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.     

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.     

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 allocation in the sexually monomorphic fairy martin

Offspring sex ratios were examined at the population and family level in the sexually monomorphic, socially monogamous fairy martin Petrochelidon ariel at five colony sites over a 4-year period (1993–1996). The sex of 465 nestlings from 169 broods was determined using sex-specific PCR at the CHD locus. In accordance with predicted sex allocation patterns, population sex ratios at hatching and fledging did not differ from parity in any year and the variance in brood sex ratios did not deviate from the binomial distribution. Further, brood sex ratio did not vary with hatching date during the season, brood number, brood size or colony size. The sex ratio of broods with extra-pair young did not differ from those without, while the sex ratio of broods fathered by males that gained extra-pair fertilizations did not differ from broods fathered by other males. Extra-pair chicks were as likely to be male as female. Neither the total number of feeding visits to the brood nor the relative feeding contribution by the sexes varied significantly with brood sex ratio. Brood sex ratios were also unrelated to paternal size, condition and breeding experience or maternal condition and breeding experience. However, contrary to our prediction, brood sex ratio was negatively correlated with maternal size. Generally, these results were consistent with our expectations that brood sex ratios would not vary with environmental factors or parental characteristics, and would not influence the level of parental provisioning. However, the finding that females with longer tarsi produced an excess of daughters is difficult to reconcile with our current understanding of fairy martin life history and breeding ecology.     

Facultative Adjustment of Brood Sex Ratio in Response to Indirect Manipulation of Behaviour

Sex allocation theory states that parents should adjust their offspring sex ratio according to the expected fitness returns from sons and daughters. Several recent studies indicate that such adaptive manipulation of offspring sex ratio is achievable, and that it may be influenced by e.g. morphological characters. Here we manipulate behaviour through interspecific cross-fostering of great tits ( Parus major ) and blue tits ( Cyanistes caeruleus ), and investigate its effect on the offspring sex ratio of adults that were themselves cross-fostered as chicks. The experience of being raised by a different species has previously been shown to result in aberrant species assortative behaviour and song, and a lowered dominance status during winter. Brood sex ratios of conspecifically breeding pairs with and without cross-fostered members were compared. Broods with at least one cross-fostered parent contained significantly more males than did control broods. Sex of cross-fostered parents did not influence the brood sex ratio. We conclude that female great tits and blue tits seem to be able to adjust the sex ratio of their broods, and that changes in their own or their partners' behaviour may elicit such adjustments.     

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.     

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.     

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.     

Do female Drosophila melanogaster adaptively bias offspring sex ratios in relation to the age of their mate?

Modification of offspring sex ratios in response to parental quality is predicted when the long-term fitness returns of sons and daughters differ. One factor that may influence a mother's sex allocation decision is the quality (or attractiveness) of her mate. We investigated whether the sex ratios of offspring produced by female Drosophila melanogaster are biased with respect to the age of the males to which they are mated, and whether there is an adaptive basis for this phenomenon. We found that females mated to old males (13 d post-eclosion) initially produced a greater proportion of daughters than did females mated to young males (1 d post-eclosion). This pattern does not appear to be due to a systematic difference in the numbers or mortality of the X- and Y-bearing sperm originating from old and young fathers, as the overall sex ratios of all offspring produced from a single copulation did not differ between broods fathered by the two types of males. The sons of older males fared worse in competitive mating assays than did the sons of younger males, while daughters of old and young males were of comparable fitness. These results suggest that there is an adaptive basis for the observed sex ratio modification.     

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.     

Postfledging parental care in Savannah sparrows: sex, size and survival

We investigated postfledging parental care in a philopatric population of Savannah sparrows,Passerculus sandwichensis , breeding on Kent Island, New Brunswick, Canada in an effort to understand the factors influencing adult birds' decisions about parental investment in offspring. Brood division was not based on offspring sex: male and female parents were equally likely to care for sons or daughters. The total duration of parental care, from hatching to independence, was similar for sons and daughters (median=23 days), regardless of the sex of the care-giving parent. The duration of parental care also corresponded closely to the time required for juveniles to acquire basic foraging skills. Despite high levels of extrapair paternity, male Savannah sparrows invested as much in postfledging care and were as effective as females in caring for fledglings, based on recruitment of fledglings into the breeding population the following year. Male parents were more likely to care for smaller fledglings and for offspring from early broods (presumably to enable females to dedicate their efforts towards second clutches). Caring for fledglings was costly for parents: survivorship decreased as a function of the duration of postfledging parental care and the number of fledglings cared for. Parental survivorship, however, was not affected by the sex of the fledglings cared for. This study suggests that sex-biased provisioning may be unlikely except in species with strongly sexually dimorphic offspring, biased offspring sex ratios and sex-biased natal dispersal. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

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.     

Sex allocation in black-capped chickadees Poecile atricapilla

Optimal sex allocation for individuals can be predicted from a number of different hypotheses. Fisherian models of sex allocation predict equal investment in males and females up to the end of parental care and predict brood compositions based on the relative costs of producing males and females. The Trivers-Willard hypothesis predicts that individual females should alter the sex ratio of their broods based on their own condition if it has a differential impact on the lifetime reproductive success of their sons and daughters. The Charnov model of sex allocation predicts that females should alter sex allocation based on paternal attributes that may differentially benefit sons versus daughters. Because females are the heterogametic sex in birds, many recent studies have focussed on primary sex ratio biases. In black-capped chickadees Poecile atricapilla , males are larger than females suggesting they may be more costly to raise than females. Female condition affects competitive ability in contests for mates, and thus may be related to variance in fecundity. Females prefer high-ranking males as both social and extrapair partners. These observations suggest that females might vary the sex ratio of their broods based on the predictions of any of the above models. Here, we report on the results of PCR based sex determination of 1093 nestlings in 175 broods sampled from 1992 to 2001. Population-wide, we found a mean brood sex ratio of 0.525±0.016, with no significant deviation from a predicted binomial distribution. We found no effect of clutch size, female condition, hatch date, parental rank or paternity. Our results reject the idea that female black-capped chickadees systematically vary sex allocation in their broods.     

Variably male-biased sex ratio in a marine bird with females larger than males

When the costs of rearing males and females differ progeny sex ratios are expected to be biased toward the less expensive sex. Blue-footed booby (Sula nebouxii) females are larger and roughly 32% heavier than males, thus presumably more costly to rear. We recorded hatching and fledging sex ratios in 1989, and fledging sex ratios during the next 5 years. In 1989, the sample of 751 chicks showed male bias at hatching (56%) and at fledging (57% at ˜90 days). Fledging sex ratios during the five subsequent reproductive seasons were at unity (1 year) or male-biased, varying from 56% to 70%. Male bias was greater during years when mean sea surface temperature was warmer and food was presumably in short supply. During two warm-water years (only) fledging sex ratio varied with hatching date. Proportions of male fledglings increased with date from 0.48 to 0.73 in 1994, and from 0.33 to 0.79 in 1995. Similar results were obtained when the analysis was repeated using only broods with no nestling mortality, suggesting that the overall increase in the proportion of males over the season was the result of sex ratio adjustments at hatching. The male-biased sex ratio, and the increased male bias during poor breeding conditions supports the idea that daughters may be more costly than sons, and that their relative cost increases in poor conditions. Received: 3 February 1998 / Accepted: 12 September 1998     

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.     

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.     

Brood parasitism increases provisioning rate, and reduces offspring recruitment and adult return rates, in a cowbird host

Interspecific brood parasitism in birds presents a special problem for the host because the parasitic offspring exploit their foster parents, causing them to invest more energy in their current reproductive effort. Nestling brown-headed cowbirds (Molothrus ater) are a burden to relatively small hosts and may reduce fledgling quality and adult survival. We documented food-provisioning rates of one small host, the prothonotary warbler (Protonotaria citrea), at broods that were similar in age (containing nestlings 8–9 days old), but that varied in composition (number of warbler and cowbird nestlings) and mass, and measured the effect of brood parasitism on offspring recruitment and adult returns in the host. The rate of food provisioning increased with brood mass, and males and females contributed equally to feeding nestlings. Controlling for brood mass, the provisioning rate was higher for nests with cowbirds than those without. Recruitment of warbler fledglings from unparasitized nests was 1.6 and 3.7 times higher than that of fledglings from nests containing one or two cowbirds, respectively. Returns of double-brooded adult male and female warblers decreased with an increase in the number of cowbirds raised, but the decrease was more pronounced in males. Reduced returns of warbler adults and recruitment of warbler fledglings with increased cowbird parasitism was likely a result of reduced survival. Cowbird parasitism increased the warblers’ investment in current reproductive effort, while exerting additional costs to current reproduction and residual reproductive value. Our study provides the strongest evidence to date for negative effects of cowbird parasitism on recruitment of host fledglings and survival of host adults.     

No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus)

Sex allocation theory predicts that parents should manipulatebrood sex ratio in order to maximise the combined reproductivevalue of their progeny. Females mating with high quality malesshould, therefore, be expected to produce brood sex ratiosbiased towards sons, as male offspring would receive a relativelygreater advantage from inheritance of their father's characteristicsthan would their female siblings. Furthermore, it has been suggested that sex allocation in chicks fathered through extrapair fertilizations should also be biased towards sons. Contraryto these predictions, we found no evidence that the distributionof sex ratios in a sample of 1483 chicks from 154 broods ofblue tits (Parus caeruleus) deviated significantly from thatof a binomial distribution around an even sex ratio. In addition,we found no significant effect on brood sex ratio of the individualquality of either parent as indicated by their biometrics, feather mite loads, time of breeding, or parental survival. This suggeststhat females in our population were either unable to manipulateoffspring sex allocation or did not do so because selectionpressures were not strong enough to produce a significant shiftaway from random sex allocation. The paternity of 986 chicks from 103 broods was determined using DNA microsatellite typing.Extrapair males sired 115 chicks (11.7%) from 41 broods (39.8%).There was no significant effect of paternity (within-pair versusextrapair) on the sex of individual offspring. We suggest that,in addition to the weakness of selection pressures, the possiblemechanisms responsible for the allocation of sex may not besufficiently accurate to control offspring sex at the levelof the individual egg.     

Do females adjust the sex of their offspring in relation to the breeding sex ratio?

When the adult sex ratio differs between years in local populations, but still is predictable between adjacent years, it has been proposed that the best strategy would be to bias the offspring sex ratio in favour of the rare sex. We tested this hypothesis using a data set of great reed warbler offspring, sexed by molecular techniques, that were collected over 11 breeding seasons at two adjacent reed marshes. Three important assumptions for this hypothesis are fulfilled in the studied great reed warbler population. First, a substantial proportion of great reed warblers are living in small local populations where sex ratio distortions would be sufficiently large and common. Second, breeding adults and their offspring return to breed in the local population to a high degree. Third, females have a possibility to assess the breeding sex ratio before laying their eggs. At our study site, the breeding sex ratio was positively correlated between successive years. However, contrary to our prediction, female great reed warblers seemed not to adjust their offspring sex ratio in relation to the local breeding sex ratio.