were then incubated overnight
at 4°C. The next day the plates were blocked with 5% milk powder (Mix `N
Drink, Saco Foods Inc., Middleton, WI, USA) diluted in 0.01 mol
l–1 PBS, pH 7.2 and Tween 20 for at least 2 h at room
temperature. During the incubation, plasma samples from females and offspring
were diluted 1:50 in diluent (1% powdered milk in PBS and Tween 20). For egg
assays, yolk samples were diluted 1:10. After washing the plate, samples were
added in duplicate. At least two blank wells were included on each plate that
contained diluent only. After sample addition, the plates were again incubated
overnight at 4°C. On the third day, 100 µl of the labeling antibody
(AP-conjugated rabbit, anti-chicken IgG, Sigma catalogue no. A-9171) diluted
1:1000 were added to every well of the plates after washing. The plates were
then incubated for 1 h at 37°C. After washing, 100 µl of substrate
buffer were added to every well of the plates. The plates were then
immediately transferred to a Bio-Rad Benchmark microplate reader (catalogue
no. 170-6850). The plates were read at 30 s intervals for 14 min using a 405
nm wavelength filter. Antibody titers are the slope of the substrate
conversion. Antibody titers were calculated in the same manner as described
above for IgG concentrations.
AR ELISA
A commercial ELISA kit was used to quantify antibody responses to the AR
vaccine (AffiniTech REO 1000, Madison, NJ, USA). Assay procedures followed the
kit instructions, except that plasma samples were diluted 1:50 and yolk
samples were diluted 1:10 in the sample diluent. To minimize interassay
variability, the mean optical density for each sample was expressed as a
percentage of its plate positive control optical density.
Statistical analyses
Before conducting analyses, normality of residuals and homogeneity of
variance were checked. LPS and AR antibody titers were log transformed to
achieve normality. Data were analyzed using mixed models (Proc Mixed, SAS
version 9.1) in which female identity, day by female identity, and offspring
treatment by female treatment nested within female identity were included as
random factors. Denominator degrees of freedom were determined by the
Satterthwaite method. Sample sizes represent 12 families with LPS-immunized
mothers, nine families with AR-immunized mothers, and 11 families with control
mothers. Analyses of chick growth were divided into early growth prior to
offspring immunization (growth from hatching to day 4) and later growth after
offspring immunization (growth from day 8 to day 14 post-hatch). There were no
significant differences in body size among offspring in the three offspring
treatment groups prior to immunization (all P>0.4). Therefore, in
analyses of early growth, offspring treatment group was not included.
Offspring sex did not contribute significantly to any of the models and was,
therefore, excluded.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Effect of maternal treatment on antibody levels in mothers
All females immunized with LPS or AR mounted an antibody response as a
result of the challenge, and no control females produced detectable levels of
LPS- or AR-specific antibodies. Consequently, antibody titers in maternal
circulation varied by treatment group. As expected, LPS antibody levels were
highest in the females immunized with LPS and not different from background in
control females and females immunized with AR (F2,30=8.61,
P=0.001). Similarly, AR antibody levels were highest in females
immunized with AR and not different from background in control females and
females immunized with LPS (F2,30=73.09,
P<0.0001). Total IgG concentrations in maternal circulation were
not significantly impacted by maternal treatment
(F2,30=2.46, P=0.10).
Maternal antibody transmission
Antibody levels in maternal circulation and in eggs were significantly
positively correlated (IgG: R2=0.32, P=0.001,
N=31; LPS: R2=0.94, P<0.0001,
N=31; AR: R2=0.88, P<0.0001,
N=31). Similarly, antibody levels in maternal circulation and in
offspring circulation on day 6 post-hatch were positively correlated [IgG:
R2=0.44, P<0.0001, N=31
(Fig. 1); LPS:
R2=0.72, P<0.0001, N=31; AR:
R2=0.71, P<0.0001, N=31], although
antibody levels in chick circulation were lower than antibody levels in
maternal circulation. There was no difference in maternally derived antibody
levels between male and female chicks on day 6 (IgG:
F1,151=0.09, P=0.77; LPS:
F1,136=0.46, P=0.50; AR:
F1,137=1.47, P=0.23).
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Effect of maternal treatment on day 6 antibody levels in chicks
Chicks whose mothers were immunized with LPS had higher levels of LPS
antibodies than did chicks whose mothers were immunized with AR or who were
not immunized (F2,26=26.65, P<0.0001)
(Table 1). Offspring whose
mothers were immunized with AR had higher levels of AR-specific antibodies
than did chicks whose mothers were immunized with LPS or who were not
immunized (F2,30.9=47.66, P<0.0001)
(Table 1). However, offspring
of immunized mothers did not have significantly higher total IgG
concentrations than offspring of control mothers
(F2,30.5=2.82, P=0.075)
(Table 1).
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Antibody levels after chick immunization
On day 11, neither maternal nor chick treatment significantly affected
total IgG levels in offspring circulation (maternal treatment:
F2,28.6=1.79, P=0.18; chick treatment:
F2,41.8=1.02, P=0.37; maternal treatment x
chick treatment: F4,40.2=0.75, P=0.56). LPS
antibody titers in offspring circulation on day 11 were still affected by
maternal treatment but were not affected by chick treatment (maternal
treatment: F2,32.8=31.65, P<0.0001; chick
treatment: F2,55.2=0.69, P=0.51; maternal
treatment x chick treatment: F4,54.6=0.23,
P=0.92). Similarly, AR antibody titers were affected by maternal
treatment, but not chick treatment (maternal treatment:
F2,28.2=26.23, P<0.0001; chick treatment:
F2,53.1=0.53, P=0.59; maternal treatment x
chick treatment: F4,51.4=0.12, P=0.97).
Changes in offspring antibody levels during the experiment
In general, between days 6 and 11 total IgG concentration and titers of
LPS- and AR-specific antibodies declined in chick circulation [IgG day 6
mean=8.97±0.38 (± s.e.m.), day 11 mean=4.58±0.19; LPS day
6 mean=2.72±0.63, day 11 mean=0.80±0.15; AR day 6
mean=4.88±1.03, day 11 mean=1.79±0.40]. Within chicks, antibody
levels on days 6 and 11 were significantly positively correlated (IgG:
R2=0.38, P<0.0001, N=111; LPS:
R2=0.74, P<0.0001, N=111; AR:
R2=0.94, P<0.0001, N=109).
Effect of maternal immunization on early offspring growth
Maternal antigen treatment did not significantly affect early mass gain or
tarsus growth of offspring before immunization (tarsus: maternal treatment
x age: F4,60=1.22, P=0.31; mass: maternal
treatment x age: F4,60=0.59, P=0.67).
However, offspring of control mothers had significantly reduced early wing
growth in comparison to the offspring of either LPS- or AR-immunized mothers
(maternal treatment x age: F4,60=3.26,
P=0.017).
Effect of maternal and offspring immunizations on later offspring growth
Maternal treatment did not influence tarsal growth rate
(Table 2). However, tarsal
growth was impacted by offspring treatment
(Table 2). Control,
non-immunized offspring had faster tarsal growth than LPS- or AR-immunized
offspring. Mass gain was also not significantly impacted by maternal
treatment, but was influenced by offspring treatment
(Table 2). Again control
offspring were significantly heavier than immunized offspring. Wing growth was
influenced both by maternal treatment and by offspring treatment
(Table 2). Offspring of control
mothers had slower wing growth than offspring of LPS- or AR-immunized mothers.
Conversely, non-immunized offspring exhibited faster wing growth than LPS- or
AR-immunized offspring.
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Effect of a novel immunization on growth rates
I had predicted that offspring with maternal antibodies specific for the
immunization they received would have elevated growth in comparison to
offspring immunized with a novel antigen. To more directly test this
prediction, I categorized offspring on the basis of whether they had
experimentally induced maternal antibodies specific for the immunization they
received, experimentally induced maternal antibodies for a different antigen
challenge than they received, or were not immunized (control group).
Tarsal growth rates were significantly impacted by immunization with a novel antigen (immunization x age: F6,137=5.85, P<0.0001) (Fig. 2A). Control, non-immunized, offspring had the highest growth rates, offspring immunized with a novel antigen (one their mothers had not been exposed to) had the lowest growth rates, and offspring with specific maternal antibodies for the antigen challenge had intermediate growth rates. Mass gain was also impacted by immunization with a novel antigen (immunization: F2,57.9=4.89, P=0.011) (Fig. 2B). Again control offspring exhibited the greatest mass gain, offspring immunized with a novel antigen gained the least mass, and offspring with specific maternal antibodies had intermediate mass gain. Wing growth was similarly affected by immunization (immunization: F2,64=5.02, P=0.0094) (Fig. 2C). Control offspring and offspring immunized with the same antigen as their mothers exhibited equivalent wing growth, but offspring immunized with a novel antigen had significantly reduced growth.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and
the primary effect of maternal immunization was to elevate specific antibody
titers. Indeed maternal immunization significantly altered antibody
transmission to offspring as measured by antibody levels in offspring on day 6
post-hatch. By day 11 post-hatch, maternal immunization still had significant
effects on offspring antibody measures. Conversely, chick treatment did not
affect specific or total antibody levels. Because antibody levels declined
between day 6 and day 11 post-hatch, it appears that endogenous antibody
synthesis does not begin until some time after day 11 in precocial (well
developed at hatch) quail.
In general, offspring immunization reduced growth rates. However, the
presence of specific maternal antibodies partially ameliorated the growth
suppressive effects of immunization. By contrast, possession of experimentally
elevated maternal antibodies for a different antigen did not ameliorate growth
suppression. Offspring that received the same antigenic challenge as their
mother, or were in the control group, exhibited faster tarsal growth and
greater wing growth and mass gain than offspring immunized with a novel
antigen for which they did not have maternal antibodies. This effect occurred
even though the antigens used in the study were non-replicating and the young
had ad libitum access to food. This provides further support for a
trade-off between immunocompetence and growth
(Soler et al., 2003;
Brommer, 2004). In response to
exposure to antigens, macrophages release inflammatory cytokines and provoke
an inflammatory response. The production of these cytokines is also necessary
to stimulate the adaptive immune response. However, this stimulation of the
inflammatory response greatly increases the cost of antigenic exposure and may
explain the reduction in growth or condition that is often observed after
immunization with even fairly innocuous antigens
(Siegel et al., 1982;
Demas et al., 1997;
Ots et al., 2001;
Martin et al., 2003).
Maternal antibodies provide offspring, at least temporarily, with specific
immunity to local diseases. When offspring encounter the same pathogens as
their mothers, maternal antibodies provide protection without invoking the
innate immune system of offspring
(Brambell, 1970). Innate
immunity is particularly expensive to growing young because the inflammatory
response induces anorexia and diverts nutrients needed for growth to the acute
phase response (Klasing, 1994;
Klasing and Leshchinsky,
1999). Maternal antibodies allow offspring to maintain rapid
growth when infected, by suppressing stimulation of the innate immune system
(Klasing and Leshchinsky,
1999). Therefore, it is not simply the presence or absence of
maternal IgG that may influence offspring growth (e.g.
Gustafsson et al., 1994), but
also the specific types of antibodies that are transferred in relation to the
antigens that offspring are exposed to.
For example, LPS has been demonstrated to elicit a sustained inflammatory
response in Japanese quail chicks as measured by interleukin-1 (IL-1) activity
(Klasing and Leshchinsky,
1999). However, chicks of LPS-immunized mothers exhibited reduced
levels of IL-1 activity presumably because maternal antibodies prevent LPS
from binding macrophage LPS receptors to trigger the release of inflammatory
cytokines (Klasing and Leshchinsky,
1999). This may reduce growth suppression in LPS-immunized chicks
whose mothers were also immunized with LPS as observed here. Unfortunately,
maternal antibodies do not completely eliminate the growth suppression
associated with immunization. It remains to be determined whether this is a
dose-dependent effect such that high levels of specific maternal antibodies
are able to completely block stimulation of the innate response, whereas lower
levels do not. Alternatively, maternal antibodies may be unable to completely
block involvement of the offspring immune response, regardless of
concentration. Antigenic exposure during development has an important
educational role in the differentiation of the specific immune response and it
may consequently be essential for the offspring immune system to be actively
involved in responses to antigenic exposure, irrespective of potential effects
on morphological growth.
Unexpectedly, offspring of control mothers had significantly reduced early
wing growth in comparison to the offspring of immunized mothers. This may
suggest that immunized mothers made a terminal investment in reproduction as a
result of the immunization (Bonneaud et
al., 2004). However, this seems unlikely given that offspring did
not differ prior to immunization in any other size measure and immunized
mothers did not lay larger eggs than control mothers. Instead, this may
suggest that offspring of control mothers invest more in tarsal growth and
mass gain, rather than wing growth.
Precocial young have been predicted to begin endogenous antibody production
earlier after hatch relative to altricial (poorly developed at hatch) young
because they hatch at a later developmental stage
(Apanius, 1998;
Klasing and Leshchinsky,
1999). However, I did not find any evidence in this study that
Japanese quail chicks begin to produce antibodies within the first 11 days
post-hatch. Even though offspring were given a fairly short period of time to
respond to the immunization, one would expect that antibody titers should
increase after immunization, if offspring are capable of mounting a specific
response. Instead, the titers of maternally derived antibodies and total IgG
concentrations declined in these quail chicks over the measured time period.
Conversely, similar measurements in semi-precocial and altricial birds have
revealed an increase in both specific and total antibody levels within the
first 10 days to 2 weeks post-hatch
(Gasparini et al., 2006;
Grindstaff et al., 2006;
Pihlaja et al., 2006). The
lower relative proportion of yolk in altricial species than in precocial
species suggests that altricial young receive lower levels of maternally
derived antibodies (Klasing and
Leshchinsky, 1999). Therefore, it may be important for altricial
species to accelerate antibody production to minimize reliance on the more
nutritionally expensive mechanisms of innate immunity.
Maternal antibodies have a critical role in providing offspring with
humoral immune protection early in life
(Grindstaff et al., 2003) and
may also affect early endogenous antibody production by offspring
(Gasparini et al., 2006;
Grindstaff et al., 2006;
Reid et al., 2006). One
primary determinant of the diversity of antibodies transmitted to offspring is
the maternal antigenic environment (this study)
(Gasparini et al., 2001).
Furthermore, these results suggest that if offspring are exposed to the same
antigens as mothers during the period of maternal immune protection, maternal
antibodies may also play an important role in reducing growth suppression
after infection. Because offspring with initially high levels of maternal
antibodies maintain detectable levels of antibodies in circulation longer than
young with low initial antibody levels (J.L.G., unpublished)
(Nicoara et al., 1999), the
primary benefit of enhanced antibody transmission is likely to be an extension
of the period of protection for offspring. This may allow offspring to
complete the majority of the growth period before maternal protection is lost.
In the wild, offspring of mothers with higher circulating levels of antibodies
should maintain maternal protection for a greater proportion of the growth
period than offspring of mothers with low antibody levels. Future research
should assess the mechanisms through which maternal antibodies allow offspring
to maintain growth after infection and the interactions between maternal
antibodies and stimulation of the inflammatory response.
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Apanius, V. (1998). Ontogeny of immune function. In Avian Growth and Development: Evolution within the Altricial-precocial Spectrum (ed. J. M. Starck and R. E. Ricklefs), pp. 203-222. New York: Oxford University Press.
Bonneaud, C., Mazuc, J., Chastel, O., Westerdahl, H. and Sorci, G. (2004). Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58,2823 -2830.[CrossRef][Medline]
Brambell, F. W. R. (1970). The Transmission of Passive Immunity from Mother to Young. Amsterdam: North Holland.
Brommer, J. E. (2004). Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc. R. Soc. Lond. B Biol. Sci. 271,S110 -S113.[CrossRef]
Buechler, K., Fitze, P. S., Gottstein, B., Jacot, A. and Richner, H. (2002). Parasite-induced maternal response in a natural bird population. J. Anim. Ecol. 71,247 -252.[CrossRef]
Demas, G. E., Chefer, V., Talan, M. I. and Nelson, R. J. (1997). Metabolic costs of mounting an antigen-stimulated immune response in adult and aged C57BL/6J mice. Am. J. Physiol. 42,R1631 -R1637.
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