Parental Care II: Eggs
JodyLee Estrada Duek, Ph.D.
With assistance from Dr. Gary Ritchison
http://people.eku.edu/ritchisong/avianreproduction2.html
The Avian Egg
• Birds' eggs, like the birds themselves, vary enormously in size.
• The largest egg from a living bird belongs to the ostrich.
• It is over 2000 times larger than the smallest egg produced by a
hummingbird (see photo to the right; Source:
http://www.pma.edmonton.ab.ca/vexhibit/eggs/vexhome/sizeshap.htm).
– Ostrich eggs are about 180 mm long and 140 mm wide and weigh 1.2 kg.
– Hummingbird eggs are 13 mm long and 8 mm wide and they weigh only half of a gram.
• The extinct Elephant Bird from Madagascar produced an egg 7 times
larger than that of the Ostrich!
Emu egg & embryo
http://www.digimorph.org/specimens/Dromaius_novaehollandiae/egg/
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Parental investment in
eggs and offspring can
profoundly influence the
phenotype, survival and
evolutionary fitness of an
organism.
Avian eggs are excellent
models to examine
maternal allocation of
energy through egg size
variation.
Dzialowski and
Sotherland (2004) used
the natural range in Emu
(Dromaius
novaehollandiae) egg size,
from 400 g to >700 g, to
examine influence of
maternal investment in
eggs on morphology and
physiology of hatchlings.
Egg composition and hatchling phenotype
• Female Emus provisioned larger eggs with a greater absolute amount of energy,
nutrients and water in the yolk and albumen.
• Variation in maternal investment was reflected in differences in hatchling size,
which increased isometrically with egg size.
• Egg size also influenced physiology of developing Emu embryos; late-term
embryonic metabolic rate positively correlated with egg size and embryos
developing in larger eggs consume more yolk
• Large eggs produced hatchlings that were both heavier (yolk-free wet and dry
mass) and structurally larger (tibiotarsus and culmen lengths) than hatchlings
emerging from smaller eggs.
• As with many other precocial birds, larger hatchlings also contained more water,
which was reflected in a greater blood volume.
• Emu maternal investment in offspring, measured by egg size and composition, is
significantly correlated with the morphology and physiology of hatchlings and, in
turn, may influence the success of these organisms during the first days of the
juvenile stage.
Avian mothers create different phenotypes by
hormone deposition in their eggs
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In birds, mothers deposit substantial amounts of androgens in their eggs, and experimental
evidence indicates that these maternal androgens influence the chick's early development.
Despite the well-known organizing role of sex steroids on brain and behavior, studies on avian
maternal egg hormones almost exclusively focus on the chick phase.
Eising et al. (2005) found in Black-headed Gulls maternal androgens in the egg enhance
development of nuptial plumage and frequency of aggressive and sexual displays (see Figure
above) almost 1 year after hatching.
The long-lasting effects may be mediated by an upregulation of androgen receptors later in life.
Alternatively, early hormone exposure may influence the hypothalamus-pituitary-gonad axis,
resulting in higher androgen production later in life.
The long-lasting effects of egg androgens are almost certainly beneficial for Darwinian fitness.
Successful territory establishment and defense by means of aggressive interactions are essential
for reproductive success in this colonial breeder.
displays are also important for mate selection.
maternal hormone deposition may profoundly influence differentiation of fitness related traits.
Since these hormones suppress early immune function of the chick and reduce long-term survival,
mothers faced with a trade-off between offspring with lower survival prospects but higher yearly
reproductive success, or with higher chances of survival and lower annual reproductive output.
By producing eggs that differ in levels of maternal hormones, mothers seem to produce a variety
of phenotypes, perhaps an adaptive strategy in unpredictable environmental conditions.
Since natural selection acts upon such phenotypic variation, shaping a population's demography,
the role of maternal androgens in this selective process may be much greater than anticipated
Enhanced social behaviors (frequency h-1) and dominance in 10-month-old gulls from
eggs injected with androgens (black bars) compared to birds from eggs injected with oil
(open bars). O, oblique display; F, forward display; C, charge; P, aggressive peck;
D, displacement. Sex did not affect behavior.
Lesser Black-backed Gulls
© Arthur Grosset
Weaker Birds Use Steroids to Boost
Offspring
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Verboven et al. (2003) reported that female gulls in poor condition were more likely to give
their chicks a hormone boost to improve their chances of survival.
experimentally enhanced maternal condition by supplementary feeding Lesser Black-backed
Gulls (Larus fuscus) during egg formation and compared the concentrations of steroids
(including testosterone) in their eggs with those in eggs laid by control females.
Egg androgens could affect offspring performance directly through chick development
and/or indirectly through changes in the competitive ability of a chick relative to its siblings.
Contrary to expectation, females with experimentally enhanced body condition laid eggs
with lower levels of androgens.
This suggests that less healthy females pass on more steroids than healthy ones in a bid to
enhance the performance of their young.
Verboven originally thought gulls in good condition would put more steroids in their eggs.
discovered that healthy birds don’t tend to give their eggs the extra boost.
compared the situation to struggling athletes who take performance-enhancing drugs: A
poor sports person wants to use steroids to conceal poor performance but if you are good
you don’t need to use them.
Vertebrate sex determination systems (next slide)
• Phylogeny of major vertebrate clades showing sex determining
systems found in members of the respective clade
• ‘Multiple’ indicates involvement of more than one pair of
chromosomes in sex determination.
• TSD: temperature-dependent sex determination (From: Ezaz 2006).
Vertebrate sex determination systems
XX/XY
ZZ/ZW
TSD
Avian sex determination
• Ellegren 2001 -- molecular determinants in birds remain a mystery.
• different from mammals, with no homolog to mammals’ maleness gene
• failure to identify such a gene in birds is probably a reflection of the fact
that, despite the occurrence of two sexes being nearly universal throughout
the animal kingdom, the genes involved seem unrelated
• This raises obstacles for comparative gene studies of sexual development.
• In birds, females are heterogametic, with the Z and W sex chromosomes.
• Males are homogametic (ZZ).
• However, it is not clear whether it is the presence of the female-specific W
chromosome that triggers female development, or the dose of Z
chromosome that confers maleness.
• An intriguing additional possibility is that both Z and W matter!
• In marsupials, Y is a dominant testis determining chromosome, while X
determines the choice between pouch and scrotum.
• Possible that the two sex chromosomes mediate different aspects of sex
differentiation in birds.
Sex determination in birds
• Two potential mechanisms for determination among birds. (A) the
presence of the W chromosome triggers femaleness or (B) the
presence of two Z chromosomes confers maleness.
XY and ZW systems
Red-necked Grebe nest
Source:
http://www.wetlands.org/programs/RussiaCD/eng/
3/32/321/red-05.htm
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Relationships between Vertebrate ZW and XY Sex Chromosome Systems Current
Biology, Volume 16, Issue 17, 5 September 2006, Pages R736-R743 Tariq Ezaz, Rami Stiglec,
Frederic Veyrunes and Jennifer A. Marshall Graves
H.J. Muller suggested sex chromosome pairs evolved from a pair of autosomes.
theory adapted to explain variations in snake ZW chromosomes and later mammal XY;
assume the two systems arose independently
S. Ohno pointed out similarities between the mammal X and the bird/reptile Z forty years
ago, but his speculation that they had a common evolutionary origin, or at least evolved
from similar regions of the genome, has been undermined by comparative gene mapping,
and it is currently commonly accepted that mammal XY and reptile ZW systems evolved
independently from a common ancestor.
Now have evidence for the alternative theory, that ZW/XY transitions occurred during
evolution, citing examples from fish and amphibians, and probably reptiles.
comparative genomics and cytogenetics leads to reconsideration of Ohno's idea and new
hypothesis that mammal XY system arose directly from ancient reptile ZW system.
Posits that XY system arose directly from the ancient reptile ZW system found in fish,
amphibians, reptiles and birds
Incubation temperature and avian sex ratios
• Although common in reptiles, incubation temperature has not been
considered a factor in sex ratios in birds.
• However, Goth and Booth (2005) found incubation temperature does affect
sex ratios in megapodes, which are exceptional among birds because they
use environmental heat sources for incubation.
• In the Australian Brush-turkey (Alectura lathami), a mound-building
megapode, more males hatch at low incubation temperatures and more
females hatch at high temperatures, whereas the proportion is 1:1 at the
average temperature found in natural mounds.
• Chicks from lower temperatures weigh less, which probably affects
offspring survival, but are not smaller.
• Megapodes possess heteromorphic sex chromosomes like other birds,
which eliminates temperature-dependent sex determination, as described
for reptiles, as the mechanism behind skewed sex ratios at high and low
temperatures.
• Goth and Booth (2005) suggest sex -biased temperature-sensitive embryo
mortality because mortality greater at the lower and higher temperatures,
and minimal at middle temperature where sex ratio was 1:1.
Female birds can bias the sex of
their chicks 1
• Whether a bird is more likely to lay a male or female egg depends on which sex will
have the greatest chance of doing well.
• Rutstein et al. (2004) adjusted the food intake of female Zebra Finches [see photo
of female (left) and male (right) Zebra Finches] & found that well-fed females more
likely to produce daughters, while less well nourished birds likely to have sons.
• female offspring need to be better nourished than males to survive and grow.
• In most animals sex ratio is close to 50:50 and extremely resistant to change.
• In mammals, including humans, the sex of the baby is determined by whether the
sex chromosome in the sperm is male or female.
• But in birds, it is the female’s egg rather than the male’s sperm that determines sex
• Thus the female has the potential to determine the sex of her young by whether
she ovulates male or female eggs.
Female birds can bias the sex of their chicks 2
• female Zebra Finches seem to be able to exert control over whether to produce a
male or female egg depending on which of the two is most likely to be successful.
• Our research tells us that they do it, and we understand why.
• The big question is: how do they do it?
• In many animals, females need to be well-nourished and in good condition if they
are to breed, as eggs are costly to produce.
• Bigger eggs tend to lead to bigger young that are more likely to survive.
• Such ‘sex ratio adjustment’ is well documented in certain insects, such as bees and
wasps, but is less well understood in birds and mammals.
• Birds are an excellent model to use in the study of sex ratio adjustment because,
using molecular techniques, scientists can establish the sex of each egg soon after
laying.
• Further, all the resources given to the developing embryo are present in the egg at
laying.
• Thus the size and the content of the egg are measures of the amount of resources
that the female has allocated to that egg, which affects its subsequent survival
chances.
Female birds can bias the sex of their chicks 3
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The authors manipulated the diet quality of Zebra Finches to look at the effects of
body condition on female investment.
females able to exert a strong degree of control over production of male and
female eggs.
When females fed on a low quality diet, eggs were considerably lighter than those
laid when they were fed a high quality diet, and they also laid far more male eggs
on a low quality diet.
This is the converse situation to that described 30 years ago for mammals, but it
makes sense for Zebra Finches.
Previous research has shown that under poor nutritional conditions, female Zebra
Finches grow more slowly and survive less well compared to males.
Therefore, females are producing more of the sex with the highest survival chances
under those conditions.
Mother House Finches Control Baby's Sex 1
• female House Finches tip the odds in their babies' favor by pre-determining gender.
• Female House Finches (Carpodacus mexicanus) adjust sex and growth of their
offspring to account for the order in which the eggs are laid, thereby reducing
mortality of their sons and daughters by 10 - 20%.
• Badyaev et al. (2002) studied two populations of House Finches that have diverged
significantly over the past 20 years.
• They found patterns in how a baby finch's sex and position in the laying order
affected both its growth pattern and chance of survival.
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In Montana, first-born females exhibited better survival odds than males.
in Alabama, first-born males survived more often.
• Such differences seem to drive maternal finches to select whether sons or
daughters hatch first.
• Breeding females in both Montana and Alabama populations lay male and female
eggs in different sequences within clutches thus placing sons and daughters in the
most advantageous positions for survival in that particular environment
Mother Finches Control Baby's Sex 2
Photo by Alexander Badyaev
• Exactly how finch mothers control offspring sex, survival and growth
remains a mystery, but such adjustments facilitate adaptation to local
environments.
• Observing such acclimatization provides empirical support for the
hypothesis that parental effects play a crucial role at the initial stages
of population divergence by enabling establishment of populations in
novel environments
Internest differentiation among eggs
• In some species, such as the Common Murre, where different
females lay eggs with very different markings, the uniqueness may
have a purpose. Distinctive patterns, as in the eggs shown, help
females identify their own egg in a colony where thousands of eggs
may dot a cliff face.
Source:
http://www.absc.usgs.gov/research/seabird_foragefish/seabirds/fla
sh_cards/common_murre.html
Evolution of egg color and patterning in birds 1
• Avian eggs differ dramatically in color and patterning among species
• Kilner (2006) reviewed the literature that suggests that just a few
selective agents can explain much of the variation in egg appearance.
• Ancestrally, bird eggs were probably white and immaculate.
• Ancient diversification in nest location, and hence in the clutch's
vulnerability to attack by predators, can explain basic differences
between bird families in egg appearance.
• The ancestral white egg has been retained by species whose nests
are safe from attack by predators, while those that moved to a more
vulnerable nest site are now more likely to lay brown eggs, covered in
speckles, just as Wallace hypothesized more than a century ago.
• Even blue eggs might be cryptic in a subset of nests built in
vegetation.
White eggs
• Eggs of kingfishers and other cavity nesting birds, such as
woodpeckers and some owls, are often white.
• The brightness of the eggs may help the parents to more easily locate
them in the cavity. Shown here is the egg of a Barn Owl.
Source:
http://www.amonline.net.au/bird
s/gallery/eggs.htm
http://www.skullsunlimited.com/bird-eggs.htm
Evolution of egg color and patterning in birds 2
• It is possible that some species have turned ancient adaptations to
new functions, for example
• to signal female quality,
• to protect eggs from damaging solar radiation,
• to add structural strength to shells when calcium is in short supply.
• The threat of predation, together with the use of varying nest sites,
appears to have increased the diversity of egg coloring seen among
species within families, and among clutches within species.
Evolution of egg color and patterning in birds 3
• Brood parasites and their hosts have probably secondarily influenced
the diversity of egg appearance.
• Each drives the evolution of the other's egg color and patterning, as
hosts attempt to avoid exploitation by rejecting odd-looking eggs
from their nests, and parasites attempt to outwit their hosts by laying
eggs that will escape detection.
• This co-evolutionary arms race has increased variation in egg
appearance both within and between species, in parasites and in
hosts, sometimes resulting in the evolution of egg color
polymorphisms.
• It has also reduced variation in egg appearance within host clutches,
although the benefit thus gained by hosts is not clear.
Egg-laying
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"Initially the female stood motionless in the nest cup.
The first sign of egg- laying was usually intensified breathing, occasionally with rhythmic
opening and closing of the bill that pointed either horizontally forwards or upwards.
head drawn in and the body feathers were fluffed out; the Coal Tit raised its crown
feathers.
tail kept horizontal or elevated up to about 45 degrees.
Tip of the tail started nodding movements synchronously with rhythmic depressions of
the rump.
These movements which apparently were caused by throes of parturition when the egg
traveled down the oviduct, were almost invisible to begin with but gathered in strength
and ended with a sudden elevation of the rump that marked the moment of egg-laying.
Then the bird “froze” in a motionless posture, termed “recovery phase.”
This last rise of the rump clearly indicated that the egg had just been laid.
Duration of egg-laying varies a great deal even within species.
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The opening and closing of the bill and rhythmic movements of the back and tip of the tail occurs repeatedly for
up to 4 minutes in the Prairie Warbler, presumably corresponding to the duration of egg- laying.
For 3 eggs of the Goldcrest, only 8-9 seconds elapsed between the first visible sign of pressure and the moment
of egg- laying.
In tits, this period varied from about 10 to 77 seconds, mostlv 20-30 seconds.
The Cuckoo (Cuculus canorth) which is a brood parasite, is known to lay the egg remarkably swift, usually within
10 seconds with a lower limit of only 3-4 seconds.
Presumably this short duration for cuckoos is an adaptation to parasitic behavior."--From: Haftorn (1996).