Increased lifetime reproductive success of first‐hatched siblings in Common Kestrels Falco tinnunculus

Order of birth has profound consequences on offspring across taxa during development and can have effects on individuals later in life. In birds, differential maternal allocation and investment in their progeny lead to variance in the environmental conditions that offspring experience during growth within the brood. In particular, laying and hatching order have been proposed to influence individual quality during the growing period, but little is known about the fitness consequences that these two factors have for offspring from a lifetime perspective. We explored the effect of laying and hatching order on post‐fledgling survival (measured as recruitment probability) and lifetime reproductive success (LRS) in Common Kestrels Falco tinnunculus, using a long‐term and individual‐based dataset. First‐hatched chicks showed higher survival probability and LRS than their siblings. This effect was not due to body condition of the individuals at adulthood, the quality of their mates or the reproductive outcome compared with later‐hatched individuals. Instead, first‐hatched chicks had a higher recruitment probability. This could be explained by the higher body condition attained by first‐hatched chicks at the end of the nesting period, perhaps due to an enhanced competitive advantage for food over their siblings at the time of hatching. Laying order, in contrast to hatching order, appeared to have little or no effect on LRS. Our results suggest that hatching order within siblings predicts fitness, and that better early‐life conditions during growth experienced by first‐hatched chicks improve first survival and then recruitment, resulting in an enhanced LRS.     

Hatching order affects offspring growth,survival and adult dominance in the joint‐laying Pukeko Porphyrio melanotus melanotus

In birds with asynchronous hatching, hatching order is an important factor in determining offspring phenotype. Many previous studies have demonstrated that later‐hatched offspring show reduced growth and survival during development. However, few studies have followed individuals from hatching to adulthood to test whether the effects of hatching order persist into later life. Here, we explore patterns of hatching order and fitness‐related traits in the Pukeko Porphyrio melanotus melanotus, a cooperatively breeding bird that lives in stable social groups that form linear dominance hierarchies. Pukeko groups sometimes contain two breeding females that lay eggs in the same nest (joint‐laying). Thus, competition between nest‐mates can influence the relative fitness of each laying female. We show that in both single‐clutch and joint‐clutch nests, earlier‐hatched Pukeko chicks grow faster and survive better than later‐hatched brood‐mates. Moreover, earlier‐hatched chicks achieve higher dominance ranks as adults, making this study one of the first to find a relationship between hatching order and adult dominance in wild birds. Finally, we show that in groups with two breeding females, the chicks of the primary female hatch earlier than the chicks of the secondary female. As a result, the offspring of the primary female may be at a competitive advantage, which could have important implications for social dynamics in this species.     

Adaptive sex allocation in relation to hatching synchrony and offspring quality in house wrens

Increased variance in the reproductive success of males relative to females favors mothers that optimally allocate sons and daughters to maximize their fitness return. In altricial songbirds, one influence on the fitness prospects of offspring arises through the order in which nestlings hatch from their eggs, which affects individual mass and size before nest leaving. In house wrens (Troglodytes aedon), the influence of hatching order depends on the degree of hatching synchrony, with greater variation in nestling mass and size within broods hatching asynchronously than in those hatching synchronously. Early-hatching nestlings in asynchronous broods were heavier and larger than their later-hatching siblings and nestlings in synchronous broods. The effect of hatching order was also sex specific, as the mass of males in asynchronous broods was more strongly influenced by hatching order than the mass of females, with increased variation in the mass of males relative to that of females. As predicted, mothers hatching their eggs asynchronously biased first-laid, first-hatching eggs toward sons and late-laid, late-hatching eggs toward daughters, whereas females hatching their eggs synchronously distributed the sexes randomly among the eggs of their clutch. We conclude that females allocate the sex of their offspring among the eggs of their clutch in a manner that maximizes their own fitness.     

Maternal compensation for hatching asynchrony in the collared flycatcher Ficedula albicollis

Several hypotheses have been proposed to explain the adaptiveness of hatching asynchrony for the parents, but delayed hatching is generally detrimental for the late hatched young. These offspring often experience competitive disadvantage and delayed development. If hatching asynchrony has a reason other than producing competitive differences among offspring, it would be advantageous, not only for the offspring but even for the parents, to compensate for its detrimental effects. In some species, increasing investment into later laid eggs has been reported and discussed as a compensation mechanism, but its effect on nestling growth and fledging size has not been examined in details. In this study we investigated nestling growth and size at fledging in terms of body mass and length of primaries in relation to the accurate laying and hatching order in collared flycatcher Ficedula albicollis broods. We found that females laid larger eggs at the end of the laying sequence, and this helped to decrease the disadvantages for the last offspring. The last offspring had lower body mass growth rate and fledged with shorter feathers, but in both cases the larger the last egg was, the smaller the lag of the offspring was. We conclude, that even if females were not able to fully compensate for the detrimental effects of hatching asynchrony, larger eggs may improve the survival prospects of late hatched nestlings.     

Long-term consequences of early ontogeny in free-living Great Tits Parus major

Environmental factors during early development may have profound effects on subsequent life-history traits in many bird species. In wild birds, sex-specific effects of early ontogeny on natal dispersal and future reproduction are not well understood. The objective of this work was to determine whether hatching date and pre-fledging mass and condition of free-living Great Tits Parus major have any subsequent effect on individuals’ natal dispersal and reproductive performance at first breeding. Both males and females dispersed longer distances in coniferous than in deciduous forests, while dispersal was condition-dependent only in males (heavier as nestlings dispersed farther). In females, mass and condition at pre-fledging stage correlated significantly with clutch size, but not with subsequent reproductive performance as measured by fledging success or offspring quality. In contrast, heavier males as nestlings had higher future fledging success and heavier offspring in their broods compared with those in worse condition as nestlings. The hatching date of female as well as male parents was the only parental parameter related to the number of eggs hatched at first breeding. These results indicate that pre-fledging mass and condition predict subsequent fitness components in this bird species. We suggest that sex-specific relationships between a disperser’s condition and its selectivity with respect to breeding habitat and subsequent performance need to be considered in future models of life-history evolution.     

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

Ovulation order mediates a trade-off between pre-hatching and post-hatching viability in an altricial bird

Simultaneously dependent siblings often compete for parentally provided resources. This competition may lead to mortality, the probability of which may be a function, in part, of the individual offspring's production order. In birds, serial ovulation followed by hatching asynchrony of simultaneous dependents leads to differences in post-hatching survival that largely depend on ovulation (laying) order. This has led to the widespread assumption that early-laid eggs are of greater value and therefore should possess different maternally manipulated characteristics than later-laid eggs. However, this perspective ignores the potential effect of laying order on pre-hatching viability, an effect which some studies suggest should offset the effect of laying order on post-hatching viability. I examined the relationship between laying order and hatching and fledging probability in wild, free-living Lincoln's sparrows (Melospiza lincolnii). In broods with complete hatching success, first-laid and therefore first-hatched offspring had the highest probability of fledging, and fledging probability declined with increasing laying order. However, first-laid eggs were less likely than later-laid eggs to hatch. This effect of laying order on pre-hatching viability seemed to offset that on post-hatching viability, and, consistently, maternal investment in egg size varied little if at all with respect to laying order. These results suggest that ovulation order mediates a trade-off between pre-hatching and post-hatching viability and should encourage a re-evaluation of the solitary role post-embryonic survival often plays when researchers make assumptions about the value of propagules based on the order in which they are produced.     

Paternal body size affects reproductive success in laboratory-held zebrafish (<Emphasis Type="Italic">Danio rerio</Emphasis>)

Across many fish species, large females tend to exhibit higher individual reproductive success due to elevated fecundity and the provisioning of better conditioned eggs and offspring compared to small females. By contrast, effects of paternal body size on reproductive success are less well understood. We disentangled the maternal- and paternal-size dependent effects on reproductive output and early life history in zebrafish (Danio rerio). In the laboratory, females and males from four size categories (small, medium-sized, large and very large) were allowed to spawn freely in a full factorial design with 10 replicates per size combination. As expected, larger females produced more eggs and better conditioned offspring compared to smaller females. Male body size further contributed to zebrafish reproductive success: offspring sired by large males exhibited higher hatching probability and these offspring also hatched earlier and larger than offspring fertilized by small males. However, the largest males experienced lower mating success and received fewer eggs than males of the smaller size classes. While male body size substantially affected reproductive success in zebrafish, it remained unclear whether and to what degree direct paternal effects (e.g., related to sperm quality) or indirect paternal effects stemming from differential allocation patterns by females were the mechanism behind our findings. Answering this question constitutes an important future research topic.     

Differential effects of offspring and maternal inbreeding on egg laying and offspring performance in the burying beetle Nicrophorus vespilloides

We investigate the effect of offspring and maternal inbreeding on maternal and offspring traits associated with early offspring fitness in the burying beetle Nicrophorus vespilloides. We conducted two experiments. In the first experiment, we manipulated maternal inbreeding only (keeping offspring outbred) by generating mothers that were outbred, moderately inbred or highly inbred. Meanwhile, in the second experiment, we manipulated offspring inbreeding only (keeping females outbred) by generating offspring that were outbred, moderately inbred or highly inbred. In both experiments, we monitored subsequent effects on breeding success (number of larvae), maternal traits (clutch size, delay until laying, laying skew, laying spread and egg size) and offspring traits (hatching success, larval survival, duration of larval development and average larval mass). Maternal inbreeding reduced breeding success, and this effect was mediated through lower hatching success and greater larval mortality. Furthermore, inbred mothers produced clutches where egg laying was less skewed towards the early part of laying than outbred females. This reduction in the skew in egg laying is beneficial for larval survival, suggesting that inbred females adjusted their laying patterns facultatively, thereby partially compensating for the detrimental effects of maternal inbreeding on offspring. Finally, we found evidence of a nonlinear effect of offspring inbreeding coefficient on number of larvae dispersing. Offspring inbreeding affected larval survival and larval development time but also unexpectedly affected maternal traits (clutch size and delay until laying), suggesting that females adjust clutch size and the delay until laying in response to being related to their mate.     

Against the odds? Nestling sex ratio variation in green-rumped parrotlets

We investigated nestling sex ratio variation in the green-rumpedparrotlet (Forpus passerinus), a small neotropical parrot breedingin central Venezuela. There are strong theoretical reasons topredict a female-biased sex ratio in this system according tothe local resource hypothesis; juvenile males are philopatricand there are high levels of competition between male siblingsfor access to breeding females. Data were collected from twobreeding sites over a 14-year period incorporating 564 broodswith a total of 2728 nestlings. The mean percentage of malenestlings across years was 51%. Despite extreme hatching asynchronyin this system and increased survival of earlier hatched offspring,there was no bias in sex allocation associated with egg sequence.Patterns in sex allocation were not associated with clutch size,age, or size of the breeding female or breeding site. The potentialfor selective resorption of eggs was considered; however, nosignificant relationship was found between extended laying intervalsand the sex of subsequent eggs. Together, these results suggestthat female parrotlets are unable to regulate the sex ratioof their clutch at laying or that facultative manipulation ofnestling sex ratio may not confer a fitness benefit to breedersin these populations.     

Absence of seasonal variation in great tit offspring sex ratios

When the timing of breeding affects the reproductive value of sons and daughters differently, parents are expected to increase their fitness by changing the offspring sex ratio during the course of the breeding season. Previous studies have shown that in great tits Parus major hatching date has a stronger effect on the fitness of juvenile males than on that of juvenile females. We tested whether this difference was reflected in a seasonal decline in the proportion of sons per breeding attempt. Although offspring sex ratio was more variable than would be expected from a binomial distribution, there was no significant relationship between the proportion of sons and the laying date of the clutch. Moreover, individual females did not adjust the sex ratio of their offspring following an experimental delay of breeding. This study therefore fails to demonstrate adaptive seasonal variation in great tit offspring sex ratios.     

Influence of mate preference and laying order on maternal allocation in a monogamous parrot species with extreme hatching asynchrony

It is well established that in many avian species, prenatal maternal resource allocation varies both between and within clutches and may affect offspring fitness. Differential allocation of maternal resources, in terms of egg weight and yolk composition, may therefore allow the female to adjust brood reduction and to fine-tune reproductive investment in accordance with the expected fitness returns. The adaptive value of such maternal resource allocation is thought to be context-dependent as well as species-specific. We investigated the effects of female preference for her mate on the allocation of prenatal maternal resources in the budgerigar, Melopsittacus undulatus, a monogamous species of parrot that shows an extreme hatching asynchrony. We assessed mate preferences in a two-way preference test and allowed females two breeding rounds: one with the preferred and one with the non-preferred partner. We found no effect of preference on either latency to lay or clutch size, but females mated with the preferred partner laid eggs that contained significantly more yolk. Their eggs also contained significantly more androstenedione but not testosterone. Our results suggest that in this species, female preference may influence maternal resource allocation, and that the functional roles of each androgen in the yolk should be considered separately. In addition, we found a significant effect of laying order on egg and yolk weight as well as on yolk testosterone and androstenedione levels. These measures, however, did not change linearly with the laying order and render it unlikely that female budgerigars compensate for the extreme hatching asynchrony by adjusting within-clutch allocation of prenatal maternal resources.     

Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates

Evolutionary biologists typically assume that the number of eggs fertilized or developing embryos produced is correlated with an individual's fitness. Using microsatellite markers, we document for the first time estimates of realized fitness quantified as the number of offspring surviving to adulthood in an insect under field conditions. In a territorial damselfly whose males defend tree hole oviposition sites, patterns of offspring survivorship could not be anticipated by adults. Fewer than half of the parents contributing eggs to a larval habitat realized any reproductive success from their investment. The best fitness correlate was the span over which eggs in a clutch hatched. Among parents, female fecundity and male fertilization success were poor predictors of realized fitness. Although body size was correlated with female clutch size and male mating success, larger parents did not realize greater fitness than smaller ones. The uncoupling of traditional fitness surrogates from realized fitness provides strong empirical evidence that selection at the larval stage constrains selection on mated adults.     

Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs

Male and female offspring can differ in their susceptibility to pre-natal (e.g. egg quality) and post-natal (e.g. sib–sib competition) conditions, and parents can therefore increase their individual fitness by adjusting these maternal effects according to offspring sex. In birds, egg mass and laying/hatching order are the main determinants of offspring viability, but these effects can act differently on each sex. In a previous study, relatively large last-laid (c-)eggs of yellow-legged gulls (Larus michahellis) were more likely to carry a female embryo. This suggests compensatory allocation of maternal resources to daughters from c-eggs, which suffer reduced viability. In the present study, we supplemented yellow-legged gulls with food during the laying period to experimentally test whether their nutritional conditions were responsible for the observed covariation between c-egg sex and mass. As predicted, food supplementation enhanced female c-eggs'' mass more than that of male c-eggs. Thus, this experiment indicates that mothers strategically allocated their resources to c-eggs, possibly in order to compensate for the larger susceptibility of daughters to hatching (and laying) order. The results also suggested that mothers decided on resource allocation depending on the sex of already ovulated c-eggs, rather than ovulating ova of either sex depending on food availability.     

Differential effects of egg albumen content on barn swallow nestlings in relation to hatch order

In diverse animal taxa, egg mass variation mediates maternal effects with long-term consequences for offspring ontogeny and fitness. Patterns of egg mass variation with laying order differ considerably among birds, but no study has experimentally investigated the function of variation in albumen or yolk egg content in the wild. In barn swallows (Hirundo rustica), absolute and relative albumen mass increased with egg laying order. Experimental albumen removal delayed hatching, had larger negative effects on growth of late-hatched nestlings, and reduced nestling survival. Laying order positively predicted hatch order. Because nestling competitive ability depends on size, and albumen egg content influences hatchling size, present results suggest that by increasing albumen content of late eggs mothers reduce hatching asynchrony and enhance growth particularly of late-hatched nestlings. Thus, variation in albumen mass with laying order may function to mitigate the negative phenotypic consequences of hatching late in species that adopt a 'brood-survival' strategy.     

Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development

We tested the hypothesis that mother birds counterbalance the negative effects of hatching asynchrony for later-hatched chicks by increasing the yolk androgen concentrations in consecutive eggs of their clutch. In doing so, they may adaptively tune each offspring's competitive ability and, thus, growth and survival. However, evidence in support of this hypothesis is contradictory. The yolk concentrations of maternal androgens in the eggs of black-headed gulls increase significantly with the laying order of the eggs in a clutch. We experimentally tested the functional consequences of this increase on chick development under natural conditions by injecting eggs with either an oil or androgen solution. We created experimental clutches in which androgen levels either stayed constant or increased with laying order while controlling for differences in egg quality by using only first-laid eggs. We then compared development, growth and survival between these broods. Androgen treatment enhanced embryonic development because androgen-treated eggs hatched half a day earlier than controls, while their size at hatching was similar to oil-treated controls. Androgen treatment did not increase chick survival, but it enhanced growth. Androgen-treated, third-hatched chicks had a higher body mass and longer legs than third-hatched chicks that hatched from oil-treated eggs. At the same time, growth of first chicks (which were all oil treated) was reduced by the presence of two androgen-treated siblings, suggesting that yolk androgens enhance the competitive ability of later-hatched chicks. Our results support the hypothesis that transfer of different amounts of androgens to the eggs of a clutch is a mechanism by which mothers maximize their reproductive output.     

Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird

Maternal and environmental effects can profoundly influence offspring phenotypes, independent of genetic effects. Within avian broods, both the asymmetric post‐hatching environment created by hatching asynchrony and the differential maternal investment through the laying sequence have important consequences for individual nestlings in terms of the allocation of resources to body structures with different contributions to fitness. The purpose of this study was to evaluate the relative importance of post‐hatching environmental and maternal effects in generating variation in offspring phenotypes. First, an observational study showed that within blue tit, Cyanistes caeruleus, broods, late‐hatched nestlings allocated resources to tarsus development, maintained mass gain and head‐bill growth and directed resources away from the development of fourth primary feathers. Second, a hatching order manipulation experiment resulted in nestlings from first‐laid eggs hatching last, thereby allowing comparison with both late and early‐hatched nestlings. Experimental nestlings had growth patterns which were closer to late‐hatched nestlings, suggesting that within‐brood growth patterns are determined by post‐hatching environmental effects. Therefore, we conclude that post‐hatching environmental effects play an important role in generating variation in offspring phenotypes.     

The evolution of sexual size dimorphism in the house finch. V. Maternal effects

The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.     

Egg size, offspring sex and hatching asynchrony in zebra finches Taeniopygia guttata

Experimental synchronization of onset of incubation was employed in laboratory held zebra finches Taeniopygia guttata to study whether differential resource allocation and possible bias of offspring sex in subsequent eggs in the laying order could mitigate the effects of hatching asynchrony. We found that egg mass increased with laying order, but offspring sex was not related to laying order. Among synchronized clutches, eggs hatched more synchronously than eggs from control nests. Survival probability was related to egg mass, and as expected, this effect differed between experimental groups: it was positive among synchronized broods and not significantly related among asynchronous broods. This suggests that increase in egg mass with the laying order might reduce disparities between early and late hatching chicks. Female nestlings survived better than male nestlings. However their growth was impaired in synchronized broods, whilst growth of males was not affected by hatching synchronization.     

Hatching asynchrony and brood reduction influence immune response in Common Kestrel Falco tinnunculus nestlings

The onset of incubation before the end of laying imposes asynchrony at hatching and, therefore, a size hierarchy in the brood. It has been argued that hatching asynchrony might be a strategy to improve reproductive output in terms of quality or quantity of offspring. However, little is known about the mediating effect of hatching asynchrony on offspring quality when brood reduction occurs. Here, we investigate the relationship between phenotypic quality and hatching asynchrony in Common Kestrel Falco tinnunculus nestlings in Spain. Hatching asynchrony did not increase breeding success or nestling quality. Furthermore, hatching asynchrony and brood reduction had different effects on nestlings’ phytohaematogglutinin (PHA)‐mediated immune response and nestling growth. In asynchronous and reduced broods (in which at least one nestling died), nestlings showed a stronger PHA‐mediated immune response and tended to have a smaller body size compared with nestlings raised in synchronous and reduced broods. When brood reduction occurred in broods hatched synchronously, there was no effect on nestling size, but nestlings had a relatively poor PHA‐mediated immune response compared with nestlings raised in asynchronous and reduced broods. We suggest that resources for growth can be directed to immune function only in asynchronously hatched broods, resulting in improved nestling quality, as suggested by their immune response. We also found that males produced a greater PHA‐mediated immune response than females only in brood‐reduced nests without any effect on nestling size or condition, suggesting that females may trade off immune activities and body condition, size or weight. Overall, our results suggest that hatching pattern and brood reduction may mediate resource allocation to different fitness traits. They also highlight that the resolution of immune‐related trade‐offs when brood reduction occurs may differ between male and female nestlings.