Extreme gender-based post-fledging brood division in the toc-toc

The possibility that parents of one sex may preferentially investin offspring of a certain sex raises profound evolutionary questionsabout the relative worth of sons and daughters to their mothersand fathers. Post-fledging brood division—in which eachparent feeds a different subset of offspring—has beenwell documented in birds. However, a lack of empirical evidencethat this may be based on offspring sex, combined with the theoreticaldifficulty of explaining such an interaction, has led researchersto consider a gender bias in post-fledging brood division highlyunlikely. Here we show that in the toc-toc, Foudia sechellarum,post-fledging brood division is extreme and determined by sex;where brood composition allows, male parents exclusively provisionmale fledglings, whereas female parents provision female fledglings.This is the first study to provide unambiguous evidence, basedon molecular sexing, that sex-biased post-fledging brood divisioncan occur in birds. Male and female parents provisioned at thesame rate and neither offspring nor parent survival appearedto be affected by the sex of the parent or offspring, respectively.The current hypotheses predicting advantages for brood divisionand preferential care for one specific type of offspring arediscussed in the light of our results.     

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.     

No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows

Sex allocation theory predicts that parents should adjust investment in sons and daughters according to relative fitness of differently sexed offspring. In species with female preference for highly ornamented males, one advantage potentially accruing to parents from investing more in sons of the most ornamented males is that male offspring will inherit characters ensuring sexual attractiveness or high-quality genes, if ornaments honestly reveal male genetic quality. Furthermore, in species where extra-pair fertilizations occur, offspring sired by an extra-pair male are expected to more frequently be male than those of the legitimate male if the latter is of lower quality than the extra-pair male. We investigated adjustment of sex ratio of offspring in relation to ornamentation of the extra-pair and the social mate of females by direct manipulation of tails of male barn swallows Hirundo rustica . Molecular sexing of the offspring was performed using the W chromosome-linked avian chromo-helicase-DNA-binding protein (CHD) gene while paternity assessment was conducted by typing of hypervariable microsatellite loci. Extra-pair offspring sex ratio was not affected by ornamentation of their biological fathers relative to the experimental ornamentation of the parental male. Experimental ornamentation of the parental males did not affect the sex ratio of nestlings in their broods. Female barn swallows might be unable to bias offspring sex ratio at hatching according to the quality of the biological father. Alternatively, fitness benefits in terms of sexual attractiveness of sons might be balanced by the cost of compensating for little parental care provided by highly ornamented parental males, if sons are more costly to rear than daughters, or the advantage of producing more daughters, if males with large ornaments contribute differentially more to the viability of daughters than sons.     

Sex ratio variation among broods of great reed warblers Acrocephalus arundinaceus

The sex of 746 great reed warbler fledglings (from 175 broods) was determined by the use of single primer polymerase chain reaction. The reliability of the technique was confirmed as 104 of the fledglings were subsequently recorded as adults of known sex. The overall sex ratio did not differ from unity. Variation in sex ratios between broods was larger than expected from a binomial distribution. Female identity explained some of the variation of brood sex ratio indicating that certain females consistently produced sex ratios that departed from the average value in the population. The theory of sex allocation predicts that parents should adjust the sex ratio of their brood to the relative value of sons and daughters and this may vary in relation to the quality of the parents or to the time of breeding. In the great reed warbler, the proportion of sons was not related to time of breeding, or to any of five female variables. Of five male variables, males with early arrival date tended to produce more daughters. The sex ratio of fledglings that were a result of extra-pair fertilizations did not differ from that of legitimate fledglings. Hence, there is currently no evidence of that female great reed warblers invest in a higher proportion of sons when mated with attractive males.     

Prolonged offspring dependence and cooperative breeding in birds

It has been suggested that the evolution of cooperative breedingin birds is associated with unusually long periods of offspringdependence ; this appears paradoxical because cooperative breedersoften produce more broods than their noncooperatively breedingrelatives. I compared the duration of parental care betweencooperatively and noncooperatively breeding species using phylogeneticallyindependent contrasts and matched pairs. The incubation andnestling periods did not differ between the two parental caresystems, but the duration of postfledging offspring care wassignificantly longer in species that regularly breed cooperatively.This relationship remained when other factors that are thoughtto affect the duration of fledgling care (breeding habitat,body size, latitude of breeding, diet) were controlled statistically.Cooperative breeders appear to provide more prolonged postfledgingcare because additional care providers reduce the costs of parenting, offspring have less incentive to become independent,and a division of labor can develop during reproduction—helperscontinue to feed fledglings while breeders initiate the nextnesting attempt.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

The effects of the minimum threshold condition for breeding on offspring sex-ratio adjustment in the lesser kestrel

We propose a model for sex-ratio adjustment complementary to that of Trivers and Willard. In addition to the three basic assumptions of the Trivers-Willard model, our model assumes that the sex with more variable reproductive success (normally male) is also the sex less constrained for reproduction. This assumption seems realistic, because several studies have demonstrated that poor-condition males may adopt alternative mating strategies and sire some offspring, whereas females have physiological constraints for gestation or egg production that cannot be avoided. Thus, under these circumstances, sons of both poor and good condition would be more valuable for parents than daughters, whereas daughters would be relatively more valuable than sons at intermediate condition. This model predicts, therefore, a U-shaped relationship between parental condition and offspring sex ratio. We present a case study for the monogamous lesser kestrel (Falco naumanni) that fulfills the assumptions and predictions of the model. The minimum body condition for breeding, measured as pectoral thickness, was lower for sons than for daughters. Below this minimum, males had a higher chance of breeding than females. Above this minimum, however, the lifetime reproductive success was condition dependent in males but not in females. Thus, males in better body condition attain, on average, higher reproductive success than females. Offspring sex ratio varied with the size of the father's ornaments and mother condition according to the U-shaped pattern predicted by the model.     

Transmission of parental care behavior in African striped mice, Rhabdomys Pumilio

The expression of behavior, including parental care behavior, is influenced by complex interactions of the genes of an organism and the prevailing environmental conditions. Previously, we showed that the development of paternal, but not maternal, care in the African striped mouse, Rhabdomys pumilio, has a significant nongenetic maternal component. Here, we investigate the genetic component of parental care behavior from parents to offspring. We first measured the duration of parental care behavior of mothers and fathers every second day for 11 days postnatally. Subsequently, one son and one daughter from each of these litters were paired with unrelated mates when they were adults and their parental care behavior scored. Using regression models, we then compared parental care behavior of parents and their adult offspring. The transmission of parental care behavior from striped mouse fathers to sons and from mothers to both sons and daughters did not indicate a genetic component. Instead, we found a patrilineal genetic component for parental care in daughters. The reason for this unusual pattern of inheritance is not known, but this finding complements that of our other studies, showing that the expression of maternal care behavior in adult daughters is also not nongenetically influenced by their mothers. We suggest that, although females are constrained to provide maternal care in different social contexts, maternal care behavior may be influenced genetically by the father.     

Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica

Parents of sexually reproducing species should adjust their investment in production of sons and daughters in relation to the relative costs and reproductive value of offspring of either sex. Sex allocation mediated by differential allocation of care such as food provisioning, however, requires that parents can identify offspring sex. We analysed sex differences in offspring begging calls that may serve as a cue for parents to discriminate between sons and daughters. A combination of three sonagraphic variables of begging calls of nestling barn swallows allowed us to classify them according to sex at day 16, but not at day 12 after hatching, suggesting that sex differences in begging calls arise during the nestling period as the time of fledging approaches. Hence, parents may be able to discriminate between sons and daughters by auditory cues, which would enable differential allocation of food between offspring during the late nestling and early fledging stages. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Long-term fitness benefits of egg sex modification by the Seychelles warbler

Sex-ratio theory states that if the fitness costs to the parents of producing one offspring's sex relative to the other are higher, parents should discount these costs by producing fewer individuals of the more costly sex. In the co-operatively breeding Seychelles warbler (Acrocephalus sechellensis) mothers adaptively modify the sex of their single egg toward daughters, the helping sex, when living on territories with rich resources where helpers increase parental reproductive success, but toward sons, the dispersing sex, when living on territories where resources are scarce and/or no helping benefits accrue. By modifying offspring sex ratio, parents maximize their inclusive fitness benefits. Pairs in high-quality territories gained significantly more inclusive fitness benefits (through helping and reproducing offspring) from the production of daughters than from sons, and vice versa in low-quality territories (through reproducing offspring). Experimental manipulation of the offspring's sex shows that the consequences of sex allocation are adaptive for parents on high-quality territories. On high-quality territories with female production, breeding pairs raising step-daughters gained significantly higher inclusive benefits (through indirect and direct fitness gains) than by raising step-sons.     

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.     

Provisioning in western bluebirds is not related to offspring sex

Parents should invest more in one sex of offspring if the fitnessreturn per unit investment is higher for that sex. Sex-biasedprovisioning may occur when sons and daughters differ in theirneeds or when there is local resource competition or enhancement.We used feeding observations and sex-ratio manipulations todetermine if sex-biased provisioning occurs in western bluebirds(Sialia mexicana). The sex ratio of the brood had no effecton feeding rates by adults at unmanipulated nests over a 6-yearperiod. Adult males and females also did not differ in the numberof feedings made to sons and daughters in 13 videotaped nests.Likewise, adult feeding rates to nests experimentally biasedtoward sons or daughters did not differ significantly. Nesdingsthat were closest to the nest hole and that reached highestwere the most likely to be fed. Sons and daughters did not differin the begging behaviors most likely to result in a feeding.We conclude that sex-biased provisioning does not occur in thispopulation of western bluebirds and diat nesding behavior maybe a more important determinant of feeding.     

Does the differential cost of sons and daughters lead to sex ratio adjustment in great frigatebirds Fregataminor?

Sex allocation theory predicts that if benefits of producing sons and daughters differ and outweigh the costs of sex ratio adjustment, parents should produce more of the offspring that provide them with greater fitness. Potential benefits may be more likely to outweigh costs where sexual size dimorphism and, in birds, single‐egg clutches exist. Great frigatebirds Fregataminor are seabirds in which females are larger than males and clutch size is one egg. In our study population, sexual size dimorphism develops primarily during the period of complete juvenile dependence on parental care, consistent with a higher cost of producing daughters than sons. Over the course of the 1998 breeding season there was a shift from early season prevalence of daughters to late‐season prevalence of sons. Variation in food availability at time of egg laying, as indexed by sea surface temperature (SST), was a strong predictor of offspring sex in 1998. In contrast, SST in 2003 was not a predictor of offspring sex, nor was there a seasonal shift in the hatching sex ratio, despite a seasonal shift in SST. Besides food availability, we tested two additional factors in 2003 that could explain sex ratio adjustment in relation to the cost of reproduction. Offspring sex in 2003 was not related to natural or experimentally induced variation in maternal body condition; pre‐laying food supplements raised the body condition of females at the time of egg laying but did not affect offspring sex or egg mass. In addition, offspring sex was not predicted by the length of maternal telomere restriction fragments (TRFs), an index of age and possibly of reproductive experience. Broad confidence intervals on effect size suggest that undetected effects of maternal condition on offspring sex ratio could easily exist, but confidence intervals were narrower on the non‐significant effects of SST and TRF length on offspring sex ratio. The cause of different seasonal patterns of hatching sex ratio and different SST effects in 1998 and 2003 is unclear.     

Low serum vitamin A mothers breastfeed daughters more often than sons in drought-ridden northern Kenya: a test of the Trivers–Willard hypothesis

The Trivers–Willard hypothesis predicts that natural selection should favor unequal parental investment between daughters and sons based upon maternal condition and offspring reproductive potential. Specifically, it predicts that mothers in good condition should increase investment toward sons, while mothers in poor condition should favor daughters. Previous tests of the hypothesis in human populations overwhelmingly focused on economic resources as maternal condition indicators. We test the Trivers–Willard hypothesis using maternal nutrition—energy and vitamin A status representing macro- and micronutrition, respectively—as the indicator for maternal condition, with breastfeeding frequency recalls serving as the indicator for parental investment. Data from exclusively breastfeeding mothers (n=83) in drought-ridden Ariaal agropastoral villages of northern Kenya were used to test the hypothesis that mothers in poor condition will breastfeed daughters more frequently than sons. Poor condition was defined as having a body mass index <18.5 or serum retinol (vitamin A) concentration <1.05 µmol/l. A linear regression model was applied using breastfeeding frequency as the dependent variable and respective maternal condition, infant's sex, and the maternal condition–infant's sex interaction as the predictors, controlling for covariates. Results supported the hypothesis only in the vitamin A model which predicts that low-vitamin-A mothers breastfeed daughters significantly more frequently than sons (11 vs. 6 times/day), while vitamin-A-sufficient mothers breastfeed daughters and sons equivalently (9 times). These results indicate that maternal nutritional status, particularly micronutrient status, can contribute to the investigation of the evolutionary hypothesis of sex-biased parental investment.     

Parents’ genetic dissimilarity and offspring sex in a polygynous mammal

Offspring quality may benefit from genetic dissimilarity between parents. However, genetic dissimilarity may trade‐off with additive genetic benefits. We hypothesized that when sexual selection produces sex‐specific selective scenarios, the relative benefits of additive genetic vs. dissimilarity may differ for sons and daughters. Here we study a sample of 666 red deer (Cervus elaphus) microsatellite genotypes, including males, females and their foetuses, from 20 wild populations in Spain (the main analyses are based on 241 different foetuses and 190 mother‐foetus pairs). We found that parental lineages were more dissimilar in daughters than in sons. On average, every mother was less related to her mate than to the sample of fathers in the population when producing daughters not sons. Male foetuses conceived early in the rutting season were much more inbred than any other foetuses. These differences maintained through gestation length, ruling out intrauterine mortality as a cause for the results, and indicating that the potential mechanism producing the association between parents’ dissimilarity and offspring sex should operate close to mating or conception time. Our findings highlight the relevance of considering the sex of offspring when studying genetic similarity between parents.     

Relationships of vervet mothers with sons and daughters from one through three years of age

Social relationships between mothers and juvenile offspring were examined in captive, socially-living vervet monkeys (Cercopithecus aethiops sabaeus) to assess the effects of offspring age and sex, and the mother's dominance rank on behavioural interactions. The results indicate that both high-and low-ranking mothers approach and groom their daughters more than they approach and groom their sons. The frequency of both aggressive behaviour toward offspring and support of offspring in agonistic encounters with other group members is influenced by the mother's dominance rank, but not by offsprin sex. Compared to sons, daughters (particularly daughters of high-ranking females) approach and groom their mothers more often, and support their mothers more often in intra-group aggression. The results are discussed in terms of several predictions from parental investment theory and the concept of mutualism.     

SEX-RATIO MANIPULATION IN COLOR-BANDED POPULATIONS OF ZEBRA FINCHES

Significant correlations were found between attractiveness of leg-band color (determined by preference tests [Burley et al., 1982]) and sex ratio of offspring in two long-term breeding experiments involving zebra finches. In both experiments, birds with attractive band colors produced more same-sex offspring, while birds with unattractive band colors produced more opposite-sex offspring. The results of these experiments are consistent with those of a previous experiment (Burley, 1981). To explain the earlier results, I hypothesized that parents adjust their allocation to sons and daughters to produce offspring they “expect” to be most attractive. The purpose of such sex-ratio manipulation is to enhance fitness by the production of offspring with superior mate-getting opportunities. Two alternative hypotheses are presented here. One is that sex ratios change with parental age and/or experience. Evidence does not support this hypothesis. There were no temporal trends in sex ratio independent of band color. A second possibility is that sex ratios reflect differential parental ability to rear sons and daughters. This hypothesis cannot be conclusively tested on the basis of present evidence, but available evidence does not support it. Within color classes, weights of sons and daughters did not differ. Evidence indicates that parents effect secondary sex-ratio manipulation through the selective rejection of young, usually within six days of hatching. There is no evidence of manipulation prior to egg-laying. The costs associated with brood reduction probably set limits on the extent to which secondary manipulation can be profitably employed.     

Deferred independence and prolonged infantile behaviour in young varied tits, Parus varius, of an island population

In identical conditions under captivity, island fledglings of the varied tit, Parus varius, showed begging behaviour for about three times as long as did mainland fledglings. Moreover, the begging posture and call were exaggerated in island fledglings. The exaggerated begging behaviour and its long maintenance in island fledglings are considered to contribute to the extended duration of postfledging parental care which has been observed in the field. The prolongation of begging behaviour and parental care in island varied tits seems to have been evolved as a result of the low food availability which is expected from the smaller seasonal flush of food and the high population density of the birds.     

Sex ratio adjustments in common terns: influence of mate condition and maternal experience

Adaptive sex allocation has frequently been studied in sexually size dimorphic species, but far less is known about patterns of sex allocation in species without pronounced sexual size dimorphism. Parental optimal investment can be predicted under circumstances in which sons and daughters differ in costs and/or fitness returns. In common terns Sterna hirundo, previous studies suggest that sons are the more costly sex to produce and rear. We investigated whether hatching and fledging sex ratio and sex‐specific chick mortality correlated with the ecological environment (laying date, clutch size, hatching order and year quality) and parental traits (condition, arrival date, experience and breeding success), over seven consecutive years. Population‐wide sex ratios and sex‐specific mortality did not differ from parity, but clutch size, mass of the father, maternal breeding experience and to some extent year quality correlated with hatching sex ratio. The proportion of sons tended to increase in productive years and when the father was heavier, suggesting the possibility that females invest more in sons when the environmental and the partner conditions are good. The proportion of daughters increased with clutch size and maternal breeding experience, suggesting a decline in breeding performance or a resources balance solved by producing more of the cheaper sex. No clear patterns of sex‐specific mortality were found, neither global nor related to parental traits. Our results suggest lines for future studies on adaptive sex allocation in sexually nearly monomorphic species, where adjustment of sex ratio related to parental factors and differential allocation between the offspring may also occur.     

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

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