Better‐surviving barn swallow mothers produce more and better‐surviving sons

Sex allocation theory predicts that parents are selected to bias their progeny sex ratio (SR) toward the sex that will benefit the most from parental quality. Because parental quality may differentially affect survival of sons and daughters, a pivotal test of the adaptive value of SR adjustment is whether parents overproduce offspring of the sex that accrues larger fitness advantages from high parental quality. However, this crucial test of the long‐term fitness consequences of sex allocation decisions has seldom been performed. In this study of the barn swallow (Hirundo rustica), we showed a positive correlation between the proportion of sons and maternal annual survival. We then experimentally demonstrated that this association did not depend on the differential costs of rearing offspring of either sex. Finally, we showed that maternal lifespan positively predicted lifespan of sons but not of daughters. Because in barn swallows lifespan is a strong determinant of lifetime reproductive success, the results suggest that mothers overproduce offspring of the sex that benefits the most from maternal quality. Hence, irrespective of mechanisms causing the SR bias and mother–son covariation in lifespan, we provide strong evidence that sex allocation decisions of mothers can highly impact on their lifetime fitness.     

Reproducing lizards modify sex allocation in response to operational sex ratios

Sex-allocation theory suggests that selection may favour maternal skewing of offspring sex ratios if the fitness return from producing a son differs from that for producing a daughter. The operational sex ratio (OSR) may provide information about this potential fitness differential. Previous studies have reached conflicting conclusions about whether or not OSR influences sex allocation in viviparous lizards. Our experimental trials with oviparous lizards (Amphibolurus muricatus) showed that OSR influenced offspring sex ratios, but in a direction opposite to that predicted by theory: females kept in male-biased enclosures overproduced sons rather than daughters (i.e. overproduced the more abundant sex). This response may enhance fitness if local OSRs predict survival probabilities of offspring of each sex, rather than the intensity of sexual competition.     

Paternal reproductive success drives sex allocation in a wild mammal

Parents should bias sex allocation toward offspring of the sex most likely to provide higher fitness returns. Trivers and Willard proposed that for polygynous mammals, females should adjust sex‐ratio at conception or bias allocation of resources toward the most profitable sex, according to their own body condition. However, the possibility that mammalian fathers may influence sex allocation has seldom been considered. Here, we show that the probability of having a son increased from 0.31 to 0.60 with sire reproductive success in wild bighorn sheep (Ovis canadensis). Furthermore, our results suggest that females fertilized by relatively unsuccessful sires allocated more energy during lactation to daughters than to sons, while the opposite occurred for females fertilized by successful sires. The pattern of sex‐biased offspring production appears adaptive because paternal reproductive success reduced the fitness of daughters and increased the average annual weaning success of sons, independently of maternal allocation to the offspring. Our results illustrate that sex allocation can be driven by paternal phenotype, with profound influences on the strength of sexual selection and on conflicts of interest between parents.     

You are what your mother eats: evidence for maternal preconception diet influencing foetal sex in humans

Facultative adjustment of sex ratios by mothers occurs in some animals, and has been linked to resource availability. In mammals, the search for consistent patterns is complicated by variations in mating systems, social hierarchies and litter sizes. Humans have low fecundity, high maternal investment and a potentially high differential between the numbers of offspring produced by sons and daughters: these conditions should favour the evolution of facultative sex ratio variation. Yet little is known of natural mechanisms of sex allocation in humans. Here, using data from 740 British women who were unaware of their foetus's gender, we show that foetal sex is associated with maternal diet at conception. Fifty six per cent of women in the highest third of preconceptional energy intake bore boys, compared with 45% in the lowest third. Intakes during pregnancy were not associated with sex, suggesting that the foetus does not manipulate maternal diet. Our results support hypotheses predicting investment in costly male offspring when resources are plentiful. Dietary changes may therefore explain the falling proportion of male births in industrialized countries. The results are relevant to the current debate about the artificial selection of offspring sex in fertility treatment and commercial 'gender clinics'.     

The role of fathers in mammalian sex allocation

Parents should bias resource allocation towards the sex most likely to provide higher fitness returns by adjusting the birth sex ratio and/or through differential care of sons and daughters. Sex allocation research in mammals to date has been focused almost exclusively on maternal traits, but fathers may also play an important role. Future studies should investigate the influence of paternal quality on the fitness of sons and daughters, and possible conflicts of interest between mothers and fathers. There is also a crucial need for more studies examining whether relative levels of maternal care in sons and daughters depend on paternal quality.     

Of mammals and milk: how maternal stress affects nursing offspring

1. A large body of research shows that maternal stress during an offspring’s early life can impact its phenotype in both the short and long term. In the Vertebrata, most research has been focused on maternal stress during the prenatal period. However, the postnatal period is particularly important in mammals because maternal milk provides a conduit by which maternal hormones secreted in response to stressors (glucocorticoids, GCs) can reach offspring. Moreover, lactation outlasts gestation in many species.
2. Though GCs were first detected in milk over 40 years ago, few studies have explored how they affect nursing offspring, and no reviews have been written on how maternal stress affects nursing offspring in the natural world.
3. We discuss the evolution of milk and highlight its importance in each of the three mammalian lineages: monotremes (subclass Monotremata), marsupials (infraclass Marsupialia), and eutherians (infraclass Placentalia). Most research on the effects of milk GCs on offspring has been focused on eutherians, but monotremes and marsupials rely on their mothers’ milk for a proportionally longer period of time, and so research on these taxa may yield more insight.
4. We show that GCs are important for milk production, both during an individual nursing bout and over the entire lactation period, and review evidence of GCs moving from maternal blood to milk, and eventually to nursing offspring. We examine evidence from rodents and primates of associations between GC levels in lactating females (either blood or milk) and offspring behaviour and growth rates. We discuss ways that maternal stress may impact these offspring phenotypes outside of milk GCs, such as changes to: (1) milk output, (2) other milk constituents (e.g. macronutrients, growth factors, cytokines), and (3) maternal care behaviour.
5. Critical to understanding the fitness impacts of elevated maternal GC levels during lactation is to place this within the context of the natural environment. Species-specific traits and natural histories will help us to understand why such maternal stress produces different offspring phenotypes that equip them to cope with and succeed in the environment they are about to enter.

     

Importance of breeding season and maternal investment in studies of sex-ratio adjustment: a case study using tree swallows

The control of primary sex-ratio by vertebrates has become a major focus in biology in recent years. Evolutionary theory predicts that a differential effect of maternal characteristics on the fitness of sons and daughters is an important route, whereby selection is expected to favour a bias towards the production of one sex. However, despite experimental evidence for adaptive brood sex-ratio manipulation, support for this prediction remains a major challenge in vertebrates where inconsistencies between correlative studies are frequently reported. Here, we used a large dataset (2215 nestlings over 3 years) from a wild population of tree swallows (Tachycineta bicolor) and show that variations in breeding conditions affect female sex allocation in this species. Our results also suggest that such variation in sex allocation, owing to breeding season heterogeneity, modifies the relationships between maternal characteristics and maternal investment. Indeed, we detect a positive effect of maternal age on brood sex-ratio when age also affects offspring condition (in a low-quality breeding season). Our results indicate that including measures of both breeding season quality and maternal investment will help to better understand sex allocation patterns.     

Effect of paternal age on the birth sex ratio in captive populations of aye‐aye (Daubentonia madagascariensis (Gmelin))

For the management of captive populations of zoo animals, it is important to elucidate factors that affect the offspring birth sex ratio. On the basis of the sex allocation theory, the Trivers–Willard and mate attractive/quality hypotheses predict that maternal and paternal conditions affect offspring birth sex ratios. We examined these predictions for the birth sex ratio of aye‐aye Daubentonia madagascariensis (Gmelin) by analyzing the pedigree information in the International Studbook. We found that the birth sex ratio of the aye‐aye was affected by the paternal age, but not maternal age and other environmental factors (birth year, season, and institution). The younger the sire, the more the offspring sex ratio was biased toward males. These results are useful for the effective population management of captive aye‐aye and illustrated the usefulness of the sex allocation theory in the sex ratio management of zoo animals.     

Maternal condition and facultative sex ratios in populations with overlapping generations

Facultative investment in offspring sex is related to maternal condition in many organisms. In mammals, empirical support for condition-dependent sex allocation is equivocal, and there is some doubt as to theoretical expectations. Much theory has been developed to make predictions for condition-dependent sex ratios in populations with discrete generations. However, the extension of these predictions to populations with overlapping generations (OLGs; e.g., mammals) has been limited, leaving doubt as to the specific prediction for maternal-condition-dependent sex ratios in mammals. We develop a population genetics model that incorporates maternal effects on multiple offspring fitness components in a population with OLGs. Using a rare-gene and evolutionarily stable strategy approach, we demonstrate that sex ratio predictions of this model are identical to those for equivalent discrete generations models. We show that the predicted sex ratios depend on the sex-specific ratio of R(o) (offspring lifetime fitness) for offspring of good and poor mothers. This offspring lifetime fitness rule indicates that empirical research on conditional sex ratios should consider all three components of offspring R(o) (juvenile survival, adult life span, and fertility).     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.     

Maternal Testosterone and Offspring Sex-Ratio in Birds and Mammals: A Meta-Analysis

Sex allocation theory predicts that parents should bias offspring sex to maximize their fitness in a given context. Quantifying the fitness benefits of offspring sex-ratio biases would be facilitated by a better knowledge of their underlying mechanism(s) and associated costs. The hypothesis that steroid hormones are involved in sex determination has gained in popularity recently. Being influenced by external stimuli and involved in a range of physiological processes, they could be a ubiquitous mediator of environmental conditions influencing sex-ratio with low fitness costs. Previous studies indicated that higher maternal testosterone levels led to the overproduction of sons around conception in both birds and mammals. We conducted a systematic review (including meta-analysis) of these studies and, as predicted, we found a weak positive and significant overall effect of maternal testosterone on the proportion of sons. Neither taxa, nor the type of study (experimental/observational), or the timing of timing testosterone manipulation/measure were significant predictors of offspring sex-ratio, which may be explained by low statistical power in addition to low variability between effect sizes. Our meta-analysis provides evidence for a general positive influence of maternal testosterone around conception on the proportion of sons across birds and mammals, although less confidently so for the latter. It begs for more large-scale experimental studies, especially on mammals, and ideally in the wild. It may also have some important consequences for the poultry industry.     

Condition and reproductive investment in the western mosquitofish (Gambusia affinis): little evidence for condition‐dependent sex‐biased investment

In sexually reproducing species, resources may theoretically be distributed with bias to the production of male or female offspring in response to the condition of the mother, commonly recognized as sex allocation. Using a recently characterized sex‐specific molecular marker, we tested for maternal sex allocation (i.e. maternal primary sex ratio bias and sex‐specific offspring investment) in captive laboratory‐bred western mosquitofish (Gambusia affinis) at early stages of offspring development. We found no statistical evidence to support sex allocation in G. affinis, based on maternal condition. In addition, we found little evidence for correlations between maternal condition and investment in the condition (mass) of individual offspring (of one sex or the other), although we did find that larger mothers tended to have higher fecundity.     

Disentangling sex allocation in a viviparous reptile with temperature‐dependent sex determination: a multifactorial approach

Females are predicted to alter sex allocation when ecological, physiological and behavioural variables have different consequences on the fitness of male and female offspring. Traditionally, tests of sex allocation have examined single causative factors, often ignoring possible interactions between multiple factors. Here, we used a multifactorial approach to examine sex allocation in the viviparous skink, Niveoscincus ocellatus. We integrated a 16‐year observational field study with a manipulative laboratory experiment to explore whether the effects of the maternal thermal environment interact with the resources available to females for reproduction to affect sex allocation decisions. We found strong effects of temperature on sex allocation in the field, with females born in warm conditions and males in cold conditions; however, this was not replicated in the laboratory. In contrast, we found no effect of female resource availability on sex allocation, either independently, or in interaction with temperature. These results corresponded with an overall lack of an effect of resource availability on any of the life history traits that we predicted would mediate the benefits of differential sex allocation in this system, suggesting that selection for sex allocation in response to resource availability may be relatively weak. Combined, these results suggest that temperature may be the predominant factor driving sex allocation in this system.     

Maternal influences on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination

Maternal and environmental factors are important sources of phenotypic variation because both factors influence offspring traits in ways that impact offspring and maternal fitness. The present study explored the effects of maternal factors (maternal body size, egg size, yolk‐steroid allocation, and oviposition‐site choice) and seasonally‐variable environmental factors on offspring phenotypes and sex ratios in a multi‐clutching lizard with environmental sex determination (Amphibolurus muricatus). Maternal identity had strong effects on offspring morphology, but the nature of maternal effects differed among successive clutches produced by females throughout the reproductive season (i.e. maternal identity by environment interactions). The among‐female and among‐clutch variation in offspring traits (including sex ratios) was not mediated through maternal body size, egg size, or variation in yolk steroid hormones. This lack of nongenetic maternal effects suggests that phenotypic variation may be generated by gene by environment interactions. These results demonstrate a significant genetic component to variation in offspring phenotypes, including sex ratios, even in species with environmental sex determination. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 256–266.     

Maternal condition and offspring sex ratio in polygynous ungulates: a case study of bighorn sheep

The Trivers and Willard model (TWM) predicts that for sexuallydimorphic polygynous mammals, mothers able to provide a highlevel of care should bias offspring sex ratio in favor of sons.Contradictory results of empirical studies, however, suggestthat selective pressures for adaptive offspring sex ratio varywith species and environmental conditions. We report the resultsof a 29-year study of marked bighorn sheep (Ovis canadensis)in a population that underwent wide changes in density and wheremost females were weighed each year. Lamb sex ratio was independentof absolute ewe mass and yearly deviations from individual orpopulation average mass, but there was a nonsignificant trendtowards fewer males being born at high population density. Bighornsheep satisfy all the assumptions of the TWM but not its prediction:lamb sex ratio is independent of maternal ability to providecare. Recent hypotheses to explain the lack of relationshipbetween maternal condition and offspring sex in ungulates areunlikely to apply to bighorn sheep. We suggest that the TWMmay only apply when social rank strongly affects the abilityto provide maternal care. Those circumstances are likely tooccur for only a few species and within a narrow range of environmentalconditions.     

PATERNAL CONDITION DRIVES PROGENY SEX‐RATIO BIAS IN A LIZARD THAT LACKS PARENTAL CARE

Sex‐allocation theory predicts that females in good condition should preferentially produce offspring of the sex that benefits the most from an increase in maternal investment. However, it is generally assumed that the condition of the sire has little effect on progeny sex ratio, particularly in species that lack parental care. We used a controlled breeding experiment and molecular paternity analyses to examine the effects of both maternal and paternal condition on progeny sex ratio and progeny fitness in the brown anole (Anolis sagrei), a polygynous lizard that lacks parental care. Contrary to the predictions of sex‐allocation theory, we found no relationship between maternal condition and progeny sex ratio. By contrast, progeny sex ratio shifted dramatically from female‐biased to male‐biased as paternal condition increased. This pattern was driven entirely by an increase in the production of sons as paternal condition improved. Despite strong natural selection favoring large size and high condition in both sons and daughters, we found no evidence that progeny survival was related to paternal condition. Our results emphasize the importance of considering the paternal phenotype in studies of sex allocation and highlight the need for further research into the pathways that link paternal condition to progeny fitness.     

Sex-ratio bias in an aphid parasitoid-hyperparasitoid association: a test of two hypotheses

Abstract.

• 1 We tested the hypothesis that biased sex ratios in the aphidiid parasitoid, Aphidius ervi, are the result of sex-specific mortality of immatures due to hyperparasitism. The solitary hyperparasitoid, Dendrocerus carpenteri, deposits its eggs on the prepupa or pupa of the primary parasitoid after its pea-aphid host is mummified.
• 2 In dichotomous choice tests, females of D.carpenteri accepted immatures of both sexes of A.ervi with equal frequency. Independent of the sex of the primary parasitoid, the probability of a mummified pea aphid being hyperparasitized did not differ between large (adult at the time of death) and small (fourth nymphal instar) mummies.
• 3 As predicted by‘host quality’models of offspring sex allocation, D.carpenteri produced a higher proportion of female than male offspring in large mummies. These laboratory results were supported by field data.
• 4 Because hyperparasitism by D.carpenteri is random with regard to host sex, it should have no influence on optimal sex allocation by the primary parasitoid.

     

Offspring are lighter at birth and smaller in adulthood when born after a brother versus a sister in humans

In mammals, including humans, it is more costly to produce sons than it is to produce daughters, with maternal survival and subsequent reproductive success diminished more by producing male over female offspring. It is therefore predicted that offspring who are produced by mothers who have previously produced sons versus daughters will be compromised by the relatively high cost their mother incurred in the previous reproductive episode. Such effects are potentially important because characters that determine offspring survival and fecundity ultimately contribute to maternal fitness. Using questionnaire-based data from a contemporary human population, I show that birthweight (irrespective of their sex) is lower in individuals born after an elder brother than in those born after an elder sister. In addition, I show that both men and women who were born after a male versus a female sibling have reduced adulthood height, a known correlate of reproductive success in both sexes. The results suggest that producing sons may have a negative effect on the fitness of subsequent offspring, which has implications for calculations of maternal fitness and for optimal sex allocation.     

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

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

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.