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.     

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live‐bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male‐biased broods had greater mating success at maturity than sons in female‐biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male‐biased brood when the reproductive success of sons is expected to be high.     

Elder brothers affect the life history of younger siblings in preindustrial humans: social consequence or biological cost?

Sex-specific sibling interactions are potentially important in human ecology. It is well established that in patrilineal societies that sons suffer from the presence of brothers because of competition for inheritance. However, offspring (of both sexes) might also suffer from being born after an elder brother because of the greater costs sons may entail for their mother. Evidence that the cost of producing sons is higher has been gained from studies of ungulates and humans, with some of this cost being manifested as lower birthweight or reproductive performance of offspring born following a male. Using church record data from preindustrial Finland, we shed light on this process by investigating the demographic ‘mechanisms' by which offspring born following an elder brother are compromised. First, we show that, for both men and women in this population, being born after an elder male sibling is associated with reduced probability of reproducing, a later age at first reproduction, and longer interbirth intervals. Second, we show that the primary effect of interest is a reduced probability of reproducing in those born after an elder brother (even among only those who married). Finally, we show that the total number of elder brothers who survived to adulthood has a negative effect on male offspring only, and this effect is independent of the elder brother effect above. We highlight that differences in the success of human offspring are not always social in origin as is often perceived but can also be biological, resulting from differential costs for mothers of producing male versus female offspring.     

Violent men have more sons: further evidence for the generalized Trivers-Willard hypothesis (gTWH)

The generalized Trivers-Willard hypothesis (gTWH) [Kanazawa, S., 2005a. Big and tall parents have more sons; further generalizations of the Trivers-Willard hypothesis. J. Theor. Biol. 235, 583-590] proposes that parents who possess any heritable trait which increases the male reproductive success at a greater rate than female reproductive success in a given environment have a higher-than-expected offspring sex ratio, and parents who possess any heritable trait which increases the female reproductive success at a greater rate than male reproductive success in a given environment have a lower-than-expected offspring sex ratio. One heritable trait which increases the reproductive success of sons significantly more than that of daughters in the ancestral environment is the tendency toward violence and aggression. I therefore predict that violent parents have a higher-than-expected offspring sex ratio (more sons). The analysis of both American samples and a British sample demonstrates that battered women, who are mated to violent men, have significantly more sons than daughters.     

Reproductive costs of sons and daughters in Rocky Mountain bighorn sheep

Differential maternal investment theory predicts that in sexuallydimorphic and polygynous species mothers should invest morein sons than in daughters. We tested the hypothesis that bighornewes that raise sons incur greater reproductive costs than ewesthat raise daughters. Although ewe mass gain during lactationand subsequent winter body mass loss were independent of lambsex, lambs born the year following the weaning of a son hadlower survival than lambs born after a daughter. The effectsof lamb sex on subsequent reproductive success of ewes becamemore evident at high population density. Lamb sex did not affectmaternal survival. Population density, weather, and ewe agedid not alter the relationship between lamb sex and subsequentreproductive success of the ewe. The year after weaning a son,ewes were more likely to have a daughter than a son, while ewesthat had previously weaned a daughter had similar numbers ofsons and daughters. Our results show that for bighorn sheepewes, sons have a greater life-history cost than daughters,suggesting a differential maternal investment in the sexes.     

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1.  Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment.
2.  We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus , by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by −2/+2 pups) of their offspring in a laboratory setting.
3.  We found that mothers clearly biased their allocation to female rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring.
4.  The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial.
5.  The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.     

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.     

Offspring sex ratio produced by female guppies in the wild correlates with sexual ornaments of their sons

The attractiveness hypothesis predicts that females produce broods with male-biased sex ratios when they mate with attractive males. This hypothesis presumes that sons in broods with male-biased sex ratios sired by attractive males have high reproductive success, whereas the reproductive success of daughters is relatively constant, regardless of the attractiveness of their sires. However, there is little direct evidence for this assumption. We have examined the relationships between offspring sex ratios and (1) sexual ornamentation of sons and (2) body size of daughters in broods from wild female guppies Poecilia reticulata. Wild pregnant females were collected and allowed to give birth in the laboratory. Body size and sexual ornamentation of offspring were measured at maturity. Our analysis revealed a significant positive correlation between offspring sex ratios (the proportion of sons per brood) and the total length as well as the area of orange spots of sons, two attributes that influence female mating preferences in guppies. The sex ratio was not associated with the body size of daughters. These results suggest that by performing adaptive sex allocation according to the expected reproductive success of sons and daughters, female guppies can enhance the overall fitness of their offspring.     

Beautiful parents have more daughters: a further implication of the generalized Trivers-Willard hypothesis (gTWH)

The generalized Trivers-Willard hypothesis (gTWH) [Kanazawa, S., 2005. Big and tall parents have more sons: further generalizations of the Trivers-Willard hypothesis. J. Theor. Biol. 235, 583-590) proposes that parents who possess any heritable trait which increases the male reproductive success at a greater rate than female reproductive success in a given environment will have a higher-than-expected offspring sex ratio, and parents who possess any heritable trait which increases the female reproductive success at a greater rate than male reproductive success in a given environment will have a lower-than-expected offspring sex ratio. One heritable trait which increases the reproductive success of daughters much more than that of sons is physical attractiveness. I therefore predict that physically attractive parents have a lower-than-expected offspring sex ratio (more daughters). Further, if beautiful parents have more daughters and physical attractiveness is heritable, then, over evolutionary history, women should gradually become more attractive than men. The analysis of the National Longitudinal Study of Adolescent Health (Add Health) confirm both of these hypotheses. Very attractive individuals are 26% less likely to have a son, and women are significantly more physically attractive than men in the representative American sample.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

Males from populations with higher competitive mating success produce sons with lower fitness

Female mate choice can result in direct benefits to the female or indirect benefits through her offspring. Females can increase their fitness by mating with males whose genes encode increased survivorship and reproductive output. Alternatively, male investment in enhanced mating success may come at the cost of reduced investment in offspring fitness. Here, we measure male mating success in a mating arena that allows for male–male, male–female and female–female interactions in Drosophila melanogaster. We then use isofemale line population measurements to correlate male mating success with sperm competitive ability, the number of offspring produced and the indirect benefits of the number of offspring produced by daughters and sons. We find that males from populations that gain more copulations do not increase female fitness through increased offspring production, nor do these males fare better in sperm competition. Instead, we find that these populations have a reduced reproductive output of sons, indicating a potential reproductive trade‐off between male mating success and offspring quality.     

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

Sons are made from old stores: sperm storage effects on sex ratio in a lizard

Sperm storage is a widespread phenomenon across taxa and mating systems but its consequences for central fitness parameters, such as sex ratios, has rarely been investigated. In Australian painted dragon lizards (Ctenophorus pictus), we describe elsewhere that male reproductive success via sperm competition is largely an effect of sperm storage. That is, sperm being stored in the female reproductive tract out-compete more recently inseminated sperm in subsequent ovarian cycles. Here we look at the consequences of such sperm storage for sex allocation in the same species, which has genetic sex determination. We show that stored sperm have a 23% higher probability of producing sons than daughters. Thus, shifts in sex ratio, for example over the reproductive season, can partly be explained by different survival of son-producing sperm or some unidentified female mechanism taking effect during prolonged storage.     

Maternal Natal Environment and Breeding Territory Predict the Condition and Sex Ratio of Offspring

Females in a variety of taxa adjust offspring sex ratios to prevailing ecological conditions. However, little is known about whether conditions experienced during a female’s early ontogeny influence the sex ratio of her offspring. We tested for past and present ecological predictors of offspring sex ratios among known-age females that were produced as offspring and bred as adults in a population of house wrens. The body condition of offspring that a female produced and the proportion of her offspring that were male were negatively correlated with the size of the brood in which she herself was reared. The proportion of sons within broods was negatively correlated with maternal hatching date, and varied positively with the quality of a female’s current breeding territory as predicted. However, females producing relatively more sons than daughters were less likely to return to breed in the population the following year. Although correlative, our results suggest that the rearing environment can have enduring effects on later maternal investment and sex allocation. Moreover, the overproduction of sons relative to daughters may increase costs to a female’s residual reproductive value, constraining the extent to which sons might be produced in high-quality breeding conditions. Sex allocation in birds remains a contentious subject, largely because effects on offspring sex ratios are small. Our results suggest that offspring sex ratios are shaped by various processes and trade-offs that act throughout the female life history and ultimately reduce the extent of sex-ratio adjustment relative to classic theoretical predictions.     

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.     

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.     

Offspring sex ratio allocation in the parasitic jaeger: selection for pale females and melanic males?

The maintenance of plumage color polymorphism in the parasiticjaeger (Stercorarius parasiticus) is still not well understood.Earlier studies indicated that selection may favor pale femalesand melanic males. If so, females would maximize their fitness,producing pale female and melanic male offspring. We thereforepredicted that females might bias their offspring sex ratiotoward daughters in pale pairs and toward sons in melanic pairs.Females might also choose to mate assortatively in relationto plumage color, thereby maximizing the probability of producingeither pale or melanic offspring. Because females are largerthan males, differential rearing costs may affect the offspringsex ratio independent of parental plumage color. We examinedoffspring sex ratio allocation, breeding variables indicativeof parental quality, and mating pattern in relation to plumagecolor in a colony of parasitic jaegers in northern Norway. Jaegerstended to mate assortatively in relation to plumage color. Thereproductive performance declined with season, and matched pairsappeared to be of lower quality than mixed pairs. The proportionof male offspring increased with hatching date in matched paleand mixed pairs, whereas the situation was reversed in matchedmelanic pairs. Matched pale pairs produced an overall surplusof favorable pale but costly daughters despite their lower quality,while melanic pairs produced a surplus of favorable melanicsons. However, differential offspring rearing costs and parentalrearing capacity may have additionally affected the realizedoffspring sex ratio. Mixed pairs producing an overall surplusof pale and melanic daughters allocated their resources accordingto differential rearing costs and parental quality only. Wesuggest that both strategies of sex ratio allocation togetherwith differences in reproductive success in matched versus mixedpairs may have a balancing effect on the mating pattern betweenplumage morphs and may contribute to the maintenance of thecolor polymorphism in this species.     

Different optimal offspring sizes for sons versus daughters may favor the evolution of temperature-dependent sex determination in viviparous lizards

Temperature-dependent sex determination (TSD) has evolved independently in at least two lineages of viviparous Australian scincid lizards, but its adaptive significance remains unclear. We studied a montane lizard species (Eulamprus heatwolei) with TSD. Our data suggest that mothers can modify the body sizes of their offspring by selecting specific thermal regimes during pregnancy (mothers with higher and more stable temperatures produced smaller offspring), but cannot influence sons versus daughters differentially in this way. A field mark-recapture study shows that optimal offspring size differs between the sexes: larger body size at birth enhanced the survival of sons but reduced the survival of daughters. Thus, a pregnant female can optimize the fitness of either her sons or her daughters (via yolk allocation and thermoregulation), but cannot simultaneously optimize both. One evolutionary solution to reduce this fitness cost is to modify the sex-determining mechanism so that a single litter consists entirely of either sons or daughters; TSD provides such a mechanism. Previous work has implicated a sex difference in optimal offspring size as a selective force for TSD in turtles. Hence, opposing fitness determinants of sons and daughters may have favored evolutionary transitions from genetic sex determination to TSD in both oviparous turtles and viviparous lizards.     

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.     

Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination

Life-history traits such as offspring size, number and sex ratio are affected by maternal feeding rates in many kinds of animals, but the consequences of variation in maternal diet quality (rather than quantity) are poorly understood. We manipulated dietary quality of reproducing female lizards (Amphibolurus muricatus; Agamidae), a species with temperature-dependent sex determination, to examine strategies of reproductive allocation. Females maintained on a poor-quality diet produced fewer clutches but massively (twofold) larger eggs with lower concentrations of yolk testosterone than did conspecific females given a high-quality diet. Although all eggs were incubated at the same temperature, and yolk steroid hormone levels were not correlated with offspring sex, the nutrient-deprived females produced highly male-biased sex ratios among their offspring. These responses to maternal nutrition generate a link between sex and offspring size, in a direction likely to enhance maternal fitness if large body size enhances reproductive success more in sons than in daughters (as seems plausible, given the mating system of this species). Overall, our results show that sex determination in these animals is more complex, and responsive to a wider range of environmental cues, than that suggested by the classification of 'environmental sex determination'.