BIO 554/754
Avian Reproduction:
Anatomy & the Bird Egg Ornithology |
 |
- Gonads - paired testes in males & usually a single ovary in
females
- Ovary
- most birds have only left ovary but 2 ovaries
are typical of many raptors
- contains from 500 to several thousand primary
oocytes
- Testes & follicles increase dramatically in size as the
breeding season approaches.
- As day length increases, photic stimulation of
the hypothalamus results in the secretion of Gonadotropin releasing
hormone (GnRH below). When activated by GnRH, the anterior pituitary
secretes two gonadotropin hormones, follicle-stimulating hormone (FSH)
and luteinizing hormone (LH). FSH acts on sperm-producing structures in
the testes, while LH acts on the interstitial cells of the testes causing
them to secrete the steroid hormone testosterone. The pituitary gland
monitors the amount of testosterone in the blood, thus creating a negative
feedback loop to maintain hormone levels within a set range (Akins and
Burns 2001).
- Ambient visual cues, such as daylight, activate
photosensitive loci in the brain both indirectly, through the eyes, and
directly, through the skull. The hypothalamus of the bird brain contains
special cells that are sensitive to extremely low light levels,
intensities comparable to the amount of light that can penetrate brain
tissue (Akins and Burns 2001).
From: Akins and Burns (2001)
The pattern of testosterone secretion in free-living populations
of Song Sparrows.
Plasma levels peak in April and May as breeding got underway and then were maintained at a lower “breeding baseline” during the
rest of the breeding season. As prebasic molt ensued, plasma levels of testosterone were basal and remained so throughout autumn and winter.
From: Wingfield and Hahn (1994).
Plasma levels peak in April and May as breeding got underway and then were maintained at a lower “breeding baseline” during the
rest of the breeding season. As prebasic molt ensued, plasma levels of testosterone were basal and remained so throughout autumn and winter.
From: Wingfield and Hahn (1994).
Biological
actions of the steroid hormone testosterone. The morphological, physiological and behavioral actions
of testosterone that are essential
for male reproductive function are given on the right hand and lower sides of the figure. The “costs” of prolonged high levels of testosterone are given on the
left hand side in italics. The patterns of plasma testosterone levels may be a function of secretion patterns to maintain male reproductive function, and “costs”
of testosterone that require that plasma levels be low. From Wingfield et al. (2000).
for male reproductive function are given on the right hand and lower sides of the figure. The “costs” of prolonged high levels of testosterone are given on the
left hand side in italics. The patterns of plasma testosterone levels may be a function of secretion patterns to maintain male reproductive function, and “costs”
of testosterone that require that plasma levels be low. From Wingfield et al. (2000).
Testosterone
increases availability of carotenoids --
Androgens and carotenoids play a fundamental role in the expression of
secondary sex traits in animals that communicate information on individual
quality. In birds, androgens regulate song, aggression, and a variety of
sexual ornaments and displays, whereas carotenoids are responsible for the
red, yellow, and orange colors of the integument. Parallel, but independent,
research lines suggest that the evolutionary stability of each signaling
system stems from tradeoffs with immune function: androgens can be
immunosuppressive, and carotenoids diverted to coloration prevent their use
as immunostimulants. Despite strong similarities in the patterns of sex, age
and seasonal variation, social function, and proximate control, there has
been little success at integrating potential links between the two signaling
systems. These parallel patterns led us to hypothesize that testosterone
increases the bioavailability of circulating carotenoids. To test this
hypothesis, Blas
et al. (2006) manipulated
testosterone levels of Red-legged Partridges (Alectoris rufa) while
monitoring carotenoids, color, and immune function. Testosterone treatment
increased the concentration of carotenoids in plasma and liver by >20%.
Plasma carotenoids were in turn responsible for individual differences in
coloration and immune response. These results provide experimental evidence
for a link between testosterone levels and immunoenhancing carotenoids that (i)
reconciles conflicting evidence for the immunosuppressive nature of androgens,
(ii) provides physiological grounds for a connection between two of
the main signaling systems in animals, (iii) explains how these
signaling systems can be evolutionary stable and honest, and (iv) may
explain the high prevalence of sexual dimorphism in carotenoid-based
coloration in animals.
|
 Red-legged Partridge (Photo by G. Bortolotti) |
- occurs in seminiferous tubules of the testes (shown below)
- occurs best at slightly cooler temperatures, so spermatogenesis
may occur primarily at night when body temperatures are slightly lower
Light photomicrograph of a section of a testis showing a seminiferous tubule during full
semen production. SG indicates spermatogonia; PS, primary spermatocyte; Ss, secondary spermatocyte;
MS, mature spermatocyte; and L, lumen (original magnification ×800) (Samour 2002).
- sperm are stored at the terminal end of the vas
deferens (seminal glomus), and this creates a swelling called the cloacal
protuberance
Male birds have paired abdominal testes lying
cranioventral to the first kidney lobe. Testes increase dramatically in size
during the breeding season. The vas deferens emerges medially and passes
caudally to the cloaca where it has a common opening with the ureter in the
Urodeum. The terminal vas deferens is swollen as a storage organ: the seminal
glomus (or seminal vesicle as in the drawing to the right).
As in mammals, sperm formation is temperature sensitive, and maturation is
assisted by nocturnal drops in temperature, or by the development of
scrotal-like external thermoregulatory swellings holding the seminal
glomera.In addition, male birds tend to have relatively low extragonadal sperm reserves and sperm are ejaculated soon after production in the testes. |
 |
 Cloacal protuberance |
 Longitudinal section of the cloaca of a male budgerigar during the culmination phase of the breeding cycle. SG indicates seminal glomus; P, proctodeum; and C, cloaca (original magnification ×12) (Samour 2002). |
Sperm
competition and testes size --
Comparative analyses suggest that a variety of ecological and behavioural
factors contribute to the
tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, Pitcher et al. (2005) examined several ecological
and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate
analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding
density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also
larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts,
monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that
sperm depletion may play a role in the evolution of testes size. These results suggest that traditional ecological and behavioural variables, such as
social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.
tremendous variability in extrapair mating among birds. In an analysis of 1010 species of birds, Pitcher et al. (2005) examined several ecological
and behavioural factors in relation to testes size; an index of sperm competition and the extent of extrapair mating. In univariate and multivariate
analyses, testes size was significantly larger in species that breed colonially than in species that breed solitarily, suggesting that higher breeding
density is associated with greater sperm competition. After controlling for phylogenetic effects and other ecological variables, testes size was also
larger in taxa that did not participate in feeding their offspring. In analyses of both the raw species data and phylogenetically independent contrasts,
monogamous taxa had smaller testes than taxa with multiple social mates, and testes size tended to increase with clutch size, which suggests that
sperm depletion may play a role in the evolution of testes size. These results suggest that traditional ecological and behavioural variables, such as
social mating system, breeding density and male parental care can account for a significant portion of the variation in sperm competition in birds.
Testis size increases with colony size in Cliff
Swallows -- By using a
sample of over 800 male Cliff Swallows (Petrochelidon pyrrhonota) that
died during a rare climatic event in their Nebraska study area in 1996, Brown
and Brown (2003) investigated how testis size was related to body size, age,
parasite load, and a bird's past colony-size history. Testis volume increased
with body size. After correcting for body size, testis volume was lowest for
birds age 1 and 2 years but did not vary with age for males 3 years old or
more. Birds occupying parasite-free (fumigated) colonies had significantly
larger testes than did birds at nonfumigated sites. Testis volume increased
significantly with the size of the breeding colonies a bird had used in the
past. These results show within a species that larger testes are favored in
more social environments, probably reflecting a response to increased rates
of extrapair copulation (and thus sperm competition) among Cliff Swallows in
large colonies. The presence of ectoparasites, by inflating levels of plasma
corticosterone, may in turn reduce testis mass. These data provide no support
for the hypothesis that large testes, perhaps by producing more testosterone,
are immunosuppressive and thus costly for that reason.
|
|
Cliff Swallows
- Most birds have only one ovary and one oviduct. In early stages of
embryonic development, each female bird has two ovaries; only the left one
develops into a functional organ. In some birds, such as hawks, the right
ovary and oviduct usually develop. A mature ovary looks like a cluster of
grapes. and may contain up to 4,000 small ova which can develop into
mature ova.
- With fertilization, the ovum
(egg) becomes a
developing embryo
- The
embryo passes through the oviduct; typically takes about 24 hours (for
passerines & most other birds)
- The demand for calcium to make the egg shell is very high, and so
the circulating levels of blood calcium in birds are greatly elevated
compared to mammals, typically twice as much.
 |
In most birds, only the left ovary
and oviduct persist. The ovary enlarges greatly during the breeding season.
Active ovaries resemble bunches of tiny grapes -- the developing follicles.
The oviduct opens medially to it in a funnel-shaped ostium. Ovulation results
in the release of an egg from a mature follicle on the surface of the ovary.
The egg, with extensive food reserves in the form of concentric layers of yolk,
ispicked
up by the ostium and ciliary currents carry
it into the magnumregion.
Over about three hours the egg receives a coating of albumen.
The egg then passes into the isthmus, where the shell membranes are deposited. This takes about one hour. The egg them moves to theuterus, or shell gland, where the calcareous shell is added and, in some birds, pigment is added in characteristic patterns. The egg then passes into the vagina and cloaca for laying. |
 |
Variation among bird species in the relative amount of yolk in eggs and the amount of energy available to the developing embryo (kJ-g -1, or kilojoules per gram). From top to bottom, the hatchlings are an altricial Brown Creeper, a semiprecocial Least Tern, a precocial Ruddy Duck, a superprecocial Mallee Fowl (Leipoa ocellata), and a Brown Kiwi (Apteryx australis). Kiwis are ‘outliers.’ Female kiwis produce extremely large eggs for their size (with substantial amounts of yolk), but young typically remain in the nest for several days and so are best classified as semiprecocial (From: Sotherland and Rahn 1987).
Kiwi lays an egg
The left egg found inside the female
oviraptorosaurian. The
texture of the shell pieces probably resembles the original texture of the egg. Credit: Yen-nien Cheng |
Eggs discovered inside dinosaur -- The discovery of eggs inside a
dinosaur has provided new clues about dinosaur reproductive biology and more
support for the hypothesis that birds evolved from dinosaurs. The pair of
eggs are the first found inside a dinosaur. Sato et al. (2005) found that the
dinosaur produced eggs in some ways like a crocodile and in other ways like a
bird. Crocodiles have two ovaries enabling them to lay a clutch of eggs.
Birds have a single ovary and lay only one egg at a time. The dinosaur's
egg-producing capability lay somewhere in between, suggesting a possible link
with modern birds. It had two ovaries, but produce only one egg at a time
from each ovary.
Sato et al. (2005) studied a dinosaur from a group of dinosaurs called oviraptorosaurians. This type of dinosaur — probably 3 - 4 meters long — is a subgroup of the theropods. The dinosaur was excavated in |
Dinosaur egg
Female
birds can bias the sex of their chicks.-- 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 below right] & found that well-fed females were more likely to
produce daughters, while less well nourished birds were more likely to have
sons. This is exactly as predicted by the fact that female offspring need to
be better nourished than males if they are to survive and grow well.
 The authors noted that: “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 what sex the chick will be. Thus the female has the potential to determine the sex of her young by whether she ovulates male or female eggs. In some way, 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. The authors explained: “We manipulated the diet quality of Zebra Finches to look at the effects of body condition on female investment. We found that females were able to exert a strong degree of control over the production of male and female eggs. When females were fed on a low quality diet, they laid eggs that were considerably lighter than those laid when they were fed on 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.” |
 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. |
Avian sex determination (Ellegren 2001) -- The molecular
determinants behind sexual development in birds remain a mystery. The process
is known to be different from that in mammals, with no homolog to the gene
that confers maleness in mammals found in birds. The 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 virtually unrelated among metazoan phyla. These
differences raise obstacles for comparative or candidate gene approaches in
studies of sexual development.
In birds, females are the heterogametic sex, with one copy each of 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, for example, Y acts as a dominant testis determining chromosome, while the X chromosome determines the choice between pouch and scrotum. Maybe a system where the two sex chromosomes mediate different aspects of sex differentiation is also used in birds. |
Vertebrate sex determination systems. Phylogeny of major vertebrate clades showing the 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).
in birds. However, Goth and Booth (2005)
found that 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 the skewed sex ratios at high and low
temperatures. Instead, Goth and Booth (2005) suggest a sex -biased
temperature-sensitive embryo mortality because mortality was greater at the
lower and higher temperatures, and minimal at the middle temperature where the
sex ratio was 1:1.- For most birds, copulation involves a 'cloacal kiss', with the
male on the female's back & twisting his tail under the female's
- copulation typically lasts just a few seconds (but there are
exceptions - see Phony phallus puts sperm ahead in bird first below)
Bald Eagles mating
White-throated Kingfishers mating
Phony
phallus puts sperm ahead in bird first-- "These birds
would be at it for 10-20 minutes," said co-author Tim Birkhead of the
Red-billed Buffalo Weaver. Males use their organ to rub females and improve
their sperm's chance of success. Few male birds have a phallus; most achieve
fertilization via a cloacal kiss. So 19th-century reports of a mock member in
the Buffalo Weaver sent Winterbotton et al. (2001) to
|
|
- males in a few species, including most waterfowl & ostriches
(see diagram below), have an intromittent organ; most males do not
Diagram of the left lateral view of a retracted and erect phallus of a male Emu or Rhea. The top drawing
represents the phallus within the pouch. A. vas deferens, B. urideum, C. proctodeum, D. pocket to contain phallus,
E. erectile wall of phallus, F inverted hollow tube of phallus, G. phallic sulcus, H. erectile tissue, and I. erect phallus
with blind hollow tube. (Source: http://www.cassowary.com/workshop.html)
Examples of genital covariation in waterfowl.
(A) Harlequin Duck (Histrionicus histrionicus) and (B) African Goose (Anser
cygnoides), two species with a short phallus and no forced copulations, in
which females have simple vaginas. (C) Long-tailed Duck (Clangula hyemalis),
and (D) Mallard (Anas
platyrhynchos), two species
with a long phallus and high levels of forced copulations, in which females
have very elaborate vaginas (size bars = 2 cm). ] = Phallus, * = Testis, star =
Muscular base of the male phallus, > = upper and lower limits of the vagina
(From: Brennan
et al. 2007).
Eversion of a male Muscovy duck penis
Explosive
eversion and functional morphology of the duck penis -- Coevolution of male and female genitalia
in waterfowl has been hypothesized to occur through sexual conflict. This
hypothesis raises questions about the functional morphology of the waterfowl
penis and the mechanics of copulation in waterfowl. Brennan et al. (2010) used
high-speed video of phallus eversion and histology to describe for the first
time the functional morphology of the avian penis. Eversion of the 20 cm
muscovy duck penis is explosive, taking an average of 0.36 sec, and achieving a
maximum velocity of 1.6 m sec−1. The collagen matrix of the penis is
very thin and not arranged in an axial-orthogonal array, resulting in a penis
that is flexible when erect. To test the hypothesis that female genital
novelties make intromission difficult during forced copulations, Brennan et al.
(2010) investigated penile eversion into glass tubes that presented different
mechanical challenges to eversion. Eversion occurred successfully in a straight
tube and a counterclockwise spiral tube that matched the chirality of the
waterfowl penis, but eversion was significantly less successful into glass
tubes with a clockwise spiral or a 135° bend, which mimicked female vaginal
geometry. These results support the hypothesis that duck vaginal complexity
functions to exclude the penis during forced copulations, and coevolved with
the waterfowl penis via antagonistic sexual conflict.
 Avian sperm |
 Avian sperm storage tubules |
Photomicrographs of sperm storage tubules contained stained and unstained spermatozoa from domestic chicken (Gallus domesticus)
hens (a, b) and turkey (Meleagris gallopavo) hens (c, d). Arrows indicate stained spermatozoa; arrowheads designate unstained spermatozoa.
Scale bars = 25 micrometers. From: King et al. (2002).
King et al. (2002) found that spermatozoa from two different
inseminations (one with stained sperm, one with unstained sperm) generally
segregated into different storage tubules in both chicken and turkey hens. Storage tubules contained mixed populations of spermatozoa were
found in only 4% of chicken and 12% of turkey storage tubules examined. They concluded that the mechanism of last-male precedence does
not appear to be due to the stratification of spermatozoa within the tubules.
segregated into different storage tubules in both chicken and turkey hens. Storage tubules contained mixed populations of spermatozoa were
found in only 4% of chicken and 12% of turkey storage tubules examined. They concluded that the mechanism of last-male precedence does
not appear to be due to the stratification of spermatozoa within the tubules.
 |
Innervation of sperm storage tubules (Freedman et al. 2001) --
Immunohistochemical staining of a turkey uterovaginal junction and sperm
storage tubules. This micrograph shows a fluorescing neuron (green) near some
sperm storage tubules (SST). The blue areas (se) are the surface epithelium
lining the lumen of the uterovaginal junction and the epithelium of the sperm
storage tubules. The arrow points to a magenta-stained area of one SST that
indicates the presence of actin (a protein found in smooth muscle. The total
image is 19 micrometers across. This association between neurons and SSTs provides evidence that SSTs are innervated and suggests that the storage and release of sperm from SSTs can, perhaps, be controlled. |
That sperm in the SSTs are invariably positioned with their heads directed towards the distal end of the tubule suggests that egress from the SSTs is passive. Sperm are lost from the SSTs more or less continuously at a constant per capita rate. They enter the uterus and are carried passively to the infundibulum. Sperm accumulate or move relatively slowly through the infundibulum so that there is usually a population available to fertilize each ovum as it is ovulated. On ovulation, the ovum is captured by the prehensile, funnel-shaped infundibulum and the sperm swarm over the surface of the ovum; their target is the germinal disc, which contains the female pronucleus. At this stage, the ovum is bounded by the inner perivitelline layers (IPVL). The clustering of sperm and holes made by sperm in the IPVL around the germinal disc suggest that sperm might use chemical signals to locate the germinal disc.
In contrast to most other taxa, where only a single sperm enters the ovum, polyspermy is typical in birds. Several sperm enter the germinal disc region, hydrolyzing the IPVL via the acrosome reaction of the sperm, whereby the release of enzymes from the sperm acrosome enables the sperm nucleus to enter the ovum. However, only a single spermatozoon fuses with the female pronucleus and the remaining sperm are shifted to the periphery of the germinal disc and play no further part in development. Fertilization includes the penetration of ovum by sperm as well as the fusion of the male and female pronuclei (syngamy). Because embryo development begins almost immediately, many cell divisions have occurred by the time the ovum has become incorporated into the egg and the egg is laid (in most species) 24 hr later.
 Scanning electron photomicrograph of a budgerigar spermatozoon. A indicates acrosome; H, head; and T, tail (original magnification ×20000) (Samour 2002). |
 Transmission electron photomicrograph of the longitudinal section of part of the nucleus and midpiece of a Budgerigar spermatozoon. N indicates nucleus; PC, proximal centriole; DC, distal centriole; F, axial filament complex; and M, mitochondria (original magnification ×30000) (Samour 2002). |
Light photomicrograph of a zona-free hamster ovum with
numerous budgerigar spermatozoa bound to its surface
(original magnification ×215) (Samour 2002).
Repelling clingy exes helps snipe save sperm -- Writer Gore Vidal once said that
he never passed up an opportunity to have sex or appear on television. Some
male birds would disagree on at least one count. Having mated with a female,
a male Great Snipe (Gallinago media) will reject her further advances
and even chase her away. Male Great Snipe form leks to eye up the talent
before choosing a mate. A few males get the most sex. Popular birds can get
more than half of the matings, perhaps 10 a day. Hence their pickiness,
suggest Saether et al. (2001). As male Great Snipe take no part in caring for
their offspring, it was thought they had nothing to lose by mating as much as
possible. But top males, overburdened with potential partners, must share
sperm with care and spread their favors around. Sperm budgeting is the only
possible explanation for male snipes' ungrateful behavior. Like a
nightclub, Great Snipe leks see their share of aggravation. "All four
kinds of mating conflicts happen" - male choice, female choice, and male
and female competition - explains Saether. Males are more likely to repel
clingy exes if there are a lot of other females around. Females fight with
one another, and males from neighboring territories chase their rivals'
females away. Hostility towards old flames might be a bid to maintain order.
"If a male gets rid of an unwanted female it's one less problem to worry
about," says Saether. Female snipe probably seek to mate again so that
they can get enough sperm to fertilize their eggs. Rejected females tend to
lower their sights and settle for less popular males. -- John Whitfield, Nature
Science Update
|
 |
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 - amnion
- surrounds only the embryo
- inner layer of cells secretes amniotic fluid in
which the embryo floats; fluid keeps the embryo from drying out and
protects it
- chorion - surrounds all embryonic structures & serves as a
protective membrane
- allantois (or allantoic sac)
- grows larger as embryo grows, fuses with the
chorion & is called the chorio-allantoic membrane
- works together with chorion to permit
respiration (exchange of oxygen and carbon dioxide) and excretion
- important in storage of nitrogenous wastes (uric
acid)
Relative egg mass (corrected for adult mass) is greater in species with longer embryonic periods (days) among 64 passerine species in tropical
Egg size variation among tropical and temperate songbirds -- Species with “slow” life history strategies (long life, low fecundity) are thought to produce high-quality offspring by investing in larger, but fewer, young. Larger eggs are indeed associated with fewer eggs across taxa and can yield higher-quality offspring. Tropical passerines appear to follow theory because they commonly exhibit slow life history strategies and produce larger, but fewer, eggs compared with northern species. Martin (2008) found that relative egg mass (corrected for adult mass) varies extensively in the tropics and subtropics for the same clutch size, and proposed a hypothesis to explain egg size variation both within the tropics and between latitudes: Relative egg mass increases in species with cooler egg temperatures and longer embryonic periods to offset associated increases in energetic requirements of embryos. Egg temperatures of birds are determined by parental incubation behavior and are often cooler among tropical passerines because of reduced parental attentiveness of eggs. Cooler egg temperatures and longer embryonic periods explained the enigmatic variation in egg mass within and among regions, based on field studies in tropical
Egg composition and hatchling phenotype -- Parental investment in eggs and,
consequently, in offspring can profoundly influence the phenotype, survival
and evolutionary fitness of an organism. Avian eggs are excellent model
systems to examine maternal allocation of energy translated through egg size
variation. Dzialowski1and Sotherland (2004) used the natural range in Emu (Dromaius
novaehollandiae) egg size, from 400 g to >700 g, to examine the
influence of maternal investment in eggs on the morphology and physiology of
hatchlings. 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 the
physiology of developing Emu embryos, such that late-term embryonic metabolic
rate was positively correlated with egg size and embryos developing in larger
eggs consumed more yolk during development. 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.
|
- Eggs consists of 4 primary components:
- yolk
- energy-rich supply of food
- 21 - 36% lipids & 16 - 22% proteins (with
the rest being water)
- the yolk is suspended in the center of the egg
by twisted strands of protein fibers called chalazae (shown below)
Yolk contains maternal antibodies -- Antibodies are deposited in eggs
during yolk formation through the deposition of immunoglobulins, primarily
IgY (also called IgG), in the yolk. In Chickens (Gallus domesticus),
maternal IgY is catabolized by offspring over the first 14 days post-hatching
and, by about 5 days post-hatching, offspring begin to synthesize their own
IgY. As a result, after approximately two weeks the circulating IgY in young
is principally of endogenous origin. Adult levels are attained between six
weeks and six months of age. However, maternal antibodies may continue to
affect offspring phenotype even after they are catabolized by influencing
growth and developmental rates. In the absence of maternal IgY in chickens
(due to surgical bursectomy of the mother during her own embryogenesis), the
number of cells in the spleen that help lymphocytes (helper T cells) attack
antigens (foreign proteins on pathogens) is depressed. Also, the immune
responsiveness of offspring is depressed, which could lower the survival of
offspring particularly in harsh disease environments (Grindstaff et al.
2003).
|
 Antibodies 'attack' pathogens or toxins they produce by binding to antigens (e.g., proteins in the membranes of bacteria) via their 'binding sites' (the black areas above). This binding can neutralize toxins and attract white blood cells that eliminate pathogens (by phagocytosis). |
Maternal secretion of antibodies and absorption by the young occur only prenatally in birds (with the exception of pigeon crop milk)
(From: Boulinier and Staszewski 2008).
The familiar color of a chicken’s
egg yolk (a) is in stark contrast to the richly pigmented egg yolk of a
lesser Black-backed Gull, Larus
fuscus (b). Such high
maternal investment of carotenoids into egg yolk is typical among wild bird
species, suggesting that these biologically active pigments serve important
functions in the developing bird (From: Blount et al. 2000).
|
Why egg yolk is yellow (or red) (Blount et al. 2000) -- Egg yolk
in birds is colored yellowish-red by carotenoids. Until recently, there has
been no adaptive explanation of why many egg-laying animals provision their
eggs so richly with carotenoids. It now appears that, in developing birds,
carotenoids protect vulnerable tissues against damage caused by free
radicals. Athough embryonic tissues depend on oxidizable, unsaturated fatty
acids in yolk, their abundance makes the tissues susceptible to peroxidation
caused by reactive oxidative metabolites and by free radicals, which are
produced as normal by-products of metabolism. Protection against lipid
peroxidation in young birds is afforded by the actions of yolk-derived
carotenoids and other antioxidants, like vitamin E. Antioxidants also protect
passively-acquired antibodies (IgY; see above) against break-down. Thus,
maternal investment in egg composition, including carotenoids, might have a
greater influence on offspring viability than has been realized. The use of
carotenoid pigments in the sexual displays of female birds might indicate
their ability to produce high quality eggs and chicks.
|
- albumen
- 90% water & 10% protein
- the embryo's water supply, but also serves as a
'shock-absorber' to help protect the embryo
- buffers embryo from sudden changes in
temperature
- shell membranes
- attached to the shell are two membranes, the
inner and outer shell membranes. They protect the egg from bacterial
invasion and help prevent rapid evaporation of moisture from the egg.
Keratin fibers from the outer shell membrane can be seen above, attached to the
calcium carbonate crystals that make up the main shell structure.
(Source: http://www.rit.edu/~tld0898/SEM.html)
- shell
- protects the embryo
- contains thousands of pores (see diagram below)
that permit gas exchange
- generally white in cavity-nesters & colored
and patterned in open nesters (see Ecology of egg colors below)
- color is added to the eggshell from pigments
secreted by cells in the wall of the uterus
Thousands of tiny pores like the one pictured above, cover the shell, providing a passage for gas exchange.
(Source: http://www.rit.edu/~tld0898/SEM.html)
Weaker
Birds Use Steroids to Boost Offspring -- 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. Verboven and her
colleagues 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
noted that “We originally thought that gulls in good condition would
put more steroids in their eggs. But we discovered that healthy birds don’t
tend to give their eggs the extra boost.” She compared the situation to
struggling athletes who take performance-enhancing drugs. She added: “A poor
sports person maybe wants to use steroids to conceal poor performance but if
you are good you don’t need to use them.”
|
Avian mothers create different phenotypes by
hormone deposition in their eggs --
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 that, in
Black-headed Gulls, maternal androgens in the egg enhance the development of
the nuptial plumage and the 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, the early hormone exposure may have influenced 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. In addition, the displays are important for mate selection.
Clearly, in birds, maternal hormone deposition in eggs may profoundly
influence individual differentiation of fitness related traits. Since these
hormones suppress early immune function of the chick and reduce long-term
survival, mothers may be faced with a trade-off between producing offspring
with lower survival prospects but higher reproductive success per year, 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 until now.
|
Egg colors and markings have strong adaptive values. Originally, birds' eggs were probably all white, as reptile eggs are. Eggs that are laid on the ground or in open nests in trees, rather than in cavities, often exhibit cryptic coloration. The eggs blend in with their surroundings and are much less visible to potential predators (e.g., aKilldeer nest).
Sometimes eggs that are laid in open nests are white at first. They then become stained by the mud and rotting vegetation in the nest. Grebes lay white eggs that become stained and cryptically colored over time.
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 below, help females identify their own egg in a colony where thousands of eggs may dot a cliff face.
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.
"Initially the female stood motionless in the nest cup. The first sign of approaching egg- laying was usually intensified breathing, occasionally with rhythmic opening and closing of the bill that pointed either horizontally forwards or more or less upwards. The head was drawn in and the body feathers were somewhat fluffed out; the Coal Tit in addition raised its crown feathers. The tail was kept horizontal or elevated up to about 45 degrees”. Then the 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. 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 is an adaptation to its parasitic behavior."--- From: Haftorn (1996).
Female birds turns part of the cloaca and the last segment of the
oviduct inside out ("like a glove"). The vent is then everted and the
egg emerges far outside at the end of the bulge. As a result, the egg does not
contact the walls of the cloaca and get contaminated by feces. In addition, the
intestine and inner part of the cloaca are kept shut by the emerging egg, and
their contents cannot leave when the hen strains to deliver the egg. Therefore,
eggs are always clean when laid (van der Molen 2002).
Wandering Albatross laying an egg
Kiwi laying an egg
Akins, C. & M. Burns. 2001. Visual control of sexual behavior. In R. G. Cook (Ed.), Avian visual cognition [On-line]. Available:www.pigeon.psy.tufts.edu/avc/akins/
Birkhead,
T. R. and J.-P. Brillard. 2007. Reproductive isolation in birds: postcopulatory
prezygotic barriers. Trends in Ecology and Evolution 22: in press.
Blas, J., L. Perez-Rodriguez, G.
R. Bortolotti, J. Vinuela, and T. A. Marchant. 2006. Testosterone increases
bioavailability of carotenoids: insights into the honesty of sexual signaling. Blount, J. D., D. C. Houston, and A. P. Møller. 2000. Why egg yolk is yellow. Trends in Ecology and Evolution 15: 47-49.
Boulinier, H. and V. Staszewski. 2008. Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology and Evolution, in press.
Brennan, P. L. R., C. J. Clark, and R. O. Prum. 2010. Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia. Proceedings of the Royal Society B, online early.
Brennan, P. L., R. O. Prum, K. G. McCracken, M. D. Sorenson, R. E. Wilson, and T. R. Birkhead. 2007. Coevolution of male and female genital morphology in waterfowl. PLoS ONE 2: e418.
Brown, C.R. and M. B. Brown. 2003. Testis size increases with colony size in cliff swallows. Behavioral Ecology 14:569-575.
Burley, R. W. and D. V. Vadhera. 1989. The avian egg. John Wiley,
Dzialowskil, E. M. and P. R. Sotherland. 2004. Maternal effects of egg size on emu Dromaius novaehollandiae egg composition and hatchling phenotype. J. Exp. Biol. 207:597-606.
Eising, C. M., W.
Müller & T. G.G. Groothuis. 2005. Avian
mothers create different phenotypes by hormone deposition in their eggs.
Proc. Royal Soc. London, Biol. Letters: early on-line.
Ellegren, H. 2001. Hens, cocks
and avian sex determination: a quest for genes on Z or W? European Molecular Biology
Organization Reports 2:192-196.Ezaz, T., R. Stiglec, F. Veyrunes, and J. A. Marshall Graves. 2006. Relationships between Vertebrate ZW and XY Sex Chromosome Systems. Current Biology 16: R736-R743.
Freedman, S. L., V. G. Akuffo, and M. R. Bakst. 2001. Evidence for the innervation of sperm storage tubules in the oviduct of the turkey (Meleagris gallopavo). Reproduction 121: 809-814.
Gosler, A.G., J. P. Higham, and S. J. Reynolds. 2005. Why are birds’ eggs speckled? Ecology Letters 8: 1105-1113.
Goth, A. and D. T. Booth. 2005. Temperature-dependent sex ratio in a bird. Biology Letters 1: 31-33.
Grindstaff, J. L., E. D. Brodie III, and E. D. Ketterson. 2003. Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc. Royal Soc. Lond. B 270: 2309-2319.
Kilner, R. M. 2006. The evolution of egg colour and patterning in birds. Biological Reviews 81: 383–406.
Haftorn, S. 1996. Egg-laying behavior in tits. Condor 98:863-865.
King, L.M., J. P. Brillard, W.M. Garrett, M.R. Bakst, and A.M. Donoghue. 2002. Segregation of spermatozoa within sperm storage tubules of fowl and turkey hens. Reproduction 123:79-86.
Lack, D. 1958. The significance of the colour of turdine eggs. Ibis 100: 145-166.
Martin, T. E. 2008. Egg size variation among tropical and temperate songbirds: an embryonic temperature hypothesis. Proceedings of the National
Pettingill, O.S., Jr. 1985. Ornithology in Laboratory and Field, Fifth ed. Academic Press,
Pitcher, T. E., P. O. Dunn & L. A. Whittingham. 2005. Sperm competition and the evolution of testes size in birds. Journal of Evolutionary Biology 18: 557-567.
Rosenzweig, M.R., A.L. Leiman and S.M. Breedlove. 1996. Biological Psychology. Sinauer Associates,
Rutstein, A.N., P. J. B. Slater, and J. A. Graves. 2004. Diet quality and resource allocation in the zebra finch. Proc. R. Soc. Lond. B (Suppl.). Published online, 20 February 2004.
Saether, S. A., P. Fiske, & J. A. Kalas. 2001. Male mate choice, sexual conflict and strategic allocation of copulations in a lekking bird. Proceedings of the Royal Society
Samour, Jaime H. 2002. The Reproductive Biology of the Budgerigar (Melopsittacus undulatus): Semen Preservation Techniques and Artificial Insemination Procedures. Journal of Avian Medicine and Surgery 16: 39-49.
Sato, T., Yen-nien Cheng, Xiao-chun Wu, D. K. Zelenitsky, & Yu-fu Hsiao. 2005. A Pair of Shelled Eggs Inside A Female Dinosaur. Science 308:375.
Siefferman, L., K. J. Navara, and G. E. Hill. 2006. Egg coloration is correlated with female condition in Eastern Bluebirds (Sialia sialis). Behavioral Ecology and Sociobiology 59: 651-656.
Sotherland, P. R. and H. Rahn. 1987. On the composition of bird eggs. Condor 89: 48-65.
van der Molen, W. H. 2002. Laying an egg. http://www.afn.org/~poultry/egghen.htm.
Verboven, N., P. Monaghan, D.M. Evans, H. Schwabl, N. Evans, C. Whitelaw, and R.G. Nager. 2003. Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the Lesser Black-backed Gull (Larus fuscus). Proceedings of the Royal Society: Biological Sciences 270: 2223 - 2232
Visser, M. E., L. J. M. Holleman, and S. P. Caro. 2009. Temperature has a causal effect on avian timing of reproduction. Proceedings of the Royal Society B: online early.
Welty, J.C. and L. Baptista. 1988. The life of birds, fourth ed. Saunders College Publishing,
Wingfield, J. C., and T. P. Hahn. 1994. Testosterone and territorial behaviour in sedentary and migratory sparrows: Animal Behaviour 47: 77–89.
Wingfield, J. C., J. D. Jacobs, A. D. Tramontin,
Winterbotton, M., T. Burke, & T. R. Birkhead. 2001. The phalloid organ, orgasm and sperm competition in a polygandrous bird: the red-billed buffalo weaver. Behavioural Ecology and Sociobiology 50: 474-482.
Back to Avian Biology
No comments:
Post a Comment