Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Social science

Human reproductive assistance

What is the biological explanation for menopause, and for female survival beyond it? A study suggests that competition for help in ancestral societies may have been key to the evolution of this unusual human trait.

Humans stand out spectacularly from other species. We have language and cumulative culture, and we cooperate in large groups of unrelated individuals. We also have a distinctive life history, characterized by long juvenile dependence and menopause — the cessation of female reproductive function that occurs only about two-thirds of the way through the protracted adult lifespan. Recent research has examined how ancestral social structure and interaction networks may help to explain our cooperative tendencies1,2. According to a study by Mace and Alvergne3 published in Proceedings of the Royal Society, these social tendencies may also have contributed to the evolution of menopause, by channelling competition for assistance among women.

The saying goes that it takes a village to raise a child (Fig. 1). And, indeed, our ancestors evolved as cooperative breeders4,5, dependent on helpers for successful reproduction. In these circumstances, adults must weigh up the relative costs and benefits of themselves reproducing or acting as helpers. Kin helpers must decide which relative to help in order to most efficiently promote the spread of their shared genes, and non-kin helpers must consider how help might influence opportunities for mating or other benefits. Thus, the combination of kin and non-kin available to provide assistance influences the reproductive patterns in a community.

Figure 1: Competition breeds success.
figure1

Mace and Alvergne's study3 of demographic data from women (such as those shown here) in some Gambian villages shows that competition for assistance from kin and non-kin is a key contributor to female reproductive success, and may help to explain the evolution of menopause.

In most vertebrate cooperative breeders, such as meerkats or magpies, younger females forgo reproduction to help older females reproduce. In humans, however, the pattern is reversed. To assess whether competition for help among people may explain this profound difference, Mace and Alvergne studied historical demographic data (obtained between 1949 and 1975) from farming villages in Gambia. In these villages, extended families resided in a single compound, with males remaining in their birth compound and adult females moving to others to marry, a situation termed virilocality. It is reasonable to hypothesize that menopause evolved within a virilocal social system, because African apes also show a virilocal pattern of female dispersal and so, presumably, did our earliest human ancestors6. Even if this were not the case, we know that menopause has been maintained for thousands of years in a world of predominantly virilocal human societies, such that virilocality and menopause must be compatible under the pressure of natural selection.

There is an asymmetry of relatedness in virilocal societies, in which the older women of a compound are genetically related to the offspring of their son's wives, but younger immigrant women do not share genes with their mother-in-law's children. If women compete for the assistance that they can give each other, the asymmetry of relatedness to each other's offspring might explain why older women are most willing to forgo reproduction to help7. However, Mace and Alvergne's data analysis3 contradicts this hypothesis. They show that it is in fact the reproductive rate of older women that improves as the number of competing women in a compound increases, whereas reproduction in younger women declines.

A simple explanation for this trend could be that older women, whom Mace and Alvergne show are more closely related to other adults in the compound, have a greater influence on the distribution of goods and services. Yet when the authors analysed the data further to take into account mother–daughter pairs, they found the reverse trend, with an older woman's reproductive output decreasing when her daughter begins to reproduce. This effect occurs even if the daughter no longer lives in the same compound. Although the authors acknowledge that daughters often do not disperse far (staying within the same village, for example), such that dispersed individuals may still help each other, the complexity of findings returns the focus of menopause research to the previously popular idea of mother–daughter helping.

Under the 'grandmother hypothesis', menopause is theorized to have evolved mainly so that mothers would aid their own daughters' reproduction. This hypothesis stems from the idea that the greater food-provisioning capacity of older women in ancestral societies might have had sufficient impact on their daughters' fertility and grandchildren's survival to favour the evolution of reproductive cessation in order to make women available to help8. But although the helping effects of grandmothers are often statistically significant, studies show that they are probably not great enough to outweigh the loss of genetic contribution that could otherwise be attained through direct reproduction9. Furthermore, the grandmother hypothesis does not explain how menopause has been maintained in virilocal populations. Mace and Alvergne's finding that the effects of competition on reproductive success in overlapping generations extend to women who do not reside in the same household helps to resolve this potential inconsistency.

However, to understand how menopause is maintained in societies in which daughters disperse far away, other social interactions must be considered. Women in ancestral societies often lived with kin of both sexes1, such that reproductive-age females competed for subsidies offered by pair-bonded mates, kin of various ages and males hoping to entice future mating. Mothers and daughters were probably not each other's main food provisioners4, so an analysis of female reproductive success must also take into account help from others, especially provisioning males.

How do outside helpers choose where to invest their help? We suggest that the answer may come, perhaps surprisingly, from social insects. Some species of insects that live in colonies can detect an individual's relative fertility from the smell of pheromones and other chemical secretions10. They then adjust their behaviour, such that low-fertility females are not allowed to breed11 and low-fertility queens are replaced12 by more-fertile breeders. One species even shows the typical human pattern — all young colony females are reproductively active and then progress to a post-reproductive worker stage as they age13.

Perhaps similar responses evolved in ancestral human societies, and ageing females with detectably decreasing fertility were less favoured by helpers and potential investing mates in the social group. Withdrawal of food provisioning might then have amplified the age-specific decline in fertility from slight to extreme — a possible explanation for the precipitous decline of a woman's fertility with age, which occurs long before her children reproduce, and to an extent that is far more pronounced than the impact of daughters' reproduction, as measured by Mace and Alvergne. Under this scenario, evolutionary pressure would have favoured older females helping descendants, rather than trying to reproduce without help, thereby promoting the evolution and maintenance of menopause.

Although it is not yet definitively clear why menopause evolved, Mace and Alvergne's findings show that competition for help probably had a key role — another example of how complexity in ancestral human social structure was involved in the evolution of critical human traits. It is exciting to ponder on which other intriguing, and exceptional, aspects of human biology may be more completely understood by considering the social elements of our history.

References

  1. 1

    Hill, K. et al. Science 331, 1286–1288 (2011).

    CAS  ADS  Article  Google Scholar 

  2. 2

    Apicella, C. L., Marlowe, F. W., Fowler, J. H. & Christakis, N. A. Nature 481, 497–501 (2012).

    CAS  ADS  Article  Google Scholar 

  3. 3

    Mace, R. & Alvergne, A. Proc. R. Soc. B http://dx.doi.org/10.1098/rspb.2011.2424 (2012).

  4. 4

    Hill, K. & Hurtado, A. M. Proc. R. Soc. B 276, 3863–3870 (2009).

    Article  Google Scholar 

  5. 5

    Hrdy, S. B. Mother and Others: The Evolutionary Origins of Mutual Understanding (Harvard Univ. Press, 2009).

    Google Scholar 

  6. 6

    Chapais, B. Primeval Kinship: How Pair-Bonding Gave Birth to Human Society (Harvard Univ. Press, 2008).

    Google Scholar 

  7. 7

    Johnstone, R. A. & Kant, M. A. Proc. R. Soc. B 277, 3765–3771 (2010).

    Article  Google Scholar 

  8. 8

    Hawkes, K., O'Connell, J. F., Blurton Jones, N. G., Alvarez, H. & Charnov, E. L. Proc. Natl Acad. Sci. USA 95, 1336–1339 (1998).

    CAS  ADS  Article  Google Scholar 

  9. 9

    Hill, K. & Hurtado A. M. Ache Life History: The Ecology and Demography of a Foraging People (Aldine de Gruyter, 1996).

    Google Scholar 

  10. 10

    Liebig, J., Peters, C., Oldham, N., Marcstäder, C. & Hölldobler, B. Proc. Natl Acad. Sci. USA 97, 4124–4131 (2000).

    CAS  ADS  Article  Google Scholar 

  11. 11

    Cuvillier-Hot, V., Lenoir, A. & Peeters, C. Behav. Ecol. 15, 970–975 (2004).

    Article  Google Scholar 

  12. 12

    Seeley, T. D. Honeybee Ecology (Princeton Univ. Press, 1985).

    Google Scholar 

  13. 13

    Tsuji, K. Anim. Behav. 39, 843–849 (1990).

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Kim Hill or A. Magdalena Hurtado.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hill, K., Hurtado, A. Human reproductive assistance. Nature 483, 160–161 (2012). https://doi.org/10.1038/483160a

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing