The importance of elders: Extending Hamilton’s force of selection to include intergenerational transfers

Abstract

In classical evolutionary models, the force of natural selection diminishes with age toward zero by last reproduction. However, intergenerational resource transfers and other late-life contributions in social species may select for postreproductive longevity. We present a formal framework for estimating indirect fitness contributions via production transfers in a skills-intensive foraging niche, reflecting kinship and cooperation among group members. Among contemporary human hunter-gatherers and horticulturalists, indirect fitness contributions from transfers exceed direct reproductive contributions from before menopause until ages when surpluses end, around the modal age of adult death (∼70 y). Under reasonable assumptions, these benefits are the equivalent to having up to several more offspring after age 50. Despite early independence, minimal production surplus, and a shorter lifespan, chimpanzees could theoretically make indirect contributions if they adopted reliable food-sharing practices. Our results for chimpanzees hypothetically adopting hunter-gatherer subsistence suggest that a skills-intensive foraging ecology with late independence and late peak production could select for human-like life histories via positive feedback between longevity and late-life transfers. In contrast, life history changes preceding subsistence shifts would not favor further life extension or subsistence shifts. Our results formalize the theory that longevity can be favored under socioecological conditions characterized by parental and alloparental care funded through transfers of mid- to late-life production surpluses. We also extend our analysis beyond food transfers to illustrate the potential for indirect fitness contributions from pedagogy, or information transfers. While we focus mostly on humans, our approach is adaptable to any context or species where transfers can affect fitness.

Apolipoprotein- ε 4 is associated with higher fecundity in a natural fertility population

“…Finally, the negative impacts of the APOE- ε 4 allele at older ages may have played an important role in its selection. We have documented that older age individuals play an important role in subsidizing the food supply of children and grandchildren, both among the Tsimane and other subsistence populations ( 53 , 54 ). This raises the intriguing possibility that the evolution of the APOE- ε3 allele may be related to brain expansion and the maintenance of cognitive abilities and subsistence productivity in old age.…”

“…The lower risk of cognitive decline in APOE- ε 2 and APOE- ε 3 carriers suggests a testable hypothesis that older individuals could support the fertility of their descendants. Given that multigenerational resource flows are common in subsistence populations, increased investment in descendent kin due to later survival of APOE- ε 2 carriers ( 53 , 54 ) could potentially have offset the higher fertility of APOE- ε 4 carriers. Other populations living under high infectious load should be evaluated for direct association of APOE- ε 2 with fecundity.…”

No time to die: Evolution of a post‐reproductive life stage

“…Extensive discussions of this hypothesis have been published (see Peccei, 2001b;Sear & Mace, 2008) with some studies suggesting that grandmothering has been a key component to extending human longevity (Chan et al, 2016;Kim et al, 2012Kim et al, , 2014. This idea requires a very particular form of social structure to work, with limited dispersal of kin, significant post-natal parental care, and the presence of overlapping generations in which intergenerational transfer of resources can occur (Davison & Gurven, 2022;Hooper et al, 2015;Kaplan & Robson, 2002). There are two interlinked grandmother hypotheses relating the evolution of sterility to the duration of the post-reproductive stage: (1) that because the fitness benefits of producing children decline with maternal age due to somatic ageing, the indirect fitness benefits of helping rear grandchildren eventually outweigh the direct fitness effects from producing 'own' children leading to the evolution of a sterile life stage that allows more resources to be devoted to grandchildren; (2) that while age-related sterility itself arises for other reasons, prolonged survival of postreproductive females has been favoured because of the additional inclusive fitness gains from helping more grandchildren survive, given that continued reproduction is not possible.…”

“…Indeed in African lions, grandmothers can only help via lactation if they have a cub themselves (Packer et al., 1998). For a state of permanent sterility to evolve under the first hypothesis, continued reproduction in old age needs to carry substantial fitness costs (Davison & Gurven, 2022), such as those produced by intergenerational conflict between kin (see Section Avoidance of intergenerational competition (or the reproductive conflict hypothesis) below). Central to the grandmother hypothesis is that grandmothers gain more fitness benefits investing in grand‐offspring while in a post‐reproductive state in comparison with what they would be able to do at the same age had they continued to reproduce themselves.…”

The importance of age‐specific gene expression

“…One can anticipate that there will be different parts of these pathways under different control (Gomez‐Verjan et al, 2018). Most of these differences were likely to provide selective advantage for their carriers to have been maintained during the course of our evolution (Davison & Gurven, 2022).…”