Limited support for the X-linked grandmother hypothesis in pre-industrial Finland.

The level of kin help often depends on the degree of relatedness between a helper and the helped. In humans, grandmother help is known to increase the survival of grandchildren, though this benefit can differ between maternal grandmothers (MGMs) and paternal grandmothers (PGMs) and between grandsons and granddaughters. The X-linked grandmother hypothesis posits that differential X-chromosome relatedness between grandmothers and their grandchildren is a leading driver of differential grandchild survival between grandmother lineages and grandchild sexes. We tested this hypothesis using time-event models on a large, multigenerational dataset from pre-industrial Finland. We found that the presence of an MGM increases grandson survival more than PGM presence, and that granddaughter survival is higher than that of grandsons in the presence of a PGM. However, there was no support for the key prediction that the presence of PGMs improves granddaughter survival more than that of MGMs, diminishing the overall support for the hypothesis. Our results call for alternative explanations for differences in the effects of maternal and paternal kin to grandchild survival in humans.

What have humans done for evolutionary biology? Contributions from genes to populations.

Many fundamental concepts in evolutionary biology were discovered using non-human study systems. Humans are poorly suited to key study designs used to advance this field, and are subject to cultural, technological, and medical influences often considered to restrict the pertinence of human studies to other species and general contexts. Whether studies using current and recent human populations provide insights that have broader biological relevance in evolutionary biology is, therefore, frequently questioned. We first surveyed researchers in evolutionary biology and related fields on their opinions regarding whether studies on contemporary humans can advance evolutionary biology. Almost all 442 participants agreed that humans still evolve, but fewer agreed that this occurs through natural selection. Most agreed that human studies made valuable contributions to evolutionary biology, although those less exposed to human studies expressed more negative views. With a series of examples, we discuss strengths and limitations of evolutionary studies on contemporary humans. These show that human studies provide fundamental insights into evolutionary processes, improve understanding of the biology of many other species, and will make valuable contributions to evolutionary biology in the future.

Natural and sexual selection in a monogamous historical human population.

Whether and how human populations exposed to the agricultural revolution are still affected by Darwinian selection remains controversial among social scientists, biologists, and the general public. Although methods of studying selection in natural populations are well established, our understanding of selection in humans has been limited by the availability of suitable datasets. Here, we present a study comparing the maximum strengths of natural and sexual selection in humans that includes the effects of sex and wealth on different episodes of selection. Our dataset was compiled from church records of preindustrial Finnish populations characterized by socially imposed monogamy, and it contains a complete distribution of survival, mating, and reproductive success for 5,923 individuals born 1760-1849. Individual differences in early survival and fertility (natural selection) were responsible for most variation in fitness, even among wealthier individuals. Variance in mating success explained most of the higher variance in reproductive success in males compared with females, but mating success also influenced reproductive success in females, allowing for sexual selection to operate in both sexes. The detected opportunity for selection is in line with measurements for other species but higher than most previous reports for human samples. This disparity results from biological, demographic, economic, and social differences across populations as well as from failures by most previous studies to account for variation in fitness introduced by nonreproductive individuals. Our results emphasize that the demographic, cultural, and technological changes of the last 10,000 y did not preclude the potential for natural and sexual selection in our species.

Evolutionary demography of agricultural expansion in preindustrial northern Finland.

A shift from nomadic foraging to sedentary agriculture was a major turning point in human evolutionary history, increasing our population size and eventually leading to the development of modern societies. We however lack understanding of the changes in life histories that contributed to the increased population growth rate of agriculturalists, because comparable individual-based reproductive records of sympatric populations of agriculturalists and foragers are rarely found. Here, we compared key life-history traits and population growth rate using comprehensive data from the seventieth to nineteenth century Northern Finland: indigenous Sami were nomadic hunter-fishers and reindeer herders, whereas sympatric agricultural Finns relied predominantly on animal husbandry. We found that agriculture-based families had higher lifetime fecundity, faster birth spacing and lower maternal mortality. Furthermore, agricultural Finns had 6.2% higher annual population growth rate than traditional Sami, which was accounted by differences between the subsistence modes in age-specific fecundity but not in mortality. Our results provide, to our knowledge, the most detailed demonstration yet of the demographic changes and evolutionary benefits that resulted from agricultural revolution.

The role of mating effort and co-residence history in step-grandparental investment.

The prevalence of divorce in both parental and grandparental generations has led to a rise in the number of children who now have families that include both biological and step-grandparents. Despite the thorough examination of biological grandparents' contributions in the recent literature, there remains a scarcity of studies focusing on the investment of step-grandparents. Using population-based data from a sample of 2494 parents in Germany, we assessed grandparental investment through financial support and assistance with childcare of grandparents (N = 4238) and step-grandparents (N = 486). The study revealed that step-grandparents provided lower levels of investment in their grandchildren compared with biological grandparents. Furthermore, the study identified that a longer duration of co-residence between step-grandparents and parents earlier in life did not correspond to an increase or decrease in step-grandparental investment. However, investment by separated biological grandparents increased with the increasing length of co-residence with parents. In line with the scarce literature on step-grandparental investment, these findings indicate that mating effort may be the most important motivation for step-grandparental investment.

Divergent selection on, but no genetic conflict over, female and male timing and rate of reproduction in a human population.

The sexes often have different phenotypic optima for important life-history traits, and because of a largely shared genome this can lead to a conflict over trait expression. In mammals, the obligate costs of reproduction are higher for females, making reproductive timing and rate especially liable to conflict between the sexes. While studies from wild vertebrates support such sexual conflict, it remains unexplored in humans. We used a pedigreed human population from preindustrial Finland to estimate sexual conflict over age at first and last reproduction, reproductive lifespan and reproductive rate. We found that the phenotypic selection gradients differed between the sexes. We next established significant heritabilities in both sexes for all traits. All traits, except reproductive rate, showed strongly positive intersexual genetic correlations and were strongly genetically correlated with fitness in both sexes. Moreover, the genetic correlations with fitness were almost identical in men and women. For reproductive rate, the intersexual correlation and the correlation with fitness were weaker but again similar between the sexes. Thus, in this population, an apparent sexual conflict at the phenotypic level did not reflect an underlying genetic conflict over the studied reproductive traits. These findings emphasize the need for incorporating genetic perspectives into studies of human life-history evolution.

Sex, age, and family structure influence dispersal behaviour after a forced migration.

Dispersal does not only mean moving from one environment to another, but can also refer to shifting from one social group to another. Individual characteristics such as sex, age and family structure might influence an individual's propensity to disperse. In this study, we use a unique dataset of an evacuated World War II Finnish population, to test how sex, age, number of siblings and birth order influence an individual's dispersal away from their own social group at a time when society was rapidly changing. We found that young women dispersed more than young men, but the difference decreased with age. This suggests that young men might benefit more from staying near a familiar social group, whereas young women could benefit more from moving elsewhere to find work or spouses. We also found that having more younger brothers increased the propensity for firstborns to disperse more than for laterborns, indicating that younger brothers might pressure firstborn individuals into leaving. However, sisters did not have the same effect as brothers. Overall, the results show that individual characteristics are important in understanding dispersal behaviour, but environmental properties such as social structure and the period of flux after World War II might upend the standard predictions concerning residence and dispersal. Social media summary: Individual characteristics influence dispersal away from social group after a forced migration in a Finnish population.

Parental Investment by Birth Fathers and Stepfathers : Roles of Mating Effort and Childhood Co-residence Duration.

This study investigates the determinants of paternal investment by birth fathers and stepfathers. Inclusive fitness theory predicts higher parental investment in birth children than stepchildren, and this has consistently been found in previous studies. Here we investigate whether paternal investment varies with childhood co-residence duration and differs between stepfathers and divorced birth fathers by comparing the investment of (1) stepfathers, (2) birth fathers who are separated from the child's mother, and (3) birth fathers who still are in a relationship with her. Path analysis was conducted using cross-sectional data from adolescents and younger adults (aged 17-19, 27-29, and 37-39 years) from the German Family Panel (pairfam), collected in 2010-2011 (n = 8326). As proxies of paternal investment, we used financial and practical help, emotional support, intimacy, and emotional closeness, as reported by the children. We found that birth fathers who were still in a relationship with the mother invested the most, and stepfathers invested the least. Furthermore, the investment of both separated fathers and stepfathers increased with the duration of co-residence with the child. However, in the case of financial help and intimacy, the effect of childhood co-residence duration was stronger in stepfathers than in separated fathers. Our findings support inclusive fitness theory and mating effort theory in explaining social behavior and family dynamics in this population. Furthermore, social environment, such as childhood co-residence was associated with paternal investment.

Food and fitness: associations between crop yields and life-history traits in a longitudinally monitored pre-industrial human population.

Severe food shortage is associated with increased mortality and reduced reproductive success in contemporary and historical human populations. Studies of wild animal populations have shown that subtle variation in environmental conditions can influence patterns of mortality, fecundity and natural selection, but the fitness implications of such subtle variation on human populations are unclear. Here, we use longitudinal data on local grain production, births, marriages and mortality so as to assess the impact of crop yield variation on individual age-specific mortality and fecundity in two pre-industrial Finnish populations. Although crop yields and fitness traits showed profound year-to-year variation across the 70-year study period, associations between crop yields and mortality or fecundity were generally weak. However, post-reproductive individuals of both sexes, and individuals of lower socio-economic status experienced higher mortality when crop yields were low. This is the first longitudinal, individual-based study of the associations between environmental variation and fitness traits in pre-industrial humans, which emphasizes the importance of a portfolio of mechanisms for coping with low food availability in such populations. The results are consistent with evolutionary ecological predictions that natural selection for resilience to food shortage is likely to weaken with age and be most severe on those with the fewest resources.

Correction to: Female-biased sex ratios in urban centers create a "fertility trap" in post-war Finland.

[This corrects the article DOI: 10.1093/beheco/arab007.].

The interplay of grandparental investment according to the survival status of other grandparent types.

Inclusive fitness theory predicts that grandparental investment in grandchildren aims to maximise their inclusive fitness. Owing to an increasing overlap between successive generations in modern affluent populations, the importance of grandparental investment remains high. Despite the growing literature, there is limited knowledge regarding how the survival status of different grandparent types influences each other's investment in grandchildren. This question was studied by using the Involved Grandparenting and Child Well-Being Survey, which provided nationally representative data of English and Welsh adolescents aged 11-16-years. We applied Bayesian structural equation modeling (BSEM) where grandparental investment in grandchildren was modelled using multi-indicator unobserved latent variable. Our results showed that maternal grandmothers' investment was increased by having a living maternal grandfather but not vice versa. Having a living maternal grandmother was also associated with decreased investment of paternal grandparents while the opposite was not found. These findings indicate that the association between the survival status of other grandparents and the focal grandparents' investment varies between grandparent types.

Mothers with higher twinning propensity had lower fertility in pre-industrial Europe.

Historically, mothers producing twins gave birth, on average, more often than non-twinners. This observation has been interpreted as twinners having higher intrinsic fertility - a tendency to conceive easily irrespective of age and other factors - which has shaped both hypotheses about why twinning persists and varies across populations, and the design of medical studies on female fertility. Here we show in >20k pre-industrial European mothers that this interpretation results from an ecological fallacy: twinners had more births not due to higher intrinsic fertility, but because mothers that gave birth more accumulated more opportunities to produce twins. Controlling for variation in the exposure to the risk of twinning reveals that mothers with higher twinning propensity - a physiological predisposition to producing twins - had fewer births, and when twin mortality was high, fewer offspring reaching adulthood. Twinning rates may thus be driven by variation in its mortality costs, rather than variation in intrinsic fertility.

Female-biased sex ratios in urban centers create a "fertility trap" in post-war Finland.

Because sex ratios are a key factor regulating mating success and subsequent fitness both across and within species, there is widespread interest in how population-wide sex ratio imbalances affect marriage markets and the formation of families in human societies. Although most modern cities have more women than men and suffer from low fertility rates, the effects of female-biased sex ratios have garnered less attention than male-biased ratios. Here, we analyze how sex ratios are linked to marriages, reproductive histories, dispersal, and urbanization by taking advantage of a natural experiment in which an entire population was forcibly displaced during World War II to other local Finnish populations of varying sizes and sex ratios. Using a discrete time-event generalized linear mixed-effects model, and including factors that change across time, such as annual sex ratio, we show how sex ratios, reproduction, and migration are connected in a female-dominated environment. Young childless women migrated toward urban centers where work was available to women, and away from male-biased rural areas. In such areas where there were more females, women were less likely to start reproduction. Despite this constraint, women showed little flexibility in mate choice, with no evidence for an increase in partner age difference in female-biased areas. We propose that together these behaviors and conditions combine to generate an "urban fertility trap" which may have important consequences for our understanding of the fertility dynamics of today including the current fertility decline across the developed world.

Offspring fertility and grandchild survival enhanced by maternal grandmothers in a pre-industrial human society.

Help is directed towards kin in many cooperative species, but its nature and intensity can vary by context. Humans are one of few species in which grandmothers invest in grandchildren, and this may have served as an important driver of our unusual life history. But helping behaviour is hardly uniform, and insight into the importance of grandmothering in human evolution depends on understanding the contextual expression of helping benefits. Here, we use an eighteenth-nineteenth century pre-industrial genealogical dataset from Finland to investigate whether maternal or paternal grandmother presence (lineage relative to focal individuals) differentially affects two key fitness outcomes of descendants: fertility and survival. We found grandmother presence shortened spacing between births, particularly at younger mother ages and earlier birth orders. Maternal grandmother presence increased the likelihood of focal grandchild survival, regardless of whether grandmothers had grandchildren only through daughters, sons, or both. In contrast, paternal grandmother presence was not associated with descendants' fertility or survival. We discuss these results in terms of current hypotheses for lineage differences in helping outcomes.

Male twins reduce fitness of female co-twins in humans.

In mammals, including humans, female fetuses that are exposed to testosterone from adjacent male fetuses in utero can have masculinized anatomy and behavior. However, the reproductive consequences of such prebirth sex-ratio effects for offspring and their implications for maternal fitness remain unexplored. Here we investigate the effects of being gestated with a male co-twin for daughter lifetime reproductive success, and the fitness consequences for mothers of producing mixed-sex twins in preindustrial (1734-1888) Finns. We show that daughters born with a male co-twin have reduced lifetime reproductive success compared to those born with a female co-twin. This reduction arises because such daughters have decreased probabilities of marrying as well as reduced fecundity. Mothers who produce opposite-sex twins consequently have fewer grandchildren (and hence lower fitness) than mothers who produce same-sex twins. Our results are unlikely to be a consequence of females born with male co-twins receiving less nutrition because such females do not have reduced survival and increases in food availability fail to improve their reproductive success. Nor are our results explained by after-birth social factors (females growing up with similarly aged brothers) because females born with a male co-twin have reduced success even when their co-twin dies shortly after birth and are raised as singletons after birth. Our findings suggest that hormonal interactions between opposite-sex fetuses known to influence female morphology and behavior can also have negative effects on daughter fecundity and, hence, maternal fitness, and bear significant implications for adaptive sex allocation in mammals.

Limits to Fitness Benefits of Prolonged Post-reproductive Lifespan in Women.

Recent advances in medicine and life-expectancy gains have fueled multidisciplinary research into the limits of human lifespan [1-3]. Ultimately, how long humans can live for may depend on selection favoring extended longevity in our evolutionary past [4]. Human females have an unusually extended post-reproductive lifespan, which has been explained by the fitness benefits provided from helping to raise grandchildren following menopause [5, 6]. However, formal tests of whether such grandmothering benefits wane with grandmother age and explain the observed length of post-reproductive lifespan are missing. This is critical for understanding prevailing selection pressures on longevity but to date has been overlooked as a possible mechanism driving the evolution of lifespan. Here, we use extensive data from pre-industrial humans to show that fitness gains from grandmothering are dependent on grandmother age, affecting selection on the length of post-reproductive lifespan. We find both opportunities and ability to help grandchildren declined with age, while the hazard of death of women increased greatly in their late 60s and 70s compared to menopausal ages, together implying waning selection on subsequent longevity. The presence of maternal grandmothers aged 50-75 increased grandchild survival after weaning, confirming the fitness advantage of post-reproductive lifespan. However, co-residence with paternal grandmothers aged 75+ was detrimental to grandchild survival, with those grandmothers close to death and presumably in poorer health particularly associated with lower grandchild survival. The age limitations of gaining inclusive fitness from grandmothering suggests that grandmothering can select for post-reproductive longevity only up to a certain point.

Age-specific genetic and maternal effects in fecundity of preindustrial Finnish women.

A population's potential for evolutionary change depends on the amount of genetic variability expressed in traits under selection. Studies attempting to measure this variability typically do so over the life span of individuals, but theory suggests that the amount of additive genetic variance can change during the course of individuals' lives. Here we use pedigree data from historical Finns and a quantitative genetic framework to investigate how female fecundity, throughout an individual's reproductive life, is influenced by "maternal" versus additive genetic effects. We show that although maternal effects explain variation in female fecundity early in life, these effects wane with female age. Moreover, this decline in maternal effects is associated with a concomitant increase in additive genetic variance with age. Our results thus highlight that single over-lifetime estimates of trait heritability may give a misleading view of a trait's potential to respond to changing selection pressures.

Sex and size matters: Selection on personality in natural prey-predator interactions.

Optimal life-history strategies are currently considered to be a major driving force for the maintenance of animal personalities. In this experimental study we tested whether naturally occurring predation causes personality-dependent mortality of a marine isopod (Idotea balthica), which could maintain personality variation in nature. Moreover, as isopods are known to have sex-differences in behaviour, we were interested in whether personality-dependent predation was sex-specific. We also hypothesised that predation pressure among personality types could vary according to habitat type, as it has been shown in correlative studies that habitat may influence personality variation. We used natural predator (European perch Perca fluviatilis) of I. balthica and studied relative mortality of males and females with a different personality types in laboratory settings with two different habitats. We found that survival in males was lower than in females for high active individuals. Moreover, survival under predation was linked to body size differently in females and males. This, however, depended on personality class as larger size was advantageous for low-active males and middle- and high-active females. Conversely, smaller size was advantageous for low-active females and middle-active males. Size did not affect survival in high-active males. Our results suggest that predation can encourage life-history differences between sexes leading to different optimal life-history strategies and also maintains consistent activity for both sexes.

Grandmotherhood across the demographic transition.

Grandmothers provide key care to their grandchildren in both contemporary and historic human populations. The length of the grandmother-grandchild relationship provides a basis for such interactions, but its variation and determinants have rarely been studied in different contexts, despite changes in age-specific mortality and fertility rates likely having affected grandmotherhood patterns across the demographic transition. Understanding how often and long grandmothers have been available for their grandchildren in different conditions may help explain the large differences between grandmaternal effects found in different societies, and is vital for developing theories concerning the evolution of menopause, post-reproductive longevity, and family living. Using an extensive genealogical dataset from Finland spanning the demographic transition, we quantify the length of grandmotherhood and its determinants from 1790-1959. We found that shared time between grandmothers and grandchildren was consistently low before the demographic transition, only increasing greatly during the 20th century. Whilst reduced childhood mortality and increasing adult longevity had a role in this change, grandmaternal age at birth remained consistent across the study period. Our findings further understanding of the temporal context of grandmother-grandchild relationships, and emphasise the need to consider the demography of grandmotherhood in a number of disciplines, including biology (e.g. evolution of the family), sociology (e.g. changing family structures), population health (e.g. changing age structures), and economics (e.g. workforce retention).