Behavioral Ecology Vol. 12 No. 4: 381-385
© 2001 International Society for Behavioral Ecology
Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects?
a School of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK b Department of Biochemistry and Nutrition, Scottish Agricultural College, Ayr KA6 5HW, UK
Address correspondence to N. J. Royle. E-mail: n.royle{at}lancaster.ac.uk .
Received 5 April 2000; revised 20 August 2000; accepted 24 August 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Maternally derived traits, such as within-clutch variation in the amount of testosterone deposited in egg yolks, may have profound effects on offspring fitness. Offspring with elevated levels of testosterone may benefit from increased competitive ability through effects on aggression and growth rate. However, elevated levels of testosterone are also associated with costs of increased peroxidative damage from free radicals and consequent oxidative stress. Diet-derived antioxidants, such as vitamin E and various carotenoids, provide protection against the deleterious effects of oxidative stress. Here we show that within-clutch variation in yolk testosterone is the opposite to that of yolk antioxidant concentration in the lesser black-backed gull Larus fuscus. We provide evidence that suggests that these two direct maternal effects are, in fact, complementary and, in conjunction with an indirect maternal effect (the onset of incubation), may provide an adaptive mechanism for parental favoritism in response to environmental variability. The potential implications of these findings with respect to previous investigations on variation in yolk testosterone concentrations and on the understanding of intrafamilial dynamics are discussed.
Key words: brood reduction, carotenoids, maternal effects, parental favoritism, sibling competition, testosterone.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Parents have a major influence on the fitness of their offspring because of the additive effects of inherited traits and parental effects, such as propagule size or quality (Bernardo, 1996
). Parental effects, and particularly maternal effects, may
provide an adaptive phenotypic response to environmental variation, with
consequent effects on variation in offspring fitness
(Mousseau and Fox, 1998). In
birds, onset of incubation before the clutch is completed results in hatching
asynchrony (Stoleson and Beissinger,
1995). When parents feed divisible resources to dependent young,
offspring compete for food (Mock and
Parker, 1997). When food supplies are in shorter supply than
offspring demand, variation in offspring size as a consequence of hatching
asynchrony may result in brood reduction. Variation in the timing of the onset
of incubation can exert considerable effects on both individual offspring and
brood survival, but it is not the only maternal effect important in avian
"family planning."
Recently an extra layer of complexity has been uncovered by Schwabl
(1993), who found that female
canaries Serinus canaria deposited variable amounts of steroid
hormones, such as testosterone, in the yolks of their eggs depending on laying
order. Eggs laid later in the clutch contained more testosterone and hatched
more aggressive chicks, which begged with greater vigor than their nest mates
(Schwabl, 1993,
1996b). These chicks had
subsequently higher growth rates, which partially offset the handicap of
hatching last (Schwabl,
1996b). Offspring competitive ability was thus both directly
(hormones) and indirectly (incubation onset) maternally influenced. In
contrast, siblicidal cattle egrets Bubulcus ibis had increased
steroid hormone concentrations in earlier laid eggs, so the competitive
advantage of hatching first is most likely enhanced, rather than compensated
by the maternally conferred hormones
(Schwabl et al., 1997).
We have recently shown that concentrations of yolk antioxidants derived
from the mother's diet (vitamin E and various carotenoids) are found in higher
concentrations in earlier laid eggs of lesser black-backed gulls Larus
fuscus (Royle et al.,
1999). Antioxidants deactivate reactive oxidative metabolites and
free radicals, which are by-products of normal metabolism and immune defense,
and which can cause extensive DNA, protein, and lipid damage (oxidative
stress; von Schantz et al.,
1999). High levels of steroid hormones, such as testosterone, may
exact a cost through their suppressive effects on the immune system
(Ketterson and Nolan, 1999).
In addition, steroid hormones are known to impair enzymic antioxidant defenses
and directly induce oxidative stress (von
Schantz et al., 1999). Thus, one maternal effect (yolk antioxidant
concentration) could complement another potentially costly maternal effect
(yolk steroid hormone concentration) and have an influence on variation in
offspring fitness.
Here we investigate yolk testosterone and antioxidant concentrations in
relation to laying order of eggs in the lesser black-backed gull, which has a
small, modal clutch size, appreciable egg size polymorphism, hatching
asynchrony, and facultative brood reduction
(Bolton, 1991;
Royle and Hamer, 1998). Much
work has already been done in relation to the effects of variation in egg size
and hatching asynchrony on the fitness prospects of offspring in gulls (e.g.,
Bolton, 1991;
Bolton et al., 1992;
Davis and Quinn, 1997; Parsons,
1970,
1975;
Royle and Hamer, 1998), making
the lesser black-backed gull an ideal species for indirect elucidation of the
possible fitness consequences of maternal effects.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
General procedures
We collected eggs, with permission from the landowner, from Tarnbrook Fell, Abbeystead, Lancashire, UK, in May 1999. Details on the study site and sampling methods can be found in Royle and Hamer (1998
) and Royle et al.
(1999). All clutches were
initiated within 2 days of each other, and only birds laying a total of three
eggs (the modal clutch size) had their eggs removed, sequentially, as laid,
for analysis. Throughout the paper we refer to first-laid eggs as a-eggs,
second-laid eggs as b-eggs, and last-laid eggs as c-eggs. Fresh eggs were kept
at 4°C, and once all complete clutches had been collected, eggs were
weighed whole, before being dissected and their components weighed. Each yolk
was thoroughly homogenized to avoid problems associated with variation in
concentrations of hormones with egg yolk layers
(Lipar et al., 1999b), and
after homonogenization two samples (one for the androgen analysis and one for
the antioxidant analysis) from each yolk (ca. 1 g), were placed into labeled
Eppendorf tubes and frozen at —20°C until analysis.
Androgen analysis
Samples (ca. 0.4 g) in assay buffer (0.6 ml) were homogenized, incubated at
room temperature for 30 min, then briefly vortexed before incubating overnight
at 4°C. After incubation the samples were vortexed before centrifugation
for 10 min, and the top 0.5 ml of supernatant was removed. Subsequently, 0.2
ml samples of the supernatant, in assay buffer, were extracted twice using 3
ml of diethyl ether. Pooled ether fractions decanted from the snap-frozen
samples were then evaporated to dryness under a gentle stream of air. The
residue was redissolved in 1.5 ml of assay buffer. We assessed total
extraction efficiencies by adding known quantities of tritiated testosterone
solution to samples before extraction; extraction efficiencies were, on
average, 69%. We measured concentrations of testosterone (T) and
5
-dihydrotestosterone (DHT) by radioimmunoassay (BIOTRAK; Amersham
Pharmacia Biotech). Standards (T and DHT) were used throughout to calculate T
and DHT concentrations of unknowns. Samples were measured in duplicate to
determine total androgen concentrations initially (T and DHT), and then, also
in duplicate, DHT only. Detection limits were approximately 3 pg and 5 pg per
tube for T and DHT, respectively. We analyzed samples using two assays.
Interassay coefficient of variation (CV) was 2.5% for T and DHT (total) and
6.1% for DHT. Intra-assay coefficients of variation were 3.6% and 1.5% for T
and DHT combined and for DHT, respectively, in assay 1. In assay 2, CVs were
4.2% (T and DHT) and 3.7% (DHT). Androgen concentrations are given as
picograms (pg) per mg of yolk.
Antioxidant analysis
We analyzed carotenoids using the methods of Surai and Speake
(1998). Yolk samples were
homogenized in 1 volume of distilled water, then 2 ml of the homogenate was
mixed with 6 ml of ethanol/distilled water (2:1, v/v). Hexane (5 ml) was
added, and the mixture was shaken vigorously for 5 min. Separation of the
hexane phase, containing the carotenoids, by centrifugation preceded
collection and analysis using high-performance liquid chromatography (HPLC). A
Spherisorb S30DS2 3 µm C18 reverse-phase HPLC column (25 cm x 4.6 mm;
Phase Separations, Clwyd, UK), with a mobile phase of acetonitrile-methanol
(85:15) and acetronitrile-dichlorometh-ane-methanol (70:20:10) in gradient
elution (Granado et al., 1998)
and detection absorbance at 445 nm was used to separate specific carotenoids.
We identified peaks by comparing them with carotenoid standards (Sigma, Poole,
UK; Hoffmann La Roche, Switzerland).
We determined vitamins A and E using the methods of Surai et al.
(1999). A brief outline is
given here. Samples were saponified with ethanolic KOH in the presence of
pyrogallol and then vitamins A and E were extracted from the mixture with
petroleum spirit. The extract was dried under nitrogen, redissolved in
methanol, and injected onto a Spherisorb S30DS2 3 µm C18 reverse-phase HPLC
column (Phase Separations). Chromatography was performed using a mobile phase
of methanol/distilled water (97:3, v/v) at a flow rate of 1.05 ml/min.
Fluorescence detection of retinol involved excitation and emission wavelengths
of 330 and 480 nm, respectively. The relevant wavelengths for tocopherol
detection were 295 and 330 nm. Calibrations were performed using standard
solutions of -tocopherol and all-trans-retinol in methanol. We
used tocol as an internal standard. Concentrations of antioxidants are given
as µg/g of yolk.
Statistical analysis
We measured data on within-clutch variation in size or concentration of
constituents using repeated-measures ANOVA after testing for normality. Effect
size (Eta2; a measure of the total variation attributable to a
factor, where a small effect is <0.25 and a large effect is >0.5,
approximately) is presented for all ANOVA analyses, and estimates of
statistical power (1 — ß) are given for nonsignificant results were
there is a good chance of committing a type 2 error (i.e.,.05 < p
<.20). Unless otherwise stated, all means are presented ± 1 SE.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Egg mass (Eta2 = 0.62), albumen mass (Eta2 = 0.56), yolk mass (Eta2 = 0.40), and shell mass (Eta2 = 0.44) all declined substantially with laying order (Table 1). In contrast, total androgen concentration (T and DHT) increased with laying order (F2,28 = 16.01, p <.0005, Eta2 = 0.53; Figure 1a). DHT accounted for the larger proportion of the two androgens (a-eggs, 82.4%; b-eggs, 66.2%; c-eggs, 68.8%) and also increased significantly with laying order (F2,28 = 7.93, p =.002, Eta2 = 0.36). However, total carotenoid concentration of yolks showed a strong decline with laying sequence, with a-egg yolks being almost twice as concentrated with carotenoids as c-egg yolks (F2,28 = 25.82, p <.0005, Eta2 = 0.65; Figure 1b). There was considerable variation among females in the total amount of carotenoids deposited in egg yolks. Females laying larger eggs deposited greater proportionate amounts of yolk carotenoids than females laying smaller eggs (Spearman's rank correlation of yolk mass against total carotenoid concentration; a-eggs, r15 =.51, p =.05; b-eggs, r15 =.52, p =.046; c-eggs, r14 =.60, p =.023). Specific carotenoid concentrations are given in Table 2. Vitamin E (
-tocopherol) concentrations also decreased
strongly with laying order (F2,28 = 29.97, p
<.0005, Eta2 = 0.68; Figure
1c), whereas vitamin A (retinol) concentrations in egg yolks were
independent of laying order (F2,28 = 1.85, p
=.18, Eta2 = 0.12, power = 0.35;
Figure 1d).
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Maternally derived androgen and antioxidant concentrations in yolks were significantly related to egg laying order, but with opposing effects. The concentration of androgens in egg yolk increased with laying order, whereas yolk antioxidants showed a strong decline in concentration in successively laid eggs. In contrast, vitamin A, which is present at high concentrations in the liver (Surai et al., 2000
), and has a primarily systemic role
(Pitt, 1985), was not
differentially deposited in yolks of eggs of different laying sequence within
clutches. These results suggest that there are opposing maternal effects
associated with the way in which concentrations of androgens and antioxidants
are deposited in the yolks of successively laid eggs in the lesser
black-backed gull.
The pattern of androgen deposition in the eggs of lesser black-backed gulls
is similar to that of canaries (Schwabl,
1993) and red-winged blackbirds
(Lipar et al., 1999a), species
that commonly exhibit nonlethal competition for food among siblings and
facultative brood reduction. In the only two species where overt aggression
among brood mates is common and androgen concentrations have been measured
(cattle egrets: Schwabl et al.,
1997; white storks:
Sásvari et
al., 1999), the amounts of testosterone deposited declined with
successive offspring. Thus, depending on the life-history strategy of the
species involved, variation in within-clutch yolk androgen concentration
apparently either enhances or, as suggested by the data presented in this
paper, counteracts the effects of hatching asynchrony. This is based on the
assumption that, because testosterone may enhance aggression and growth
(Schwabl, 1993,
1996b), offspring exhibiting
elevated androgen levels will have a competitive advantage over their nest
mates. Consequently, it seems somewhat paradoxical that in the lesser
black-backed gull, the eggs with the lowest reproductive value (c-eggs) also
have the highest concentrations of maternally conferred androgens. The effects
of hatching asynchrony are generally more important than within-clutch
variation in egg quality in determining the outcomes of sibling rivalry
(Mock and Parker, 1997), so,
if variation in within-clutch concentration of yolk androgens is adaptive
(Schwabl, 1993;
Schwabl et al., 1997), how do
elevated levels of androgens in the eggs of lowest reproductive value maximize
reproductive success?
Although it is commonly assumed that yolk androgens have a positive effect
on offspring, fitness benefits of increased testosterone concentrations have
only been demonstrated in one species so far (canaries: Schwabl,
1993,
1996b). Moreover, such
benefits were only related to an increased success in competition with
siblings during the early nestling phase of development. In fact, the effect
of elevated androgen levels on growth and competitiveness of offspring is far
from clear. A study on domestic chickens Gallus domesticus, for
example, indicated that elevated levels of testosterone had no positive effect
on growth or protein gain of male embryos and had a negative effect on the
growth of female embryos (Henry and Burke,
1999). More recently, Sockman and Schwabl
(2000) found that high levels
of yolk androgens reduced survival in American kestrels Falco
sparvarius.
There are several potential costs associated with elevated androgen levels.
An increase in metabolic rate associated with high androgen levels causes an
increase in oxidative stress, and may result in suppression of the immune
system
(R
berg et
al., 1998). In addition to being an immunosuppressant
(Ketterson and Nolan, 1999),
testosterone is also known to directly induce oxidative stress in a range of
different tissues (von Schantz et al.,
1999). Antioxidants such as vitamin E and various carotenoids have
been shown to reduce the deleterious effects of free radicals on the immune
response and in a variety of different molecules
(Burton and Ingold, 1984;
von Schantz et al., 1999).
Consequently, lesser black-backed gull embryos developing in c-eggs with
elevated androgen concentrations but low levels of antioxidants will be much
more susceptible to oxidative stress than offspring from a- or b-eggs. This
may explain the higher rate of hatching failure of c-eggs in this species
(Royle et al., 1999).
The size of antioxidant reserves may also critically affect survival of
offspring both during and immediately after hatching. Hatching is particularly
stressful due to the onset of pulmonary respiration
(Royle et al., 1999), and the
efficiency of antioxidant assimilation from food is low during the first few
days after hatching (Surai,
1999), so that c-chicks will be under the greatest stress. Chick
mortality rates are highest in the first few days after hatching, particularly
for c-chicks (Bolton, 1991;
Royle, 2000). Although this is
primarily a consequence of the effects of hatching asynchrony
(Royle and Hamer, 1998), when
hatching asynchrony is experimentally controlled, chicks hatching from c-eggs
still have higher relative mortality rates than a- or b-chicks
(Parsons, 1975). C-chicks are
also more vulnerable to pathogens than a- or b-chicks
(Hario and Rudback, 1999).
These patterns of mortality are consistent with the effects of an increase in
oxidative stress due to relatively low antioxidant capacity, which would be
compounded by elevated levels of testosterone. Schwabl
(1996b) found that canary
chicks with elevated levels of testosterone begged more often and had faster
growth than controls, and that this difference was apparent within 22 h of
hatching. If the same effect is also applicable for gull chicks showing
elevated levels of testosterone, it is highly probable that such chicks will
have higher metabolic costs during the first few days after hatching. Unless
these extra metabolic costs can be sustained, mortality will be inevitable.
Consistent with this scenario, c-chicks are more aggressive
(Davis and Quinn, 1997), have
faster growth than a- or b-chicks (Royle,
2000) and have similar posthatching survival prospects to that of
their earlier hatching siblings when food supplies are abundant.
If egg yolk androgen and antioxidants are adaptive maternal effects, we
would expect environmental variation to influence patterns of deposition
(Mousseau and Fox, 1998).
Total vitamin E and carotenoid levels in egg yolks are determined by their
availability in the mother's diet, as they cannot be synthesised or stored for
long periods in the liver (Surai et al.,
1996,
1998). The variation in the
total amount deposited in a clutch of eggs therefore reflects differences in
foraging ability of parents. Despite the large variation in total antioxidant
reserves of clutches laid by different females, the pattern of deposition in
relation to laying sequence is ubiquitous, even between years
(Royle et al., 1999). However,
females laying larger eggs (an indicator of high parental quality;
Bolton, 1991) had relatively
greater concentrations of yolk carotenoids, especially for c-eggs. This
suggests that when resources allow, the disparity in within-clutch carotenoid
concentration is reduced, and offspring hatching from eggs of lower
reproductive value will benefit from increased antioxidant capacity. In
studies by Schwabl (1996a) and
Sásvari et al.
(1999), within-clutch
variation in yolk testosterone concentration was reduced when conditions for
breeding were more favorable. Testosterone deposition in eggs has also been
shown to be affected by mate attractiveness
(Gil et al., 1999). Thus, both
yolk androgen and antioxidant concentrations are strongly influenced by
environment.
Given this strong environmental influence, we propose the following
hypothesis to account for the paradoxical pattern of yolk androgen and
antioxidant concentration within clutches of eggs laid by lesser black-backed
gulls. If posthatching food supply is favorable, then the metabolic costs, and
consequent oxidative stress, of chicks with high androgen levels will be
reduced (especially chicks hatching from relatively antioxidant-deficient
c-eggs), while the beneficial effects associated with testosterone, such as
increased aggression and growth, will assist c-chicks to overcome the handicap
imposed by hatching asynchrony and maximize returns on parental investment.
Conversely, when conditions are unfavorable or food is insufficient for
parents to rear the whole brood, higher oxidative stress, due to low
antioxidative capacity and high testosterone levels, means c-chicks will be
less competitive and have lower survival prospects than their siblings. From a
parental perspective this has the beneficial effect of minimizing the costs of
wasted parental investment in offspring that die before independence
(Royle 2000;
Royle and Hamer, 1998). The
effect of elevated levels of testosterone on offspring fitness prospects is
thus likely to be highly dependent on food availability. The combination of
two direct, but opposing, maternal effects (antioxidant and androgen
concentrations), in conjunction with an indirect maternal effect (hatching
asynchrony) provides parents with a way to maximize returns on investment
under stochastic resource availability. This hypothesis remains to be
experimentally tested.
Although not conclusive with regard to the influence of antioxidants and
androgens on offspring fitness, the results presented here suggest that
previous studies on testosterone in bird eggs may have to be reevaluated, as
the potentially beneficial effects of testosterone on offspring fitness are
only likely to be expressed under certain environmental conditions. Sockman
and Schwabl's (2000) recent
finding that there is a survival cost to offspring from androgen-treated eggs
in American kestrels provides support for a context-dependent role of
maternally derived steroid hormones in shaping the outcomes of parental
favoritism. The potential fitness benefits need to be assessed experimentally,
with due consideration to costs. In the lesser black-backed gull, at least,
antioxidant capacity may be a more important maternal effect.
Further study of the combined influence of direct and indirect maternal
effects may also illuminate the study of hatching asynchrony, which is
characterized by a vast array of hypotheses. The current study indicates that
consideration of the effects of single measures of egg quality with respect to
hatching asynchrony will provide an incomplete picture of the influence of
maternal effects on offspring fitness. In addition, although the primary
consequence of variation in direct maternal effects may be expressed during
the nestling period of parental care, there may be pervasive influences of
such effects on offspring adult phenotypes
(Clark and Galef 1995;
Lindström
1999), which are largely unexplored in birds.
|
ACKNOWLEDGEMENTS |
|---|
This work was funded by a Royal Society Research Grant awarded to N.J.R. We thank Rod Banks at the Grosvenor Estate, Abbeystead, for permission to collect the eggs used in the analysis. Thanks also to Mark Bacon and Harry Lathom for assistance with the radioimmunoassay, Geoff Holroyd for logistical support at Lancaster, the Scottish Executive Rural Affairs Department for financial support to P.F.S, and Hoffmann La Roche Ltd. (Basel, Switzerland) for providing tocol, zeaxanthin, lycopene, and ß-cryptoxanthin.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bernardo J, 1996. The particular maternal effects of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36: 216-236.
Bolton M, 1991. Determinants of chick survival in the lesser black-backed gull: relative contributions of egg size and parental quality. J Anim Ecol 60: 949-960.
Bolton M, Houston D, Monaghan P, 1992. Nutritional constraints on egg formation in the lesser black-backed gull: an experimental study. J Anim Ecol 61: 521-532.
Burton GW, Ingold KU, 1984. ß-Carotene: an
unusual type of lipid antioxidant. Science
224: 569-573.
Clark MM, Galef BG, 1995. Prenatal influences on reproductive life history strategies. Trends Ecol Evol 10: 151-153.
Davis J, Quinn JS, 1997. Distribution of parental investment and sibling competition in the herring gull Larus argentatus. Behaviour 134: 961-974.
Gil D, Graves J, Hazon N, Wells A, 1999. Male
attractiveness and differential testosterone investment in zebra finch eggs.
Science 286:
126-128.
Granado F, Olmedilla B, Gil-Martinez E, Blanco I, 1998. Lutein ester in serum after supplementation in human subjects. Br J Nutr 80: 445-449.[Web of Science][Medline]
Hario M, Rudback E, 1999. Dying in the midst of plenty—the third chick fate in nominate lesser black-backed gulls Larus fuscus. Ornis Fenn 76: 71-77.
Henry MH, Burke WH, 1999. The effects of in ovo
administration of testosterone or an antiandrogen on growth of chick embryos
and embryonic muscle characteristics. Poultry Sci
78: 1006-1013.
Ketterson ED, Nolan V, 1999. Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154: S4-S25.[Web of Science]
Lindström J, 1999. Early development and fitness in birds and mammals. Trends Ecol Evol 14: 343-348.[Medline]
Lipar JL, Ketterson ED, Nolan V, 1999a. Intra-clutch variation in testosterone content of red-winged blackbird eggs. Auk 116: 231-235.
Lipar JL, Ketterson ED, Nolan V, Casto JM, 1999b. Egg yolk layers vary in the concentration of steroid hormones in two avian species. Gen Comp Endocrinol 115: 220-227.[Web of Science][Medline]
Mock DW, Parker GA, 1997. The evolution of sibling rivalry. Oxford: Oxford University Press.
Mousseau TA, Fox CW, 1998. The adaptive significance of maternal effects. Trends Ecol Evol 13: 403-407.
Parsons J, 1970. Relationship between egg size and post-hatching chick mortality in the herring gull Larus argentatus. Nature 228: 1221-1222.[Medline]
Parsons J, 1975. Asynchronous hatching and chicks mortality in the herring gull Larus argentatus. Ibis 117: 517-520.
Pitt G, 1985. Vitamin A. In: Fat-soluble vitamins—their biochemistry and applications (Diplock AT, ed). London: Heinemann; 1-75.
Rberg L, Grahn M, Hasselquist D,
Svensson E, 1998. On the adaptive significance of stress-induced
immunosuppression. Proc R Soc Lond B
265: 1637-1641.[Medline]
Royle NJ, 2000. Overproduction in the lesser black-backed gull—can marginal chicks overcome the initial handicap of hatching asynchrony? J Avian Biol 31: 335-344.
Royle NJ, Hamer KC, 1998. Hatching asynchrony and sibling size hierarchies in gulls: effects on parental investment decisions, brood reduction and reproductive success. J Avian Biol 29: 266-272.
Royle NJ, Surai PF, McCartney RJ, Speake BK, 1999. Parental investment and egg yolk lipid composition in gulls. Funct Ecol 13: 298-306.
Sasvári L, Hegyi Z, Péczely P, 1999. Brood reduction in white storks mediated through asymmetries in plasma testosterone concentrations in chicks. Ethology 105: 569-582.
Schwabl H, 1993. Yolk is a source of maternal
testosterone for developing birds. Proc Natl Acad Sci USA
90: 11446-11450.
Schwabl H, 1996a. Environmental modifies the testosterone levels of a female bird and its eggs. J Exp Zool 276: 157-163.[Web of Science][Medline]
Schwabl H, 1996b. Maternal testosterone in the avian egg enhances post-natal growth. Comp Biochem Physiol A 114: 271-276.
Schwabl H, Mock DW, Gieg JA, 1997. A hormonal mechanism for parental favouritism. Nature 386: 231.[Medline]
Sockman, KW, Schwabl, H, 2000. Yolk androgens reduce offspring survival. Proc R Soc Lond B 267: 1451-1456.[Medline]
Stoleson SH, Beissinger SR, 1995. Hatching asynchrony and the onset of incubation in birds, revisited—when is the critical period? Curr Ornithol 12: 191-270.
Surai PF, 1999. Vitamin E in avian reproduction. Poultry Avian Biol Rev 10: 1-60.
Surai PF, Ionov IA, Kuklenko TV, Kostjuk IA, MacPherson A, Speake BK, Noble RC, Sparks NHC, 1998. Effects of supplementing the hen's diet with vitamin A in the accumulation of vitamins A and E, ascorbic acid and carotenoids in the egg yolk and in the embryonic liver. Br Poultry Sci 39: 257-263.[Web of Science][Medline]
Surai PF, Noble RC, Speake BK, 1996. Tissue-specific differences in antioxidant distribution and susceptibility to lipid peroxidation during development of the chick embryo. Biochimica Biophys Acta 1304: 1-10.[Medline]
Surai PF, Royle NJ, Sparks NHC, 2000. Fatty acid, carotenoid and vitamin A composition of tissues of free living gulls. Comp Biochem Physiol A 126: 387-396.
Surai PF, Speake BK, 1998. Distribution of carotenoids from the yolk to the chick embryo. J Nutr Biochem 9: 645-651.
Surai PF, Speake BK, Noble RC, Sparks NHC, 1999. Tissue-specific antioxidant profiles and susceptibility to lipid peroxidation of the newly hatched chick. Biol Trace Elem Res 68: 63-78.[Web of Science][Medline]
von Schantz T, Bensch S, Grahn M, Hasselquist D, Wittzell H, 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266: 1-12.[Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. F Russell and V. Lummaa Maternal effects in cooperative breeders: from hymenopterans to humans Phil Trans R Soc B, April 27, 2009; 364(1520): 1143 - 1167. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Uller, J. Hollander, L. Astheimer, and M. Olsson Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard J. Exp. Biol., April 15, 2009; 212(8): 1087 - 1091. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. I. Sandell, M. Tobler, and D. Hasselquist Yolk androgens and the development of avian immunity: an experiment in jackdaws (Corvus monedula) J. Exp. Biol., March 15, 2009; 212(6): 815 - 822. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Tobler and M. I. Sandell Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch J. Exp. Biol., January 1, 2009; 212(1): 89 - 94. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Helfenstein, S. Losdat, V. Saladin, and H. Richner Females of carotenoid-supplemented males are more faithful and produce higher quality offspring Behav. Ecol., November 1, 2008; 19(6): 1165 - 1172. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. N Robb, R. A McDonald, D. E Chamberlain, S. J. Reynolds, T. J.E Harrison, and S. Bearhop Winter feeding of birds increases productivity in the subsequent breeding season Biol Lett, April 23, 2008; 4(2): 220 - 223. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Alonso-Alvarez, S. Bertrand, B. Faivre, O. Chastel, and G. Sorci Testosterone and oxidative stress: the oxidation handicap hypothesis Proc R Soc B, March 22, 2007; 274(1611): 819 - 825. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Muller, T. G.G Groothuis, A. Kasprzik, C. Dijkstra, R. V Alatalo, and H. Siitari Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks Proc R Soc B, September 22, 2005; 272(1575): 1971 - 1977. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. N. Rutstein, L. Gilbert, P. J. B. Slater, and J. A. Graves Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch Behav. Ecol., January 1, 2005; 16(1): 62 - 69. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. Muller, C. M. Eising, C. Dijkstra, and T. G. G. Groothuis Within-clutch patterns of yolk testosterone vary with the onset of incubation in black-headed gulls Behav. Ecol., November 1, 2004; 15(6): 893 - 397. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Boonstra Coping with Changing Northern Environments: The Role of the Stress Axis in Birds and Mammals Integr. Comp. Biol., April 1, 2004; 44(2): 95 - 108. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Reinhold Maternal Effects and the Evolution of Behavioral and Morphological Characters: A Literature Review Indicates the Importance of Extended Maternal Care J. Hered., November 1, 2002; 93(6): 400 - 405. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. V. Badyaev, G. E. Hill, M. L. Beck, A. A. Dervan, R. A. Duckworth, K. J. McGraw, P. M. Nolan, and L. A. Whittingham Sex-Biased Hatching Order and Adaptive Population Divergence in a Passerine Bird Science, January 11, 2002; 295(5553): 316 - 318. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||