Production and : History Strategies for Females in Humans and Other Ronald Lee Formal Demography workshop UC Berkeley, Dept of Demography June 7, 2017

Ronald Lee, UC Berkeley, June 7 2017 1 Lee’s articles on the of sociality and life histories

• Ronald Lee and Karen Kramer (2002) “Children’s Economic Roles in the Context of the Maya Family Life Cycle: Cain, • Chu, C. Y. and Ronald D. Lee. (2012) “Sexual Dimorphism and Caldwell, and Chayanov Revisited,” Population and : A Unified Economic Analysis,” Theoretical Development Review, 28 (3):475-499 (September 2002). Population . PMID: 22699007; PMCID: PMC3462896 http://dx.doi.org/10.1016/j.tpb.2012.06.002 • Lee, Ronald, Hillard Kaplan, and Karen L. Kramer (2002) “Children and Elderly in the Economic Life Cycle of the • Lee, Ronald D. and C.Y. Cyrus Chu (2012) “The Evolution of Household: A Comparative Study of Three Groups of Transfers and Life Histories,” Experimental Gerontology. Horticulturalists and Hunter-Gatherers,” paper prepared for PMID:22750486 PMCID:PMC3436974 the Annual Meeting of the Population Association of http://dx.doi.org/10.1016/j.exger.2012.06.004 America, May 9-11, 2002 in Atlanta, Georgia. • Lee, Ronald (2012) “Intergenerational transfers, the • Ronald Lee “Rethinking the Evolutionary Theory of Aging: biological life cycle and human society.” Population and Transfers, not Births, Shape in Social Species,” Public Policy: Essays in Honor of Paul Demeny, Supplement Proceedings of the National Academy of Sciences v.100, n. to Population and Development Review 38: 23–35. PMC ID: 16 (August 5, 2003), pp.9637-9642. PMID: 12878733; PMC3647612 PMCID: PMC170970 http://popcouncil.org/pdfs/PDRSupplements/Vol38_PopPub licPolicy/Lee_pp23-35.pdf • Chu, C.Y. and Ronald Lee (2006) “The co-evolution of intergenerational transfers and longevity: an optimal life • Chu, C. Y. and Ronald D. Lee. (2013) “On the Evolution of history approach. Theoretical Population Biology. Volume Intergenerational Division of Labor, and 69. Issue 2. March 2006. Pp. 193-201. PMID: 16406044; Transfers Among Adults and Offspring.” Journal of PMCID: 1513193 Theoretical Biology. 332: 171–180. http://www.pubmedcentral.nih.gov/articlerender.fcgi?tool http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3763024/ =pmcentrez&artid=1513193 • Ronald Lee (2014) “Intergenerational Transfers, Social • Lee, Ronald and Carl Boe (2007) “Intergenerational Arrangements, Life Histories, and the Elderly” in Maxine Transfers, Life Histories and the Evolution of Sociality,” Weinstein and Meredith A. Lane, Eds., Sociality, Hierarchy, paper prepared for Workshop on Sociality and Longevity, Health: Comparative Biodemography: Papers from a Azores, June 2007. (unpublished). Workshop (National Academies Press, Washington, D.C.) • Chu, C. Y. Cyrus, Hung-Ken Chien, and Ronald D. Lee (2008) • Chu, C. Y. Cyrus, Hung-Ken Chien, and Ronald Lee (2010) “Explaining the Optimality of U-Shaped Age-Specific “The Evolutionary Theory of Time Preferences and Mortality,” Theoretical Population Biology 73:2 (March Intergenerational Transfers.” Journal of Economic Behavior 2008), 171-180. PMID: 18178233; PMCID: 2291574; and Organization. 76:3, December 2010, pp. 451-464. PMID: doi:10.1016/j.tpb.2007.11.005 21218165; PMCID: 3014627 • Lee, Ronald (2008) “Sociality, Selection and Survival: simulated evolution of mortality with intergenerational transfers and food sharing.” PNAS. published May 5, 2008, 10.1073/pnas.0710234105 (Social Sciences). PMID: 18458325; PMCID: PCM2438215

Ronald Lee, EHBEA, London, 2016 2 Other literature referenced

• Hamilton WD (1966) The moulding • Howell N (2010) of senescence by . J Theor Biol 12:12–45. • Hill K, Hurtado AM (1996) Ache Life History: The and Demography of a Foraging People (Aldine De Gruyter, New York). • Kaplan H (1994) Evolutionary and wealth flows theories of fertility: Empirical tests and new models. Pop Dev Rev 20:753–791.

Ronald Lee, EHBEA, London, 2016 3 We take our human “life history traits” for granted, but they have evolved • General level of human fertility • Age at sexual maturity • Age at menopause • Range of investment in each child (“quality”) • Range of lengths of birth intervals • Prevalence of twinning • Number of births occurring at once • Monogamy? Polygyny? • Male contribution to child rearing • Length of life • Shapes of age schedules • Relative sizes of males and females

Ronald Lee, UC Berkeley, June 7 2017 4 Reproductive fitness is the ability of organism (or ) to get itself or its descendants into subsequent generations

One phenotype (the physical individual) has higher “reproductive fitness” than another if it is able to increase the frequency of its or descendants in subsequent generations. Life history theory is about how different traits and collections of traits influence reproductive fitness, and why specific bundles of traits have evolved. Natural selection results from differences in reproductive fitness. I will discuss some aspects of life history theory relevant to fertility. Nontechnical, but the references given earlier give mathematical details.

Ronald Lee, UC Berkeley, June 7 2017 5 Stephen Stearns, The Evolution of Life Histories, 1992:23. “Demography, the key to life history theory, allows us to calculate the strength of selection on life history traits for many conditions.”

For example, does natural selection act more strongly on fertility at younger or older ages? On mortality at younger or older ages? By how much?

But…it is easy to overstate the relevance of demography by itself (which Stearns would never do).

Consider the following line of analysis, the calculation of fitness sensitivities based on pure demography, following on Hamilton (1966).

Ronald Lee, UC Berkeley, June 7 2017 6 I. The pure demography story ω −rx Lotka’s Equation for stable growth rate, r: 1= ∫ e l( x) m( x) dx 0 How sensitive is intrinsic growth rate r to a perturbation δ(a) in mortality Fa at age a? Differentiate and solve. dr = ( ) daδ A ( ) f • The effect on r is proportional to remaining expected net fertility above age a, F(a) (1.0 at reaching sex maturity, declining to 0 with age), and

inversely proportional to mean age of childbearing, Af. • The force of selection against mortality at age a will be proportional to F(a)/Af according to Hamilton (1966). • Strong selection against mortality before sexual maturity, declining selection until menopause, and zero selection after menopause, with rapid increase. Classic theory of why we senescence, become disabled etc. Ronald Lee, UC Berkeley, June 7 2017 7 Similar analysis says force of selection for higher fertility at age a is proportional to l(a), the proportion of births surviving to age a.

If this analysis were correct, natural selection would always be tending to raise fertility.

In this case, humans would be pathetically unevolved as a species.

A grey grouper fish, laying 380 million eggs per year, or orchids, producing many millions of seeds, each weighing < one millionth of a gram, would be vastly superior to humans with a TFR of 4 to 6 (pre-contact hunter gatherers) or some dung with TFR=6.

Ronald Lee, UC Berkeley, June 7 2017 8 Dung beetles – over 5000 species; some have TFR=6. Some mate for life; some have parental care.

Ronald Lee, UC Berkeley, June 7 2017 9 • The analysis is misleading for fertility, as Hamilton realized.

• Here is Lotka on the importance of fertility in population dynamics:

Ronald Lee, UC Berkeley, June 7 2017 10 Alfred Lotka (1925), Elements of Physical Biology, p.129

“The equation … expressing the rate of growth of the species in terms of the birth rate and rate, while it renders correctly the quantitative relations, … is open to misinterpretation. …it might be taken to imply that growth of an aggregate of living organisms takes place by births of new individuals into the aggregate. This, of course, is not the case. The new material enters the aggregate in another way, namely in the form of food consumed by the existing organisms. Births and the preliminaries of procreation do not in themselves add anything to the aggregate…. The final result may not depend very greatly on the number of births….”

Ronald Lee, UC Berkeley, June 7 2017 11 Illustration of why differentiating the accounting identity (Lotka equation) can be highly misleading: For birds, the number of fledglings is not monotonic in number of eggs.

Ronald Lee, UC Berkeley, June 7 2017 12 Many experiments with artificial manipulation of clutch size; from Evolution by Stephen Stearns and Rolf Hoekstra (Oxford, 2000) • Why increasing clutch size did not raise reproductive fitness • Weight of fledglings was reduced in 68% of studies • Survival to next breeding season was reduced in 53% • Weight of parents was reduced in 41% • Survival of parents to next breeding season was reduced in 36% • Future reproduction of parents was reduced in 57% • Future reproduction of offspring from larger clutches was reduced in every case measured. • These are reasons beyond simple number of fledglings, explaining why the observed model clutch size is less than the one maximizing fledglings in chart.

Ronald Lee, UC Berkeley, June 7 2017 13 Evolutionary influences on fertility are much more complex • Understanding requires insights from • Demography • Anthropology • Economics • Sociology • Various branches of Biology

Ronald Lee, UC Berkeley, June 7 2017 14 In economic-demography, the quantity- quality tradeoff • In simple form, parents choose a total amount to invest in having children, say C. • They then choose how to allocate C between number of offspring, N, and quality per offspring, Q, with C=NQ

• However, effects of quantity clearly go far beyond Q-Q tradeoff; there are many more potential consequences of varying quantity, for health and survival of parents, for example.

Ronald Lee, UC Berkeley, June 7 2017 15 II. Life history theory with energy included (food) Here is one analytic setup. This approach is called “optimal life history”. • Organism is “born” with some initial state, e.g. body size. • At each age it acquires energy through foraging (hunting, grazing, , photosynthesis, etc.) according to a function of body size. • At each age it allocates this energy to three uses (budget constraint) • Survival • Fertility • Body growth (which then affects future energy acquisition) • Find the allocation at each age among these three that maximizes reproductive fitness, and characterize the resulting life history. • Solution by dynamic optimization. See e.g. papers by Chu and Lee.

Ronald Lee, UC Berkeley, June 7 2017 16 One simple but powerful result

• If the budget constraint is linear (fixed energy cost per birth, per reduction in age specific mortality, and per unit body growth) then the optimal solution will be: • First invest in growth and survival (with zero fertility) until some specific age; • Then invest in survival and fertility (with no further growth). • This corresponds approximately to a “determinate growth” life history, like most mammals and birds, but unlike most fish and plants. • Actual dichotomy is not perfect; human adolescents may grow somewhat after reaching sexual maturity etc., but basic story is correct. • Cognitive development, and knowledge, and skills may continue to grow, complicating the story. • With “indeterminate growth” organism allocates energy to all three uses from the start.

Ronald Lee, UC Berkeley, June 7 2017 17 III. Evolution of downward intergenerational transfers to offspring, continuing parental care.

• The self-sufficient individuals just described (without intergenerational transfers after birth) have limited life history options. • Constrained at all times by the food energy they themselves can acquire. • Allocate energy among growth, survival, reproduction • Postponing reproduction to invest in growth and development risks death with no descendants. • Self-sufficiency may severely limit life history options. • Self-sufficient organism might raise fitness if had access to a credit market • Could borrow to invest in growth, development (brain size?) and survival (Armor?) • Could repay loan during highly productive adult years • Would this raise fitness? Only for some species. This depends on • interest rate on loan • marginal fitness value of investment in growth and development. • Like question today of whether a young adult should borrow to pay for college, or go straight to labor market. • But pure fantasy, because there are no financial institutions in nature.

Ronald Lee, June 2017, University of Montreal 18 But downward intergenerational transfers (adults to offspring) are similar to credit market in nature • Young receive transfers of food and care from parents, make similar transfers to each of their offspring as adults • “Rate of interest” (amount invested in all offspring relative to amount received) is higher if: • Fertility is higher (more offspring to raise) • Survival to reproductive maturity is lower (about 50% in human; 1/400,000,000 for grey grouper fish) • Longer life raises adult years for payback period and reduces amount to be repaid. • For some species in some circumstances, intergenerational transfers and longevity co-evolve given appropriate preconditions. • Self-reinforcing upward spiral of transfers and longevity. • Increased investment per offspring will also go with fewer offspring, lower fertility.

Ronald Lee, June 2017, University of Montreal 19 • One puzzle: Why do humans and toothed whales have long survival after menopause? (postreproductive survival) • No more direct reproduction, so Hamilton analysis predicts explosive mortality after menopause. • However, post-reproductive individuals continue to feed and assist their young offspring and grand offspring. • These intergenerational transfers continue to raise their own reproductive fitness, so continued survival is selected (kin selection). • This is also the “grandmother hypothesis” in anthropology (Hawkes et al) that highlights important role of Hadza grandmothers in providing food for their descendants. • Roles of grandmothers vs grandfathers are controversial, but implications are same.

Ronald Lee, UC Berkeley, June 7 2017 20 Intergenerational transfers to kids in humans

• Costly development of brain dictates slow body growth, late maturation, long nutritional dependency. • At some ages, brain development costs up to 70% of caloric intake of human children. • Reproduction requires • Massive intergenerational transfers from adults to children • Male participation • Cooperative breeding and social sharing including non-kin • Hunter-gatherers invest 10-13 years of per capita consumption to achieve one child surviving to maturity (calculated for Ache, Piro, Macheguenga hunter-gatherer groups; Kaplan, 1994; Lee, Kaplan, Kramer).

Ronald Lee, June 2017, University of Montreal 21 Per Capita Consumption and Labor Income of Hunter-Gatherer Groups, average of Amazon Basin and Botswana (divided by average labor income at ages 30-49) 1.2 49

- 1.0

0.8 Even elderly produce Breakeven surplus for kids 0.6 at age 20

0.4 Hunter gatherer consumption Hunter-gatherer group: 0.2 Hunter gatherer labor income Ache, Piro, Macheguenga, !Kung Per Capita Value / Avg. Labor / Avg. Income Capita Per 30 Value 0.0 Source: Calculated from data in 0 10 20 30 40 50 60 70 80 90 Kaplan, 1994; Howell, 2010. Age Ronald Lee, June 2017, University of Montreal 22 IV. Evolution of cooperative breeding and social sharing

Heavy intergenerational transfers and extended parental care create new vulnerabilities leading to new advantages for social sharing (Lee, 2008) 1. Parental death entails death of dependent offspring. For humans with 18- 20 year child dependency, this is a huge risk and inefficiency. • This creates big payoff to any form of life insurance providing for continued care after parental death. • Sharing food and care in broader social groups including non-kin can provide a form of life insurance. • Limitation of food sharing: sometimes other adults kill the children of a dead mother or father, to avoid the costs of supporting them (Hill and Hurtado, 1994)

Ronald Lee, June 2017, University of Montreal 23 2. The Chayanov Ratio over the family lifecycle: Consumers/Workers. The “lifecycle squeeze”. Ratio doubles during the “squeeze”. (Here Ukrainian peasants; hunter-gatherer life cycle gives similar result.) Dependency burden varies systematically over human life history, with consumers per producer in families doubling after 15 or 20 years of childbearing (Chayanov effect). Inefficient.

Randomness of birth and death lead to additional variations in individual social units.

Living in larger social groups smoothes out these variations so the age structure and dependency ratio are closer to their stable values. A. V. Chayanov, The Theory of Peasant Economy, Ch. 1, Figure 1-1; early 20th century.

Ronald Lee, June 2017, University of Montreal 24 But social sharing with non-kin in turn shapes the evolution of life histories (lessons from micro-simulations, Lee 2008) • With food sharing and life insurance, parental survival matters less, so selection for survival is weakened--including postreproductive survival. • Likelihood of having surviving offspring or grandoffspring to care for is raised, strengthening selection for postreproductive survival. • With food sharing an individual’s high fertility has less negative impact on other offspring so higher fertility is selected (Free Riding). • In groups of close kin, when an offspring dies the resources that would have been devoted to its future care are recaptured by surviving kin and promote their fitness. • Death of an infant is not very costly, but death of an older offspring is costly—fewer future costs to be recaptured. • Partly for this reason child mortality has a strong downward age gradient and is higher in close kin groups than when there is less sharing.

Ronald Lee, June 2017, University of Montreal 25 V. Production and reproduction – female specialization across species (Lee and Chu, 2016 in process) In most species, females continue to reproduce from sexual maturity until death. • Typically they continue to forage to acquire food throughout their as well. • Typically the male does not contribute food, but in some species (some birds, humans, owl monkeys, grey lemurs) he does. • Chimpanzees, a close relative of humans, are an example. • One birth at a time • Longish birth intervals of around 6 years. • Do not feed offspring after weaning. • Mother acquires all her own food, including while pregnant and lactating.

Ronald Lee, UC Berkeley, June 7 2017 27 V. Production and reproduction – female specialization across species (Lee and Chu, 2016 in process) • Might further efficiency gains be possible through female specialization in fertility or production (foraging)? • Suppose there are increasing returns to scale in reproduction (perhaps in bearing offspring, or in lactation, or other aspects of care besides foraging). • Costs of reproduction include • Growing and maintaining internal reproductive organs • Competing for mate or choosing mate • Reduction in foraging efficiency while pregnant or lactating (mammals) • Time costs of guarding dependent young • Efficiency cost of organism designed both for foraging and reproduction • Perhaps there are gains to concentrating fertility in some females while other females are producers rather than reproducers.

Ronald Lee, UC Berkeley, June 7 2017 28 Examples of options in nature

1. Chimpanzees and most other species mix fertility and foraging throughout their lives, with long (6 year) birth intervals and only one dependent offspring at a time. 2. Humans concentrate reproduction in the first half of the adult life cycle, and concentrate production in the second half, so that only some fraction of females are actually reproductive at any time. • Menopause • Birth intervals that are half or two thirds of Chimps • Several dependent offspring at a time • Requires extensive help from kin and non-kin as described. • Specialization within the life cycle of each female.

Ronald Lee, UC Berkeley, June 7 2017 29 (continued) 3. African wild dogs (similar to wolves, naked mole rats, some ants…) • One alpha female reproduces and lactates up to 70 pups per year • Other females are hormonally suppressed, do not reproduce, and join males in hunting. • Single pair of wild dogs is not able to reproduce; hunting requires larger group. • Specialization is among somatically identical females, one of whom dominates others, but other females have chance of becoming alphas themselves. 4. Eusocial insects (bees, ants, termites), here honey bees • One queen has been fed specially since larval stage and is completely specialized in reproduction following maiden flight to be inseminated. • Other females (could be up to 70,000) are workers: brood care, forage, guard, etc. They are genetically similar to queen but somatically different due to her special feeding with royal jelly.

Ronald Lee, UC Berkeley, June 7 2017 30 And economies of scale in production interact with economies of scale in reproduction • This interaction of scale economies determines the size of group, e.g. hive for honey bees, or cooperating group of wild dogs, or sharing group for humans. • For details, see math model in abstract of Lee and Chu (2016) paper which is in progress. • Idea is to vary two parameters in the model to generate the cases of chimpanzees, humans, African wild dogs, and eusocial insects.

Ronald Lee, UC Berkeley, June 7 2017 31