Abstracts (first author)

Talk Plenary (Sat 24)

Sex differences in natural selection on reproductive scheduling and longevity in humans

Author(s): Lummaa V


Despite senescence with age, most animals retain ability to reproduce until relatively close to death. Humans provide an interesting case because with mid-life menopause, women show a radical de-coupling of senescence in reproductive and somatic systems, leading to up to half of total lifespan spent post-reproductive. By contrast, men maintain reproductive ability until much later ages. Although men thus sire offspring at older ages than women, nearly all contemporary human populations exhibit sexual dimorphism in lifespan with women outliving men by on average of five years. While proximate causes for such fertility and lifespan differences between the sexes are well-known, our understanding of the underlying evolutionary forces is much more limited. I use pedigree data on pre-industrial Finnish men and women collected by local clergymen: (1) to address different evolutionary hypothesis for the benefits of menopause and post-reproductive longevity in women; (2) to assess whether selection on overall lifespan differs between the sexes; (3) and to estimate sex-specific heritabilities for, and genetic correlations between, lifespan and fitness to predict evolutionary trajectories for lifespan and sexual dimorphism. Understanding sex differences in rates of senescence in reproduction and survival, both key life-history traits, provides insights into how differing selection pressures can mould rates of senescence and ultimate longevity within a species. I hope to illustrate that although evolutionary studies on contemporary human populations suffer from many limitations, some of the data available on humans offer interesting research opportunities also for evolutionary biologists with potential implications for studies on demography, public health or anthropology.

Abstracts (coauthor)


Understanding life-history trade-offs is fundamental to explaining the diversity of life-history strategies in nature, and determining the genetic basis of trade-offs can identify how evolutionary constraint maintains life-history variation. Humans have evolved an unusual life-history compared to other primates, characterized by the menopause and long female post-reproductive lifespan (PRL). These have been hypothesized to evolve to enable (i) reduced reproduction when the costs of reproducing exceed the benefits, and (ii) enhanced grandchild survival. Previous tests of these hypotheses have examined phenotypic correlations between female reproductive rate and (i) PRL and (ii) offspring survival. However, environmental effects can mask genetic associations, and the direction and magnitude of these genetic correlations must be examined to determine the evolutionary potential of such traits. Using genealogical data from preindustrial Finnish church records for eight populations, we applied a multivariate quantitative genetic framework to examine the genetic basis of female reproductive rate, measured by inter-birth interval (IBI). We examined how additive genetic effects on IBI changed with age, and how age-specific genetic effects varied across environmental conditions. We determined the genetic trade-offs between IBI and both PRL and offspring survival, and how these trade-offs varied across ages and environments. Pilot analyses on four populations show a genetic basis to all traits, and suggest that genetic trade-offs between IBI and the other traits increased with age in poor environmental conditions, but were weak and age-independent in good conditions. IBI and PRL were positively related to lifetime fitness, suggesting that genetic trade-offs act as an evolutionary constraint. Our results will reveal new insight into human life-history evolution and generally highlight the fact that genetic correlations between traits may be age- and environment-dependent.


A central issue in evolutionary biology concerns the long-term reliability of predictions of evolutionary change. Theory predicts that the genetic architecture of life history traits (summarised by the additive genetic variance-covariance matrix, G) will change over time and thus affect how traits respond to selection. However, studies have found support both for fast changes as well as for a great consistency in G over time. It thus remains unclear how rapidly and in what manner G itself changes in response to changes in selection pressures or environment.

The demographic transition to low mortality and fertility rates in many recent human populations involves a drastic environmental change, but its consequences for the evolutionary potential of traits have rarely been addressed. We use genealogical data from 8 parishes in Finland, from natural high (5-6 offspring) to recent low (< 2 offspring) fertility over 350 years to address this question at the genetic level. We study four key life history traits; age at first and last reproduction, number of offspring and longevity, all of which show significant phenotypic changes during the time period. We use the animal model quantitative genetic approach to study whether and how the genetic architecture underlying these traits has also changed, by comparing the full G matrix in the periods before and after the demographic transition.

First, we establish significant additive genetic variance and heritability for all traits during both time periods. Second, we present the genetic covariances and correlations between all four traits during both periods. Third, we compare the overall G matrix of the two periods to elucidate if and how G has changed during the demographic transition. The results provide a novel insight in how traits can respond to selection in contemporary human populations and whether the potential for such responses might have changed along with the recent demographic and societal changes.


Among terrestrial mammals, elephants share the features with great apes and humans, of having long lifespan and offspring with long dependency. In humans, these traits combine with female menopause and an extended post-reproductive lifespan. Some have suggested that elephants, too, have a comparable post-reproductive lifespan to women, with survival into 60s in the wild and max. known age >80yrs. However, little data exists on the frequency of post-reproductive lifespan or its fitness benefits in long-lived species except humans. Long lifespan after last birth has been proposed to evolve because of the long offspring dependency and detrimental effects of early mother loss on their fitness. Here we use extensive (n>8000) individual-based multigenerational demographic records on semi-captive Asian elephants in Myanmar to investigate first, the patterns of post-reproductive survival in females and second, the short- and long-term importance of maternal care to offspring survival. We found that first, the age-specific fecundity clearly decreases after age 50, but the pattern does not correspond to the total loss of fecundity in old age found in human females. The elephant post-reproductive phase covers only one tenth of the whole lifespan, in contrast to almost half of that in women. Secondly, maternal death during the first years reduces calf survival considerably, but such effects wane rapidly with age, so that beyond age 5, mother’s death no longer increases calf risk of death. Calves surviving mother’s immediate death do not show long-term effects in later ages. Thus, Asian elephants show decreased fertility in advanced ages, but it differs distinctly from human age-specific fertility and the subsequent post-reproductive survival pattern. Our results imply that the long lifespan in elephants is not sufficiently explained only by long needed maternal care for calves and more generally, that longevity by itself does not necessarily lead to evolution of menopause.


In highly seasonal environments, many species maximise offspring survival by reproducing at the time of year with peak resource availability. However, elephants do not have a single breeding season with females undergoing reproductive cycles throughout the year. Whether females concentrate most births on periods of maximum offspring survival is unknown, as are the proximate factors that could affect seasonal variation in birth rate. Long-term effects of birth season on patterns of mortality and fertility are also yet to be investigated. These topics are of particular importance in elephants, which are extremely long-lived and endangered, as understanding variation in mortality and reproductive success could contribute towards conservation of the species. We use individual-based longitudinal data for 2350 semi-captive logging elephants from Myanmar that occupy regions with a tropical monsoon climate, to investigate immediate and long term fertility and mortality responses to season. We supplement this long-term data with a 1 year subsample of 70 elephants for which monthly measurements of body weight, body condition and stress hormone (cortisol) levels were collected, to investigate the physiological correlates of seasonal conditions. Our results show significant variation in probability of birth by month, and an interaction between birth order and probability of birth, with higher seasonality of births in first-born individuals. There was no long-term effect of birth month on mortality, but females born in the monsoon season subsequently had earlier peak in fertility and earlier age at last reproduction in comparison to those born in the cool or dry seasons. The seasonal pattern of births did not coincide with high rainfall periods, but was rather associated with seasonal variation in workload and also matches individual level variation in cortisol in the subsample. This is a rare test of effects of early conditions on individual fitness in a non-model species.


Group living can be associated with cooperation and even cooperative breeding whereby non-reproductive individuals help to raise offspring that are not their own. However, it can also lead to evolutionary conflict, which is a less studied phenomenon. Humans are considered to be cooperative breeders, since mothers commonly gain help in raising offspring from other (usually related) group members, such as grandmothers and siblings. Nevertheless, simultaneous breeding in the same household among reproductive-aged females, such as mothers-in-law and daughters-in-law, has also been linked with reduced success. The importance of cooperation and conflict is likely to vary according to ecology and social structure of populations, leading to differential selection pressures on dispersal patterns. We used life-history data on humans collected from church book records from 19th century Eastern Finland where joint-families were traditionally common. In joint families several adult offspring, usually sons, stayed in their natal farm with their families. This creates a situation where reproductive-aged women are not related to other women in the family, leading to possible conflict over resources and lowered fitness, but cooperation between women is also possible. We analyse mother’s fecundity and survival of her offspring in relation to the presence and reproductive history of other reproductive-aged women in the family by event history analysis, whist controlling for potential confounders such as presence of other family members and temporal variation in mortality and fertility rates. Preliminary analysis suggest that living in larger joint families was beneficial for women’s fitness, both in terms of fecundity and offspring survival, compared to smaller nuclear families. These results suggest that in this population cooperation between family members was more important than conflict, potentially favouring reduced dispersal among adult siblings


The sexes often have different phenotypic optima for important life-history traits and because they share much of their 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 vertebrate populations show support for such sexual conflict, it remains unexplored in humans. We used a pedigreed human population from pre-industrial 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. For age at first and last reproduction and reproductive lifespan, the relationships with fitness (number of grandchildren) tended to be nonlinear in women, suggesting an intermediate optimum value, while they were linear in men. Both sexes showed a linear decrease in fitness with increasing reproductive rate. 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. These findings illustrate that apparent sexual conflict at the phenotypic level is not necessarily indicative of an underlying genetic conflict and further emphasize the need for incorporating a genetic perspective into studies of human life-history evolution.


Climate change has intensified interest in understanding how climatic variability affects animal life histories. Despite this, little is known of their effect on survival in those species. Asian elephants (Elephas maximus) are endangered across their natural distribution, and inhabit regions often characterised by high seasonality of both temperature and rainfall. We investigated the effects of monthly climatic variation on survival and causes of death in Asian elephants of all ages and both sexes, using a unique demographic dataset of 839 semi-captive longitudinally monitored elephants from four sites in Myanmar between 1965 and 2000. Temperature had a pronounced effect on survival, with the lowest predicted survival during the hottest and coldest months in both sexes across all ages. Because during a year the elephants spent twice as long in temperatures higher than their optimum (24C) rather than temperatures below it, most deaths occurred during the “too hot” rather than the “too cold” period. Decreased survival at higher temperatures resulted partially from increased deaths from heat stroke and infectious disease, whilst the lower survival in the coldest months is associated with an increase in non-infectious diseases or poor health in general. Variation in survival was also related to rainfall with the highest survival rates during the wettest months. Our results show that even the normal-range monsoon variation in climate can exert large impact on elephant survival in Myanmar leading to large absolute differences in mortality, particularly among the youngest age classes. The persistence of a long-term trend towards higher global temperatures combined with the possibility of higher variation in temperature between seasons may pose a growing challenge to the survival of species such as the endangered Asian elephants.


Understanding dispersal behaviour and its determinants is critical for studies on life history maximising strategies. Though many previous studies have investigated the causes of dispersal, very few have focused on the importance of sibship, especially in humans. Using a large demographic historical dataset (n=4000), we investigate the influence of sibling competition and cooperation on dispersal behaviour. Specifically, we test whether the probability, the timing and the range of dispersal depend on the presence of same-sex or opposite-sex siblings and on their reproductive status. This study is the first to investigate in detail the importance of siblings’ interactions for dispersal behaviour in humans and has important implications for the understanding of the evolution of family dynamics and fitness maximising strategies in humans and in other species.


Environmental conditions during development can affect later-life health, but the evolutionary mechanisms underpinning these observations remain debated. The silver spoon (SS) hypothesis proposes that poor developmental conditions adversely affect development, leading to lower survival and fertility and increased metabolic disease risk, independent of later-life conditions. Meanwhile, the predictive adaptive response (PAR) hypothesis proposes that metabolic disease results from selection for development which is plastic with regard to environmental conditions, under which survival and fertility are maximised where conditions match in later life. If conditions change, metabolic disease results, but because the benefits of developmental plasticity exceed the costs, metabolic disease is not selected against. The observation that humans conceived during famine but raised in affluent conditions show later health problems is consistent with this idea. However, the proposed evolutionary mechanisms for putative developmental plasticity have rarely been empirically tested in humans. In particular, there are few studies examining the fitness consequences of conditions during development in varying later-life conditions. We tested the effects of early-life environmental conditions on later survival and fertility using data collected from several pre-industrial Finnish populations. We tested effects of early-life conditions on fitness during (i) varying later-life conditions, and (ii) adverse environmental conditions (a severe famine). Our results suggest that adverse early conditions decrease later fitness irrespective of later-life conditions, and that individuals born in poor conditions have lower survival and fertility during later-life famine. Our results do not support the PAR hypothesis, but are consistent with predictions of the SS hypothesis, which suggests that the early environmental conditions influence development in a manner which may persist into later life.


Chairman: Octávio S. Paulo
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XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon


Computational Biology & Population Genomics Group