Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla)

The capacity for mothers to transmit induced resistance against a specific parasite to their young may be an essential maternal effect that determines the fitness of offspring. In a previous study, antibodies against the Lyme disease agent Borrelia burgdorferi sensu lato were detected in kittiwake ( Rissa tridactyla ) eggs in relation to the exposure of birds to the tick vector Ixodes uriae . However, as yet, there has been no demonstration of a direct relationship between antibody concentrations in parents and young in a natural population. Here, we show, using the kittiwake– Borrelia system, the existence of a positive relationship between antibody concentrations in maternal serum and that in eggs and chick serum. No such relationship was found between paternal serum and eggs or young. These results suggest the existence of an adaptive maternal effect, an effect that should have important implications for the ecology and evolution of host–parasite interactions.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

Maternal allocation in eggs when counting on helpers in a cooperatively breeding bird

For cooperatively breeding birds, it has been proposed that breeders should reduce their investment in eggs when they count on helpers, because this can be compensated for by helpers provisioning of nestlings. Data from some species have supported this prediction, but this is not the case in others. It has also been proposed that mothers should not reduce but rather increase investment if the presence of helpers enhances the reproductive value of offspring, a pattern that might also influence egg production as long as helpers are predictable for laying females. Here, we studied maternal expenditure in eggs and clutches in the Iberian magpie, to see whether mothers reduce their expenditure at the egg stage in the presence of helpers. Our results show that investment in clutches varied depending on the year, date in the season and age of the mother, but there were no reductions in maternal expenditure per individual egg when they counted on helpers. On the contrary, a pattern emerged in the opposite direction of more investment in eggs associated with the future presence of helpers at the nestling stage. Our data suggest that the predictability of helpers, along with the type of benefits accrued from the contribution of helpers, may be crucial to understanding the reaction of mothers at egg production.     

Determinants of within- and among-clutch variation in yolk corticosterone in the European starling

Maternal glucocorticoids are known to affect offspring phenotype in numerous vertebrate taxa. In birds, the maternal transfer of corticosterone to eggs was recently proposed as a hormonal mechanism by which offspring phenotype is matched to the relative quality of the maternal environment. However, current hypotheses lack supporting information on both intra- and inter-clutch variation in yolk corticosterone for wild birds. As such, we examined variation in yolk corticosterone levels in a wild population of European starlings (Sturnus vulgaris). Maternal condition, clutch size and nesting density were all negatively related to yolk corticosterone deposition; females with high condition indices, those laying larger clutches and those nesting in high-density associations deposited lower amounts of the hormone into eggs than those with low condition indices, laying small clutches and nesting in isolation. Alternatively, we found no effects of maternal age or human disturbance on yolk corticosterone deposition. Intra-clutch variation of yolk corticosterone was significant, with levels increasing across the laying sequence in all clutch sizes examined, with the difference between first and last-laid eggs being greater in large versus small clutches. Given the reported effects of yolk corticosterone on offspring size and growth, intra-clutch variation in yolk corticosterone has the potential to alter the competitive environment within a brood. Furthermore, our results indicate that variation in yolk corticosterone can originate from variation in both the mother's quality as well as the quality of her breeding environment. The presence of inter-female variation in particular is an important pre-requisite in testing whether the exposure of offspring to maternally-derived corticosterone is a mechanistic link between offspring phenotypic plasticity and maternal quality.     

The effect of maternal state on the steroid and macronutrient content of lesser black-backed gull eggs

It has been proposed that female birds can influence the phenotype of their offspring by provisioning eggs with variable amounts of nutrients and maternal hormones. Egg quality is strongly influenced by maternal body reserves and the amount of food available at the time of egg formation. This study investigated the effects of maternal state and food availability on the capacity of female lesser black-backed gulls Larus fuscus to provision their eggs with macronutrients and steroid hormones. Maternal state was reduced by increasing egg-production effort, whereas extra food was provided to reverse this effect. Compared with eggs of first clutches, eggs of experimentally induced replacement clutches exhibited a lower yolk/albumen ratio and contained more yolk testosterone. During one of the three years in which the study was performed, replacement eggs also contained more 17β-estradiol. Food provisioning during the relaying interval did not affect changes in yolk/albumen ratio or steroid concentrations, but fed females produced bigger eggs in their replacement clutch. This study demonstrates significant within-female consistency in egg size, macronutrient content, and yolk steroid concentration, and it shows that these egg characteristics are influenced by maternal state, food availability, and the timing of breeding.     

Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: the yellow-legged gull Larus michahellis

Female birds transfer antibodies to their offspring via the egg yolk, thus possibly providing passive immunity against infectious diseases to which hatchlings may be exposed, thereby affecting their fitness. It is nonetheless unclear whether the amount of maternal antibodies transmitted into egg yolks varies with female quality and egg laying order. In this paper, we investigated the transfer of maternal antibodies against type A influenza viruses (anti-AIV antibodies) by a long-lived colonial seabird, the yellow-legged gull (Larus michahellis), in relation to fluctuating asymmetry in females, i.e. the random deviation from perfect symmetry in bilaterally symmetric morphological and anatomical traits. In particular, we tested whether females with greater asymmetry transmitted fewer antibodies to their eggs, and whether within-clutch variation in yolk antibodies varied according to the maternal level of fluctuating asymmetry. We found that asymmetric females were in worse physical condition, produced fewer antibodies, and transmitted lower amounts of antibodies to their eggs. We also found that, within a given clutch, yolk antibody level decreased with egg laying order, but this laying order effect was more pronounced in clutches laid by the more asymmetric females. Overall, our results support the hypothesis that maternal quality interacts with egg laying order in determining the amount of maternal antibodies transmitted to the yolks. They also highlight the usefulness of fluctuating asymmetry as a sensitive indicator of female quality and immunocompetence in birds.     

Females produce larger eggs for large males in a paternal mouthbrooding fish.

When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.     

Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird

Mothers can improve the quality of their offspring by increasing the level of certain components in their eggs. To examine whether or not mothers increase deposition of such components in eggs as a function of food availability, we food-supplemented black-legged kittiwake females (Rissa tridactyla) before and during egg laying and compared deposition of androgens and antibodies into eggs of first and experimentally induced replacement clutches. Food-supplemented females transferred lower amounts of androgens and antibodies into eggs of induced replacement clutches than did non-food-supplemented mothers, whereas first clutches presented no differences between treatments. Our results suggest that when females are in lower condition, they transfer more androgens and antibodies into eggs to facilitate chick development despite potential long-term costs for juveniles. Females in prime condition may avoid these potential long-term costs because they can provide their chicks with more and higher quality resources.     

Pre-hatching maternal effects inhibit nestling humoral immune response in the tawny owl Strix aluco

Although evidence is accumulating that mothers can transfer antibodies to their offspring, little is known about the consequences of such a transfer to the offspring immune system. Because maternal antibodies are effective only during a short period of time after their transfer to offspring, one hypothesis is that maternal antibodies provides a transitory antigen-specific protection to offspring, thus lessening the need for offspring to mount their own humoral immune response towards these specific antigens. In birds, this scenario predicts that offspring immune response towards a specific antigen is inhibited to a larger extent in hatchlings than in older nestlings. We tested this hypothesis in tawny owls Strix aluco by cross-fostering clutches between nests and then challenging siblings with a vaccine either two times (at 4- and 11-d-old) or only one time at 11-d-old to compare the strength of the humoral response between nestlings born from mothers with naturally high and low levels of antibodies against this vaccine. Because maternal antibodies are expected to be effective only during a short period of time after hatching, we predict that maternal antibodies should inhibit the immune response of nestlings vaccinated from the fourth day after hatching more than in nestlings vaccinated only at a later age. As expected, the inhibitory effect of maternal antibodies was stronger in nestlings vaccinated soon after hatching than in siblings injected at a later age. Therefore, in wild avian populations pre-hatching maternal effects may confer offspring with a transitory immune protection in the first days following hatching.     

Factors influencing offspring traits in the oviparous multi-clutched lizard,<Emphasis Type="Italic">Calotes versicolor</Emphasis> (Agamidae)

The determinants of offspring size and number in the tropical oviparous multi-clutched lizard,Calotes versicolor, were examined using both univariate and multivariate (path) analyses. InC. versicolor maternal snout-vent length (SVL) and body condition influence clutch mass and clutch size but have no significant influence on offspring size. The positive effect of maternal SVL and body condition on offspring number is counterbalanced by a negative effect of breeding time on egg mass. In fact, breeding time directly influences the offspring body mass and condition through variation in the egg mass. There is a trade-off between offspring mass and condition with offspring number, and breeding time influences both. Offspring hatched from the eggs of early (May–June) or mid (July–August) breeding periods invariably show lower mass and condition than those hatched from the eggs of late breeding season (September–October). Yet, there is no variation in offspring SVL among early, mid and late clutches. Thus, inC. versicolor offspring SVL is optimized while body mass and condition are not optimized.     

Maternal resource variation across the laying sequence in Canada geese Branta canadensis maxima

Variation in maternal investments to offspring presumably reflects an optimization of resource allocation such that a female's fitness is maximized. In birds, both egg size and yolk constituents are examples of resources that can vary among offspring within a clutch. Egg size and maternally-derived steroid hormone concentrations present in yolk have been characterized for many species that lay small clutches or have altricial young, but little information is available for species that lay moderate to large clutches of precocial young. In this study, we recorded laying position, measured fresh egg mass and determined maternally-derived testosterone and estradiol concentrations present in yolks for whole clutches of free-living Canada geese Branta canadensis maxima to assess variation in maternal resources within clutches. We found that egg size varied non-linearly across the laying sequence such that first laid eggs were small, the largest eggs in the clutch occurred in the second and third positions, and size declined in eggs laid in subsequent positions. Concentration of testosterone in the yolk followed a pattern in which the first and second laid eggs have the highest concentrations within a clutch and declining concentrations in subsequently laid eggs. In contrast, maternally-derived yolk estradiol concentrations (measured in a subset of clutches) did not change across the laying sequence.     

Individual variation in parental tradeoffs between the number and size of offspring at the pre- and post-natal stages

Life-history theory predicts that parents refer to the resources they hold to determine their breeding strategy. In multi-brooded species, it is hypothesized that single-brooded parents produce larger clutches and raise offspring with a brood survival strategy, whereas multi-brooded parents only do this under good breeding conditions. Under poor conditions, they produce smaller clutches and raise offspring with a brood reduction strategy. We tested this hypothesis in the Brown-cheeked Laughing Thrush Trochalopteron henrici, which can breed twice a year on the Tibetan Plateau, by investigating the life-history traits and provisioning behaviours of single- and double-brooded parents. Single-brooded parents laid larger clutches of smaller eggs and produced more and larger fledglings than double-brooded parents in their first brood. Double-brooded parents produced smaller clutches of larger eggs but fledged larger nestlings in their first brood than in their second brood. As single-brooded parents only need to raise one brood a year, then producing and raising as many offspring as possible (i.e. the brood survival strategy in a large brood) can maximize their reproductive success. For double-brooded parents, producing and raising fewer offspring in the first brood (i.e. the brood survival strategy in a small brood) can ensure their nesting success during a short breeding cycle. Additionally, producing more offspring but raising larger nestlings in the second brood (i.e. the brood reduction strategy in a large brood) can select for offspring of higher quality within the brood. Our findings indicate that different tradeoffs between single- and double-brooded parents in egg-laying and nestling-raising may be an adaptation to the seasonal variation in environmental conditions.     

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.     

Prenatal sex ratios influence sexual dimorphism in a reptile

The prenatal environment influences offspring traits in a variety of ways and in a wide range of taxa. For example, maternal allocation of steroids to the eggs influences offspring traits in birds, and in some mammals the intrauterine position influences morphological, behavioural, and physiological traits due to sex-related steroid transfer between sibling fetuses. We show that similar phenomena occur in the common lizard (Lacerta vivipara), a viviparous reptile. Females developing in male-biased clutches had a more masculine allometry (relatively larger heads) at parturition than females developing in female-biased clutches. Males were correspondingly feminized in female-biased clutches. The effects could either be due to diffusion of steroids produced by the offspring or by a general tendency for females to allocate steroids according to the sex ratio of her clutch. Subsequent to parturition, the sexes differed in their growth trajectories depending on sex ratio environment. In males, the difference in allometry between sex ratio environments remained over time, whereas in females the corresponding effect disappeared.     

Maternal Care in the Burrower Bug <Emphasis Type="Italic">Adomerus triguttulus</Emphasis>: Defensive Behavior

Some burrower bugs (Heteroptera: Cydnidae) show complex patterns of maternal care, including defense against predators and the provisioning of food to nymphs. Recently, the subsocial cydnid bugs have attracted the interest of researchers as model systems to study the behavioral ecology of parental investment. However, there have been few attempts to quantify the fitness benefits of maternal behavior other than provisioning. Here, we examined the maternal behavior of Adomerus triguttulus and its adaptive significance in terms of offspring survival in the field. A. triguttulus young depend on fallen nutlets of myrmecophorous mints, Lamium spp. Under field conditions, females attend offspring, from eggs to second instar nymphs, in nests on the ground under the litter. When disturbed, the females showed aggressive responses against the source of disturbance. The females often carried spherical clutches of eggs away from the nest when heavily disturbed. Female-removal experiments in the field demonstrated a defensive function of the female behavior; predators, such as ants, attacked egg clutches without females and the clutches often disappeared during the experiment. Egg clutches without females sometimes also suffered from fungal infection. Selective factors on maternal defensive behavior in A. triguttulus are discussed in terms of habitat properties possibly emerging from insect–plant associations.     

Maternal androgens in eggs of communally breeding guira cuckoos (Guira guira)

Variation of maternal androgens in avian eggs may be a mechanism of maternal influence on offspring development, growth, and/or behavior. We studied yolk androgen concentrations in eggs of guira cuckoos (Guira guira) to understand how females might enhance the success of offspring in a complex communal breeding system. We measured concentrations of androstenedione, 5alpha-dihydrotestosterone, and testosterone in yolks and identified eggs and clutches of individuals in joint nests by yolk protein electrophoresis. Androstenedione had the highest yolk concentration, at least 10 times higher than that of testosterone and 5alpha-dihydrotestosterone. The first eggs of individual females that laid two or three eggs in a joint nest had lower androstenedione concentrations than their second and third eggs, the latter having a lower probability of being ejected from the nest. This implies that guira cuckoo females may influence offspring survival and competitiveness in communal nests by means of differential allocation of androstenedione and laying tactics. There was significant variation in yolk androstenedione among females, but the order in which females entered laying in the communal clutch had no effect on the concentrations. Androstenedione yolk concentrations increased with communal clutch size, which may indicate that higher levels of competition in larger groups lead to higher yolk androgen concentrations. Finally, androstenedione concentrations were higher in clutches in the later wetter periods of the rainy season than during the earlier drier period. This may be explained by the high frequency of large clutches in the later periods, with more females contributing to a joint clutch.     

Maternal effects due to male attractiveness affect offspring development in the zebra finch

Maternal effects occur when offspring phenotype is influenced by environmental factors experienced by the mother. Mothers are predicted to invest differentially in offspring in ways that will maximize offspring fitness depending on the environment she expects them to encounter. Here, we test for maternal effects in response to mate attractiveness on offspring developmental traits in the zebra finch Taeniopygia guttata. We controlled for parental genetic quality by manipulating male attractiveness using coloured leg rings and by randomly assigning mating pairs. The potential confounding effect of differential nestling care was controlled for by cross-fostering clutches and by allowing for variance due to foster father attractiveness in general linear models. We found a difference in egg mass investment between attractiveness groups and, importantly, we found that all of the offspring traits we measured varied with the attractiveness of the father. This provides strong evidence for maternal effects in response to mate attractiveness. Furthermore, due to the experiment design, we can conclude that these effects were mediated by differential investment of egg resources and not due to genetic differences or differences in nestling care.     

Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex

Mothers influence their offspring phenotype by varying egg quality. Such maternal effects may be mediated by transmission of antibodies and antioxidants. Mothers should adjust allocation of maternal substances depending on embryonic sex because of differences in reproductive value, potentially dependent on paternal genetic effects as reflected by secondary sexual characters. We manipulated sexual attractiveness of male barn swallows (Hirundo rustica) and investigated maternal investment in eggs in relation to offspring sex. Mothers allocated more antibodies against a pathogen to eggs with a daughter than a son. However, concentration of antioxidants was independent of embryonic sex. Sex-dependent allocation was independent of paternal attractiveness. Thus, mothers adjusted allocation of substances to offspring in a complex manner, that may be part of a strategy of favouritism of daughters, which have larger mortality than sons. Such effects may have important consequences for secondary and tertiary sex ratios, but also for ontogeny of adult phenotype.     

Reproductive tradeoffs and yolk steroids in female leopard geckos, Eublepharis macularius

Life history theory predicts tradeoffs among reproductive traits, but the physiological mechanisms underlying such tradeoffs remain unclear. Here we examine reproductive tradeoffs and their association with yolk steroids in an oviparous lizard. Female leopard geckos lay two eggs in a clutch, produce multiple clutches in a breeding season, and reproduce for several years. We detected a significant tradeoff between egg size and the number of clutches laid by females during their first two breeding seasons. Total reproductive effort was strongly condition-dependent in the first season, but much less so in the second season. Although these and other tradeoffs were unmistakable, they were not associated with levels of androstenedione, oestradiol, or testosterone in egg yolk. Female condition and egg size, however, were inversely related to dihydrotestosterone (DHT) levels in egg yolk. Finally, steroid levels in egg yolk were not directly related to steroid levels in the maternal circulation when follicles were developing, indicating that steroid transfer to eggs is regulated. These findings suggest that maternal allocation of DHT could mitigate tradeoffs that lead to poor offspring quality (i.e. poor female condition) and small offspring size (i.e. small egg size).     

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird

Glucocorticoids circulating in breeding birds during egg production accumulate within eggs, and may provide a potent form of maternal effect on offspring phenotype. However, whether these steroids affect offspring development remains unclear. Here, we employed a non-invasive technique that experimentally elevated the maternal transfer of corticosterone to eggs in a wild population of house wrens. Feeding corticosterone-injected mealworms to free-living females prior to and during egg production increased the number of eggs that females produced and increased corticosterone concentrations in egg yolks. This treatment also resulted in an increase in the amount of yolk allocated to eggs. Offspring hatching from these eggs begged for food at a higher rate than control offspring and eventually attained increased prefledging body condition, a trait predictive of their probability of recruitment as breeding adults in the study population. Our results indicate that an increase in maternal glucocorticoids within the physiological range can enhance maternal investment and offspring development.