Eggs, egg formation and the timing of breeding

The eggs of birds contain all the nutrients necessary for the developing embryo. The female has to obtain these nutrients, and while in some species these may be gathered and stored over a period of time, in many species they seem to be obtained on a daily basis. Obtaining the calcium necessary for the eggshell may pose special problems for some species, which may have to give up valuable feeding time in order to search for calcium.
Egg size varies considerably, even within species, and the reasons for this are not clear. In the Great Tit Parus major , large eggs produce nestlings which have a higher chance of hatching, surviving to fledging and surviving after fledging. However, large eggs require the female to acquire more nutrients to form them, and large chicks may sometimes be at a disadvantage. The amount of energy required to form a larger egg often seems small unless the metabolic costs of egg formation are taken into account.     

Host selection by Homalodisca vitripennis: the interplay between feeding, egg maturation, egg load, and oviposition

For some phytophagous insects, egg maturation may be dependent on adult feeding. Accordingly, rates of egg maturation may be dependent on the quality and quantity of available food sources. In turn, oviposition behavior could be affected by diet quality via changes in egg load (number of mature eggs carried by a female). Experiments were conducted to determine whether adult feeding may affect oviposition behavior of the glassy-winged sharpshooter, Homalodisca vitripennis. No-choice tests demonstrated that eggs accumulated in glassy-winged sharpshooter abdomens as time since last oviposition increased largely as a function of feeding plant species. In choice tests, glassy-winged sharpshooter females were observed most frequently on the plant species that imparted the greatest egg maturation rate in no-choice tests. Direct tests of the effects of egg load on glassy-winged sharpshooter oviposition behavior found that females were more likely to deposit eggs as egg load increased. Similarly, acceptance of a low-ranked oviposition plant species by female glassy-winged sharpshooters increased with egg load and time since last oviposition. The results indicate that adult feeding affected glassy-winged sharpshooter egg maturation, plant species varied in quality for providing nutrients for egg maturation, and egg load affected oviposition behavior. Thus, the quantity and quality of available feeding plant species may affect glassy-winged sharpshooter egg maturation rates, which in turn may affect the plant species female glassy-winged sharpshooters select for oviposition.     

Effects of experimental calcium availability,egg parameters and laying order on Great Tit Parus major eggshell pigmentation patterns

Many bird species lay eggs speckled with protoporphyrin‐based spots, however, for most of them the function of eggshell spotting is unknown. A plausible hypothesis is that protoporphyrin might have a structural function in strengthening the eggshell and is therefore deposited when calcium is scarce. In this study, we experimentally provided Great Tit Parus major females with supplemental calcium to examine its effect on the protoporphyrin‐based maculation of their eggs. In addition, we studied variation in eggshell pigmentation patterns in relation to other egg parameters and laying order. Calcium‐supplemented females laid larger eggs but shell thickness was not significantly affected by the treatment. Calcium supplementation may reduce the time and energy females devote to searching for calcium‐rich material, so that they can collect more nutrients and so lay larger eggs. Furthermore, pigment darkness was associated with egg volume and shape, which suggests that female quality and environmental food availability may also influence the shell pigmentation pattern. Within clutches, later‐laid eggs had larger and darker spots that were distributed more unevenly on the shell surface. This within‐clutch pattern could be explained by the increase in egg volume and egg shape and a decline in shell thickness with egg‐laying order, which characteristics were all related to shell‐spotting pattern. Eggs with a coronal ring had thinner shells, but pigment intensity and spot size were not related to shell thickness. Thus, our results suggest that concentrated spotting distribution may have a mechanical function, supporting the structural‐function hypothesis.     

The source of the nutrients required for egg production in zebra finches Poephila guttata

The source of nutrients used for egg formation are poorly known for most bird species. This study of the zebra finch Poephila guttata showed that food intake did not increase during egg production, but the decline in female body reserves of protein and fat were sufficient to account for most of the nutrients in a clutch of four eggs. Female birds significantly reduced their activity levels during ova enlargement, which may play a role in diverting resources to egg production. Birds increased their intake of calcium-rich food items when eggs were being laid, and this intake accounted for all the calcium needed for eggshell formation. The zebra finch depends heavily on stored body reserves for egg formation, which is probably unusual in small passerines.     

Egg mass in an asynchronously hatching parrot: does variation offset constraints imposed by laying order?

Life history theory predicts phenotypic trade-offs between the number and quality of offspring produced. Intraspecific variation in egg mass is common in birds and increased egg size can have positive effects on offspring fitness. However, evidence of a trade-off with clutch size is limited. We analyzed variation in mass of 5,743 Green-rumped parrotlet (Forpus passerinus) eggs laid over 15 years to evaluate the potential for facultative adjustment of egg mass and factors governing variation. Heavier eggs had an increased probability of both hatching and fledging but egg mass did not affect postfledging recruitment. Offspring egg mass differed between populations and the potential for seasonal adjustment to egg mass may be related to environmental factors such as seed density. Egg mass was moderately heritable (h ²=0.42) which accounts for some of the individual variation detected, and these results are likely attributable to strong maternal effects. We found an effect of female age on egg mass, but no effects of previous reproductive experience. Finally, egg mass was strongly governed by position within the laying sequence, independent of clutch size, and such adjustment may facilitate brood reduction under some conditions in this highly asynchronous species.     

Fitness consequences of egg-size variation in the lesser snow goose

We investigated the relationship between eggsize variation and (a) egg hatching success, (b) chick survival to fledging and recruitment, and (c) adult female survival, over 12 years in the lesser snow goose (Anser caerulescens caerulescens). By comparing the means and variances of egg size for successful and unsuccessful eggs, our aim was to assess the relative fitness of eggs of different sizes and to determine the type of selection operating on egg size in this species. As both egg size and reproductive success vary with age in the lesser snow goose we controlled for the effects of female age. Egg-size variation is very marked in this population, varying by up to 52% for eggs hatching successfully. However, there was no relationship between egg size and post-hatching survival of goslings to fledging or recruitment, either within or between broods, pooling across years. Egg size varied significantly between successful and unsuccessful clutches in only 2 of 33 individual year comparisons. First-laid eggs surviving to onset of incubation, and eggs hatching successfully, were on average larger than unsuccessful eggs, but this was probably due to the confounding effects of female age-specific and sequence-specific egg survival. Variance of egg size differed significantly between successful and unsuccessful eggs in only 3 of 24, and 0 of 21, individual year comparisons for pre- and post-hatching survival respectively. We therefore found little evidence for a relationship between egg-size variation and offspring fitness, or for strong directional, normalising or diversifying selection operating on egg size, in the lesser snow goose. In addition, there was only weak support for the hypothesis that egg-size variation is maintained by temporal variation in selection pressure (sensu Ankney and Bisset 1973). It is likely that egg-size variation represents the pleiotropic expression of alleles affecting more general physiological or metabolic processes. While this does not rule out the existence of alleles with more direct effects on egg size we suggest that their contribution to heritable egg size is small.     

Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird

Blue-green colours in avian eggs have been proposed as post-mating signals of female phenotypic quality to their mates. Egg colour may not only indicate female value, but also the quality of the eggs themselves and of resulting offspring. To date, there has been no demonstration of an association between egg colour and egg or offspring immune quality. We here show that the intensity of blue-green colour of pied flycatcher Ficedula hypoleuca eggs reflects the amount of maternal antibodies in the yolk, a form of passive immunity crucial for offspring performance. Moreover, egg colour predicts fledging success. Also, incubating females in better condition lay more colourful eggs. The immunoglobulin level in incubating females is positively associated with that in the eggs. These results support the signalling hypothesis of eggshell coloration, underlining its role as an indicator of trans-generational transmission of immune defences in birds.     

THE TIMING OF BIRDS' BREEDING SEASONS

Examination of survival rdtes of nestlings and fledglings of some species show that there is a strong tendency for those young which are hatched earliest in the season to have the greatest chance of surviving to breed. Since natural selection so strongly favours parents who leave many surviving young, the question arises as to why other birds breed later than the date at which they could most successfully raise their young.
It is suggested that the food supply for the breeding females immediately prior to the breeding season may limit their ability to form eggs and the females may thus not be able to lay at the time which would result in young being in the nest at the best time for raising them, but as soon after this time as the female is able to produce her eggs. Not all species are likely to be prevented, by food shortage, from breeding at the best time for raising young and the groups of birds most likely to be affected are discussed.     

Multiple responses to increasing spring temperatures in the breeding cycle of blue and great tits (Cyanistes caeruleus,Parus major)

Many bird species start laying their eggs earlier in response to increasing spring temperatures, but the causes of variation between and within species have not been fully explained. Moreover, synchronization of the nestling period with the food supply not only depends on first‐egg dates but also on additional reproductive parameters including laying interruptions, incubation time and nestling growth rate. We studied the breeding cycle of two sympatric and closely related species, the blue tit Cyanistes caeruleus and the great tit Parus major in a rich oak‐beech forest, and found that both advanced their mean first‐egg dates by 11–12 days over the last three decades. In addition, the time from first egg to fledging has shortened by 2–3 days, through a decrease in laying interruptions, incubation time (not statistically significant) and nestling development time. This decrease is correlated with a gradual increase of temperatures during laying, suggesting a major effect of the reduction in laying interruptions. In both species, the occurrence of second clutches has strongly decreased over time. As a consequence, the average time of fledging (all broods combined) has advanced by 15.4 and 18.6 days for blue and great tits, respectively, and variance in fledging dates has decreased by 70–75%. Indirect estimates of the food peak suggest that both species have maintained synchronization with the food supply. We found consistent selection for large clutch size, early laying and short nest time (laying to fledging), but no consistent changes in selection over time. Analyses of within‐individual variation show that most of the change can be explained by individual plasticity in laying date, fledging date and nest time. This study highlights the importance of studying all components of the reproductive cycle, including second clutches, in order to assess how natural populations respond to climate change.     

Speckled eggs: water-loss and incubation behaviour in the great tit Parus major

Many small passerine birds worldwide lay white eggs speckled with red, brown and black protoporphyrin pigment spots (maculation). Unlike some patterns of avian eggshell pigmentation which clearly serve a crypsis or signalling function, the ubiquity of maculation among passerines suggests that its origins lie in another function, not specific to any particular ecological or behavioural group. Elsewhere, we have presented evidence that protoporphyrin pigments serve a structural function related to eggshell thickness and calcium availability: eggshell maculation in the great tit Parus major increases with decreasing soil calcium levels, pigments demarcate thinner areas of shell, and both the pigment intensity and distribution are related to shell thickness. Here we show that maculation also affects the rate of water loss from the egg during incubation (≈ Mass Loss per Day or MLD, which is critical to egg viability), but not that of unincubated eggs. We also demonstrate, both by observation and experiment, that the effect of female incubation behaviour on MLD compensates in some way for variation in egg characteristics, and that differences between females in the degree of such compensation are related to differences in clutch maculation. Our results suggest that, while a principal function of maculation in this species may be to strengthen the eggshell, it may also reduce eggshell permeability when large amounts of pigment are used, and that this necessitates a behavioural adjustment from the female during incubation. We discuss these findings and make further testable predictions from our model.     

Mechanisms of Fertilization in Fishes

SYNOPSIS. Sperm motility in fishes is, in general, initiatedby simple dilution of the epididymal suspension. A few simpleorganic compounds and poorly characterized proteincontaining"factors" associated with fish eggs seem to enhance sperm motility.True chemotaxis in fish sperm has not been demonstrated. Ultimately,sperm-egg interaction leads to a large, transient increase inthe concentration of free calcium in the egg's cytoplasm. Thiscalcium increase is responsible for lifting the egg's developmentalblock; some mechanisms by which the calcium flux may accomplishthis are discussed. A pH change is apparently not involved inturning on synthetic activity in fish eggs. Electrophysiologicalevents and the fusion of cortical vesicles with the plasma membrane,which are among the earliest changes in the egg resulting fromfertilization, are apparently not necessary for developmentof fish eggs. Synthesis of RNA and protein required for normalcleavage, axiation and organogenesis occurs during and soonafter the calcium transient. Completion of the egg's secondmaturation division occurs within minutes after fertilization.Ooplasmic segregation (by some totally unknown mechanism) andopposition of male and female pronuclei complete the transformationof the egg into a functional zygote.     

Do Male Pied Flycatchers (Ficedula hypoleuca) Adjust Their Feeding Effort According to Egg Colour?

The colour of blue‐green bird eggs has been hypothesized to signal female quality to attending males, who may adjust their level of investment in the brood accordingly. The hypothesis has gained support in studies of Spanish pied flycatchers Ficedula hypoleuca. We performed a cross‐fostering experiment in a Norwegian population of pied flycatchers to provide an independent test of the sexually selected egg colour hypothesis in this species. Egg colour was not significantly correlated with estimates of female quality (clutch size, average egg volume, first egg laying date and feeding rate). There was a significant decrease in chroma and increase in brightness and egg volume during the laying sequence, with some marked differences between six‐egg and seven‐egg clutches that might reflect differences in female quality. However, we found no significant influence of egg colour (foster or original clutch) on male feeding rate or offspring viability (hatching success, average mass and fledging success) and no significant difference in feeding rate for males with six‐egg and seven‐egg foster or original clutches. We conclude that Norwegian male pied flycatchers do not use egg colour as a cue to female quality, thus questioning the generality of previous support for the sexually selected egg colour hypothesis from this species.     

Rates and consequences of relaying in Cassin's auklets Ptychoramphus aleuticus and rhinoceros auklets Cerorhinca monocerata breeding in a seasonal environment

We removed first eggs from early‐laying females to measure rates and consequences of relaying in Cassin's auklets Ptychoramphus aleuticus and rhinoceros auklets Cerorhinca monocerata at Triangle Island, British Columbia, Canada. Based on egg size and composition, the investment that Cassin's auklets made in first eggs was very close to that predicted from adult body mass, whereas rhinoceros auklets invested more. In both species, a high percentage of females relaid (90% of Cassin's and 87% of rhinoceros auklets). Breeding success declined weakly with later laying among control Cassin's auklet pairs, but pairs that we induced to relay bred more successfully than naturally late pairs, and similar to values predicted from laying dates of their first eggs. Their chicks also fledged heavier and younger than late control chicks, and similar to values in early control chicks, but followed the population‐wide seasonal decline in wing length at fledging. Nestling diets were dominated by Neocalanus copepods until late in the season, a sign that feeding conditions remained favourable until late. In contrast, rhinoceros auklet pairs induced to relay followed the population‐wide seasonal decline in breeding success, which was driven by a decline in hatching success. Pacific sandlance Ammodytes hexapterus, thought to be a preferred prey species, virtually disappeared from nestling diets in mid‐to‐late season, yet there was no seasonal decline in fledging mass. However, chicks from replacement eggs followed the declines among control chicks in both age and wing length at fledging. Despite the female having produced a replacement egg, and despite delayed breeding, there appeared to be little immediate consequence associated with relaying for Cassin's auklets, except for a tendency for their chicks to fledge with short wings. Consequences were more marked in rhinoceros auklets (greatly reduced hatching success, and having their chicks fledge with short wings), and this may have been due to the large investment made in eggs, and/or to delayed breeding. Results of this study show that attributes of Cassin's and rhinoceros auklets that lay at different times in the season can be important in driving seasonal declines in breeding performance, as found in studies on other Alcidae. They also show how decisions taken during the egg stage can have variable yet potentially important implications for fitness, even in relatively long‐lived species that lay single‐egg clutches.     

Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca

A recent hypothesis proposes that the bright colors, especiallyblue and green, of many avian eggs may function as signals offemale or offspring phenotypic quality or condition to malesin species with biparental care, inducing them to allocate moreeffort to their offspring. The pigment determining blue andgreen egg colors is an antioxidant whose availability for eggshellcoloring may be limited. To test the signaling function on aspecies with blue eggs, the pied flycatcher Ficedula hypoleuca,we measured egg color with a spectrophotometer on the day oflaying and obtained two principal components from their reflectancespectra that together explained 99% of variation and representedshell lightness, and hue and saturation, respectively. We alsomeasured female immunocompetence during the nestling periodthrough the response to phytohemagglutinin as a measure of cell-mediatedimmunity and the response to a tetanus vaccination as a measureof humoral immunity. The total amount of immunoglobulins inblood of females and of nestlings before fledging was also estimated.Mean within-clutch egg darkness was positively associated withboth measures of female immunocompetence, while better femalecondition was associated with colors tending away from intermediateand toward short wavelengths. Ageing female laid lighter eggs.The mean within-brood level of nestling IgY was also associatedwith mean within-clutch egg colors tending away from intermediateand toward short wavelengths. Mean egg darkness decreased linearlyduring the laying sequence, suggesting pigment limitation. Maleswere observed frequently visiting nests during the laying period,allowing them to observe eggs before the start of incubation.These results support the signaling hypothesis for explainingbright colors of avian eggs.     

DEVELOPMENTAL CONSEQUENCES OF AN EVOLUTIONARY CHANGE IN EGG SIZE: AN EXPERIMENTAL TEST

Larvae of two species of sea urchins (Strongylocentrotus droebachiensis and S. purpuratus) differ in initial form and in the rate of development. To determine whether these differences are attributable to the large interspecific difference in egg size, we experimentally reduced egg size by isolating blastomeres from embryos. The rate of development of feeding larvae derived from isolated blastomeres was quantified using a novel morphometric method. If the differences early in the life histories of these two species are due strictly to differences in egg size, then experimental reduction of the size of S. droebachiensis eggs should yield an initial larval form and rate of development similar to that of S. purpuratus. Our experimental manipulations of egg size produced three clear results: 1) smaller eggs yielded larvae that were smaller and had simpler body forms, 2) smaller eggs resulted in slower development through the early feeding larval stages, and 3) effects of egg size were restricted to early larval stages. Larvae from experimentally reduced eggs of the larger species had rates of development similar to those of the smaller species. Thus, cytoplasmic volumes of the eggs, not genetic differences expressed during development, account for differences in larval form and the rate of form change. This is the first definitive demonstration of the causal relationship between egg size (parental investment per offspring) and life-history characteristics in marine benthic invertebrates. Because larval form influences feeding capability, the epigenetic effects of egg size on larval form are likely to have important functional consequences. Adaptive evolution of egg size may be constrained by the developmental relationships between egg size and larval form: evolutionary changes in egg size alone can result in concerted changes in larval form and function; likewise evolutionary changes in larval form and function can be achieved through changes in egg size. These findings may have broader implications for other taxa in which larval morphology and, consequently, performance may be influenced by changes in egg size.     

Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention

The evolutionary transition between oviparity and viviparity in squamate reptiles presumably occurs via a gradual increase in the duration of egg retention, the production of thinner eggshells, and increases in the vascularity of maternal and embryonic tissues. The 'ease' of this transition may differ among taxa. For example, in the genus Sceloporus , the scalaris species group contains both oviparous and viviparous species, and female Sceloporus scalaris can extend egg retention facultatively in response to the absence of a suitable site for oviposition without impairing embryonic development. In contrast, the undulatus species group contains only oviparous species, and, while female Sceloporus virgatus can extend egg retention, doing so retards embryonic development. I tested several hypotheses that would explain the greater ability of 5. scalaris than S. virgatus to extend egg retention. In this study, female S. scalaris retained eggs for 19 d without affecting the mortality of embryos, total developmental time, or dry mass of hatchlings. In contrast, when female S. virgatus retained eggs for 18 d, embryos had very high mortality and eggs took significantly longer to hatch than control (non-retained) eggs, although the dry mass of hatchlings was not affected. The ability of S. scalaris females to retain eggs with little negative effect on embryonic development was associated with relatively large chorioallantois, relatively thin eggshells, and relatively small clutch masses. These observations suggest that phylogenetic differences in the ability to extend egg retention may facilitate or constrain the evolution of viviparity in some lineages.     

COURTSHIP FEEDING AND THE FITNESS OF FEMALE KATYDIDS (ORTHOPTERA: TETTIGONIIDAE)

Katydid males (Requena verticalis) produce spermatophores with a large sperm-free spermatophylax, which is eaten by the female after mating. In this study, I asked 1) how do spermatophylax nutrients affect the fitness of the mated female and her progeny? 2) does this male-produced food substitute for other food in the diet of the female, or is it a source of specialized nutrients? and 3) does an increase in the size of the spermatophylax eaten influence female reproduction in the same way as the additional spermatophylaxes that would be obtained from multiple mating? An experimental increase either in dietary protein or the number of spermatophylaxes eaten increased the number of eggs produced. However, spermatophylax size had no effect on egg number. An increase in either the size or number of spermatophylaxes eaten resulted in an increase in egg size. There was no influence of protein in the general diet on egg size. This suggests that males provide nutrition not available from other sources. Although there were no direct effects of number of spermatophylaxes eaten by females on the overwintering survival of their progeny, offspring from females producing larger eggs had a relatively higher probability of surviving winter. The amount of spermatophylax eaten had no influence on the mean adult size of progeny but significantly increased the mean date at which sons matured to adulthood. There was no influence of dietary protein on these variables. Since maturation date is positively correlated with adult size in both sexes, it is suggested that the influence of courtship feeding on maturation date may result in an increase in adult size and thus the fitness of sons. A significant correlation between the size of the female and the mean size of her sons (but not daughters) suggests that there is also a heritable component to body size.     

Eggs to die for: cell death during Drosophila oogenesis

Extensive programmed cell death occurs in the female germline of many species ranging from C. elegans to humans. One purpose for germline apoptosis is to remove defective cells unable to develop into fertile eggs. In addition, recent work suggests that the death of specific germline cells may also play a vital role by providing essential nutrients to the surviving oocytes. In Drosophila, the genetic control of germline apoptosis and the proteins that carry out the death sentences are beginning to emerge from studies of female sterile mutations. These studies suggest that the morphological changes that occur during the late stages of Drosophila oogenesis may be initiated and driven by a modified form of programmed cell death.     

Body-size effect on egg size in eublepharid geckos (Squamata: Eublepharidae), lizards with invariant clutch size: negative allometry for egg size in ectotherms is not universal

Within a single clutch, smaller species of ectotherms generally lay a smaller number of relatively larger eggs than do larger species. Many hypotheses explaining both the interspecific negative allometry in egg size and egg size–number trade-off postulate the existence of an upper limit to the egg size of larger species. Specifically, in lizards, large eggs of large species could have too long a duration of incubation, or they could be too large to pass through the pelvic opening, which is presumably constrained mechanically in larger species. Alternatively, negative allometry could be a result of limits affecting eggs of smaller species. Under the latter concept, hatchling size in smaller species may be close to the lower limit imposed by ecological interactions or physiological processes, and therefore smaller species have to invest in relatively larger offspring. Contrary to these lower limit hypotheses, explanations based on the existence of an upper limit always predict negative egg-size allometry even in animals with invariant clutch size, in which naturally there is no egg size–number trade-off. We studied egg-size allometry in lizards of the family Eublepharidae, a monophyletic group of primitive geckos with large variance in body size and an invariant number of two eggs per clutch. We found an isometric relationship between egg and female size that does not support the upper limit hypotheses.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 527–532.     

Sperm morphology and the evolution of intracellular sperm–egg interactions

Sperm morphology is incredibly diverse, even among closely related species, yet the coevolution between males and females of fertilization recognition systems is necessary for successful karyogamy (male and female pronuclear fusion). In most species, the entire sperm enters the egg during fertilization so sperm morphological diversity may impact the intracellular sperm–egg interactions necessary for karyogamy. We quantified morphological variation of sperm inside eggs prior to and following karyogamy in several species of Drosophila to understand whether evolution of sperm morphology could influence intracellular sperm–egg interactions (ISEIs). We measured seven parameters that describe ISEIs among species to determine whether these parameters varied both within a species across development and across species at the same developmental stage. We used heterospecific crosses to test the relative role of male origin, female origin, and interaction between the male and female in determining ISEIs. We found that sperm shape changed within a species as development proceeded and, at particular development stages, species varied in some ISEIs. Parental origin had an effect on some ISEIs, with a general trend for a stronger female effect. Overall, our findings identify conserved and variable ISEIs among species and demonstrate the potential to contribute understanding to gamete evolution and development.