Sexual dimorphism,survival, and parental investment in relation to offspring sex in a precocial bird

Differential growth rate between males and females, owing to a sexual size dimorphism, has been proposed as a mechanism driving sex‐biased survival. How parents respond to this selection pressure through sex ratio manipulation and sex‐biased parental investment can have a dramatic influence on fitness. We determined how differential growth rates during early life resulting from sexual size dimorphism affected survival of young and how parents may respond in a precocial bird, the black brant Branta bernicla nigricans. We hypothesized that more rapidly growing male goslings would suffer greater mortality than females during brood rearing and that parents would respond to this by manipulating their primary sex ratio and parental investment. Male brant goslings suffered a 19.5% reduction in survival relative to female goslings and, based on simulation, we determined that a female biased population sex ratio at fledging was never overcome even though previous work demonstrated a slight male‐biased post‐fledging survival rate. Contrary to the Fisherian sex ratio adjustment hypothesis we found that individual adult female brant did not manipulate their primary sex ratio (50.39% male, n = 645), in response to the sex‐biased population level sex ratio. However, female condition at the start of the parental care period was a good predictor of their primary sex ratio. Finally, we examined how females changed their behavior in response to primary sex ratio of their broods. We hypothesized that parents would take male biased broods to areas with increased growth rates. Parents with male biased primary sex ratios took broods to areas with higher growth rates. These factors together suggest that sex‐biased growth rates during early life can dramatically affect population dynamics through sex‐biased survival and recruitment which in turn affects decisions parents make about sex allocation and sex‐biased parental investment in offspring to maximize fitness.     

Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby

Sex allocation theory predicts that mothers in good conditionshould bias their brood sex ratio in response to the differentialbenefits obtained from increased maternal expenditure in sonsand daughters. Although there is well-documented variationof offspring sex ratios in several bird species according tomaternal condition, the assumption that maternal condition has different fitness consequences for male and for female offspringremains unclear. The blue-footed booby (Sula nebouxii) is asexually size-dimorphic seabird, with females approximately31% heavier than males. It has been reported that the sex ratiois male biased in years with poor feeding conditions, whichsuggests that either females adjust their sex ratio in accordancewith their condition or that they suffer differential brood mortality before their sex can be determined. In this studyI tested whether the condition of mothers affected their daughters'fitness more than their sons' fitness. I manipulated maternalinvestment by trimming the flight feathers and thereby handicappingfemales during the chick-rearing period. Adult females in thehandicapped group had a poorer physical condition at end ofchick growth, as measured by mass and by the residuals of masson wing length compared to control birds. Female chicks wereaffected by the handicapping experiment, showing a lower massand shorter wing length (reduced approximately 8% in both measures)than controls. However, this effect was not found in male chicks.Hatching sex ratios were also related to female body conditionat hatching. The brood sex ratio of females in poor conditionwas male biased but was female biased for females in good condition.Overall, these results suggest that the variation in the sexratio in blue-footed boobies is an adaptive response to thedisadvantage daughters face from being reared under poor conditions.     

Sex ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird

When the cost of rearing sons and daughters differs and the subsequent survival and reproductive success of one sex is more dependent than the other, on the amount of parental investment, adult females tend to produce more chicks of the more dependent sex if the females are in good condition themselves. One method of varying the total investment in each sex is through modifying the sex ratio of offspring produced. This study shows that in broods of European Shags Phalacrocorax aristotelis , the sex ratio varied with laying date. Presumably in this species, the lifetime reproductive success of males is more dependent on the level of parental investment. Early breeders are in better condition, the brood sex ratio of early broods was male biased (0.63), while that of late broods was female biased (0.36). The overall difference in sex ratio found between early and late nests could be attributed to manipulation of sex in the first laid egg. In early broods, 77% of the first hatched chicks were male but only 30% of the first hatched chicks in late broods were male. The sex combination of the first two chicks in a brood significantly affected growth as measured by asymptotic mass.     

Unusual pattern of sex‐specific mortality in relation to initial brood sex composition in the black‐billed magpie Pica pica

In sexually size‐dimorphic species, brood sex composition may exert differential effects on sex‐specific mortality. We investigated the sex‐specific mortality and body condition in relation to brood sex composition in nestlings of the black‐billed magpie Pica pica. Neither significantly sex‐biased production at hatching nor overall sex‐biased mortality during the nestling period was found. Sex‐specific mortality as a function of brood sex composition, however, differed between female and male nestlings. We found higher mortality for females in male‐biased broods and higher mortality for males in female‐biased broods, a phenomenon that we call ‘rarer‐sex disadvantage’. As a result, fledging sex ratios became more biased in the direction of bias at hatching, a phenomenon that cannot be readily explained by previous hypotheses for sex‐specific mortality. Two temporal variables, fledging date and laying date, were also correlated with sex‐specific mortality: female nestlings in earlier broods experienced higher mortality than male nestlings whereas male nestlings in later broods experienced higher mortality. We suggest that this unusual pattern of mortality may be explained by adaptive adjustments of brood sex composition by parents, either through the effects of a slight sex difference in offspring dispersal patterns on parental fitness, or owing to sex differences as regards the benefits of early fledging.     

Brood sex ratio in the Kentish plover

How and why do the mating opportunities of males and femalesdiffer in natural population of animals? Previously we showedthat females have higher mating opportunities than males inthe Kentish plover Charadrius alexandrinus. Both parents incubatethe eggs, and males provide more brood care than females; thusit is not obvious why the females find new mates sooner thanthe males. In this study we investigated whether the sex-biasedmating opportunities stem from biased offspring sex ratios.We determined the sex of newly hatched, precocial chicks usingCHD gene markers. Among fully sexed broods, 0.461 ± 0.024(SE) of chicks (454 chicks in 158 broods) were male, and thissex ratio was not significantly different from unity. The proportionof males at hatching decreased significantly over the breedingseason, which occurred consistently in all 3 years of the study.Large chicks were more likely to be males than females. Neitherparental age nor body size of male and female parents was relatedto brood sex ratio. We also sexed a number of chicks that werecaught after they left their nest (range of estimated ages 0–17days) and found that the proportion of males increased withbrood age. This relationship remained highly significant whencontrolling statistically for hatching date. As brood size decreaseddue to mortality after the chicks left their nest, these resultssuggest that the mortality of daughters was higher than thatof the sons shortly after hatching. Taken together, our resultsshow that the female-biased mating opportunities in the Kentishplover are not due to biased brood sex ratio at hatching but,at least in part, are due to female-biased chick mortality soonafter hatching.     

Offspring sex ratios in tree swallows: females in better condition produce more sons

Organisms are expected to adjust the sex ratio of their offspring in relation to the relative fitness benefits of sons and daughters. We used a molecular sexing technique that amplifies an intron of the CHD1 gene in birds to examine the sex ratio at egg-laying in socially monogamous tree swallows (Tachycineta bicolor). We examined all individuals in 40 broods (210 young), including all unhatched eggs and nestlings. Thus, the sex ratio we measured was the same as the sex ratio at laying. Overall, the mean sex ratio per brood (+/- SD) was biased significantly towards males (57 +/- 2% male). Within broods, male-biased sex ratios were associated with females in better body condition, and these females were more likely to produce sons in better condition. Tree swallows have one of the highest known levels of extra-pair paternity in birds (38-76% extra-pair young), and, as a consequence, variance in male reproductive success is greater than that of females. Thus, in tree swallows, investment in sons has the potential for higher fitness returns than investment in daughters, assuming that sons in better condition have greater reproductive success.     

Maternal Condition but Not Corticosterone Is Linked to Offspring Sex Ratio in a Passerine Bird

There is evidence of offspring sex ratio adjustment in a range of species, but the potential mechanisms remain largely unknown. Elevated maternal corticosterone (CORT) is associated with factors that can favour brood sex ratio adjustment, such as reduced maternal condition, food availability and partner attractiveness. Therefore, the steroid hormone has been suggested to play a key role in sex ratio manipulation. However, despite correlative and causal evidence CORT is linked to sex ratio manipulation in some avian species, the timing of adjustment varies between studies. Consequently, whether CORT is consistently involved in sex-ratio adjustment, and how the hormone acts as a mechanism for this adjustment remains unclear. Here we measured maternal baseline CORT and body condition in free-living blue tits (Cyanistes caeruleus) over three years and related these factors to brood sex ratio and nestling quality. In addition, a non-invasive technique was employed to experimentally elevate maternal CORT during egg laying, and its effects upon sex ratio and nestling quality were measured. We found that maternal CORT was not correlated with brood sex ratio, but mothers with elevated CORT fledged lighter offspring. Also, experimental elevation of maternal CORT did not influence brood sex ratio or nestling quality. In one year, mothers in superior body condition produced male biased broods, and maternal condition was positively correlated with both nestling mass and growth rate in all years. Unlike previous studies maternal condition was not correlated with maternal CORT. This study provides evidence that maternal condition is linked to brood sex ratio manipulation in blue tits. However, maternal baseline CORT may not be the mechanistic link between the maternal condition and sex ratio adjustment. Overall, this study serves to highlight the complexity of sex ratio adjustment in birds and the difficulties associated with identifying sex biasing mechanisms.     

Female Control of Offspring Sex Ratios Based on Male Attractiveness in the Guppy

The sex allocation hypothesis predicts that females manipulate the offspring sex ratios according to mate attractiveness. Although there is increasing evidence to support this prediction, it is possible that paternal effects may often obscure the relationship between female control of offspring sex ratios and male attractiveness. In the present study, we examined whether females played a primary role in the manipulation their offspring sex ratios based on male attractiveness, in the guppy Poecilia reticulata, a live‐bearing fish. We excluded the paternal effects by controlling the relative sexual attractiveness of the male by presenting them to the females along with a more attractive or less attractive stimulus male. The test male was perceived to be relatively more attractive by females when it was presented along with a less attractive stimulus male, or vice versa. Subsequently, test male was mated in two different roles (relatively more and less attractive) with two females. If females were responsible for offspring sex ratio manipulation, the sex ratio of the brood would be altered on the basis of the relative attractiveness of the test male. On the other hand, if males play a primary role in offspring sex ratio manipulation, the sex ratios would not differ with the relative attractiveness of the test male. We found that females gave birth to more male‐biased broods when they mated with test males in the attractive role than when they mated with males in the less attractive role. This finding suggests that females are responsible for the manipulation of offspring sex ratios based on the attractiveness of their mates.     

Maternal influences on brood sex ratios: an experimental study in tree swallows

When the reproductive value of sons and daughters differ, parents are expected to adjust the sex ratio of their offspring to produce more of the sex that provides greater fitness returns. The body condition of females or environmental factors, such as food abundance and mate quality, may influence these expected fitness returns. In a previous study of tree swallows (Tachycineta bicolor), we found that females produced more sons in their broods when they were in better body condition (mass corrected for size). We tested this relationship by experimentally clipping some flight feathers to reduce female body condition. As predicted, we found that females with clipped feathers had a lower proportion of sons in their broods and poorer body condition. However, female body condition alone was not a significant predictor of brood sex ratio in our experiment. We suggest that brood sex ratio is causally related to some other factor that covaries with body condition, most likely the foraging ability of females. The hypothesis that brood sex ratios are influenced by individual differences in female foraging ability is supported by a high repeatability of brood sex ratio for individual females. Thus, maternal effects may have a strong influence on the sex ratios of offspring.     

Cross‐fostering eggs reveals that female collared flycatchers adjust clutch sex ratios according to parental ability to invest in offspring

Across animal taxa, reproductive success is generally more variable and more strongly dependent upon body condition for males than for females; in such cases, parents able to produce offspring in above‐average condition are predicted to produce sons, whereas parents unable to produce offspring in good condition should produce daughters. We tested this hypothesis in the collared flycatcher (Ficedula albicollis) by cross‐fostering eggs among nests and using the condition of foster young that parents raised to fledging as a functional measure of their ability to produce fit offspring. As predicted, females raising heavier‐than‐average foster fledglings with their social mate initially produced male‐biased primary sex ratios, whereas those raising lighter‐than‐average foster fledglings produced female‐biased primary sex ratios. Females also produced male‐biased clutches when mated to males with large secondary sexual characters (wing patches), and tended to produce male‐biased clutches earlier within breeding seasons relative to females breeding later. However, females did not adjust the sex of individuals within their clutches; sex was distributed randomly with respect to egg size, laying order and paternity. Future research investigating the proximate mechanisms linking ecological contexts and the quality of offspring parents are able to produce with primary sex‐ratio variation could provide fundamental insight into the evolution of context‐dependent sex‐ratio adjustment.     

Maternal correlates of brood sex ratio variation in the lekking lance-tailed manakin Chiroxiphia lanceolata

Theory predicts that overall population sex ratios should be around parity. But when individual females can receive higher fitness from offspring of one sex, they may benefit by biasing their brood sex ratios accordingly. In lekking species, higher variance in male reproductive success relative to that of females predicts that male offspring gain disproportionately from favorable rearing conditions. Females should therefore produce male-biased broods when they are in a position to raise higher quality offspring: i.e., in better body condition or when they reproduce earlier in the breeding season. To investigate these hypotheses, we studied brood sex ratios of lance-tailed manakins Chiroxiphia lanceolata . We found that overall sex ratios and mean brood sex ratios were not different from random expectation. Brood sex ratios were not related to laying date or female body condition. However, we detected a quadratic relationship between brood sex ratios and maternal age: both young (1–2 years) and old (8+ years) females produced female-biased brood sex ratios. This relationship was most clear in a year also distinguished by early rainy and breeding seasons. We suggest that breeding inexperience in young females and senescence in older females is the most plausible explanation for these results, and that the relationship between female age and brood sex ratio is mediated by environmental conditions.     

Costs of rearing and sex‐ratio variation in southern grey shrike Lanius meridionalis broods

Several non‐mutually exclusive hypotheses predict adaptive variation in the offspring sex ratio. When conditions for breeding are adverse, parents are predicted to produce more offspring of the less costly sex to rear (‘the cost‐of‐reproduction hypothesis’). Moreover, they also should produce the more dispersing sex in order to diminish future competition (‘the local‐resource‐competition hypothesis’). Here, we analyse brood sex ratio according to rearing conditions in the southern shrike Lanius meridionalis, a species with moderately reversed sexual dimorphism. Our results suggest that females are more costly to rear than males in this species. Adult females proved heavier than males, and female nestling tended to be heavier than male nestlings. Moreover, the greater brood reduction, the more male‐biased was the brood, suggesting that brood reduction implied higher mortality in female nestlings. Consistent with these findings, the brood sex ratio was biased to the less costly sex (males) when breeding conditions were adverse (bad years or low‐quality male parents), supporting the cost‐of‐reproduction hypothesis. By contrast, these findings did not support the local‐resource‐competition hypothesis, which predicted female‐biased brood sex ratio under adverse conditions. As a whole, our results support the idea that birds adaptively modulate sex ratio in order to minimize reproduction costs.     

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.     

Simultaneous spawning by female stream goby Rhinogobius sp. and the association with brood cannibalism by nesting males

A laboratory experiment was conducted by varying the undersurface area of nesting substratum and the number of females in an experimental tank to elucidate the determinants of the mating pattern in the stream goby, Rhinogobius sp. cross‐band type. Males with larger nests tended to attract two or more females to their nest in a tank. Moreover, males spawned simultaneously with multiple females and entire brood cannibalism by males was rarely observed under a female‐biased sex ratio. When males spawned with a single female with low fecundity, however, entire brood cannibalism occurred at a high frequency, suggesting that a male guarding a nest with fewer eggs consumes the brood. Therefore, spawning behaviour of females that leads to a large egg mass would decrease the risk of entire brood cannibalism. In this species, simultaneous spawning by multiple females in a nest serves as a female counter‐measure against entire brood cannibalism. These results suggest that a conflict of interest between the sexes through brood cannibalism is a major determinant of simultaneous spawning.     

Adaptive Offspring Sex Ratio Depends on Male Tail Length in the Guppy

A biased sex ratio in a brood is considered to be an adaptive strategy under certain circumstances. For example, if the expected reproductive success of one sex is greater than that of the other, parents should produce more offspring of the former sex than the latter. A previous study has documented that in the guppy, Poecilia reticulata, the female offspring of males possessing proportionally longer tails exhibit smaller body sizes and show decreased reproductive outputs than those of males having shorter tails. On the other hand, the total lengths of the male offspring of the long‐tailed males are larger because of their longer tails; consequently, they exhibit greater sexual attractiveness to females. Therefore, it has been hypothesized that this asymmetry in the expected reproductive success between the male and female offspring of long‐tailed males may result in a biased sex ratio that is dependent on the tail lengths of their fathers. This hypothesis was tested in the present study. The results showed that the females that mated with long‐tailed males produced more male offspring than those that mated with short‐tailed males. Logistic regression analysis showed that the ratio of tail length to the standard length of the fathers is a determinant factor of the sex of their offspring. These results suggest that the manipulation of the offspring sex ratios by parents enhances the overall fitness of the offspring.     

Sex allocation and sex‐specific parental investment in an endangered seabird

Biased offspring sex ratio is relatively rare in birds and sex allocation can vary with environmental conditions, with the larger and more costly sex, which can be either the male or female depending on species, favoured during high food availability. Sex‐specific parental investment may lead to biased mortality and, coupled with unequal production of one sex, may result in biased adult sex ratio, with potential grave consequences on population stability. The African Penguin Spheniscus demersus, endemic to southern Africa, is an endangered monogamous seabird with bi‐parental care. Female adult African Penguins are smaller, have a higher foraging effort when breeding and higher mortality compared with adult males. In 2015, a year in which environmental conditions were favourable for breeding, African Penguin chick production on Bird Island, Algoa Bay, South Africa, was skewed towards males (1.5 males to 1 female). Males also had higher growth rates and fledging mass than females, with potentially higher post‐fledging survival. Female, but not male, parents had higher foraging effort and lower body condition with increasing number of male chicks in their brood, thereby revealing flexibility in their parental strategy, but also the costs of their investment in their current brood. The combination of male‐biased chick production and higher female mortality, possibly at the juvenile stage as a result of lower parental investment in female chicks, and/or at the adult stage as a result of higher parental investment, may contribute to a biased adult sex ratio (ASR) in this species. While further research during years of contrasting food availability is needed to confirm this trend, populations with male‐skewed ASRs have higher extinction risks and conservation strategies aiming to benefit female African Penguin might need to be developed.     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.     

Molecular markers reveal reproductive strategies of non‐pollinating fig wasps

1. Fig wasps have proved extremely useful study organisms for testing how reproductive decisions evolve in response to population structure. In particular, they provide textbook examples of how natural selection can favour female‐biased offspring sex ratios, lethal combat for mates and dimorphic mating strategies. 2. However, previous work has been challenged, because supposedly single species have been discovered to be a number of cryptic species. Consequently, new studies are required to determine population structure and reproductive decisions of individuals unambiguously assigned to species. 3. Microsatellites were used to determine species identity and reproductive patterns in three non‐pollinating Sycoscapter species associated with the same fig species. Foundress number was typically one to five and most figs contained more than one Sycoscapter species. Foundresses produced very small clutches of about one to four offspring, but one foundress may lay eggs in several figs. 4. Overall, the data were a poor match to theoretical predictions of solitary male clutches and gregarious clutches with n ? 1 females. However, sex ratios were male‐biased in solitary clutches and female‐biased in gregarious ones. 5. At the brood level (all wasps in a fig), a decrease in sex ratio with increasing brood size was only significant in one species, and sex ratio was unrelated to foundress number. In addition, figs with more foundresses contain more wasp offspring. 6. Finally, 10–22% of females developed in patches without males. As males are wingless, these females disperse unmated and are constrained to produce only sons from unfertilised eggs.     

Sex-specific hatching order, growth rates and fledging success in jackdaws Corvus monedula

In the jackdaw Corvus monedula , eggs hatch asynchronously with the youngest chicks in the brood often starving to death. So far, it is unknown whether there are sex differences in vulnerability to starvation. Adult females are smaller than males suggesting that daughters should be cheaper to produce than sons and so, less likely to starve when nest conditions are poor. Here, we determine whether sex, laying order and season interact to influence growth and fledging success. In a nestbox population of jackdaws, we found a non-significant female bias at both hatching (112:120) and fledging (37:52). Generalised linear models revealed that parents seemed to be investing differently in sons and daughters depending on their chances of success. Broods produced late in the season were significantly female biased, particularly those from small clutches. Females hatched towards the end of the season, when conditions were poor, were more likely to fledge than males. Nestlings that were relatively large at hatching were more likely to fledge. This effect was particularly important for last hatched individuals. Overall, males had a higher mortality rate than females. The most likely cause was starvation due to higher energetic requirements, because males were larger than females at fledging. We suggest that in species with brood reduction, sex-biased mortality may be at least as important as primary sex ratio manipulation in determining avian sex ratios.     

The effect of sperm storage and timing of mating on offspring sex ratios in the yellow dung fly Scatophaga stercoraria

1. Offspring sex ratios in the yellow dung fly Scatophaga stercoraria were examined in the laboratory. 2. Previous work indicated that females using previously stored sperm to fertilise their eggs produced male‐biased sex ratios. This result may have been due to female influences or the effects of sperm storage per se. 3. This pattern was not reproduced in the study presented here. Females that were allowed to mate just prior to oviposition produced similarly male‐biased sex ratios to those females that used previously stored sperm to fertilise their clutch. 4. Captive‐reared females may have perceived a lack of males in the population and thus produced a male‐biased offspring sex ratio. Alternatively, gamete ageing or extra‐chromosomal sex ratio distorters may have produced the male bias.