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.     

On the virtue of being the first born: the influence of date of birth on fitness in the mosquitofish, Gambusia affinis

We found in an earlier study that mosquitofish (Gambusia affinis and G. holbrooki) ceased reproduction in the late summer, long before the end of warm weather, stored fat, then utilized reserves to survive the winter and initiate reproduction the following spring. We hypothesized that this pattern of fat utilization was a life history adaptation that enabled the fish to acquire food resources in the autumn then allocate them to reproduction the following spring when the fitness of the young would be greater. Here we evaluate one aspect of this hypothesis by evaluating the probability of survival to maturity and fecundity of young as a function of date of birth. We placed cohorts comprising eight to ten litters of young born early‐, mid‐ or late in the reproductive season in replicate field enclosures. The entire experiment was repeated in two different years. Early‐born young had a significantly higher probability of survival to maturity but did not differ in fecundity relative to the last cohort of the season. Early‐born young also attained maturity early enough to reproduce in their year of birth while late‐born young had to overwinter before reproduction. The fitness consequences to the mother of either producing one more litter of young at the end of the season, versus instead storing fat and reproducing the following spring are not as determinate as are the effects of date of birth on offspring fitness. Females most often gain fitness by not producing one last litter and instead over‐wintering. If, however, the overwinter survival of offspring is not influenced by their size at the end of the season, then a female's fitness could be enhanced by producing one more litter late in the season. If instead the probability of overwinter survival is strongly influenced by the size of offspring at the end of the season, then our results suggest that a female gains more by deferring reproduction and storing for overwinter survival and reproduction the following spring.     

A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus)

1. Long-term effects of conditions during early development on fitness are important for life history evolution and population ecology. Using multistrata mark-recapture models on 20 years of data, we quantified the relation between rearing conditions and lifetime fitness in a long-lived shorebird, the oystercatcher (Haematopus ostralegus). We addressed specifically the relative contribution of short- and long-term effects of rearing conditions to overall fitness consequences. 2. Rearing conditions were defined by differences in natal habitat quality, in which there is a clear dichotomy in our study population. In the first year of life, fledglings from high-quality natal origin had a 1.3 times higher juvenile survival. Later in life (age 3-11), individuals of high-quality natal origin had a 1.6 times higher adult prebreeder survival. The most striking effect of natal habitat quality was that birds that were reared on high-quality territories had a higher probability of settling in high-quality habitat (44% vs. 6%). Lifetime reproductive success of individuals born in high-quality habitat was 2.2 times higher than that of individuals born in low-quality habitat. This difference increased further when fitness was calculated over several generations, due to a correlation between the quality of rearing conditions of parents and their offspring. 3. Long-term effects of early conditions contributed more to overall fitness differences as short-term consequences, contrary to common conceptions on this issue. 4. This study illustrates that investigating only short-term effects of early conditions can lead to the large underestimation of fitness consequences. We discuss how long-term consequences of early conditions may affect settlement decisions and source-sink population interactions.     

Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.     

Selection for long lifespan in men: benefits of grandfathering?

Life-history theory suggests that individuals should live until their reproductive potential declines, and the lifespan of human men is consistent with this idea. However, because women can live long after menopause and this prolonged post-reproductive life can be explained, in part, by the fitness enhancing effects of grandmothering, an alternative hypothesis is that male lifespan is influenced by the potential to gain fitness through grandfathering. Here we investigate whether men, who could not gain fitness through reproduction after their wife's menopause (i.e. married only once), enhanced their fitness through grandfathering in historical Finns. Father presence was associated with reductions in offspring age at first reproduction and birth intervals, but generally not increases in reproductive tenure lengths. Father presence had little influence on offspring lifetime fecundity and no influence on offspring lifetime reproductive success. Overall, in contrast to our results for women in the same population, men do not gain extra fitness (i.e. more grandchildren) through grandfathering. Our results suggest that if evidence for a 'grandfather' hypothesis is lacking in a monogamous society, then its general importance in shaping male lifespan during our more promiscuous evolutionary past is likely to be negligible.     

Maternal inflammation, growth retardation, and preterm birth: insights into adult cardiovascular disease

The "fetal origin of adult disease Hypothesis" originally described by Barker et al. identified the relationship between impaired in utero growth and adult cardiovascular disease risk and death. Since then, numerous clinical and experimental studies have confirmed that early developmental influences can lead to cardiovascular, pulmonary, metabolic, and psychological diseases during adulthood with and without alterations in birth weight. This so called "fetal programming" includes developmental disruption, immediate adaptation, or predictive adaptation and can lead to epigenetic changes affecting a specific organ or overall health. The intrauterine environment is dramatically impacted by the overall maternal health. Both premature birth or low birth weight can result from a variety of maternal conditions including undernutrition or dysnutrition, metabolic diseases, chronic maternal stresses induced by infections and inflammation, as well as hypercholesterolemia and smoking. Numerous animal studies have supported the importance of both maternal health and maternal environment on the long term outcomes of the offspring. With increasing rates of obesity and diabetes and survival of preterm infants born at early gestational ages, the need to elucidate mechanisms responsible for programming of adult cardiovascular disease is essential for the treatment of upcoming generations.     

Increased lifetime reproductive success of first‐hatched siblings in Common Kestrels Falco tinnunculus

Order of birth has profound consequences on offspring across taxa during development and can have effects on individuals later in life. In birds, differential maternal allocation and investment in their progeny lead to variance in the environmental conditions that offspring experience during growth within the brood. In particular, laying and hatching order have been proposed to influence individual quality during the growing period, but little is known about the fitness consequences that these two factors have for offspring from a lifetime perspective. We explored the effect of laying and hatching order on post‐fledgling survival (measured as recruitment probability) and lifetime reproductive success (LRS) in Common Kestrels Falco tinnunculus, using a long‐term and individual‐based dataset. First‐hatched chicks showed higher survival probability and LRS than their siblings. This effect was not due to body condition of the individuals at adulthood, the quality of their mates or the reproductive outcome compared with later‐hatched individuals. Instead, first‐hatched chicks had a higher recruitment probability. This could be explained by the higher body condition attained by first‐hatched chicks at the end of the nesting period, perhaps due to an enhanced competitive advantage for food over their siblings at the time of hatching. Laying order, in contrast to hatching order, appeared to have little or no effect on LRS. Our results suggest that hatching order within siblings predicts fitness, and that better early‐life conditions during growth experienced by first‐hatched chicks improve first survival and then recruitment, resulting in an enhanced LRS.     

Status,reproductive success,and marrying polygynously

A study of female reproductive histories from nineteenth-century Utah shows that although women who married polygynously had fewer children, their number of grandchildren was equal to that of women who married monogamously. Women who chose to marry high-status men polygynously traded decreased fertility for enhanced reproductive performance of offspring. High status can be associated with low fertility and yet still be consistent with fitness optimization. These results suggest how female reproductive decisions influence social structure and challenge previous assumptions concerning proximate measures of fitness.     

Position in the laying order has sex-specific consequences for reproductive success in adult black-headed gulls

Mothers who produce multiple offspring within one reproductive attempt often allocate resources differentially; some maternally derived substances are preferentially allocated to last-produced offspring and others to first-produced offspring. The combined effect of these different allocation regimes on the overall fitness of offspring produced early or late in the sequence is not well understood, partly because production order is often coupled with birth order, making it difficult-to-separate effects of pre-natal maternal allocation from those of post-natal social environments. In addition, very little is known about the influence of laying order on fitness in later life. In this study, we used a semi-natural captive colony of black-headed gulls to test whether an offspring's position in the laying order affected its early-life survival and later-life reproductive success, independent of its hatching order. Later-laid eggs were less likely to hatch, but among those that did, survival to adulthood was greater than that of first-laid eggs. In adulthood, the laying order of females did not affect their likelihood of breeding in the colony, but male offspring hatched from last-laid eggs were significantly less likely to gain a breeding position than earlier-laid males. In contrast, later-laid female parents hatched lower proportions of their clutches than first-laid females, but hatching success was unrelated to the laying order of male parents. Our results indicate that gull mothers induce complex and sex-specific effects on both the early survival of their offspring and on long-term reproductive success through laying order effects among eggs of the same breeding attempt.     

Seasonality of births in Homo sapiens in pre-industrial Finland: maximisation of offspring survivorship?

We examined the seasonal variation in human birth and infant survival rates in pre-modern Finland. If survival probabilities of children born during different seasons of the year differ and if timing of reproduction has been affected by natural selection, periodic variation in environment could have led to reproduction during the season of best infant survival expectations. Significant seasonal variation in both birth rate and survival probability was found, but the monthly birth and survival rates of newborn were uncorrelated. Hence, if there was any tendency to maximise the reproductive success, increase in some other component of fitness than the infant survival was probably targeted. The effect of major holidays on the birth rate was proved to be notable, suggesting that although the basis for seasonal variation in birth rate was biological, sociocultural factors had an impact on the timing of reproduction in humans. The overall mortality of infant boys exceeded that of infant girls in all seasons. This difference was smallest during the time of best food supplies, indicating that the development of males was less buffered against environmental disturbances than that of females.     

THE EFFECT OF BIRTH DATE ON FITNESS OF FEMALE DWARF PERCH,MICROMETRUS MINIMUS (PERCIFORMES: EMBIOTOCIDAE)

Lifetime reproductive success may vary considerably with birth date. I measured phenotypic selection on female birth date in a viviparous teleost fish (Embiotocidae: Micrometrus minimus) by sampling birth-date cohorts over time in Tomales Bay, California. Four episodes of selection were measured: survival from birth to first reproduction, reproductive success in the first breeding season, survival to second reproduction, and reproductive success in the second season. Birth date had a significant impact on fitness in the first two episodes. Early born females were more successful in their first breeding season than late born females (directional selection on birth date), but early born females were less likely to survive the period between birth and first reproduction, relative to females born in the middle of the season (stabilizing selection on birth date). The final two episodes of selection had no detectable effect on birth date. Because of the relationship between birth date and survival in the first year, overall selection on female birth date was stabilizing.     

Intergenerational effects of maternal birth season on offspring size in rural Gambia

Environmental conditions experienced in early life can influence an individual's growth and long-term health, and potentially also that of their offspring. However, such developmental effects on intergenerational outcomes have rarely been studied. Here we investigate intergenerational effects of early environment in humans using survey- and clinic-based data from rural Gambia, a population experiencing substantial seasonal stress that influences foetal growth and has long-term effects on first-generation survival. Using Fourier regression to model seasonality, we test whether (i) parental birth season has intergenerational consequences for offspring in utero growth (1982 neonates, born 1976-2009) and (ii) whether such effects have been reduced by improvements to population health in recent decades. Contrary to our predictions, we show effects of maternal birth season on offspring birth weight and head circumference only in recent maternal cohorts born after 1975. Offspring birth weight varied according to maternal birth season from 2.85 to 3.03 kg among women born during 1975-1984 and from 2.84 to 3.41 kg among those born after 1984, but the seasonality effect reversed between these cohorts. These results were not mediated by differences in maternal age or parity. Equivalent patterns were observed for offspring head circumference (statistically significant) and length (not significant), but not for ponderal index. No relationships were found between paternal birth season and offspring neonatal anthropometrics. Our results indicate that even in rural populations living under conditions of relative affluence, brief variation in environmental conditions during maternal early life may exert long-term intergenerational effects on offspring.     

Selection for increased brood size in historical human populations

Human twinning rates are considered to either reflect the direct fitness effects of twinning in variable environments, or to be a maladaptive by-product of selection for other maternal reproductive traits (e.g., polyovulation). We used historical data (1710-1890) of Sami populations from Northern Scandinavia to contrast these alternative hypotheses. We found that women who produced twins started their reproduction younger, ceased it later, had higher lifetime fecundity, raised more offspring to adulthood, and had higher fitness (individual lambda) than mothers of singletons in all populations studied. For example, an average of 1.2 offspring survived to adulthood from a twin delivery, irrespective of its sex ratio, whereas only 0.8 offspring survived to adulthood from a singleton delivery. Only if mothers started reproduction at very late age (> 37 yr), or had a very long reproductive life span (> 20 yr), was it more beneficial to produce only singletons. These findings suggest that twin deliveries among Sami could not be explained as a maladaptive by-product of selection for other maternal reproductive traits. In contrast, our results suggest that twinning was under natural selection, although the strength of selection was likely to have been context dependent.     

Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.     

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.     

Social and biological determinants of reproductive success in Swedish males and females born 1915–1929

Studying biological and social determinants of mortality and fertility provides insight into selective pressures in a population and the possibility of trade-offs between short- and long-term reproductive success. Limited data is available from post-demographic transition populations. We studied determinants of reproductive success using multi-generational data from a large, population-based cohort of 13,666 individuals born in Sweden between 1915 and 1929. We studied the effects of birthweight for gestational age, preterm birth, birth multiplicity, birth order, mother's age, mother's marital status and family socioeconomic position (SEP) upon reproductive success, measured as total number of children and grandchildren. We further tested the hypothesis that number of grandchildren would peak at intermediate family size, as predicted by some life history explanations for fertility limitation. Reproductive success was associated with both social and biological characteristics at birth. In both sexes, a higher birthweight for gestational age, a term birth and a younger mother were independently associated with a greater number of descendants. A married mother and higher family SEP were also associated with a greater number of descendants in males (but not in females), while higher birth order was associated with a greater number of descendents in females (but not males). These effects were mediated by sex-specific effects upon the probability of marriage. Marriage was also affected by other early life characteristics including birthweight, indicating how ‘biological’ characteristics may operate via social pathways. Number of grandchildren increased with increasing number of children in both sexes, providing no evidence for a trade-off between quantity of offspring and their subsequent reproductive ‘quality’.     

Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations

Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short‐term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry‐over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.     

An Old Mom Keeps You Young: Mother’s Age at Last Birth and Offspring Longevity in Nineteenth-Century Utah

This study analyzes the intergenerational effects of late childbearing on offspring’s adult longevity in a population in Utah (United States) that does not display evidence of parity-specific birth control—a so-called natural fertility population. Studies have found that for women who experience late menopause and prolonged reproduction, aging is postponed and longevity is increased. This is believed to indicate female “robustness” and the impact of biological or genetic factors. If indeed there is a genetic component involved, one would expect to also find evidence for the intergenerational transmission of longevity benefits. Our study investigates the relationship between prolonged natural fertility of mothers and their offspring’s survival rates in adulthood. Gompertz regression models (N = 7,716) revealed that the offspring of mothers who were naturally fertile until a relatively advanced age lived significantly longer. This observed positive effect of late reproduction was not independent of but conditional upon survival of the mother to the end of her fecundity (defined as age 50). Offspring’s relative risks at death beyond age 50 were 6–12 percent lower than those of their counterparts born to mothers who had an average age at last birth. Our results, which account for various early, adult, and later-life conditions, as well as shared frailty, suggest that there is a positive relationship between mother’s age at last birth and offspring longevity, and strengthen the notion that age at menopause is a good predictor of this relationship.     

Natural selection on female life-history traits in relation to socio-economic class in pre-industrial human populations

Life-history theory predicts that resource scarcity constrains individual optimal reproductive strategies and shapes the evolution of life-history traits. In species where the inherited structure of social class may lead to consistent resource differences among family lines, between-class variation in resource availability should select for divergence in optimal reproductive strategies. Evaluating this prediction requires information on the phenotypic selection and quantitative genetics of life-history trait variation in relation to individual lifetime access to resources. Here, we show using path analysis how resource availability, measured as the wealth class of the family, affected the opportunity and intensity of phenotypic selection on the key life-history traits of women living in pre-industrial Finland during the 1800s and 1900s. We found the highest opportunity for total selection and the strongest selection on earlier age at first reproduction in women of the poorest wealth class, whereas selection favoured older age at reproductive cessation in mothers of the wealthier classes. We also found clear differences in female life-history traits across wealth classes: the poorest women had the lowest age-specific survival throughout their lives, they started reproduction later, delivered fewer offspring during their lifetime, ceased reproduction younger, had poorer offspring survival to adulthood and, hence, had lower fitness compared to the wealthier women. Our results show that the amount of wealth affected the selection pressure on female life-history in a pre-industrial human population.     

Birth seasonality and calf mortality in a large population of Asian elephants

In seasonal environments, many species concentrate their reproduction in the time of year most likely to maximize offspring survival. Asian elephants (Elephas maximus) inhabit regions with seasonal climate, but females can still experience 16‐week reproductive cycles throughout the year. Whether female elephants nevertheless concentrate births on periods with maximum offspring survival prospects remains unknown. We investigated the seasonal timing of births, and effects of birth month on short‐ and long‐term mortality of Asian elephants, using a unique demographic data set of 2350 semicaptive, longitudinally monitored logging elephants from Myanmar experiencing seasonal variation in both workload and environmental conditions. Our results show variation in birth rate across the year, with 41% of births occurring between December and March. This corresponds to the cool, dry period and the beginning of the hot season, and to conceptions occurring during the resting, nonlogging period between February and June. Giving birth during the peak December to March period improves offspring survival, as the odds for survival between age 1 and 5 years are 44% higher for individuals born during the high birth rate period than those conceived during working months. Our results suggest that seasonal conditions, most likely maternal workload and/or climate, limit conception rate and calf survival in this population through effects on maternal stress, estrus cycles, or access to mates. This has implications for improving the birth rate and infant survival in captive populations by limiting workload of females of reproductive age. As working populations are currently unsustainable and supplemented through the capture of wild elephants, it is imperative to the conservation of Asian elephants to understand and alleviate the effects of seasonal conditions on vital rates in the working population in order to reduce the pressure for further capture from the wild.