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PROCEEDINGS THE ROYAL 
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Ecological and life-history factors influencing the evolution of 
maternal antibody allocation: a phylogenetic comparison 
BriAnne Addison, Kirk C. Klasing, W. Douglas Robinson, Suzanne H. Austin and Robert E. Ricklefs 
Proc. R. Soc. B published online 26 August 2009 
doi: 10.1098/rspb.2009.1296 
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PROCEEDINGS 
 OF  
THE ROYAL 
SOCIETY 
?-JFirstCite* 
i   e-publishing 
Proc. R. Soc. B 
doi:10.1098/rspb.2009.1296 
Published online 
Ecological and life-history factors 
influencing the evolution of 
maternal antibody allocation: 
a phylogenetic comparison 
BriAnne Addison1 *, Kirk C. Klasing2, W. Douglas Robinson3, 
Suzanne H. Austin3 and Robert E. Ricklefs1 
1
 Biology Department, University of Missouri-St Louis, 1 University Boulevard, St Louis, MO 63130, USA 
Department of Animal Science, University of California Davis, 1 Shields Avenue, Davis, CA 95616, USA 
3
 Oak Creek Lab of Biology, Department of Fisheries and Wildlife, Oregon State University, Corvallis, 
OR 97331, USA 
Maternally derived yolk antibodies provide neonates with immune protection in early life at negligible 
cost to mothers. However, developmental effects on the neonate's future immunity are potentially 
costly and thus could limit yolk antibody deposition. The benefits to neonatal immunity must be balanced 
against costs, which may depend on neonate vulnerability to pathogens, developmental trajectories and 
the immunological strategies best suited to a species' pace of life. We measured yolk antibodies 
and life-history features of 23 species of small Neotropical birds and assessed the evidence for each of 
several hypotheses for life history and ecological effects on the evolution of yolk antibody levels. Devel- 
opmental period and yolk antibodies are negatively related, which possibly reflect the importance of 
humoral immune priming through antigen exposure, and selection to avoid autoimmunity, in species 
with a slower pace of life. There is also a strong relationship between body size and yolk antibody con- 
centration, suggesting that larger species are architecturally equipped to produce and transfer higher 
concentrations of antibodies. These results suggest that developmental effects of maternally derived anti- 
bodies, such as imprinting effects on B-cell diversity or autoimmune effects, are important and deserve 
more consideration in future research. 
Keywords: disease ecology; immune development; maternal effects; life-history physiology; 
parasites; yolk antibodies 
1. INTRODUCTION 
Maternal influences on offspring phenotype, termed 
maternal effects (Mousseau & Fox 1998), have received 
special attention as an indirect genetic effect influencing 
an individual's life-history traits. The recent literature 
has focused on maternal allocation of hormones that 
direct resources to influence offspring behaviour, growth 
and development (Schwabl 1996; Gil 2003). However, 
few studies to date have investigated maternal provision- 
ing of antibodies, which protect offspring from pathogens, 
influencing resource allocation and development of 
immunity (Grindstaff et al. 2003; Boulinier & Staszewski 
2008; Hasselquist & Nilsson 2009). 
Maternally derived yolk antibodies protect neonates 
against environmental pathogens during early life 
(Graczyk et al. 1994; Baintner 2007; Pravieux et al. 
2007). Yolk antibodies are deposited during yolk 
formation by the active transport of circulating immuno- 
globulins across the follicle (Linden & Roth 1978; West 
* Author for correspondence (brianne.addison@gmail.com). 
Electronic supplementary material is available at http://dx.doi.org/10. 
1098/rspb.2009.1296 or via http://rspb.royalsocietypublishing.org. 
et al. 2004). The primary antibody present in avian eggs 
is immunoglobulin Y (IgY is for yolk, Rose et al. 1974; 
Tizard 2002), which is usually secreted by B-cells in 
direct response to an immune challenge. IgA and IgM 
appear at much lower concentrations and are primarily 
in the albumen of the egg. Chicken embryos undergo a 
period of rapid IgY uptake from their residual yolk, start- 
ing approximately 3 days prior to hatch and continuing 
for approximately 2 days post-hatch (Rose & Orlans 
1981). Because most IgY is produced in a specific 
response to an immune challenge, neonates receive pro- 
tection against pathogens likely to be relevant within 
their lifetime, and thus their passive immunity is shaped 
by their mothers' previous disease exposure. Maternally 
derived antibodies benefit chicks through two documen- 
ted routes; first, they directly interfere with pathogenicity 
by coating pathogens (Carlier & Truyens 1995; 
Leuridan & Van Damme 2007; Nemeth et al. 2008), 
and second, they reduce the demands on the neonate 
immune system, and thus free resources to be directed 
towards other growth or maintenance needs (Pihlaja 
et al. 2006; Gallizzi et al. 2008; Grindstaff 2008). There 
has also been a proposed imprinting effect of maternal 
antibodies    on    immune    development    of    offspring 
Received 22 July 2009 
Accepted 3 August 2009 This journal is ? 2009 The Royal Society 
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2    B. Addison et al.    Evolution of yolk antibody allocation 
(Lemke & Lange 1999), where the B-cell repertoire is 
proposed to be modelled after the antibodies present 
during development. This is usually considered a poten- 
tial benefit as there is some evidence that 'naive' offspring 
of non-naive mothers have higher responses to an antigen 
long after maternal antibodies have dissipated (Reid et al. 
2006), though it can also have negative effects if mothers 
transfer autoantibodies (Greeley et al. 2002) or if imprint- 
ing mechanisms interfere with other immune system arms 
(Lemke & Lange 1999). 
Despite their protective function, yolk antibodies make 
up only a small proportion of the total protein in the yolk. 
Presumably, maternal provisioning of antibodies also 
imposes costs that limit the amount allocated to eggs. 
These costs could be imposed on the hen during egg 
formation, or they may be imposed on the developing 
chick. The direct cost to the hen of producing antibodies 
is relatively low and is not likely to be higher than 
producing other egg proteins (Klasing 1998). Physiologi- 
cal factors might also constrain antibody synthesis by egg 
producing females. During reproduction, the immune 
system may be generally suppressed or reproductive 
resource use prioritized. For instance, during egg pro- 
duction in waterfowl, antibody synthesis changes to an 
alternate isotype (called IgYAFc), which reduces the 
inflammatory response but is also not transferred to 
yolks (Humphrey et al. 2004). Two distinct developmen- 
tal costs to chicks of maternal antibodies have been 
proposed. During B-cell development, lineages of 
pre-B-cells are positively selected if they are functional 
and bind to environmental antigens presented in the 
bursa or bind very loosely to self-antigens that might 
have molecular patterns similar to pathogenic organisms 
(Baumgarth et al. 2005). Pre-B-cells that are not func- 
tional or that bind tightly to self-antigens are negatively 
selected. The resulting set of B-cells recognizes a diverse 
set of antigens, but should not inflict damage via autoim- 
munity. However, large volumes of maternally derived 
antibodies could coat, and effectively hide, antigens that 
are important to B-cell development (Carlier & Truyens 
1995). There is evidence that maternal antibodies coat 
antigens, inhibiting the juvenile immune response (Lung 
et al. 1996; Staszewski et al. 2007). If environmental 
and self-antigens were hidden from the B-cell selection 
process, antibody diversity in later life might be compro- 
mised by a failure of positive selection at the pre-B-cell 
stage. The hiding of self-antigens could also cause 
autoimmune disorders through a failure of the negative 
selection process. The influence of maternal antibodies 
on diversification of the B-cell repertoire (Fink et al. 
2008) or autoimmune disease has a relatively short 
history in the medical literature (Zinkernagel 2001; Von 
Herrath & Bach 2002; Agarwal & Agarwal 2006; Victora 
et al. 2007). Although the costs remain poorly under- 
stood, we can assume that these costs do influence yolk 
antibody allocation decisions. 
Many ecological and life-history factors influence 
total and specific maternal antibody allocation to eggs 
(Grindstaff et al. 2003). Antibody allocation should 
match the exposure of offspring to pathogens, which 
will be determined by characteristics of the rearing habi- 
tat, the nest type and the amount of time spent in the 
nest exposed to parasites. The developmental strategy 
will not only influence exposure period, but could also 
alter the relative importance of allocation of resources to 
immune responses or maturation (Lee 2006). We investi- 
gated ecological and life-history patterns of maternal 
antibody allocation to eggs in a variety of lowland tropical 
bird species. If mothers adaptively allocated antibodies in 
response to ecological or life-history factors, we would 
expect support for two non-mutually exclusive hypoth- 
eses: (i) developmental life-history hypothesis: a fast 
life-history strategy, where growth is rapid and adaptive 
immunity is less important (Lee 2006), will select for 
higher yolk antibody levels because this will help divert 
resources towards growth, despite costs to adaptive 
immune development; and (ii) nestling ecology hypoth- 
esis: open nests and long nestling periods, where offspring 
are relatively exposed to environmental pathogens and 
vectors of disease, will select for higher yolk antibody 
levels relative to enclosed nests or short nestling periods. 
Alternatively, enclosed nests have been suggested to 
harbour more ectoparasites and so may select for higher 
yolk antibodies compared with open nests. 
2. MATERIAL AND METHODS 
We located nests of passerine birds in and around Gamboa, 
Panama, from 15 March to 30 June 2006 and from 
27 February to 25 May 2007. Gamboa is adjacent to Neotro- 
pical lowland dry forest in the Panama Canal Zone. The 
study period from February to May covers the dry-to-wet 
season transition (usually around mid-April) during the 
onset of the breeding season for most species in the area. 
Nests located during the building stage, or with only one 
egg, were used in the present study. Nests were checked 
daily, and first eggs were collected on the day the second 
egg was laid to prevent nest abandonment (except in clay- 
coloured robins Turdus grayi, where whole clutches were 
collected for another study). Collected eggs were stored at 
4?C for up to 24 h until IgY extraction. 
(a) Life-history and ecological traits 
We included the following life history and ecological variables 
in the analyses: clutch size; incubation and nestling periods; 
nest type (open or enclosed) and adult body mass. We col- 
lected life-history data by locating nests and weighing adult 
birds captured during the breeding season. We found nests 
of most species during the nest construction and egg-laying 
phases of the breeding cycle. Nests were visited daily during 
egg laying and near expected hatch and fledging dates. Eggs 
were numbered individually as they were laid, and chicks 
were marked with non-toxic markers to facilitate individual 
identification. In this study, clutch size is the mean number 
of eggs per nest. Incubation period is the time from onset of 
incubation to hatching of the first egg; onset of incubation 
in most species was on the evening the penultimate egg of a 
clutch was laid. Nestling period is the time between hatching 
of the first egg and fledging of the first hatched chick. We cate- 
gorized nests as open when they were open cups, platforms or 
scrapes on the ground. If nests were burrows, tree cavities, 
gourd- or pendant-shaped nests or cavities in termitaria, we 
categorized them as enclosed. Body masses were obtained 
from mist-netted birds at and near Gamboa. 
(b) Yolk immunoglobulin Yextraction 
and measurement 
Eggs were weighed whole and then broken open, and the 
yolks separated and weighed to the nearest 0.001 g.  For 
Proc. R. Soc. B 
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Evolution of yolk antibody allocation    B. Addison et al.    3 
extraction, we aliquoted 0.1 g of yolk into a 1.5 ml microcen- 
trifuge tube and removed the lipid by vortexing with 400 JULI 
of 3.5 per cent PEG-6000 in 0.9 per cent NaCl, incubating 
overnight at 4?C and centrifuging for 30 min at 8000g, 
4?C. The yolk pellet was discarded, and the supernatant 
reserved at 4?C for analysis. For yolk samples processed 
fresh, extraction efficiency is close to 100 per cent, as vali- 
dated with a stripped yolk pool spiked with known quantities 
of chicken IgY (B. Addison 2007, unpublished data). 
Yolk IgY was quantified by SDS-PAGE on 5 per cent gels 
run at 90 V for 30 min. Chicken IgY (purified polyclonal, 
Sigma-Aldrich, St Louis, MO, USA) standard dilutions 
were run simultaneously to generate a standard curve. 
Protein was stained with gelcode blue (Coomassie) stain 
(Pierce Biotechnology, Rockford, IL, USA) for 1 h and 
washed in distilled water overnight. Gels were then photo- 
graphed on a white light table, and the images were analysed 
for band density using the gel tool in ImageJ (NIH, figure SI, 
electronic supplementary material). Integrated density values 
were converted to concentration, in mg ml" , using the 
chicken IgY standard curve, and the values were multiplied 
by 4 to account for dilution during extraction. We used 
yolk IgY concentration in the analysis because our species 
varied greatly in egg size. 
Martinez et al. (2003) raise concerns about IgY overlap 
with other serum proteins, making SDS-PAGE methods 
for comparing among species difficult. However, to some 
degree, these concerns do not apply to our methods. First, 
we measure antibodies in yolk, which has significantly 
fewer proteins than plasma, and so concerns about protein 
overlap are to a large degree alleviated by this. Moreover, 
we use an extraction technique that separates protein from 
the plasma component of yolk and probably also selects to 
some degree for antibody-like proteins. This excludes a sig- 
nificant number of proteins from the SDS-PAGE analysis. 
To more thoroughly address these concerns, we calculated 
the amount of protein overlapping the IgY band of yolk 
plasma extracts from chicken yolk based on the table in 
Mann & Mann (2008). The emPAI (a measure of protein 
concentration) of IgY in the plasma portion only was 
reported as 1394. We calculated the emPAI values for all 
yolk plasma proteins overlapping the IgY band to total 53.3 
(an overestimate, since some of these proteins were spread 
over regions beyond the IgY band). While the degree to 
which these proteins overlap and the proportions of total 
yolk protein are likely to vary among species, we expect this 
would only introduce noise or dampen relationships. 
(c) Statistical analysis 
For all species, we calculated the mean value of IgY concen- 
tration for our comparative analysis (response variable). We 
selected nine statistical models from the parameters we 
measured, including a null model and a global model for 
AICc model ranking and multimodel inference (Burnham & 
Anderson 2002). Our candidate model set included a 
global model with all parameters, a nestling ecology model, 
a development model, the bivariate models for each of the 
individual parameters and a null model (table 1). 
We used a tree pruned from Cohen et al. (2008) to test for 
the effect of phylogeny. Using the regressionv2.m package 
(Lavin et al. 2008) in MATLAB (R2007a), we first fitted the 
best model of evolution for our traits of interest and then 
selected a set of candidate models for explaining life history 
and ecology effects on yolk IgY, accounting for phylogeny 
Table 1. List of models included in the AICc analysis of life- 
history effects on yolk IgY deposition. The parameters 
included are clutch size (species mean and clutch), 
incubation period (species mean in days, incp), nestling 
period (species mean in days, nestlp), adult body mass 
(mean in g, mass), nest type (open or closed, nesttype) and 
an evolutionary model (evolmodel). 
ID model 
global 1 clutch, incp, nestlp, mass, nesttype, 
nestlp *nesttype, incp*nestlp, evolmodel 
nestling clutch, nestlp, mass, nesttype, 
ecology 2 nestlp*nesttype, evolmodel 
development 3 incp, nestlp, mass, incp*nestlp, evolmodel 
4 clutch, evolmodel 
5 incp, evolmodel 
6 nestlp, evolmodel 
7 mass, evolmodel 
8 nesttype, evolmodel 
null evolmodel 
and our model of evolution. The regressionv2.m package 
selects the best model of evolution for the traits of interest 
by fitting the saturated model for each of several models of 
evolution, including species values (ordinary least squares, 
no phylogenetic signal), Brownian motion (phylogenetic gen- 
eralized least squares, equivalent to Felsenstein's contrasts), 
Ornstein-Uhlenbeck process (OU, drift about a fitness 
peak) or with branch lengths transformed using Pagel's A par- 
ameter. The OU and Pagel's A fitting procedures calculate 
branch length transformation parameters, d for the OU 
process that is a function of time and A for Pagel's transform- 
ation, which is constant across the tree, by restricted 
maximum likelihood (REML). Values close to 1 indicate 
that evolution is close to Brownian motion, whereas values 
close to 0 approximate a star phylogeny. 
3. RESULTS 
We obtained life history and yolk antibody values for 23 
species including dove, suboscine and oscine species 
(figure S2, electronic supplementary material). All 
species included have an altricial developmental mode, 
with incubation periods ranging from 12 to 23 days, nest- 
ling periods from 9 to 28 days, clutch size from two to 
four eggs, mass from 7.3 to 68 g and yolk antibody 
concentrations from 0.10 to 0.75 mgmL1. The 
within-species variability in IgY varied greatly by species. 
In AICc evaluation of the evolutionary models for phy- 
logenetic signal, the OLS star phylogeny was the best fit 
to the data for the global model with an AICc weight of 
0.9 (table 2). To be conservative, we also evaluated evol- 
utionary models for the null model. Both the OU and 
OLS trait evolution models had AAICc values under 2 
and can be considered to have support. Furthermore, 
the REML estimates of phylogenetic signal were A = 
0.75 (Pagel's lambda evolution model) and if =0.35 
(OU evolution model) for the null model and A = 0.39 
and d= 0.15 for the global model, such that the A- and 
^-transformed trees had shorter interior branches for 
the traits of interest. We report AICc scores for all life- 
history ecology models of yolk IgY for both OLS and 
OU evolutionary models. 
Proc. R. Soc. B 
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4    B. Addison et al.    Evolution of yolk antibody allocation 
Table 2 . Evaluation of the best-fit evolutionary model for the global model and the null model. Non-phylogenetic analysis 
(OLS) was best fit for the global model, but second to i models of a weak phylogenetic signal (OU) in the null model. 
model K n LgL AICc AAICc LAAICc AICc IP evidence ratio r2 
global ? clutch, incp, nestlp, mass, nesttype, nestlp* nesttype. incp*nestlp, evolmodel 
OLS 9 23 12.358 7.130 0.000 1.000 0.920 1.000 0.707 
OU 10 23 12.500 13.333 6.203 0.045 0.041 22.229 0.667 
A 10 23 12.358 13.617 6.487 0.039 0.036 25.626 0.669 
PGLS 9 23 6.4207 19.005 11.875 0.003 0.002 379.001 0.573 
null = evolmodel 
OU 2 23 -0.872 9.008 0.000 1.000 0.440 1.000 0 
OLS 2 23 -2.584 9.768 0.761 0.684 0.301 1.463 0 
A 3 23 -1.842 10.947 1.939 0.379 0.167 2.637 0 
PGLS 3 23 -3.768 12.136 3.128 0.209 0.092 4.779 0 
The strongest model for both the OLS and OU analyses 
was the development model of yolk IgY (AICc weights of 
0.95 and 0.81, respectively, table 3). The models that 
followed in support were the bivariate models of the par- 
ameters contained within the development model. Because 
the results for the OLS and OU analyses were qualitatively 
similar and because the AICc model weight for the top 
OLS model was greater than 0.95, we report only the 
OLS parameter estimates for the top model (table 4). 
The relationships between yolk IgY and both incubation 
and nestling periods were negative, but the interaction 
term was positive, indicating that the slopes are not 
equal. For species with longer incubation periods, the 
relationship with nestling period was weaker (figure 1). 
These patterns hold even with the exclusion of the 
common tody-flycatcher (Todirostrum cinereum) and grey- 
breasted martin (Progne chalybea), the species with the 
longest incubation and nestling periods, respectively, in 
our dataset. There was also a strong positive relationship 
between yolk IgY and adult body mass (figure 1). 
We found no support for the effects of clutch size or 
nest type on yolk IgY, and the relationship with nestling 
period was opposite to the direction expected for the 
nestling ecology hypothesis. 
4. DISCUSSION 
We evaluated models representing two hypotheses for the 
evolution of yolk IgY deposition strategies. Both in AICc 
model evaluation and in multimodel inference, factors 
related to life history and development weighted substan- 
tially more important than factors related to nestling 
ecology. Life history, specifically development period, 
has a strong effect on yolk IgY allocation in the resident 
Neotropical birds sampled in our study. Moreover, the 
effect of phylogenetic history on this trait was weak, 
suggesting that it is highly labile. The effect of develop- 
ment on yolk IgY could be operating through several 
pathways, which are not mutually exclusive. 
Larger adults deposit higher concentrations of yolk IgY 
in their eggs, which could reflect a greater capacity for 
antibody synthesis in larger animals (Davis et al. 1999; 
Magnadottir et al. 1999; Lee et al. 2008) or some other 
allometric reason (Hasselquist 2007). Alternatively, the 
offspring of larger species may have a longer development 
period (Gillooly et al. 2008); however, there was no 
relationship   between   body   mass   and   developmental 
period in our species set. The effect of body size appears to 
reflect the architectural costs of yolk antibody deposition 
to the hen. It would be interesting to investigate whether 
these differences are indeed driven largely by plasma 
cell density and productivity or whether there are also 
differences in IgY receptor expression on the yolk follicle. 
The strong negative relationship with incubation 
period most likely derives from incubation period serving 
as an index of development rate and/or pace of life. Since 
yolk IgY remains relatively inert until uptake by the 
embryo a short time before hatching (Tressler & Roth 
1987; Kaspers et al. 1991), incubation period per se 
should not be related to yolk IgY deposition. If degra- 
dation of IgY over time prior to embryonic uptake were 
of concern, we would predict a positive relationship 
between incubation period and yolk IgY, which is the 
opposite of what we found. Thus, the relationship 
between IgY and this index of pace of life fits well with 
a developmental cost to maternal antibody allocation 
(discussed subsequently). There is little information on 
comparative rates of immune development in avian 
species, and what is known is largely restricted to 
precocial species (Apanius 1998). 
Although species with longer nestling periods also 
deposit less IgY into their eggs, the relationship was 
weaker for species with long incubation periods, generat- 
ing a positive interaction between incubation and 
nestling periods in their effect on yolk IgY This could 
reflect a compromise between long development periods 
and long exposure periods, suggesting weak effects of 
nestling ecology. For instance, species with long incu- 
bation periods tend to have correspondingly long nestling 
periods (Lack 1968), which make the nestling more 
vulnerable to parasites normally found in high densities 
in the nest, such as philornid flies and mites. Nestling 
period is a poor index of the developmental period in 
the species in our dataset because many tropical species 
leave the nest at an early developmental state (Ricklefs 
1976; Remes & Martin 2002). However, it might be a 
good indication of developmental priorities in very 
early life, as species leaving the nest early probably 
expend more resources prior to nest departure on traits 
such as feather growth and muscle maturation, required 
to achieve that early nest departure. As such, the benefits 
of maternal antibodies could be of greater importance, 
while the potential developmental costs are diminished, 
for these species. 
Proc. R. Soc. B 
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Evolution of yolk antibody allocation    B. Addison et al.    5 
Table 3. AICc ranking, delta values, likelihoods and weights and model r for models of life-history effects on yolk IgY 
deposition. Analysis was done assuming a star phylogeny (OLS) and assuming stabilizing selection with drift (OU) using a 
tree compiled from the literature and presented in Cohen et al. (2008). 
model K n LgL AICc AAICc LAAICc AICc IF evidence ratio r2 
evolmodel = OLS 
3 6 23 10.517 -3.784 0.000 1.000 0.953 1.000 0.656 
7 3 23 1.648 3.968 7.752 0.021 0.020 48.220 0.297 
5 3 23 0.933 5398 9.181 0.010 0.010 98.558 0.254 
6 3 23 0.623 6.018 9.801 0.007 0.007 134.380 0.187 
1 9 23 12.358 7.130 10.913 0.004 0.004 234.317 0.707 
8 3 23 -0.255 7.773 11.557 0.003 0.003 323.223 0.176 
2 7 23 6326 8.814 12.598 0.002 0.002 543.915 0.505 
null 2 23 -2.584 9.768 13.552 0.001 0.001 876.573 0.000 
4 3 23 -2.043 11.350 15.133 0.001 0.000 1932.556 0.044 
evolmodel = OU 
3 7 23 10.658 0.151 0.000 1.000 0.814 1.000 0.624 
7 4 23 3.093 4.037 3.886 0.143 0.117 6.980 0.297 
5 4 23 1.406 7.411 7.261 0.027 0.022 37.723 0.171 
6 4 23 1.503 7.216 7.066 0.029 0.024 34.220 0.131 
null 3 23 -0.872 9.008 8.857 0.012 0.010 83.799 0.000 
8 4 23 0.171 9.880 9.729 0.008 0.006 129.632 0.078 
4 4 23 -0.651 11.524 11.373 0.003 0.003 294.864 0.019 
2 8 23 7.645 10.996 10.846 0.004 0.004 226.507 0.492 
1 10 23 12.500 13333 13.182 0.001 0.001 728.460 0.667 
Table 4. Parameter estimates of effect on yolk IgY 
deposition based on the top OLS model (assuming star 
phylogeny) that had an AICc weight greater than 0.95. 
estimate ( + s.e.) 
intercept 3.723478 1.298166 
incp -0.2828359 0.08787441 
nestlp -0.2780414 -0.08941521 
mass 0.008275306 0.002668124 
incp*nestlp 0.0171757 0.005923048 
The idea that maternally derived antibodies have a 
blocking effect on offspring immunity has been important 
for the development of vaccination schedules in human 
and veterinary medicine (Block et al. 2007; Siegrist 
2007). Although the effect of maternal antibodies on 
immune responses is well documented, it is not clear 
whether this blocking effect is exclusive to T-cell- 
mediated responses or whether it might also affect 
lymphocyte development (Carlier & Truyens 1995). 
The recognition of antigen is an important component 
of B-cell development (Tizard 2002; Baumgarth et al. 
2005), presenting a potential mechanism for a negative 
effect of maternal antibodies on immune system develop- 
ment. However, some evidence also supports a positive 
effect via immunological imprinting (Gasparini et al. 
2006; Grindstaff et al. 2006; Reid et al. 2006). The 
exact mechanism is unclear, but the B-cell repertoire 
may somehow model itself after antibodies in circulation 
(Fink et al. 2008). 
The relationship between maternal antibodies, devel- 
opment time and immunity is probably complex and 
dependent on the arm of the immune system of interest 
and possibly even the route of response to a specific 
antigen. The evidence for an effect of developmental 
period, or pace of life in general, on immunity is mixed, 
and much more needs to be done to understand what pre- 
dictions should be made for different arms of the immune 
system. Telia et al. (2002) found that slow pace of life 
species have higher cell-mediated immunity assayed by 
phytohaemagglutinin (PHA) wing web swelling, whereas 
Palacios & Martin (2006) found the opposite relationship 
using the same measure of immunity. Tieleman et al. 
(2005) found that slow pace of life species had higher 
innate immunity measured by bactericidal activity of 
blood. Lee et al. (2008) found that slow pace of life 
species had higher natural antibodies (relationship with 
incubation period) and lower complement activity 
(relationship with clutch size) in a set of species that 
includes many of the same species as this study. Different 
arms of the immune system could evolve independently, 
and the exact directional predictions probably depend a 
great deal on what aspect of immunity is measured 
(Blount et al. 2003). Perhaps, one of the best illustrations 
of this is a study of immune function in high (fast pace of 
life) and low latitude (slow pace of life) populations of 
house sparrows (Passer domesticus, Martin et al. 2006), 
which found that the slow pace of life population had a 
higher speed of humoral response measured as secondary 
antibody response to wing web injections of keyhole 
limpet haemocyanin and a higher magnitude of cell- 
mediated response measured by PHA wing web injection, 
but a lower magnitude peak of humoral response and 
lower T-cell response to KLH challenge compared with 
the fast pace of life population. It has been suggested 
that long developmental periods, and a slow pace of life, 
permit and perhaps necessitate the development of a 
stronger adaptive immune system (Lee et al. 2008). 
Species with long incubation periods have previously 
been shown to have lower parasite-induced nestling mor- 
tality (Moller 2005) and lower adult stage hematozoan 
infection     prevalence     (Ricklefs     1992),     suggesting 
Proc. R. Soc. B 
Downloaded from rspb.royalsocietypublishing.org on 26 August 2009 
6    B. Addison et al.    Evolution of yolk antibody allocation 
(a) 
S ? 
0, 
P 
10 15 20 
incubation period (d) 
25 
(b) 
6 o 
o 
10 15 20 25 
nestling period (d) 
30 
(c)  0.2 - (d) 
^      0 - 
3S 1 7 
1 -0.2 - c ) 0 a bfi 
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P bo 
5 -0.6 - t c )@ c ) 1 bo e 
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-0.05 
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( )           10 20 30 40 50 
adult ma ss (g ) 
incubation period (d)      4^, % 
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19 18 17 16 15^4ljj2i0 ^ 
Figure 1. Life-history predictors of yolk IgY deposition. Points are species means + s.e. (a) Incubation period is strongly nega- 
tively related to yolk IgY deposition, even if the common tody-flycatcher (77 cinereum, incubation period of 23 days) is excluded. 
Marker shade is coded by the nestling period, darker colours correspond to longer nestling periods, (b) Nestling period is also 
negatively related to yolk IgY deposition, again, even with the exclusion of the extreme value of the grey-breasted martin 
(7? chalybea, nestling period of 28 days). Marker shade corresponds to incubation period, (c) Adult body mass is positively 
related to yolk IgY deposition, (d) Predictive surface showing the relationship between incubation period, nestling period 
and mass corrected yolk [IgY], generated without the two extreme value species. 
potentially important effects of pace of life on immune 
development. 
Yolk IgY concentrations measured in this study 
were lower than levels measured in chickens (1.15- 
2.26 mg ml-1, Hamal et al. 2006) or quail Coturnix 
japonica (3.27-4.35 mg ml ', Grindstaff et al. 2005) 
and comparable to estimates reported in Ficedula albicollis 
(0.63 mg ml relative to chicken standard, Hargitai et al. 
2006). Several factors could contribute to the low levels 
measured in wild altricial birds. Domesticated fowls 
have better nutrition and thus more easily produce anti- 
bodies for allocation to eggs. Alternatively, the species 
studied in the wild are generally of small body size, and 
this appears to be a very important factor. Also, the altri- 
cial developmental mode, where much of the immune 
development probably occurs after hatch when maternal 
antibodies are active, may contribute to lower levels. 
Many of the studies of maternal antibodies in wild species 
have not attempted to quantify actual concentrations and 
have instead used relative values measured in immunoas- 
says. This inhibits further comparative analysis, and 
researchers are encouraged to quantify actual values 
alongside relative values whenever possible. 
Previous studies have found that hen plasma 
antibody levels and egg yolk antibodies are correlated 
(Hamal et al. 2006). For specific antigens, the slope of 
the correlation between hen plasma and yolk antibodies 
differs for different idiotypes (Tizard 2002), which 
could indicate a degree of selectivity for the movement 
of antibodies across the follicle membrane. There are 
two possible ways for adjustment of yolk antibody levels. 
Adjustment of circulating plasma antibodies allows con- 
trol both of the total antibodies deposited in yolks as 
the molecules will tend to move down a concentration 
gradient and of the proportion of different antibody 
idiotypes in the yolk. The second way to modify yolk anti- 
bodies is by adjustment of yolk follicle receptor density. It 
is not clear to what degree different species employ these 
two possible strategies. 
Much of the ecoimmunology literature has addressed 
almost exclusively benefits of maternal antibody 
allocation (Boulinier & Staszewski 2008; Hasselquist & 
Nilsson 2009), but the low levels of yolk IgY in wild 
species strongly indicate important costs. We suggest 
three physiological avenues of investigation that remain 
unexplored in a comparative context. First, we need to 
understand the role of maternally derived antibodies in 
B-cell development, in particular during pre-B-cell selec- 
tion in the bursa, and in T-cell development. Studies 
should consider the different modes of immune response, 
Proc. R. Soc. B 
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Evolution of yolk antibody allocation    B. Addison et al.    7 
T-cell dependent versus independent, for different anti- 
gen patterns. Second, we need more information on the 
time course of immune development for different arms 
of the immune system and among different life-history 
strategies. For instance, species investing little in humoral 
immunity should prioritize development of the innate 
arms of the immune system, with B-cell development 
occurring later and more rapidly. Third, we need to 
understand the long-term consequences of maternal anti- 
bodies for B-cell and T-cell repertoires, immunologic 
responsiveness and memory, immunosenescence, and 
autoimmunity. 
Overall, our analysis suggests a developmental cost 
limiting yolk IgY deposition, at least in small Neotropical 
birds. Although life history appears to be an important 
determinant of the evolution of this maternal effect, 
outstanding questions remain about the causes of inter- 
individual variability of this trait and the physiological 
activity of maternal antibodies, especially with respect 
to costs. 
All collections were under permit from Panamanian AN AM 
authorities, University of Missouri IACUC and the 
Smithsonian Tropical Research Institute. 
We would like to thank members of the Ricklefs Lab at 
UMSL and the Klasing Lab at UC Davis for discussion, 
especially Kelly Lee and Kim Livingston. Field and 
laboratory work was supported by the life history 
physiology nexus project (NSF IBN-0212587) and grants 
from Sigma Xi, the St Louis Audubon Society and the 
Whitney R. Harris World Ecology Center. An NSERC 
PGS D supported BA. We would also like to thank the 
Smithsonian Tropical Research Institute in Panama for 
assistance with field logistics. The nests would not have 
been found without the keen eyes of Jorge Herrera, 
Kathania Herrera, Lisa Miller, Betzi Perez and Ruby 
Zambrano, among others who have worked on the 
Robinson lab life history project. Finally, we would like to 
acknowledge the input of two anonymous reviewers that 
significantly improved the manuscript. 
REFERENCES 
Agarwal, K. & Agarwal, R. 2006 Effects of maternal auto- 
immune diseases on fetus and neonates. J. Neonatol. 20, 
172-175. 
Apanius, V. 1998 The immune system. In Avian growth and 
development: evolution within the altricial-precocial spectrum 
(eds J. M. Starck & R. E. Ricklefs), pp. 203-222. Oxford, 
UK: Oxford University Press. 
Baintner, K. 2007 Transmission of antibodies from mother 
to young: evolutionary strategies in a proteolytic environ- 
ment. Vet. Immunol. Immunopathol. 117, 153-161. 
(doi:10.1016/j.vetimm.2007.03.001) 
Baumgarth, N, Tung, J. W. & Herzenberg, L. A. 2005 
Inherent specificities in natural antibodies: a key to 
immune defense against pathogen invasion. Semin. 
Immunopathol. 26, 347-362. (doi: 10.1007/s00281 -004- 
0182-2) 
Block, H., Meyer-Block, K, Rebeski, D. E., Scharr, H, 
de Wit, S., Rohn, K. & Rautenschlein, S. 2007 A field 
study on the significance of vaccination against infectious 
bursal disease virus (IBDV) at the optimal time 
point in broiler flocks with maternally derived IBDV anti- 
bodies. Avian Pathol. 36, 401-485. (doi: 10.1080/ 
03079450701589175) 
Blount, J. D, Houston, D. C, Moller, A. P. & Wright, J. 
2003    Do   individual   branches    of   immune    defence 
correlate? A comparative case study of scavenging and 
non-scavenging birds. Oikos 102, 340-350. (doi: 10. 
1034/j.l600-0706.2003.12413.x) 
Boulinier, T. & Staszewski, V. 2008 Maternal transfer of 
antibodies: raising immuno-ecology issues. Trends Ecol. 
Evol. 23, 282-288. (doi:10.1016/j.tree.2007.12.006) 
Burnham, K. P. & Anderson, D. R. 2002 Model selection and 
multimodel inference: a practical information-theoretic 
approach. New York, NY: Springer-Verlag. 
Carlier, Y. & Truyens, C. 1995 Influence of maternal infec- 
tion on offspring resistance towards parasites. Parasitol. 
Today 11, 94-99. (doi:10.1016/0169-4758(95)80165-0) 
Cohen, A. A., McGraw, K. J., Wiersma, P., Williams, J. B., 
Robinson, W D., Robinson, T R., Brawn, J. D. & 
Ricklefs, R. E. 2008 Interspecific associations between 
circulating antioxidant levels and life-history variation in 
birds. Am. Nat. 172, 178-193. 
Davis, C. R, Marty, G. D, Adkison, M. A., Freiberg, E. F. & 
Hedrick, R. P. 1999 Association of plasma IgM with body 
size, histopathologic changes, and plasma chemistries in 
adult Pacific herring. Clupea pallasi. Dis. Aquat. Organ. 
38, 125-133. (doi:10.3354/dao038125) 
Fink, K, Zellweger, R., Weber, J., Manjarrez-Orduno, N., 
Holdener, M., Senn, B. M., Hengartner, H., Zinkernagel, 
R. M. & Macpherson, A. J. 2008 Long-term maternal 
imprinting of the specific B cell repertoire by maternal 
antibodies. Eur. J. Immunol. 38, 90-101. (doi: 10.1002/ 
eji.200737872) 
Gallizzi, K, Guenon, B. & Richner, H. 2008 Maternally 
transmitted parasite defence can be beneficial in the 
absence of parasites. Oikos 117, 223-230. (doi:10.1111/ 
j.2007.0030-1299.16172.x) 
Gasparini, J., McCoy, K. D., Staszewski, V., Haussy, C. & 
Boulinier, T 2006 Dynamics of anti-Borrelia antibodies 
in blacklegged kittiwake (Rissa tridactyla) chicks suggest 
a maternal educational effect. Can. J. Zool. -Revue 
Canadienne De Zoologie 84, 623-627. (doi: 10.1139/ 
Z06-024) 
Gil, D. 2003 Golden eggs: maternal manipulation of off- 
spring phenotype by egg androgen in birds. Ardeola 50, 
281-294. 
Gillooly, J. F, Londono, G. A. & Allen, A. P. 2008 Energetic 
constraints on an early developmental stage: a compara- 
tive view. Biol. Lett. 4, 123-126. (doi:10.1098/rsbl. 
2007.0460) 
Graczyk, T K, Cranfield, M. R., Shaw, M. L. & Craig, L. E. 
1994 Maternal antibodies against Plasmodium spp. in Afri- 
can black-footed penguin {Spheniscus demersus) chicks. 
J. Wildl. Dis. 30, 365-371. 
Greeley, S. A. W, Katsumata, M., Yu, L., Eisenbarth, G. S., 
Moore, D. J., Goodarzi, H, Barker, C. F, Naji, A. & 
Noorchashm, H. 2002 Elimination of maternally 
transmitted autoantibodies prevents diabetes in nonobese 
diabetic mice. Nat. Med. 8, 399-402. (doi:10.1038/ 
nm0402-399) 
Grindstaff, J. L. 2008 Maternal antibodies reduce costs of an 
immune response during development. J. Exp. Biol. 211, 
654-660. (doi:10.1242/jeb.012344) 
Grindstaff, J. L., Brodie, E. D. & Ketterson, E. D. 
2003 Immune function across generations: integrating 
mechanism and evolutionary process in maternal antibody 
transmission. Proc. R. Soc. Lond. B 270, 2309-2319. 
(doi: lO.lO98/rspb.2OO3.2485) 
Grindstaff, J. L., Demas, G. E. & Ketterson, E. D. 2005 Diet 
quality affects egg size and number but does not reduce 
maternal antibody transmission in Japanese quail Coturnix 
japonica. J. Anim. Ecol. 74, 1051-1058. (doi:10.1111/ 
j.l365-2656.2005.01002.x) 
Grindstaff, J. L., Hasselquist, D., Nilsson, J. A., Sandell, M., 
Smith, H. G. & Stjernman, M. 2006 Transgenerational 
Proc. R. Soc. B 
Downloaded from rspb.royalsocietypublishing.org on 26 August 2009 
8    B. Addison et al.    Evolution of yolk antibody allocation 
priming of immunity: maternal exposure to a bacterial 
antigen enhances offspring humoral immunity. 
Proc. R. Soc. B 273, 2551-2557. (doi:10.1098/rspb. 
2006.3608) 
Hamal, K. R, Burgess, S. C, Pevzner, I. Y. & Erf, G. F. 
2006 Maternal antibody transfer from dams to their egg 
yolks, egg whites, and chicks in meat lines of chickens. 
Poult. Sci. 85, 1364-1372. 
Hargitai, R., Prechl, J. & Torok, J. 2006 Maternal immuno- 
globulin concentration in collared flycatcher (Ficedula 
albicollis) eggs in relation to parental quality and laying 
order. Funct. Ecol. 20, 829-838. (doi:10.1111/j.l365- 
2435.2006.01171.x) 
Hasselquist, D. 2007 Comparative immunoecology in birds: 
hypotheses and tests. J. Ornithol. 148, 571-582. (doi:10. 
1007/sl0336-007-0201-x) 
Hasselquist, D. & Nilsson, J. A. 2009 Maternal transfer of 
antibodies in vertebrates: trans-generational effects on off- 
spring immunity. Phil. Trans. R. Soc. B 364, 51-60. 
(doi:10.1098/rstb.2008.0137) 
Humphrey, B. D., Calvert, C. C. & Klasing, K. C. 2004 The 
ratio of full length IgY to truncated IgY in immune com- 
plexes affects macrophage phagocytosis and the acute 
phase response of mallard ducks (Anas platyrhynchos). 
Dev. Comp. Immunol. 28, 665-672. (doi:10.1016/j.dci. 
2003.11.003) 
Kaspers, B., Schranner, I. & Losch, U. 1991 Distribution 
of immunoglobulins during embryogenesis in the 
chicken. J. Vet. Med. A Physiol. Pathol. Clin. Med. 38, 
73-79. 
Klasing, K. C. 1998 Nutritional modulation of resistance to 
infectious diseases. Poult. Sci. 77, 1119-1125. 
Lack, D. L. 1968 Ecological adaptations for breeding in birds. 
London, UK: Methuen. 
Lavin, S. R, Karasov, W. H., Ives, A. R, Middleton, K. M. & 
Garland, T. 2008 Morphometrics of the avian small 
intestine compared with that of nonffying mammals: 
a phylogenetic approach. Physiol. Biochem. Zool. 81, 
526-550. (doi:10.1086/590395) 
Lee, K. A. 2006 Linking immune defenses and life history at 
the levels of the individual and the species. Integr. Comp. 
Biol. 46, 1000-1015. (doi:10.1093/icb/icl049) 
Lee, K. A., Wikelski, M., Robinson, W. D., Robinson, T. R. 
& Klasing, K. C. 2008 Constitutive immune defences 
correlate with life-history variables in tropical birds. 
J. Anim. Ecol. 77, 356-363. (doi: 10.1111/j. 1365-2656. 
2007.01347.x) 
Lemke, H. & Lange, H. 1999 Is there a maternally induced 
immunological imprinting phase a la Konrad Lorenz? 
Scand. J. Immunol. 50, 348-354. (doi:10.1046/j.l365- 
3083.1999.00620.x) 
Leuridan, E. & Van Damme, P. 2007 Passive transmission 
and persistence of naturally acquired or vaccine-induced 
maternal antibodies against measles in newborns. Vaccine 
25, 6296-6304. (doi:10.1016/j.vaccine.2007.06.020) 
Linden, C. D. & Roth, T. F. 1978 IgG receptors on foetal 
chick yolk sac. J. Cell Sci. 33, 317-328. 
Lung, N. P., Thompson, J. P., Kollias, G. V, Olsen, J. H., 
Zdziarski, J. M. & Klein, P. A. 1996 Maternal 
immunoglobulin G antibody transfer and development 
of immunoglobulin G antibody responses in blue and 
gold macaw (Ara araraund) chicks. Am. J. Vet. Res. 57, 
1162-1167. 
Magnadottir, B., Jonsdottir, H, Helgason, S., Bjornsson, B., 
Jogensen, T 0. & Pilstrom, L. 1999 Humoral immune 
parameters in Atlantic cod (Gadus morhua L.). II. The 
effects of size and gender under different environmental 
conditions. Comp. Biochem. Physiol. B Biochem. Mol. 
Biol. 122, 181-188. (doi: 10.1016/S0305-0491 (98) 
10157-8) 
Mann, K. & Mann, M. 2008 The chicken egg yolk plasma 
and granule proteomes. Proteomics 8, 178-191. (doi: 10. 
1002/pmic.200700790) 
Martin II, L. B., Hasselquist, D. & Wikelski, M. 2006 Invest- 
ment in immune defense is linked to pace of life in house 
sparrows. Oecologia 147, 565-575. (doi:10.1007/s00442- 
005-0314-y) 
Martinez, J., Tomas, G., Merino, S., Arriero, E. & Moreno, 
J. 2003 Detection of serum immunoglobulins in wild 
birds by direct ELISA: a methodological study to validate 
the technique in different species using antichicken 
antibodies. Funct. Ecol. 17, 700-706. (doi:10.1046/j. 
1365-2435.2003.00771.x) 
Moller, A. P. 2005 Parasites, predators and the duration of 
developmental periods. Oikos 111, 291-301. (doi: 10. 
111 l/j.0030-1299.2005.14005.x) 
Mousseau, T A. & Fox, C. W. 1998 The adaptive 
significance of maternal effects. Trends Ecol. Evol. 13, 
403-407. (doi:10.1016/80169-5347(98)01472-4) 
Nemeth, N. M., Oesterle, P. T & Bowen, R. A. 2008 Passive 
immunity to West Nile virus provides limited protection in 
a common passerine species. Am. J. Trop. Med. Hyg. 79, 
283-290. 
Palacios, M. G. & Martin, T E. 2006 Incubation period and 
immune function: a comparative field study among coex- 
isting birds. Oecologia 146, 505-512. (doi: 10.1007/ 
S00442-005-0220-3) 
Pihlaja, M., Siitari, H. & Alatalo, R. V. 2006 Maternal 
antibodies in a wild altricial bird: effects on offspring 
immunity, growth and survival. J. Anim. Ecol. 75, 
1154-1164. (doi:10.1111/j.1365-2656.2006.01136.x) 
Pravieux, J. J., Poulet, H, Charreyre, C. & Juillard, V. 2007 
Protection of newborn animals through maternal immu- 
nization. J. Comp. Pathol. 137, S32-S34. (doi:10.1016/j. 
jcpa.2007.04.009) 
Reid, J. M., Arcese, P., Keller, L. F. & Hasselquist, D. 2006 
Long-term maternal effect on offspring immune response 
in song sparrows Melospiza melodia. Biol. Lett. 2, 
573-576. (doi: 10.1098/rsbl.2006.0544) 
Remes, V. & Martin, T E. 2002 Environmental influences on 
the evolution of growth and developmental rates in passer- 
ines. Evolution 56, 2505-2518. 
Ricklefs, R. E. 1976 Growth rate of birds in the humid 
New World tropics. Ibis 118, 176-207. (doi:10.1111/j. 
1474-919X.1976.tb03065.x) 
Ricklefs, R. E. 1992 Embryonic development period and the 
prevalence of avian blood parasites. Proc. Natl Acad. Sci. 
USA 89, 4722-4725. (doi: 10.1073/pnas.89.10.4722) 
Rose, M. E. & Orlans, E. 1981 Immunoglobulins in the egg, 
embryo and young chick. Dev. Comp. Immunol. 5, 15-20. 
(doi:10.1016/S0145-305X(81)80003-l) 
Rose, M. E., Orlans, E. & Buttress, N. 1974 Immunoglobu- 
lin classes in hens egg?their segregation in yolk and 
white. Eur. J. Immunol. 4, 521-523. (doi:10.1002/eji. 
1830040715) 
Schwabl, H. 1996 Maternal testosterone in the avian egg 
enhances postnatal growth. Comp. Biochem. Physiol. A 
Physiol. 114, 271-276. (doi: 10.1016/0300- 
9629(96)00009-6) 
Siegrist, C. A. 2007 The challenges of vaccine responses 
in early life: selected examples. J. Comp. Pathol. 137, 
S4-S9. (doi:10.1016/j.jcpa.2007.04.004) 
Staszewski, V, Gasparini, J., McCoy, K. D., Tveraa, T & 
Boulinier, T. 2007 Evidence of an interannual effect of 
maternal immunization on the immune response 
of juveniles in a long-lived colonial bird. J. Anim. 
Ecol. 76, 1215-1223. (doi: 10.1111/j. 1365-2656.2007. 
01293.x) 
Telia, J. L., Scheuerlein, A. & Ricklefs, R. E. 2002 Is cell- 
mediated immunity related to the evolution of life-history 
Proc. R. Soc. B 
Downloaded from rspb.royalsocietypublishing.org on 26 August 2009 
Evolution of yolk antibody allocation    B. Addison et al.    9 
strategies in birds? Proc. R. Soc. Lond. ?269, 1059-1066. 
(doi:10.1098/rspb.2001.1951) 
Tieleman, B. I., Williams, J. B., Ricklefs, R. E. & Klasing, K. 
C. 2005 Constitutive innate immunity is a component of 
the pace-of-life syndrome in tropical birds. Proc. R. Soc. B 
272, 1715-1720. (doi:10.1098/rspb.2005.3155) 
Tizard, I. 2002 The avian antibody response. Semin. Avian 
Exot. PetMed. 11, 2-14. (doi:10.1053/saep.2002.28216) 
Tressler,   R.   L.   &  Roth,  T.   F.   1987   IgG  receptors   on 
the   embryonic   chick   yolk-sac.   J.   Biol.    Chem.   262, 
15406-15412. 
Victora, G. D., Bilate, A. M. B., Socorro-Silva, A., Caldas, 
C.j Lima, R. C, Kalil, J., Coelho, V. & Victora, C. G. 
2007 Mother-child immunological interactions in early 
life     affect     long-term     humoral     autoreactivity     to 
heat shock protein 60 at age 18 years. J. Autoimmun. 29, 
38-43. (doi:10.1016/j.jaut.2007.02.018) 
Von Herrath, M. & Bach, J. F. 2002 Juvenile autoimmune 
diabetes: a pathogenic role for maternal antibodies? Nat. 
Med. 8, 331-333. (doi:10.1038/nm0402-331) 
West,  A.   R,  Herr,  A.  B.  &  Bjorkman,  R  J.  2004  The 
chicken yolk sac IgY receptor, a functional equivalent of 
the mammalian MHC-related Fc receptor, is a phos- 
pholipase    A(2)     receptor    homolog.     Immunity    20, 
601-610. 
Zinkernagel, R. M.  2001  Maternal antibodies, childhood 
infections, and autoimmune diseases. N. Engl. J. Med. 
345, 1331-1335. (doi:10.1056/NEJMra012493) 
Proc. R. Soc. B