Pre-industrial Human Population Research Articles

Genotype-by-environment interactions modulate the rate of microevolution in reproductive timing in humans.

Evidence from natural populations shows that changes in environmental conditions can cause rapid modifications in the evolutionary potential of phenotypes, partly through genotype-by-environment interactions (G×E). Therefore, the overall rate of microevolution should depend on fluctuations in environmental conditions, even when directional selection is sustained over several generations. We tested this hypothesis in a preindustrial human population that experienced a microevolutionary change in age at first reproduction (AFR) of mothers, using the annual infant mortality rate (IMR) as an indicator of environmental conditions during their early life. Using quantitative genetics analyses, we found that G×Es explained a nonnegligible fraction of the additive genetic variance in AFR and in relative fitness, as well as of the genetic covariance between AFR and fitness (i.e., the Robertson-Price covariance). The covariance was stronger for individuals exposed to unfavorable early-life environmental conditions. Our results unravel the presence of G×Es in an important life history trait and its impact on the rate of microevolution, which appears to have been sensitive to short-term fluctuations in local environmental conditions.

Early-life environment and differences in costs of reproduction in a preindustrial human population.

Reproduction is predicted to trade-off with long-term maternal survival, but the survival costs often vary between individuals, cohorts and populations, limiting our understanding of this trade-off, which is central to life-history theory. One potential factor generating variation in reproductive costs is variation in developmental conditions, but the role of early-life environment in modifying the reproduction-survival trade-off has rarely been investigated. We quantified the effect of early-life environment on the trade-off between female reproduction and survival in pre-industrial humans by analysing individual-based life-history data for >80 birth cohorts collected from Finnish church records, and between-year variation in local crop yields, annual spring temperature, and infant mortality as proxies of early-life environment. We predicted that women born during poor environmental conditions would show higher costs of reproduction in terms of survival compared to women born in better conditions. We found profound variation between the studied cohorts in the correlation between reproduction and longevity and in the early-life environment these cohorts were exposed to, but no evidence that differences in early-life environment or access to wealth affected the trade-off between reproduction and survival. Our results therefore do not support the hypothesis that differences in developmental conditions underlie the observed heterogeneity in reproduction-survival trade-off between individuals.

Equilibrium dynamics of European pre-industrial populations: the evidence of carrying capacity in human agricultural societies.

Human populations tend to grow steadily, because of the ability of people to make innovations, and thus overcome and extend the limits imposed by natural resources. It is therefore questionable whether traditional concepts of population ecology, including environmental carrying capacity, can be applied to human societies. The existence of carrying capacity cannot be simply inferred from population time-series, but it can be indicated by the tendency of populations to return to a previous state after a disturbance. So far only indirect evidence at a coarse-grained scale has indicated the historical existence of human carrying capacity. We analysed unique historical population data on 88 settlements before and after the Thirty Years War (1618-1648), one the longest and most destructive conflicts in European history, which reduced the population of Central Europe by 30-50%. The recovery rate of individual settlements after the war was positively correlated with the extent of the disturbance, so that the population size of the settlements after a period of regeneration was similar to the pre-war situation, indicating an equilibrium population size (i.e. carrying capacity). The carrying capacity of individual settlements was positively determined mostly by the fertility of the soil and the area of the cadastre, and negatively by the number of other settlements in the surroundings. Pre-industrial human population sizes were thus probably controlled by negative density dependence mediated by soil fertility, which could not increase due to limited agricultural technologies.

Solar Irradiance, Survival and Longevity in a Pre-industrial Human Population

Severe environmental irregularities, such as droughts or storms that can cause massive crop failure and famine, have repeatedly taken their toll on human populations. Although more subtle climatic variations can also have considerable effects on ecological processes (Stenseth et al. 2002), humans have generally been assumed to be sheltered from these influences. Young children, however, can be very sensitive to seasonal and regional variations in weather conditions and food availability, even outside periods of massive famine (Lummaa and Clutton–Brock 2002). In pre-industrial populations, infant mortality was commonly high; it was not rare that 20–30 % of newborns died annually before reaching the age of 1. The conditions experienced around birth may also have long lasting consequences on adult life-history (Lummaa and Clutton-Brock 2002). For instance, environmental effects experienced at young age, such as the one associated with the month of birth, have been shown to affect adult life expectancy (Doblhammer and Vaupel 2001; Gagnon 2012). Yet, evidence of climate induced cohort effects in humans remain scarce outside disastrous situations, as few longitudinal datasets allow the comparison of yearly environmental variations with survival rates (Galloway 1985; Hayward et al. 2012). Many pre-industrial populations relied mostly on subsistence agriculture and fishing, making them especially vulnerable to environmental variations (Lee et al. 2006; Rickard et al. 2010; Hayward et al. 2012). Proxies of historical environmental variations are increasingly available in reconstructed climatic variables that offer annual measures over very long periods of time (Brazdil et al. 2005). For instance, data on reconstructed solar irradiance (SI) and Northern Atlantic Oscillation (NAO) are now available over centuries (Lean et al. 1995; Luterbacher et al. 1999; Lean 2000) allowing us to investigate the effects of historical climatic variation on preindustrial human population dynamics. There are increasing evidence that SI and NAO correlate with global weather (Stenseth et al. 2002; Pustil'nik and Yom Din 2013) and ecosystem processes such as plant productivity and animal population density (Currie and O'Brien 1993; Coulson et al. 2001; Ottersen et al. 2001; Klvana et al. 2004). Yet, effects of SI and NAO on human health are not so simple to predict as they can be region specific or even have direct effects on human health. Ultraviolet radiations can caused deleterious damage to DNA which is thought to increase fetus loss and reduce lifespan (Melnikov 2012 but see Helle 2009). Nevertheless, the question remains as whether or not subtle large scale cosmic and atmospheric factors can leave a perceptible signature on population growth. To address this question, we used the detailed population Register of a pre-industrial insular Canadian population at the ile aux Coudres (Boisvert and Mayer 1994), over 180 years, and investigated if SI and NAOwere related to infant viability Electronic supplementary material The online version of this article (doi:10.1007/s10745-014-9671-7) contains supplementary material, which is available to authorized users. P. Bergeron (*) : E. Milot Groupe PRIMUS, Centre Hospitalier Universitaire de Sherbrooke, Sherbrooke J1H 5N4, Canada e-mail: Patrick.bergeron@usherbrooke.ca

The effect of socio-economic status and food availability on first birth interval in a pre-industrial human population

Individual variation in nutritional status has direct implications for fitness and thus is crucial in shaping patterns of life-history variation. Nevertheless, it is difficult to measure in natural populations, especially in humans. Here, we used longitudinal data on individual life-histories and annual crop yield variation collected from pre-industrial Finnish populations experiencing natural mortality and fertility to test the validity of first birth interval (FBI; time between marriage and first birth) as a surrogate measure of nutritional status. We evaluated whether women with different socio-economic groups differ in length of FBI, whether women of poorer socio-economic status and experiencing lower crop yields conceive slower following marriage, and whether shorter FBI is associated with higher lifetime breeding success. We found that poorer women had longer FBI and reduced probability of giving birth in months with low food availability, while the FBI of richer women was not affected by variation in food availability. Women with shorter FBI achieved higher lifetime breeding success and a faster reproductive rate. This is, to our knowledge, the first study to show a direct relationship between environmental conditions and speed of childbirth following marriage, highlighting the value of FBI as an indicator of nutritional status when direct data are lacking.

Testing the evolutionary basis of the predictive adaptive response hypothesis in a preindustrial human population

The thrifty phenotype hypothesis proposes that late-life metabolic diseases result from mismatch between early-life and adulthood nutrition. More recently, the predictive adaptive response (PAR) hypothesis has suggested that poor early-life environmental conditions induce metabolic changes that maximize health and fitness in similarly poor adult conditions, but reduce fitness if conditions later improve. Therefore, later-life survival and reproduction should be maximized where environmental conditions during development and adulthood match, but few studies in humans have addressed the consequences of poor early conditions on fitness traits in varying later conditions. We tested key evolutionary predictions of the PAR hypothesis using detailed longitudinal data with several environmental parameters from a natural fertility preindustrial human population, to investigate how combinations of early- and late-life environmental conditions affected annual probabilities of survival and reproduction. We found no suggestion that fitness was maximised when developmental and later-life conditions matched, but rather poor environmental conditions during development or later life and their combinations were associated with lower survival. Our results are more consistent with predictions of 'silver spoon' models, whereby adverse early-life conditions are detrimental to later health and fitness across all environments. Future evolutionary research on understanding metabolic disease epidemiology should focus on determining whether adaptive prediction maximizes infant survival where conditions match during development and immediately after birth, rather than drawing attention to the unlikely long-term fitness benefits of putative metabolic changes associated with poor early nutrition.

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.

Wealth, status, and fitness: a historical study of Norwegians in variable environments

Wealth and status covary with lifetime reproductive success in preindustrial human populations. Local ecology is likely to modify this association, but details of this presumed relationship are not yet known. We sought to determine whether local ecology modifies the relationship between status and fitness (number of grandchildren). Our approach to the problem was to measure variation in fitness relative to status (landless or with land) and to local ecology (inland versus coastal communities). We also analyzed life history traits that might explain observed variations in fitness. Our results confirm previous findings that both status (landless=9.9 vs. with land=16.5) and ecology (inland=12.3 vs. coast=14.1) affect the number of grandchildren produced by a female in pre-industrial society. We also found that the differences in number of children between the status groups were less pronounced on the coast (landless=12.0 vs. with land=16.1) than inland (landless=7.8 vs. with land=16.8). Our findings are novel because they suggest that the fitness consequences of human status may depend on details of local ecology. We discuss four different mechanisms that could account for these fitness differences: (1) differential reproductive rate of mothers, (2) differential marriage rate of children (3) differential survival rate of children, and (4) different social practices (breastfeeding, inheritance of property and diet).

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.

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.

Human longevity and early reproduction in pre-industrial Sami populations

Abstract Senescence is predicted to be associated with the intensity and timing of reproduction at an earlier age. Here, we examine the phenotypic association between reproduction and post-reproductive survival in three pre-industrial human populations that lived in Northern Scandinavia during 1640–1870. In both sexes longevity was independent of the total number of born or adult children, whereas early reproduction was negatively associated with the longevity of females and males. Our results thus do not support the view that reproductive investment as such has a negative impact on longevity, but suggest that survival costs are associated with the scheduling of reproduction. We discuss, however, an alternative point of view suggesting that less intense selection for early reproduction, extended parental care, and social structure allowing kin selection through the effects of close relatives are factors that have selected for the long post-reproductive life span in humans.

Natural selection and quantitative genetics of life-history traits in Western women: a twin study.

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection will cause a change among women in a contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the "baby boom" phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.

NATURAL SELECTION AND QUANTITATIVE GENETICS OF LIFE-HISTORY TRAITS IN WESTERN WOMEN: A TWIN STUDY

Whether contemporary human populations are still evolving as a result of natural selection has been hotly debated. For natural selection to cause evolutionary change in a trait, variation in the trait must be correlated with fitness and be genetically heritable and there must be no genetic constraints to evolution. These conditions have rarely been tested in human populations. In this study, data from a large twin cohort were used to assess whether selection will cause a change among women in a contemporary Western population for three life-history traits: age at menarche, age at first reproduction, and age at menopause. We control for temporal variation in fecundity (the “baby boom” phenomenon) and differences between women in educational background and religious affiliation. University-educated women have 35% lower fitness than those with less than seven years education, and Roman Catholic women have about 20% higher fitness than those of other religions. Although these differences were significant, education and religion only accounted for 2% and 1% of variance in fitness, respectively. Using structural equation modeling, we reveal significant genetic influences for all three life-history traits, with heritability estimates of 0.50, 0.23, and 0.45, respectively. However, strong genetic covariation with reproductive fitness could only be demonstrated for age at first reproduction, with much weaker covariation for age at menopause and no significant covariation for age at menarche. Selection may, therefore, lead to the evolution of earlier age at first reproduction in this population. We also estimate substantial heritable variation in fitness itself, with approximately 39% of the variance attributable to additive genetic effects, the remainder consisting of unique environmental effects and small effects from education and religion. We discuss mechanisms that could be maintaining such a high heritability for fitness. Most likely is that selection is now acting on different traits from which it did in pre-industrial human populations.

Physical work causes suppression of ovarian function in women.

The suppression of reproductive function is known to occur in women engaging in activities that require high energetic expenses, such as sport participation and subsistence work. It is still unclear, however, if reproductive suppression is a response to high levels of energy expenditure, or only to the resulting state of negative energy balance. To our knowledge, this study provides the first evidence that work-related energy expenditure alone, without associated negative energy balance, can lead to the suppression of reproductive function in women. We document suppression of ovarian function expressed as lowered salivary progesterone levels in women from an agricultural community who work hard, but remain in neutral energy balance. We propose two alternative evolutionary explanations (the 'pre-emptive ovarian suppression' hypothesis and the 'constrained down-regulation' hypothesis) for the observed results.

Sexual Conf lict and Remarriage in Preindustrial Human Populations: Causes and Fitness Consequences

Sexual conflict is said to occur when one mating partner has an opportunity to increase its fitness at the cost of the other. We analyzed the effect of remarriage on lifetime reproductive success (LRS) in three preindustrial (1700–1900) socially monogamous Sami populations. In all populations, ever-married women’s age-specific mortality rates exceeded those of ever-married men during reproductive years. After the death of a spouse, men had a higher probability of remarriage than did women of the same age. Remarried men had a higher LRS than men who married only once, but this was not true for women. The higher LRS of the twice-married men was probably due to their longer (+5 years; p < .05) reproductive lifespan (RLS) as compared to once-married men. There was no difference in the RLS of women who married once or twice. These results suggest the sexual conflict in these populations was won by men because women paid a higher cost from reproduction (i.e., reduced survival), and men were able to remarry more often than women, thereby realizing more of their higher reproductive potential. Consequently, serial monogamy seem to have been an important male reproductive strategy in these historical populations.

Direct and correlative phenotypic selection on life-history traits in three pre-industrial human populations.

Because natural selection acts simultaneously on several correlated traits, can be under both direct and correlative selection simultaneously. Correlative selection may either weaken or magnify the association between a trait and fitness. Direct effect of a single trait on fitness can be assessed by removing the effects of correlative selection with multivariate techniques. We studied the phenotypic selection on demographic life-history traits in three pre-industrial human populations, which experienced different mortality environments. We used path-analysis to estimate direct and correlative selection on different traits in females and males. Our results indicate substantial differences among the sexes in the force of phenotypic selection on key life-history traits. For females, the most important component of reproductive success was the age at first reproduction. Most important component of fitness for males was the quality of mate. In addition, our analysis revealed considerable among-population variation in the selection on life-history traits. These differences are in accord with the historical notes of among-population variation in the lifestyle and harshness of the environment, suggesting that among-population variation in life-history traits may have been a response to the environmental variation.