Simon Chapman
Natural selection will favour traits that are associated with higher reproductive success in a population.
An individual’s reproductive success can be measured as biological fitness. Individuals can increase their fitness through their genes passing on to subsequent generations, most commonly achieved by having a child. This would increase an individual’s biological fitness by 0.5 as a parent shares an average 50% of its genes with their child.
In order to maximise fitness gains across the lifespan and therefore genetic contribution to the next generation, natural selection theoretically favours continued reproduction until death. Yet not every species continues to reproduce throughout life: one of the defining biological traits of humans is that women undergo menopause and continue to live for a long time, with an average woman expected to live well over a third of their adult life post-reproductively.
The existence of menopause and extended post-reproductive life is considered one of the enduring puzzles in evolutionary biology, but to properly understand how it may have evolved we first need to understand which species are menopausal. Is it a general trait of mammals taken to a higher gear by humans, or are we part of an exclusive club?
This question has been an ongoing topic in the literature on post-reproductive lifespan. One of the reasons that there has been some confusion is due to the use of data on captive populations. In captivity, animals are not exposed to the usual sources of selection (e.g. predation, starvation, diseases), so they can and often do live far longer than in the wild. They may also have accelerated reproduction in captivity. Though it may be argued that these species are ‘true’ menopausal species, if menopause and an extended post-reproductive lifespan are not found in the wild then they should not be considered as traits of the species, and even less so traits of evolutionary relevance (see e.g. Chapman et al. 2024a).
Even using menopause synonymously with the end of reproductive capability to broaden the taxonomic perspective (the majority of mammals do not menstruate and instead reabsorb the uterine lining), menopause and a long post-reproductive lifespan have recently been shown to be an exceptionally rare trait combination. Using wild populations living in natural environments, only a small number of toothed whales join humans in showing extended post-reproductive lifespan and menopause at the species-level.
Under the evidence-based current assumption that menopause and an extended post-reproductive lifespan are rare, the next question is then how did it evolve? There are two main pathways, assuming evolutionary selection: extending lifespan beyond reproductive lifespan (‘living longer’) or reproductive lifespan being shortened compared to an already long life (‘stopping early’). There is also the non-adaptive hypothesis that post-reproductive lifespan is simply due to modern medicine and better living conditions, though this cannot explain the presence of post-reproductive life in non-industrialised nor historical societies, nor in any menopausal toothed whale species.
Once again turning to comparative analysis of menopausal and closely-related non-menopausal species, there is more support for the ‘living longer’ pathway over the ‘stopping early’ one – in the toothed whales, menopausal species have comparable reproductive lifespans but far longer lifespans than non-menopausal species of similar body size (Ellis et al. 2024), and a similar pattern is found when comparing humans to other primates.
Family-related hypotheses tend to support an extension of lifespan rather than a shortening of reproductive capability. Here, the focus is not only on direct fitness (having children oneself) but also indirect fitness (aiding others in having children), with fitness gains calculated as the proportion of genes shared with the offspring. Post-reproductive grandmothers are hypothesised to be very important for the evolution of menopause and extended post-reproductive lifespan, with each grandchild sharing 25% of their genes with the grandmother.
By helping out, grandmothers could facilitate more grandchildren surviving to maturity or even more grandchildren being born. INVEST researchers have shown that grandmothers in contemporary society are important from a sociological perspective (e.g. Lehti et al. 2019; Helle et al. 2024), and that their importance extends back into Finland’s past from a more biological perspective (Chapman et al. 2024b).
While evolutionary selection from grandmothering is lessened in the present day, their help could be the difference between life and death back when child mortality was high; living longer could lead to more grandchildren surviving. However, though there is a wealth of evidence supporting selection on lifespan from grandmothering in humans and killer whales, the presence of grandmothering behaviours in a species does not mean that it is menopausal. For example, lion grandmothers provide milk to grandoffspring, but need to have recently reproduced to be able to lactate.
Within-family reproductive conflict is thought to be a reason for reproductive lifespan not to have increased alongside lifespan (Cant & Johnstone 2008). Reproduction uses resources, so when multiple women are co-reproducing, competition for limited resources can occur with potentially devastating effects on the children. Relatedness asymmetries, particularly when dispersal is female-biased, mean the biological fitness costs of competition are far greater to the older generation (loss of direct and indirect fitness) than to the younger generation (loss of direct fitness only).
On the other hand, by limiting reproduction, an increased lifespan affords more opportunities to help kin and potentially gain biological fitness. Support for this hypothesis comes from the two most-studied menopausal species (humans and killer whales).
It appears then that for menopause to evolve, multiple conditions need to be met. The help provided by grandmothers needs to increase biological fitness enough to select for a longer lifespan, and the costs of co-reproduction need to be great enough to select against an increase in reproductive lifespan. The puzzle of menopause is still yet to be fully solved though, as there can be other factors at play that have not been identified or investigated yet.
The good news is that we are closer than ever to being able to understand the evolution of one of the traits that makes us human. The comparative work coming from the toothed whales is a relatively recent and exciting development, and one that is greatly helping clarify how selection may have acted in our own evolutionary history.
Simon Chapman is a senior researcher at the INVEST Research Flagship Centre at the University of Turku. He holds a PhD in evolutionary biology, and his main research focus is currently on kin influences on life-course outcomes.
References:
Chapman SN, Ellis S, Lahdenperä M, Croft DP, Lummaa V. (2024a) Menopause has not evolved as a general trait in mammals: A response to “Do mammals have menopause?” BioRxiv, 2024.02.29.582687
Cant MA & Johnstone RA (2008) Reproductive conflict and the separation of reproductive generations in humans. PNAS, 105:5332-5336.
Chapman SN, Lummaa V. (2024b) Grandmother effects over the Finnish demographic transition. Evolutionary Human Sciences, 6: e6
Ellis S, Franks DW, Nielsen MLK, Weiss, MN, Croft DP (2024) The evolution of menopause in toothed whales. Nature, 627: 579-585
Helle S, Tanskanen AO, Coall DA, Perry G, Daly M, Danielsbacka M (2024) Investment by maternal grandmother buffers children against the impacts of adverse early life experiences. Scientific Reports, 14:6815
Lehti H, Erola J, Tanskanen AO (2019) Tying the extended family knot – Grandparents’ influence on educational achievement. European Sociological Review, 35:29-48
