Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism

Evolutionary theory predicts that mothers of different condition should adjust the birth sex ratio of their offspring in relation to future reproductive benefits. Published studies addressing variation in mammalian sex ratios have produced surprisingly contradictory results. Explaining the source of such variation has been a challenge for sex-ratio theory, not least because no mechanism for sex-ratio adjustment is known. I conducted a meta-analysis of previous mammalian sex-ratio studies to determine if there are any overall patterns in sex-ratio variation. The contradictory nature of previous results was confirmed. However, studies that investigated indices of condition around conception show almost unanimous support for the prediction that mothers in good condition bias their litters towards sons. Recent research on the role of glucose in reproductive functioning have shown that excess glucose favours the development of male blastocysts, providing a potential mechanism for sex-ratio variation in relation to maternal condition around conception. Furthermore, many of the conflicting results from studies on sex-ratio adjustment would be explained if glucose levels in utero during early cell division contributed to the determination of offspring sex ratios.     

Timing of foetal growth spurts can explain sex ratio variation in polygynous mammals

The prediction from sex ratio theory that natural selection on sexually dimorphic mammals should favour an excess of male offspring only when mothers are in good condition, has been tested extensively but with little consistency in results. Although recent studies have shown that environmental variations may cause some of the discrepancy, there have also been reports of contrasting sex ratios under similar environmental settings. Here it is suggested that variation in timing of environmental stress and sex-specific differences in foetal growth pattern in relation to maternal condition, may explain such seeming contradictions in sex ratio variation of polygynous mammals.     

Sex-biased maternal investment in voles: importance of environmental conditions

Adaptive bias in sex allocation is traditionally proposed to be related to the condition of mothers as well as to the unequal fitness values of produced sexes. A positive relationship between mother condition and investment into male offspring is often predicted. This relationship was also recently found to depend on environmental conditions. We studied these causalities experimentally using a design where winter food supply was manipulated in eight outdoor-enclosed populations of field voles Microtus agrestis. At the beginning of the breeding season in spring, food-supplemented mothers seemed to be in a similar condition, measured as body mass, head width, body condition index and parasite load (blood parasite Trypanosoma), to non-supplemented mothers. Food supplements affected neither the litter size, the reproductive effort of mothers, nor the litter sex ratios at birth. However, food supplementation significantly increased the birth size of male offspring and improved their condition, as indicated by reduced parasite loads (intestinal Eimeria). Interestingly, mothers in good body condition produced larger male offspring only when environmental conditions were improved by food supplements. Although the adaptiveness of variation in mammalian sex ratios is still questionable, our study indicates that mothers in good condition bias their investment towards male offspring, but only when environmental conditions are favourable.     

Egg sex ratio and paternal traits: using within-individual comparisons

Empirical studies of sex ratios in birds have been limited dueto difficulties in determining offspring sex. Since molecularsexing techniques removed this constraint, the last 5 yearshas seen a great increase in studies of clutch sex ratio manipulationby female birds. Typically these studies investigate variationin clutch sex ratios across individuals in relation to environmentalcharacteristics or parental traits, and often they find no relationships. In this study we also found that clutch sex ratiosdid not vary in relation to a number of biological and environmentalfactors for 238 great tit Parus major nests. However, interestingsex ratio biases were revealed when variation in clutch sexratios was analyzed within individual females breeding in successiveyears. There was a significant positive relationship betweenthe change in sex ratio of a female's clutch from one yearto the next and the relative body condition of her partner.Females mating with males of higher body condition in yearx + 1 produced relatively male-biased sex ratios, and the oppositewas true for females mated with lower condition males. Within-individualanalysis also allowed investigations of sex ratio in relationto partner change. There was no change in sex ratios of femalespairing with the same male; however, females pairing with anew male produced clutches significantly more female biased. Comparisons of clutch sex ratios within individuals may be apowerful method for detecting sex ratio variation, and perhapsfemale birds may indeed manipulate egg sex but require personalcontextual experience for such decisions.     

Influence of resource level on maternal investment in a leaf-cutter bee (Hymenoptera: Megachilidae)

Fisher's (1930) prediction of equal investment for each sexin a panmictic population is influenced by a number of ecologicalfactors, among which resource availability plays a major role,particularly when the population exists under changing resource availability.Rosenheim et al. proposed a multifaceted parental investment modelbased on the underlying assumption that individual females determine theirsex investment according to resource availability and oocyte availabilityto maximize reproductive success. The model predicts that greater availabilityof resources used for provisions will lead to (1) an increasein the proportion of females produced (when the female is thelarger sex) and (2) an increase in the amount of provisionsper offspring and thus an increase in offspring size. I testedthese predictions by a controlled experiment using a leaf-cutterbee, Megachile apicalis. I presented two levels of food resourcesto the nesting females, which were allowed to forage and nestin cages. The experimental results supported these parentalinvestment model's predictions.     

Offspring sex ratios in relation to mutual ornamentation and extra-pair paternity in the Black Swan Cygnus atratus

In sexually dichromatic birds, females may adaptively adjust the sex ratio of their offspring prior to hatching in relation to male ornamentation, for example, by producing more sons when paired to a highly attractive partner. However, to our knowledge no studies have investigated offspring sex ratio modification in species in which both sexes are ornamented, and it is unknown whether such a process would be adaptive. Here we examine variation in offspring sex ratio in the mutually ornamented Black Swan Cygnus atratus . Brood sex ratio was not related to the degree of ornament elaboration in either parent, or to extra-pair paternity. We suggest that parental attractiveness may not be inherited in a sex-linked manner, or may be largely non-heritable. Thus, females may not benefit from biasing the sex ratio of their offspring in relation to parental attractiveness.     

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.     

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.     

Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum

The local-resource-competition hypothesis predicts that where philopatric offspring compete for resources with their mothers, offspring sex ratios will be biased in favour of the dispersing sex. This should produce variation in sex ratios between populations in relation to differences in the availability of resources for philopatric offspring. However, previous tests of local resource competition in mammals have used indirect measures of resource availability and have focused on sex-ratio variation between species or individuals rather than between local populations. Here, we show that the availability of den sites predicts the offspring sex ratio in populations of the common brushtail possum. Female possums defend access to dens, and daughters, but not sons, occupy dens within their mother's range. However, the abundances of possums in our study areas were determined principally by food availability. Consequently, in food-rich areas with a high population density, the per-capita availability of dens was low, and the cost of having a daughter should have been high. This cost was positively correlated with male bias in the sex ratio at birth. Low per capita availability of dens was correlated with male bias in the sex ratio at birth.     

Does breeding population trajectory and age of nesting females influence disparate nestling sex ratios in two populations of Cooper's hawks?

Offspring sex ratios at the termination of parental care should theoretically be skewed toward the less expensive sex, which in most avian species would be females, the smaller gender. Among birds, however, raptors offer an unusual dynamic because they exhibit reversed size dimorphism with females being larger than males. And thus theory would predict a preponderance of male offspring. Results for raptors and birds in general have been varied although population‐level estimates of sex ratios in avian offspring are generally at unity. Adaptive adjustment of sex ratios in avian offspring is difficult to predict perhaps in part due to a lack of life‐history details and short‐term investigations that cannot account for precision or repeatability of sex ratios across time. We conducted a novel comparative study of sex ratios in nestling Cooper's hawks (Accipiter cooperii) in two study populations across breeding generations during 11 years in Wisconsin, 2001–2011. One breeding population recently colonized metropolitan Milwaukee and exhibited rapidly increasing population growth, while the ex‐Milwaukee breeding population was stable. Following life‐history trade‐off theory and our prediction regarding this socially monogamous species in which reversed sexual size dimorphism is extreme, first‐time breeding one‐year‐old, second‐year females in both study populations produced a preponderance of the smaller and cheaper sex, males, whereas ASY (after‐second‐year), ≥2‐year‐old females in Milwaukee produced a nestling sex ratio near unity and predictably therefore a greater proportion of females compared to ASY females in ex‐Milwaukee who produced a preponderance of males. Adjustment of sex ratios in both study populations occurred at conception. Life histories and selective pressures related to breeding population trajectory in two age cohorts of nesting female Cooper's hawk likely vary, and it is possible that these differences influenced the sex ratios we documented for two age cohorts of female Cooper's hawks in Wisconsin.     

Offspring sex ratios correlate with pair-male condition in a cooperatively breeding fairy-wren

We examined sex allocation patterns in island and mainland populationsof cooperatively breeding white-winged fairy-wrens. The markeddifferences in social structure between island and mainlandpopulations, in addition to dramatic plumage variation amongmales both within and between populations, provided a uniquesituation in which we could investigate different predictionsfrom sex allocation theory in a single species. First, we testthe repayment (local resource enhancement) hypothesis by askingwhether females biased offspring sex ratios in relation to theassistance they derived from helpers. Second, we test the malequality (attractiveness) hypothesis, which suggests that femalesmated to attractive high-quality males should bias offspringsex ratios in favor of males. Finally, we test the idea thatfemales in good condition should bias offspring sex ratios towardmales because they are able to allocate more resources to offspring,whereas females in poor condition should have increased benefitsfrom producing more female offspring (Trivers-Willard hypothesis).We used molecular sexing techniques to assess total offspringsex ratios of 86 breeding pairs over 2 years. Both offspringand first brood sex ratios were correlated with the pair-male'sbody condition such that females increased the proportion ofmales in their brood in relation to the body condition (masscorrected for body size) of their social partner. This relationwas both significant and remarkably similar in both years ofour study and in both island and mainland populations. Althoughconfidence of paternity can be low in this and other fairy-wrenspecies, we show how this finding might be consistent with themale quality (attractiveness) hypothesis with respect to malecondition. There was no support for the repayment hypothesis;the presence of helpers had no effect on offspring sex ratios.There was weak support for both the male quality (attractiveness)hypothesis with respect to plumage color and the maternal conditionhypothesis, but their influence on offspring sex ratios wasnegligible after controlling for the effects of pair-male condition.     

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.     

Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow

We analysed the morphology of nestling barn swallows (Hirundo rustica) in relation to their sex, and laying and hatching order. In addition, we studied sex-allocation in relation to parentage, parental age and expression of a secondary sexual character of fathers. Molecular sexing was conducted using the sex chromosome-linked avian CHD1 gene. Sex of the offspring was not associated with laying or hatching order. None of nine morphological, serological and immunological variables varied in relation to offspring sex. Sexual dimorphism did not vary in relation to parental age and expression of a paternal secondary sexual character. The proportion of sons declined with brood size. Individual males and females had a similar proportion of sons during consecutive breeding years. The proportion of sons of individual females declined with age, but increased with the expression of a secondary sexual character of their current mate. The generalized lack of variation in sexual dimorphism among nestlings may suggest that barn swallows do not differentially invest in sons vs. daughters. Alternatively, male offspring may require different parental effort compared to their female siblings in order to attain the same morphological state. The lack of variation in offspring sexual dimorphism with paternal ornamentation suggests no adjustment of overall parental effort in relation to reproductive value of the two sexes. However, male-biased sex ratio among offspring of highly ornamented males may represent an adaptive sex-allocation strategy because the expression of male ornaments is heritable and highly ornamented males are at a sexual selection advantage.     

PARENTAL AGE,GAMETIC AGE,AND INBREEDING INTERACT TO MODULATE OFFSPRING VIABILITY IN DROSOPHILA MELANOGASTER

In principle, parental relatedness, parental age, and the age of parental gametes can all influence offspring fitness through inbreeding depression and the parental effects of organismal and postmeiotic gametic senescence. However, little is known about the extent to which these factors interact and contribute to fitness variation. Here, we show that, in Drosophila melanogaster, offspring viability is strongly affected by a three‐way interaction between parental relatedness, parental age, and gametic age at successive developmental stages. Overall egg‐to‐adult viability was lowest for offspring produced with old gametes of related, young parents. This overall effect was largely determined at the pupa–adult stage, although three‐way interactions between parental relatedness, parental age and gametic age also explained variation in egg hatchability and larva‐pupa survival. Controlling for the influence of parental and gametic age, we show that inbreeding depression is negligible for egg hatchability but significant at the larva–pupa and pupa–adult stages. At the pupa–adult stage, where offspring could be sexed, parental relatedness, parental age, and gametic age interacted differently in male and female offspring, with daughters suffering higher inbreeding depression than sons. Collectively, our results demonstrate that the architecture of offspring fitness is strongly influenced by a complex interaction between parental effects, inbreeding depression and offspring sex.     

Sex ratio manipulation within broods of house wrens, Troglodytes aedon

Trivers & Willard (1973, Science, 179, 90-92) developed an economic theory of parental investment to explain how the relative profitability of sons and daughters varies under specific ecological conditions. In their maternal condition hypothesis they proposed that in polygynous species, the sex of an offspring should be associated with the amount of parental care likely to be made available to it. In these species, the amount of parental investment directed towards offspring may differentially influence the fitness of male and female offspring because males in better than average condition as adults may enjoy larger fitness gains than a female would if she were in better than average condition, while the reverse may be true when conditions are poor. I tested this hypothesis by determining the sex of specific offspring within house wren broods. Because hatching is asynchronous and fledging is synchronous in this polygynous species, last-hatched young fledge having received less parental care than their broodmates. I predicted that last-hatched offspring would be more likely to be female. I found that these young were indeed more likely to be females, were more likely to have hatched from last-laid eggs and were fledging in poor condition relative to their broodmates. I propose that female house wrens behave in a manner consistent with the predictions of the Trivers & Willard hypothesis by producing female offspring last in the laying sequence of their clutches. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sex-specific fledgling success and brood sex ratio in the Great Reed Warbler (Acrocephalus arundinaceus)

We examine sex ratio variation and sex-specific probability of successful fledgling in relation to hatching date across 376 broods of Great Reed Warblers (Acrocephalus arundinaceus). The sex ratio of complete broods as well as broods with partial mortality did not deviate significantly from parity (0.5 and 0.53, respectively). Variation in sex ratio between broods was not larger than expected from binomial distribution, thus females seem not to manipulate the sex ratio of their broods in the studied population. As a consequence, sex ratio did not vary in relation to hatching date, years and fishponds. Female offspring showed lower fledgling success than their brothers, but the relationship between probability of successful fledgling and hatching date differed between sexes. Fledgling success of female offspring declined with hatching date more strongly than the success of male offspring. Thus, our study shows that Great Reed Warblers do not adjust offspring sex to match observed seasonal sex-specific variation in survival.     

Condition-dependent sex allocation in a lek-breeding wader,the ruff (Philomachus pugnax)

Sex allocation theory predicts that females should bias the production of offspring towards the sex that will maximize maternal fitness. Here we demonstrate evidence for nonrandom sex allocation by female ruffs (Philomachus pugnax), at both the individual and population level in relation to female condition. At the population level, female condition varies significantly across 3 years and is mirrored by population sex ratio, such that in years when females are in poor condition the population offspring sex ratio is female-biased, while in years when females are in better condition there was little or no bias. In the year when females were in overall poor condition, females in better condition produced more daughters. The same relationship is also revealed by comparing the sex ratios of individual females breeding in two consecutive years in different condition. As the condition of an individual female improves (across years) she tends to produce more female offspring. Although we have shown that, as in other birds, female condition is an important determinant of sex allocation, our results also suggest that such nonrandom allocation does not occur in every year, being particularly strong in a year when females, on average, are in poorer condition. We suggest that our results are consistent with the idea that skewing the sex ratio is likely to carry a cost to females and that it is adaptive only when the fitness differential between sons and daughters is sufficient to outweigh probable costs.     

Parent Barn Swallow fluctuating asymmetry and offspring quality

Fluctuating asymmetry may impair locomotion but may also reflect intrinsic phenotypic quality. I tested whether fluctuating asymmetry of adult Barn Swallows Hirundo rustica negatively influenced offspring quality, by estimating the relationship between parental asymmetry and offspring size, condition and immunocompetence during three breeding seasons. Controlling for timing of breeding, brood size and the size of a secondary sexual character (tail length), wing and outermost tail feather asymmetry of male and female parents was not significantly correlated with offspring size, condition and immunocompetence. This was the case in spite of clear differences in nestling quality among years. In addition, parents with extreme asymmetries due to tail feather damage (not representing fluctuating asymmetry) did not have nestlings of lower quality than parents with undamaged tail feathers. These results indicate that there is only a weak relation between parental asymmetry and offspring quality.     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Stress hormones: a link between maternal condition and sex-biased reproductive investment

In species where offspring fitness is sex-specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor-quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex-specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex-biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex-specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female-biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell-mediated immune (phytohemagglutinin) responses in males compared with control-born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex-biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet-hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick-rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex-biased maternal investment in offspring.