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

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.

Human uniqueness? Life history diversity among small-scale societies and chimpanzees.

BACKGROUND: Humans life histories have been described as "slow", patterned by slow growth, delayed maturity, and long life span. While it is known that human life history diverged from that of a recent common chimpanzee-human ancestor some ~4-8 mya, it is unclear how selection pressures led to these distinct traits. To provide insight, we compare wild chimpanzees and human subsistence societies in order to identify the age-specific vital rates that best explain fitness variation, selection pressures and species divergence. METHODS: We employ Life Table Response Experiments to quantify vital rate contributions to population growth rate differences. Although widespread in ecology, these methods have not been applied to human populations or to inform differences between humans and chimpanzees. We also estimate correlations between vital rate elasticities and life history traits to investigate differences in selection pressures and test several predictions based on life history theory. RESULTS: Chimpanzees' earlier maturity and higher adult mortality drive species differences in population growth, whereas infant mortality and fertility variation explain differences between human populations. Human fitness is decoupled from longevity by postreproductive survival, while chimpanzees forfeit higher potential lifetime fertility due to adult mortality attrition. Infant survival is often lower among humans, but lost fitness is recouped via short birth spacing and high peak fertility, thereby reducing selection on infant survival. Lastly, longevity and delayed maturity reduce selection on child survival, but among humans, recruitment selection is unexpectedly highest in longer-lived populations, which are also faster-growing due to high fertility. CONCLUSION: Humans differ from chimpanzees more because of delayed maturity and lower adult mortality than from differences in juvenile mortality or fertility. In both species, high child mortality reflects bet-hedging costs of quality/quantity tradeoffs borne by offspring, with high and variable child mortality likely regulating human population growth over evolutionary history. Positive correlations between survival and fertility among human subsistence populations leads to selection pressures in human subsistence societies that differ from those in modern populations undergoing demographic transition.

The optimal timing of teaching and learning across the life course.

The evolutionary biologist W. D. Hamilton (Hamilton 1966 J. Theor. Biol.12, 12-45. (doi:10.1016/0022-5193(66)90184-6)) famously showed that the force of natural selection declines with age, and reaches zero by the age of reproductive cessation. However, in social species, the transfer of fitness-enhancing resources by postreproductive adults increases the value of survival to late ages. While most research has focused on intergenerational food transfers in social animals, here we consider the potential fitness benefits of information transfer, and investigate the ecological contexts where pedagogy is likely to occur. Although the evolution of teaching is an important topic in behavioural biology and in studies of human cultural evolution, few formal models of teaching exist. Here, we present a modelling framework for predicting the timing of both information transfer and learning across the life course, and find that under a broad range of conditions, optimal patterns of information transfer in a skills-intensive ecology often involve postreproductive aged teachers. We explore several implications among human subsistence populations, evaluating the cost of hunting pedagogy and the relationship between activity skill complexity and the timing of pedagogy for several subsistence activities. Long lifespan and extended juvenility that characterize the human life history likely evolved in the context of a skills-intensive ecological niche with multi-stage pedagogy and multigenerational cooperation. This article is part of the theme issue 'Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals'.

Periodic catastrophes over human evolutionary history are necessary to explain the forager population paradox.

The rapid growth of contemporary human foragers and steady decline of chimpanzees represent puzzling population paradoxes, as any species must exhibit near-stationary growth over much of their evolutionary history. We evaluate the conditions favoring zero population growth (ZPG) among 10 small-scale subsistence human populations and five wild chimpanzee groups according to four demographic scenarios: altered mean vital rates (i.e., fertility and mortality), vital rate stochasticity, vital rate covariance, and periodic catastrophes. Among most human populations, changing mean fertility or survivorship alone requires unprecedented alterations. Stochastic variance and covariance would similarly require major adjustment to achieve ZPG in most populations. Crashes could maintain ZPG in slow-growing populations but must be frequent and severe in fast-growing populations-more extreme than observed in the ethnographic record. A combination of vital rate alteration with catastrophes is the most realistic solution to the forager population paradox. ZPG in declining chimpanzees is more readily obtainable through reducing mortality and altering covariance. While some human populations may have hovered near ZPG under harsher conditions (e.g., violence or food shortage), modern Homo sapiens were equipped with the potential to rapidly colonize new habitats and likely experienced population fluctuations and local extinctions over evolutionary history.

Resource allocation as a driver of senescence: life history tradeoffs produce age patterns of mortality.

We investigate the effects of optimal time and resource allocation on age patterns of fertility and mortality for a model organism with (1) fixed maximum lifespan, (2) distinct juvenile and adult diets, and (3) reliance on nonrenewable resources for reproduction. We ask when it is optimal to tolerate starvation vs. conserve resources and then examine the effects of these decisions on adult mortality rates. We find that (1) age-related changes in tradeoffs partition the life cycle into as many as four discrete phases with different optimal behavior and mortality patterns, and (2) given a cost of reproduction, terminal investment can produce a signal of actuarial senescence. Also, given limitations imposed by non-replenishable resources, individuals beginning adult life with more replenishable resources do not necessarily live longer, since they can engage in capital breeding and need not defer reproduction to forage; low reproductive overheads and low costs of starvation also encourage capital breeding and may lead to earlier terminal investment and earlier senescence. We conclude that, even for species with qualitatively similar life histories, differences in physiological, behavioral and environmental tradeoffs or constraints may strongly influence optimal allocation schedules and produce variation in mortality patterns and life expectancy.

Contributions of covariance: decomposing the components of stochastic population growth in Cypripedium calceolus.

Although correlations between vital rates can have important effects on evolution and demography, few studies have investigated their effects on population dynamics. Here, we extend life-table response experiments (LTREs) to variable environments, showing how to quantify contributions made by (1) mean vital rates, (2) variability driven by environmental fluctuations, (3) correlations implying demographic trade-offs and reflecting stage transition synchrony, and (4) elasticities reflecting local selection pressures. Applying our methods to the lady's slipper orchid Cypripedium calceolus, we found that mean rates accounted for 77.1% of all effects on the stochastic growth rate, variability accounted for 12.6%, elasticities accounted for 6.6%, and correlations accounted for 3.7%. Stochastic effects accounted for 17.6%, 15.3%, and 35.9% of the total in our three populations. Larger elasticities to transitions between dormancy states and stronger correlations between emergence and survival suggest that one population was under greater pressure to remain active while the other two showed survival payoffs for dormancy in poor years. Strong negative correlations between dormancy, emergence, and stasis balanced opposing contributions, resulting in near stationarity in two populations. These new methods provide an additional tool for researchers investigating stochastic population dynamics and should be useful for a broad range of applications in basic ecology and conservation biology.

How does climate change influence demographic processes of widespread species? Lessons from the comparative analysis of contrasted populations of roe deer.

How populations respond to climate change depends on the interplay between life history, resource availability, and the intensity of the change. Roe deer are income breeders, with high levels of allocation to reproduction, and are hence strongly constrained by the availability of high quality resources during spring. We investigated how recent climate change has influenced demographic processes in two populations of this widespread species. Spring began increasingly earlier over the study, allowing us to identify 2 periods with contrasting onset of spring. Both populations grew more slowly when spring was early. As expected for a long-lived and iteroparous species, adult survival had the greatest potential impact on population growth. Using perturbation analyses, we measured the relative contribution of the demographic parameters to observed variation in population growth, both within and between periods and populations. Within periods, the identity of the critical parameter depended on the variance in growth rate, but variation in recruitment was the main driver of observed demographic change between periods of contrasting spring earliness. Our results indicate that roe deer in forest habitats cannot currently cope with increasingly early springs. We hypothesise that they should shift their distribution to richer, more heterogeneous landscapes to offset energetic requirements during the critical rearing stage.