Jenni E. Pettay

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.

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.

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.

Effects of the demographic transition on the genetic variances and covariances of human life-history traits

The recent demographic transitions to lower mortality and fertility rates in most human societies have led to changes and even quick reversals in phenotypic selection pressures. This can only result in evolutionary change if the affected traits are heritable, but changes in environmental conditions may also lead to subsequent changes in the genetic variance and covariance (the G matrix) of traits. It currently remains unclear if there have been concomitant changes in the G matrix of life‐history traits following the demographic transition. Using 300 years of genealogical data from Finland, we found that four key life‐history traits were heritable both before and after the demographic transition. The estimated heritabilities allow a quantifiable genetic response to selection during both time periods, thus facilitating continued evolutionary change. Further, the G matrices remained largely stable but revealed a trend for an increased additive genetic variance and thus evolutionary potential of the population after the transition. Our results demonstrate the validity of predictions of evolutionary change in human populations even after the recent dramatic environmental change, and facilitate predictions of how our biology interacts with changing environments, with implications for global public health and demography.

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.

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.

Effects of remarriage after widowhood on long-term fitness in a monogamous historical human population

The fitness benefits of multiple mating determine the strength of sexual selection in each sex. This is traditionally quantified by the number of offspring born to once versus multiply mated individuals. In species with (bi)parental care, however, this measure may overestimate the benefits of multiple mating since having several mates can increase offspring number but decrease offspring quality. We analyzed short- and long-term fitness consequences of multiple marriages for both sexes in humans in preindustrial Finnish populations, where monogamy was socially enforced and remarriage was possible only after widowhood. Remarriage increased the lifetime number of offspring sired by men by lengthening their reproductive span but was unrelated to the lifetime number of births for women. However, neither mens nor womens long-term fitness, measured as their number of grandchildren, was significantly increased or decreased by remarriage. These associations were not modified by individual wealth. Our results suggest that despite increasing the number of offspring sired by men, the long-term fitness benefits of serial monogamy may be negligible for both sexes when parental investment is crucial for offspring success and continues to adulthood. They also demonstrate the importance of incorporating long-term fitness measures when quantifying the benefits of mating and reproductive strategies.

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.

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.

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.