Sex-specific growth patterns and effects of hatching condition on growth in the reversed sexually size-dimorphic great skua Stercorarius skua

In many sexually size-dimorphic species of birds and mammals, the larger sex, often the males, show increased environmental sensitivity during ontogeny. This is generally assumed to be due to higher energy requirements, reflected in higher absolute growth rates of the larger sex. Poor early conditions often increase the sex differences in vulnerability. However, it is not clear whether these patterns are equally pervasive in species where females are larger, as males face an additional early disadvantage due to high levels of testosterone. We investigated sex-specific growth patterns of mass, tarsus and wing of the great skua Stercorarius skua , a seabird with reversed size dimorphism. We were particularly interested in sex-specific effects of early conditions on growth. Beside data from unmanipulated nests, we present results from an egg removal experiment, which caused chicks to hatch from smaller eggs and in poorer body condition. Half of the experimental chicks were raised by pairs in which mothers were in poor body condition. At the end of the nesting period, great skua chicks exhibited a comparable degree of size dimorphism as is found in adults, although neither sex had reached final adult size. Despite females reaching larger asymptotic values of mass and tarsus, timing of growth was not different between the sexes. Absolute growth was higher for females around the time of maximum growth, which suggests that daughters face higher energetic demands. We found sex-specific effects of poor early conditions on growth patterns, although not to the extent which we had predicted. Hatching in poor body condition was related to slowed growth in females but not males. However, our experimental manipulations had no additional negative effect on growth. Our results indicate that daughters in the great skua face higher demands during growth than sons, and that early conditions are more important for the development of the larger sex in this reversed dimorphic 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.     

Hatching sex ratio and sex specific chick mortality in common terns Sterna hirundo

Bias in sex ratios at hatching and sex specific post hatching mortality in size dimorphic species has been frequently detected, and is usually skewed towards the production and survival of the smaller sex. Since common terns Sterna hirundo show a limited sexual size dimorphism, with males being only about 1–6% larger than females in a few measurements, we would expect to find small or no differences in production and survival of sons and daughters. To test this prediction, we carried out a 2-year observational study on sex ratio variation in common terns at hatching and on sex specific post hatching mortality. Sons and daughters hatched from eggs of similar volume. Post hatching mortality was heavily influenced by hatching sequence. In addition, we detected a sex specific mortality bias towards sons. Overall, hatching sex ratio and sex specific mortality resulted in fledging sex ratios 8% biased towards females. Thus, other reasons than body size may be influencing the costs of rearing sons. Son mortality was not homogeneous between brood sizes, but greater for two-chick broods. Since adults rearing two-chick broods were younger, lighter and bred consistently later than those rearing three-chick broods, it is suggested that lower capacity of two-chick brood parents adversely affected offspring survival of sons. Though not significantly, two-chick broods tended to be female biased at hatching, perhaps to counteract the greater male-biased nestling mortality. Thus, population bias in secondary sex ratio is not limited to strongly size dimorphic species, but species with a slight sexual size dimorphism can also show sex ratio bias through a combination of differential production and mortality of sons and daughters.     

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation. Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.     

Offspring sex ratio produced by female guppies in the wild correlates with sexual ornaments of their sons

The attractiveness hypothesis predicts that females produce broods with male-biased sex ratios when they mate with attractive males. This hypothesis presumes that sons in broods with male-biased sex ratios sired by attractive males have high reproductive success, whereas the reproductive success of daughters is relatively constant, regardless of the attractiveness of their sires. However, there is little direct evidence for this assumption. We have examined the relationships between offspring sex ratios and (1) sexual ornamentation of sons and (2) body size of daughters in broods from wild female guppies Poecilia reticulata. Wild pregnant females were collected and allowed to give birth in the laboratory. Body size and sexual ornamentation of offspring were measured at maturity. Our analysis revealed a significant positive correlation between offspring sex ratios (the proportion of sons per brood) and the total length as well as the area of orange spots of sons, two attributes that influence female mating preferences in guppies. The sex ratio was not associated with the body size of daughters. These results suggest that by performing adaptive sex allocation according to the expected reproductive success of sons and daughters, female guppies can enhance the overall fitness of their offspring.     

Ural owl sex allocation and parental investment under poor food conditions

Parents are expected to overproduce the less costly sex under poor food conditions. The previously regular 3-year cycle in the abundance of voles, the main prey of the Ural owl, Strix uralensis, temporarily disappeared in 1999–2001. We studied Ural owls' parental feeding investment and sex allocation during these poor-quality years. We sexed hatchlings and embryos in unhatched eggs of all 131 broods produced during these years. Population wide, the owls produced significantly more males (56%). The parental food investment in the brood was estimated by sorting out the prey remains in the bottom of nest boxes. Food delivered to 83 broods without chick mortality showed no clear sex-specific investment. Nestling mortality was equal in both sexes. Thus, evidence for an investment-driven sex allocation is weak. Neither laying date, brood size nor the female's condition correlated with offspring sex ratios. In these poor years, parents provided less food per chick and the fledging weight of daughters was reduced more than the weight of sons compared with years of high food abundance (1983 and 1986). We discuss, in relation to published studies, the possibility of a sex-allocation scenario where, under poor food conditions, a daughter's long-term fitness is reduced more than a son's.     

Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype

The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings.     

Adaptive secondary sex ratio adjustments via sex-specific infanticide in a bird

Infanticide is easiest to understand when it involves killing the offspring of others [1], but a parent may also kill its own offspring if the sacrifice of currently dependent young leads to higher survival of brood mates [2] or an improvement in the parent's likely future reproduction [3]. However, sex-specific infanticide by parents of their own offspring, although occurring in some human societies [4], is rare across species. Its rarity may be because killing one sex combines wasted parental effort with consequent biases in population sex ratios that are detrimental for the fitness of the overproduced sex [5-7]. We show that killing male offspring can be advantageous to Eclectus parrot (Eclectus roratus) mothers even though frequency-dependent selection then elevates the reproductive value of sons above that of daughters. In poorer-quality nest hollows, broods with a single female nestling had higher reproductive value than broods in which the female had a younger brother. Our data demonstrate frequent targeted removal of male nestlings within 3 days of hatching in these specific brood types and nesting conditions. The ability of Eclectus parrots to perceive the sex of their offspring relatively early may favor decisions to kill one sex before further investment in parental care.     

Sex of the first hatched chick influences survival of the brood in the herring gull (Larus argentatus)

Differences in the growth rate of male and female offspring can result in different parental rearing costs for sons and daughters. Such differences may also influence the survival chances of male and female offspring when conditions are unfavourable. In birds, hatching asynchrony leads to hierarchical competition for food between siblings. Therefore, the sex of the chick in the first hatched position in the brood may influence breeding success by affecting the extent to which the later hatched chicks can compete for resources. The interaction between brood sex composition and chick performance in the herring gull Larus argentatus was examined under different environmental conditions. When environmental conditions were relatively good, chick survival within broods was better when a female was first to hatch, an effect that was most obvious later in the season. When conditions were poorer however, sex of the first hatched chicks was not related to brood survival. In neither situation did the overall primary sex ratio differ from equality. However in the year of relatively good food availability, the first chick in the brood was more likely to be male early in the season, which was when the disadvantageous effects on brood survival of males being in this position are weakest.     

Maternal Natal Environment and Breeding Territory Predict the Condition and Sex Ratio of Offspring

Females in a variety of taxa adjust offspring sex ratios to prevailing ecological conditions. However, little is known about whether conditions experienced during a female’s early ontogeny influence the sex ratio of her offspring. We tested for past and present ecological predictors of offspring sex ratios among known-age females that were produced as offspring and bred as adults in a population of house wrens. The body condition of offspring that a female produced and the proportion of her offspring that were male were negatively correlated with the size of the brood in which she herself was reared. The proportion of sons within broods was negatively correlated with maternal hatching date, and varied positively with the quality of a female’s current breeding territory as predicted. However, females producing relatively more sons than daughters were less likely to return to breed in the population the following year. Although correlative, our results suggest that the rearing environment can have enduring effects on later maternal investment and sex allocation. Moreover, the overproduction of sons relative to daughters may increase costs to a female’s residual reproductive value, constraining the extent to which sons might be produced in high-quality breeding conditions. Sex allocation in birds remains a contentious subject, largely because effects on offspring sex ratios are small. Our results suggest that offspring sex ratios are shaped by various processes and trade-offs that act throughout the female life history and ultimately reduce the extent of sex-ratio adjustment relative to classic theoretical predictions.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

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.     

Effects of 17-β-estradiol treatment of female zebra finches on offspring sex ratio and survival

Treatment of female zebra finches (Taeniopygia guttata) with 17-beta-estradiol leads to a female-biased sex ratio in their offspring at the age of independence [Horm. Behav. 35 (1999) 135]. It is unclear whether this is due to a bias of the primary sex ratio or to sex-specific survival. We replicated this experiment and found again a significantly higher total number of daughters than sons at independence in the estradiol-treated group. This was due to higher embryonic survival of daughters compared with sons in the estradiol-treated group and the reverse in the control group. There was no effect of the hormone treatment on the primary sex ratio. Treatment with 17-beta-estradiol led to a significantly shorter hatching time and to heavier offspring at day 7 after hatching. This weight was correlated with maternal plasma estradiol levels on the day of the first egg, which were significantly higher in the estradiol-treated group than in the control group. The results do not support the idea that maternal estradiol levels influence the primary sex ratio. They indicate that maternal estradiol differentially affects survival of sons and daughters via an influence on the embryonic environment, possibly enhancing offspring growth.     

Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival

Treatment of female zebra finches (Taeniopygia guttata) with 17-beta-estradiol leads to a female-biased sex ratio in their offspring at the age of independence [Horm. Behav. 35 (1999) 135]. It is unclear whether this is due to a bias of the primary sex ratio or to sex-specific survival. We replicated this experiment and found again a significantly higher total number of daughters than sons at independence in the estradiol-treated group. This was due to higher embryonic survival of daughters compared with sons in the estradiol-treated group and the reverse in the control group. There was no effect of the hormone treatment on the primary sex ratio. Treatment with 17-beta-estradiol led to a significantly shorter hatching time and to heavier offspring at day 7 after hatching. This weight was correlated with maternal plasma estradiol levels on the day of the first egg, which were significantly higher in the estradiol-treated group than in the control group. The results do not support the idea that maternal estradiol levels influence the primary sex ratio. They indicate that maternal estradiol differentially affects survival of sons and daughters via an influence on the embryonic environment, possibly enhancing offspring growth.     

Different optimal offspring sizes for sons versus daughters may favor the evolution of temperature-dependent sex determination in viviparous lizards

Temperature-dependent sex determination (TSD) has evolved independently in at least two lineages of viviparous Australian scincid lizards, but its adaptive significance remains unclear. We studied a montane lizard species (Eulamprus heatwolei) with TSD. Our data suggest that mothers can modify the body sizes of their offspring by selecting specific thermal regimes during pregnancy (mothers with higher and more stable temperatures produced smaller offspring), but cannot influence sons versus daughters differentially in this way. A field mark-recapture study shows that optimal offspring size differs between the sexes: larger body size at birth enhanced the survival of sons but reduced the survival of daughters. Thus, a pregnant female can optimize the fitness of either her sons or her daughters (via yolk allocation and thermoregulation), but cannot simultaneously optimize both. One evolutionary solution to reduce this fitness cost is to modify the sex-determining mechanism so that a single litter consists entirely of either sons or daughters; TSD provides such a mechanism. Previous work has implicated a sex difference in optimal offspring size as a selective force for TSD in turtles. Hence, opposing fitness determinants of sons and daughters may have favored evolutionary transitions from genetic sex determination to TSD in both oviparous turtles and viviparous lizards.     

Pair bond duration influences paternal provisioning and the primary sex ratio of brown thornbill broods

Parents should vary their level of investment in sons and daughters in response to the fitness costs and benefits accrued through male and female offspring. I investigated brood sex ratio biases and parental provisioning behaviour in the brown thornbill, Acanthiza pusilla, a sexually dimorphic Australian passserine. Parents delivered more food to male-biased than female-biased broods. However, factors determining parental provisioning rates differed between the sexes. Female provisioning rates were related to brood sex ratio in both natural and experimental broods with manipulated sex ratios. In contrast, male provisioning rates were not affected by brood sex ratio in either natural or experimental broods. However, males in established pairs provisioned at a higher rate than males in new pairs. Data on the sex ratio of 109 broods suggest that female brown thornbills adjust their primary sex ratio in response to pair bond duration. Females in new pairs produced broods with significantly fewer sons than females in established pairs. This pattern would be beneficial to females if the costs of rearing sons were higher for females in new than established pairs. This may be the case since females in new pairs provisioned experimental all-male broods at elevated rates. The condition of nestlings also tended to decline more in these all-male broods than in other experimental broods. This will have additional fitness consequences because nestling mass influences recruitment in thornbills. Female thornbills may therefore obtain significant fitness benefits from adjusting their brood sex ratio in response to the status of their pair bond. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live‐bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male‐biased broods had greater mating success at maturity than sons in female‐biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male‐biased brood when the reproductive success of sons is expected to be high.     

Sex-specific fledgling success and brood sex ratio in the Great Reed Warbler (Acrocephalus arundinaceus)

We examine sex ratio variation and sex-specific probability of successful fledgling in relation to hatching date across 376 broods of Great Reed Warblers (Acrocephalus arundinaceus). The sex ratio of complete broods as well as broods with partial mortality did not deviate significantly from parity (0.5 and 0.53, respectively). Variation in sex ratio between broods was not larger than expected from binomial distribution, thus females seem not to manipulate the sex ratio of their broods in the studied population. As a consequence, sex ratio did not vary in relation to hatching date, years and fishponds. Female offspring showed lower fledgling success than their brothers, but the relationship between probability of successful fledgling and hatching date differed between sexes. Fledgling success of female offspring declined with hatching date more strongly than the success of male offspring. Thus, our study shows that Great Reed Warblers do not adjust offspring sex to match observed seasonal sex-specific variation in survival.     

Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters

Mothers can influence the phenotype of their offspring by adjustingthe quality of their eggs in relation to sex and reproductivevalue of the progeny. Maternal androgens in the eggs of vertebratesmay mediate such adaptive early maternal effects. However, theevolution of early maternal effects mediated by egg androgensmay be constrained by the inability of mothers to differentiallyallocate androgens to eggs with a male or a female if androgenshave different effects on sons and daughters. In this study,we increased the concentration of androgens in the eggs of barnswallows (Hirundo rustica) within the physiological range ofvariation and analyzed the effect on nestling growth and beggingbehavior. Egg androgens increased body size and mass of sonsbut reduced these characters in daughters when compared to twocontrol groups in a repeated-measures analysis of variance ofdata collected at different ages. However, the differentialeffect of androgen on the two sexes was no longer significantwhen the analysis was restricted to the age of 12 days, whenfinal body size is attained. In a second experiment, we testedwhether mothers differentially allocated androgens to eggs withsons rather than daughters while manipulating a paternal secondarysexual character. Androgen concentration did not vary in relationto paternal ornamentation or embryo sex. Hence, antagonisticeffects of egg androgens on sons and daughters may exist inthe very early posthatching life and may constrain the evolutionof adaptive maternal effects because mothers do not differentiallyallocate androgens in relation to embryo sex.     

Mothers adjust offspring sex to match the quality of the rearing environment

Theory predicts that mothers should adjust offspring sex ratios when the expected fitness gains or rearing costs differ between sons and daughters. Recent empirical work has linked biased offspring sex ratios to environmental quality via changes in relative maternal condition. It is unclear, however, whether females can manipulate offspring sex ratios in response to environmental quality alone (i.e. independent of maternal condition). We used a balanced within-female experimental design (i.e. females bred on both low- and high-quality diets) to show that female parrot finches (Erythrura trichroa) manipulate primary offspring sex ratios to the quality of the rearing environment, and not to their own body condition and health. Individual females produced an unbiased sex ratio on high-quality diets, but over-produced sons in poor dietary conditions, even though they maintained similar condition between diet treatments. Despite the lack of sexual size dimorphism, such sex ratio adjustment is in line with predictions from sex allocation theory because nutritionally stressed foster sons were healthier, grew faster and were more likely to survive than daughters. These findings suggest that mothers may adaptively adjust offspring sex ratios to optimally match their offspring to the expected quality of the rearing environment.