Experimental alteration of litter sex ratios in a mammal

Adaptive theory predicts that mothers would be advantaged by adjusting the sex ratio of their offspring in relation to their offspring's future reproductive success. Studies investigating sex ratio variation in mammals, including humans, have obtained notoriously inconsistent results, except when maternal condition is measured around conception. Several mechanisms for sex ratio adjustment have been proposed. Here, we test the hypothesis that glucose concentrations around conception influence sex ratios. The change in glucose levels resulted in a change in sex ratios, with more daughters being born to females with experimentally lowered glucose, and with the change in glucose levels being more predictive than the glucose levels per se. We provide evidence for a mechanism, which, in tandem with other mechanisms, could explain observed sex ratio variation in mammals.     

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'.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns

Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.     

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.     

Relative costs of offspring sex and offspring survival in a polygynous mammal

Costs of reproduction are expected to be ubiquitous in wild animal populations and understanding the drivers of variation in these costs is an important aspect of life-history evolution theory. We use a 43 year dataset from a wild population of red deer to examine the relative importance of two factors that influence the costs of reproduction to mothers, and to test whether these costs vary with changing ecological conditions. Like previous studies, our analyses indicate fitness costs of lactation: mothers whose calves survived the summer subsequently showed lower survival and fecundity than those whose calves died soon after birth, accounting for 5% and 14% of the variation in mothers'' survival and fecundity, respectively. The production of a male calf depressed maternal survival and fecundity more than production of a female, but accounted for less than 1% of the variation in either fitness component. There was no evidence for any change in the effect of calf survival or sex with increasing population density.     

Females allocate differentially to offspring size and number in response to male effects on female and offspring fitness

Female investment in offspring size and number has been observed to vary with the phenotype of their mate across diverse taxa. Recent theory motivated by these intriguing empirical patterns predicted both positive (differential allocation) and negative (reproductive compensation) effects of mating with a preferred male on female investment. These predictions, however, focused on total reproductive effort and did not distinguish between a response in offspring size and clutch size. Here, we model how specific paternal effects on fitness affect maternal allocation to offspring size and number. The specific mechanism by which males affect the fitness of females or their offspring determines whether and how females allocated differentially. Offspring size is predicted to increase when males benefit offspring survival, but decrease when males increase offspring growth rate. Clutch size is predicted to increase when males contribute to female resources (e.g. with a nuptial gift) and when males increase offspring growth rate. The predicted direction and magnitude of female responses vary with female age, but only when per-offspring paternal benefits decline with clutch size. We conclude that considering specific paternal effects on fitness in the context of maternal life-history trade-offs can help explain mixed empirical patterns of differential allocation and reproductive compensation.     

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.     

The evolutionary ecology of early weaning in Kilimanjaro,Tanzania

Public health recommendations promote prolonged breastfeeding of all children; however, parental investment (PI) theory predicts that breastfeeding will be allocated among a mothers'' offspring to maximize her reproductive success. We evaluated PI in terms of risk for weaning before age two among 283 children in Kilimanjaro, Tanzania. Results demonstrate: (i) a Trivers–Willard effect—high socioeconomic status (SES) females and low SES males were more likely to be weaned early; (ii) later-born children were less likely to be weaned early; (iii) higher birthweight children were less likely to be weaned early, and (iv) no effect of cattle (a source of supplementary milk) ownership. These associations were largely independent and remained significant in models controlling for potential confounders; however, the inverse association between early weaning and birth order lost significance in the model containing birthweight. These patterns were observed despite public health recommendations encouraging breastfeeding for at least two years.     

Maternal body condition influences magnitude of anti-predator response in offspring

Organisms exhibit plasticity in response to their environment, but there is large variation even within populations in the expression and magnitude of response. Maternal influence alters offspring survival through size advantages in growth and development. However, the relationship between maternal influence and variation in plasticity in response to predation risk is unknown. We hypothesized that variation in the magnitude of plastic responses between families is at least partly due to maternal provisioning and examined the relationship between maternal condition, egg provisioning and magnitude of plastic response to perceived predation risk (by dragonfly larvae: Aeshna spp.) in northern leopard frogs (Lithobates pipiens). Females in better body condition tended to lay more (clutch size) larger (egg diameter) eggs. Tadpoles responded to predation risk by increasing relative tail depth (morphology) and decreasing activity (behaviour). We found a positive relationship between morphological effect size and maternal condition, but no relationship between behavioural effect size and maternal condition. These novel findings suggest that limitations imposed by maternal condition can constrain phenotypic variation, ultimately influencing the capacity of populations to respond to environmental change.     

Extreme sex ratio variation in relation to change in condition around conception

Adaptive theory predicts that mothers would be advantaged by adjusting the sex ratio of their offspring in relation to their offspring's future reproductive success. Studies investigating sex ratio variation in mammals have produced notoriously inconsistent results, although recent studies suggest more consistency if sex ratio variation is related to maternal condition at conception, potentially mediated by changes in circulating glucose level. Consequently, we hypothesized that change in condition might better predict sex ratio variation than condition per se. Here, we investigate sex ratio variation in feral horses (Equus caballus), where sex ratio variation was previously shown to be related to maternal condition at conception. We used condition measures before and after conception to measure the change in condition around conception in individual mothers. The relationship with sex ratio was substantially more extreme than previously reported: 3% of females losing condition gave birth to a son, whereas 80% of those females that were gaining condition gave birth to a son. Change in condition is more predictive of sex ratio than actual condition, supporting previous studies, and shows the most extreme variation in mammals ever reported.     

Guppies control offspring size at birth in response to differences in population sex ratio

Females that invest adaptively in their offspring are predicted to channel more resources to the sex that will be at an advantage in the prevailing environmental conditions. Here, we report, for the first time, that female Trinidadian guppy, Poecilia reticulata, respond in reproductively distinct ways when faced with differences in operational sex ratio. We show that females assigned to a female‐biased sex ratio produce larger male offspring than females in an environment in which males predominate. Given the link between size at birth and fitness, and the marked reproductive skew in this species, larger male offspring are expected to have reproductive advantages in guppy populations with an excess of females. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 414–419.     

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.     

Frequency‐dependent two‐sex models: a new approach to sex ratio evolution with multiple maternal conditions

Mothers that experience different individual or environmental conditions may produce different proportions of male to female offspring. The Trivers‐Willard hypothesis, for instance, suggests that mothers with different qualities (size, health, etc.) will use different sex ratios if maternal quality differentially affects sex‐specific reproductive success. Condition‐dependent, or facultative, sex ratio strategies like these allow multiple sex ratios to coexist within a population. They also create complex population structure due to the presence of multiple maternal conditions. As a result, modeling facultative sex ratio evolution requires not only sex ratio strategies with multiple components, but also two‐sex population models with explicit stage structure. To this end, we combine nonlinear, frequency‐dependent matrix models and multidimensional adaptive dynamics to create a new framework for studying sex ratio evolution. We illustrate the applications of this framework with two case studies where the sex ratios depend one of two possible maternal conditions (age or quality). In these cases, we identify evolutionarily singular sex ratio strategies, find instances where one maternal condition produces exclusively male or female offspring, and show that sex ratio biases depend on the relative reproductive value ratios for each sex.     

Big mothers invest more in daughters – reversed sex allocation in a weakly polygynous mammal

How mothers allocate resources to offspring is central to understanding life history strategies. High quality mothers are predicted to favour investment in sons over daughters when to do so increases inclusive fitness. This is the case in ungulates with polygynous mating systems, where reproductive success is more variable among males than females, but information is scarce on sex allocation in less polygynous species. Here, for the weakly dimorphic roe deer, we show that as maternal capacity to invest increases, mothers increase allocation to daughters more than to sons, so that relative allocation to daughters increases markedly with increasing maternal quality. This cannot be explained by a between sex difference in growth priority, hence we conclude that this is evidence for active maternal discrimination. Further, we demonstrate that condition differences between offspring persist to adulthood. For high quality mothers of weakly polygynous species, daughters may be more valuable than sons.     

Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits

The study of primary sex ratio adjustment in birds is notoriousfor inconsistency of results among studies. To develop our understandingof avian sex ratio variation, experiments that test a prioripredictions and the replication of previous studies are essential.We tested if female blue tits Parus caeruleus adjust the sexratio of their offspring to the sexual attractiveness of theirmates, as was suggested by a previous benchmark study on thesame species. In 2 years, we reduced the ultraviolet (UV) reflectanceof the crown feathers of males in the period before egg layingto decrease their attractiveness. In contrast to the simpleprediction from sex allocation theory, we found that the overallproportion of male offspring did not differ between broods ofUV-reduced and control-treated males. However, in 1 year, theUV treatment influenced offspring sex ratio depending on thenatural crown UV reflectance of males before the treatment.The last result confirms the pattern found in the previous bluetit study, which suggests that these complex patterns of primarysex ratio variation are repeatable in this bird species, warrantingfurther research into the adaptive value of blue tit sex ratioadjustment to male UV coloration.     

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.     

Contrasting selection pressure on body and weapon size in a polygynous megaherbivore

Sexual size dimorphism (SSD) is a common morphological trait in ungulates, with polygyny considered the leading driver of larger male body mass and weapon size. However, not all polygynous species exhibit SSD, while molecular evidence has revealed a more complex relationship between paternity and mating system than originally predicted. SSD is, therefore, likely to be shaped by a range of social, ecological and physiological factors. We present the first definitive analysis of SSD in the common hippopotamus (Hippopotamus amphibius) using a unique morphological dataset collected from 2994 aged individuals. The results confirm that hippos exhibit SSD, but the mean body mass differed by only 5% between the sexes, which is rather limited compared with many other polygynous ungulates. However, jaw and canine mass are significantly greater in males than females (44% and 81% heavier, respectively), highlighting the considerable selection pressure for acquiring larger weapons. A predominantly aquatic lifestyle coupled with the physiological limitations of their foregut fermenting morphology likely restricts body size differences between the sexes. Indeed, hippos appear to be a rare example among ungulates whereby sexual selection favours increased weapon size over body mass, underlining the important role that species-specific ecology and physiology have in shaping SSD.     

Brood sex ratio varies with diet composition in a generalist raptor

While sex allocation has been investigated productively at both population and family levels, as yet no general theory has been developed that is capable of linking processes at these two ecological scales, and very few empirical studies have examined cross‐scale patterns. In Finnish northern goshawks (Accipiter gentilis), nestling sex ratio of local subpopulations is related to the spatial and temporal variation in the abundance of their principal avian prey, woodland grouse. Using data from an urban breeding population in Hamburg, Germany, I investigated: (1) whether brood sex ratio of goshawks varies with diet composition at the family level; (2) whether such variation could reflect adaptive adjustment; and (3) how family‐level allocation can drive population‐level patterns, such as those observed in Finland. Feral pigeons (Columba livia) were the most important prey species, with a pooled contribution to total diet of 36%. Brood sex ratio varied significantly with the proportion of pigeons in the breeding‐season diet of pairs (increasing male bias). However, there was no evidence for sex‐differential effects of diet composition, so it remains unclear whether the observed sex‐ratio variation was an adaptive response. As all study pairs inhabited an (urban) environment where pigeons were unusually abundant, family‐level sex‐ratio adjustment caused a marked male bias in offspring sex ratio at the population level (male‐biased nestling sex ratio in four of five years; pooled data: 60% males). This suggests that the large‐scale variation observed in Finnish goshawk populations mirrors sex‐ratio adjustment shown by individual families in response to small‐scale environmental conditions. Apart from linking patterns empirically across ecological scales, this study is, to my knowledge, the first to demonstrate that family‐level brood sex ratio varies with realized resource use (diet composition) in a raptor species. Previous studies either failed to find significant associations or, more commonly, violated theoretical assumptions by measuring environmental prey abundance (often integrated over large areas) rather than realized prey use of individual breeding pairs. I conducted a meta‐analysis of offspring sex‐ratio data from 17 goshawk populations across Europe to put my results into perspective. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 937–951.     

Change in offspring sex ratio over a very short season in Lincoln's Sparrows: the potential role of bill development

ABSTRACT The sex ratios of offspring are targets of natural selection that can affect parental energy expenditure and fitness, adult sex ratios, and population dynamics. Parents may manipulate offspring sex ratios based on sex differences in their offsprings' potential for reproductive success. In Lincoln's Sparrows (Melospiza lincolnii), male bill shape is associated with the quality of songs, and song quality predicts female preferences in a reproductive context. Males and females that hatch later relative to brood mates or later in the breeding season tend to develop bill shapes that are, for males, associated with low‐quality song. Because females do not sing and do not experience this selection pressure, we predicted that the sex of offspring produced late relative to their brood mates or relative to the season should be biased toward females. Using a molecular technique to sex nestlings, we found no effects of hatching order or any interaction between date of clutch initiation (season) and hatching order on offspring sex. However, we found a seasonal decline in the proportion of male offspring, from approximately 0.8 at the beginning to 0.4 at the end of a clutch initiation season only 19 d in duration. To our knowledge, this is the shortest period over which the offspring sex ratio has been shown to change in a bird population. Moreover, these findings are consistent with the hypothesis that sex differences in the potential attractiveness of offspring ultimately influence offspring sex ratios.