The question of the cost of reproduction lies at the heart of life-history evolution and aging theories. The classic disposable soma theory predicts that resources spent on offspring are diverted from body maintenance, shortening the parent's life. However, observational studies in humans give a contradictory picture: in some populations, high fertility is linked to early death, in others to longevity. Our work stands apart from neighboring studies: nearby are papers on sleep genes, cellular senescence, genetic algorithms, and horizontal gene transfer, but none addresses the genetic architecture of the reproduction-survival trade-off in humans. We fill this gap using a large genealogical dataset and a quantitative-genetic approach.
We used a crowdsourced genealogical database of marriages in the Netherlands from 1600 to 1999, focusing on people born between 1850 and 1915. For each person, dates of birth and death, number of children, and ages at first and last birth were known. To avoid a mechanical link between longevity and the opportunity to have children, the main analysis was restricted to individuals who survived to age 45. Genetic parameters were estimated using Bayesian animal models, generalized linear mixed models that use pedigree relationships to decompose phenotypic variance into additive genetic and environmental components. Heritability and genetic correlations were computed separately for men and women, as well as between the sexes.
The heritability of lifespan was about 0.21 in women and 0.19 in men among those who survived to age 45. The heritability of number of children was markedly higher in men (0.44) than in women (0.17). Genetic correlations between lifespan and number of children were weak: negative in women (-0.10), near zero or weakly positive in men (0.05). However, age at first birth showed a positive genetic correlation with lifespan in both sexes, especially in the full sample (0.36–0.40). Number of children was strongly genetically correlated with age at first birth (negatively, -0.59 to -0.76) and with age at last birth (positively, 0.87–0.92).
Our results differ from neighboring studies on related topics in that we directly estimated genetic correlations between reproductive traits and longevity in a large historical population. Unlike studies focusing on individual genes or cellular mechanisms, we showed that at the population level additive genetic variation only weakly links number of children to lifespan. This does not refute the disposable soma theory, but indicates that a simple resource-allocation trade-off is not the main genetic mechanism. A more important role may be played by shared genes influencing viability and reproductive schedule.
The field could move toward incorporating molecular genetic data, such as polygenic scores from genome-wide association studies, to test the reproducibility of the found correlations in modern populations. Also promising is studying how environmental conditions, such as nutrition, epidemics, and social norms, modify the genetic correlations between reproduction and survival. Comparisons with other historical populations in Europe and Asia will help understand how universal these patterns are.
The results are important for evolutionary biology, demography, and the epidemiology of aging, as they clarify the role of genetic factors in the trade-off between reproduction and longevity in humans.
The next step could be an analysis of genetic correlations accounting for socioeconomic status and regional differences, as well as including data on offspring health to assess intergenerational effects.
This work is directly connected to an unsolved problem in evolutionary genetics: why genetic correlations between fitness components are often weak or unstable, despite theoretical predictions. This undermines simple models of antagonistic pleiotropy and calls for more complex explanations involving environmental heterogeneity and pleiotropy through viability.
In the studied population, the heritability of number of children in men was 2.5 times higher than in women, which may reflect a greater influence of a man's hereditary qualities (e.g., resources or social status) on his reproductive success.
Not published on arXiv. Here are its page, the PDF and the formalization: you can check it yourself, not only read our account.