Beverly I. Strassmann

Contrasting patterns of Y chromosome and mtDNA variation in Africa: Evidence for sex-biased demographic processes

To investigate associations between genetic, linguistic, and geographic variation in Africa, we type 50 Y chromosome SNPs in 1122 individuals from 40 populations representing African geographic and linguistic diversity. We compare these patterns of variation with those that emerge from a similar analysis of published mtDNA HVS1 sequences from 1918 individuals from 39 African populations. For the Y chromosome, Mantel tests reveal a strong partial correlation between genetic and linguistic distances (r=0.33, P=0.001) and no correlation between genetic and geographic distances (r=−0.08, P>0.10). In contrast, mtDNA variation is weakly correlated with both language (r=0.16, P=0.046) and geography (r=0.17, P=0.035). AMOVA indicates that the amount of paternal among-group variation is much higher when populations are grouped by linguistics (ΦCT=0.21) than by geography (ΦCT=0.06). Levels of maternal genetic among-group variation are low for both linguistics and geography (ΦCT=0.03 and 0.04, respectively). When Bantu speakers are removed from these analyses, the correlation with linguistic variation disappears for the Y chromosome and strengthens for mtDNA. These data suggest that patterns of differentiation and gene flow in Africa have differed for men and women in the recent evolutionary past. We infer that sex-biased rates of admixture and/or language borrowing between expanding Bantu farmers and local hunter-gatherers played an important role in influencing patterns of genetic variation during the spread of African agriculture in the last 4000 years.

Life–history theory, fertility and reproductive success in humans

According to life‐history theory, any organism that maximizes fitness will face a trade‐off between female fertility and offspring survivorship. This trade‐off has been demonstrated in a variety of species, but explicit tests in humans have found a positive linear relationship between fitness and fertility. The failure to demonstrate a maximum beyond which additional births cease to enhance fitness is potentially at odds with the view that human fertility behaviour is currently adaptive. Here we report, to our knowledge, the first clear evidence for the predicted nonlinear relationship between female fertility and reproductive success in a human population, the Dogon of Mali, West Africa. The predicted maximum reproductive success of 4.1±0.3 surviving offspring was attained at a fertility of 10.5 births. Eighty‐three per cent of the women achieved a lifetime fertility level (7–13 births) for which the predicted mean reproductive success was within the confidence limits (3.4 to 4.8) for reproductive success at the optimal fertility level. Child mortality, rather than fertility, was the primary determinant of fitness. Since the Dogon people are farmers, our results do not support the assumptions that: (i) contemporary foragers behave more adaptively than agriculturalists, and (ii) that adaptive fertility behaviour ceased with the Neolithic revolution some 9000 years ago. We also present a new method that avoids common biases in measures of reproductive success.

Polygyny as a Risk Factor for Child Mortality Among the Dogon

The Dogon village of Sangui in the Malian Sahel had a human population of 460 in January 1988. 54% of the married men in the village had 1 wife 35% had 2 wives and 11% had 3 wives. Polygyny among the Dogon is strictly nonsororal and wives are either arranged or taken from another man. Ideally women do not live with their arranged husband until the birth of 2 children who will be raised by the maternal grandparents. The Dogon are an appropriate population in which to test for an adverse effect of polygyny upon female fitness because the interests of men are accorded higher priority than those of women in several important respects. Child mortality is the greatest burden upon Dogon women with 20% of children in the study village dying in their first year of life and 46% dying before reaching age 5 years. Findings are presented from a study of all 205 children aged 10 years and younger who resided in the village between 1986 and 1988. A re-census of the village in 1994 found that 20 children had left the village and were lost to follow-up and 9 children lived with widowed grandmothers. The effect of polygyny was subsequently tested upon the remaining final sample of 176 children. Analysis of the data found lower survivorship among children whose mothers were polygynously married especially if the mothers were first wives. The odds of death for Dogon children in polygynous work-eat groups were 7-11 times higher than for children in monogamous groups.

Sexual selection, paternal care, and concealed ovulation in humans

Abstract Changes in the social structure of early humans greatly enhanced the potential for paternal care to contribute to offspring success. Selection therefore favored females who mated with more paternal males. Since paternal care limits mating effort, males least successful as polygynists would have the most to gain by paternal behavior, while the successful polygynists would gain least. Concealed ovulation may have evolved because it promoted the paternal tendencies of the less polygynous males who advanced female reproductive success the most. Since the offspring of indulgent males would have a competitive advantage over the offspring of more polygynous males, and females revealing the time of ovulation would become increasingly scarse, all males would eventually pursue a reproductive strategy emphasizing paternal effort over mating effort. In nonhuman primates the most polygynous males mate selectively with females who are likely to be ovulating. Such males would probably not mate with females having diminished cues to the time of ovulation. The more paternally prone males could therefore consort with these females and experience a high confidence of paternity. Another characteristic of nonhuman primates is that the most successful polygynists tend to have a high dominance rank. Thus, female hominids who mated with more paternal males may have sacrificed having offspring with some of the genetic advantages that contribute to dominance. However, subsconscious physiological and psychological correlates of ovulation in humans may have tempted females to exploit infrequent, low-risk opportunities to mate outside the pair-bond with males of superior genetic fitness. These correlates may also promote conception irrespective of mating partner, or they may have helped females avoid rape.

The Evolution of Endometrial Cycles and Menstruation

According to a recent hypthesis, menstruation evolved to protect the uterus oviducts from sperm-borne pathogens by dislodging infected endometrial tissue and delivering immune cells to the uterine cavity. This hypothesis predicts the following: (1) uterine pathogens should be more prevalent before menses than after menses, (2) in the life histories of females, the timing of menstruation should track pathogen burden, and (3) in primates, the copiousness of menstruation should increase with the promiscuity of the breeding system. I tested these predictions and they were not upheld by the evidence. I propose the alternative hypothesis that the uterine endometrium is shed/resorbed whenever implantation fails because cyclical regression and renewal is energetically less costly than maintaining the endometrium in the metabolically active state required for implantation. In the regressed state. oxygen consumption (per mg protein/h) in human endometria declines nearly sevenfold. The cyclicity in endometrial oxygen consumption is one component of the whole body cyclicity in metabolic rate caused by the action of the ovarian steroids on both endometrial and nonendometrial tissue. Metabolic rate is at least 7% lower, on average, during the follicular phase than during the luteal phase in women, which signifies an estimated energy savings of 53 MJ over four cycles, or nearly six days worth of food. Thus, the menstrual cycle revs up and revs down, economizing on the energy costs of reproduction. This economy is greatest during the nonbreeding season and other periods of amenorrhea when the endometrium remains in a regressed state and ovarian cycling is absent for a prolonged period of time. Twelve months of amenorrhea save an estimated 130 MJ, or the energy required by one woman for nearly half a month. By helping females to maintain body mass, energy economy will promote female fitness in any environment in which fecundity and survivorship is constrained by the food supply. Endometrial economy may be of ancient evolutionary origin because similar reproductive structures, such as the oviduct of lizards, also regress when a fertilized egg is unlikely to be present. Regression of the endometrium is usually accompained by reabsorption, but in some species as much as one third of the endometrial and vascular tissue is shed as the menses. Rather than having and adaptive basis in ecology or behavior, variation in the degree of menstrual bleeding in primates shows a striking correlation with phylogeny. The endometrial microvasculature is designed to provide the blood supply to the endometrium and the placenta, and external bleeding appears to be a side effect of endometrial regression that arises when there is too much blood and other tissue for complete reabsortion. The copious bleeding of humans and chimps can be attributed to the large size of the uterus relative to adult female size and to the design of the microvasculature in catarrhines.

Inferring Human Population Sizes, Divergence Times and Rates of Gene Flow From Mitochondrial, X and Y Chromosome Resequencing Data

We estimate parameters of a general isolation-with-migration model using resequence data from mitochondrial DNA (mtDNA), the Y chromosome, and two loci on the X chromosome in samples of 25–50 individuals from each of 10 human populations. Application of a coalescent-based Markov chain Monte Carlo technique allows simultaneous inference of divergence times, rates of gene flow, as well as changes in effective population size. Results from comparisons between sub-Saharan African and Eurasian populations estimate that 1500 individuals founded the ancestral Eurasian population ∼40 thousand years ago (KYA). Furthermore, these small Eurasian founding populations appear to have grown much more dramatically than either African or Oceanian populations. Analyses of sub-Saharan African populations provide little evidence for a history of population bottlenecks and suggest that they began diverging from one another upward of 50 KYA. We surmise that ancestral African populations had already been geographically structured prior to the founding of ancestral Eurasian populations. African populations are shown to experience low levels of mitochondrial DNA gene flow, but high levels of Y chromosome gene flow. In particular, Y chromosome gene flow appears to be asymmetric, i.e., from the Bantu-speaking population into other African populations. Conversely, mitochondrial gene flow is more extensive between non-African populations, but appears to be absent between European and Asian populations.

Alternatives to the Grandmother Hypothesis

We conducted a meta-analysis of 17 studies that tested for an association between grandparental survival and grandchild survival in patrilineal populations. Using two different methodologies, we found that the survival of the maternal grandmother and grandfather, but not the paternal grandmother and grandfather, was associated with decreased grandoffspring mortality. These results are consistent with the findings of psychological studies in developed countries (Coall and Hertwig Behavioral and Brain Sciences 33:1-59, 2010). When tested against the predictions of five hypotheses (confidence of paternity; grandmothering, kin proximity, grandparental senescence, and local resource competition), our meta-analysis results are most in line with the local resource competition hypothesis. In patrilineal and predominantly patrilocal societies, the grandparents who are most likely to live with the grandchildren have a less beneficial association than those who do not. We consider the extent to which these results may be influenced by the methodological limitations of the source studies, including the use of retrospective designs and inadequate controls for confounding variables such as wealth.

Ecological Constraints on Marriage in Rural Ireland

Abstract Behavioral ecological studies of cooperatively breeding birds suggest that delayed dispersal and reproduction are caused by ecological constraints on independent breeding opportunities. Here we use census data on marriage and reproduction among the 19th and 20th century rural Irish to determine if the ecological constraints hypothesis can be extended to humans and what modifications might be required. We focus specifically on the following predictions: (1) marriage rates for farmers varied directly with the availability of farms; (2) the incidence of celibacy among male heirs increased as size of farm decreased; (3) emigration increased as economic opportunities in rural Ireland decreased; (4) emigration rates were inversely related to farm size; and (5) emigrants improved their chances for marriage by leaving Ireland. Despite important differences between humans and other species, we conclude that the rural Irish fall within the scope of ecological constraints theory. Unmarried siblings who remained on the home farm potentially gained some indirect fitness benefits because (1) the labor of unmarried siblings probably enhanced farm wealth; and (2) heirs of wealthier farms had higher reproductive success. The latter prediction implies that increased wealth, whether due to siblings or other causes, was reproductively valuable.

Cooperation and competition in a cliff-dwelling people

In animals that breed cooperatively, adult individuals will sometimes delay reproduction to act as helpers at the nest who raise young that are not their genetic offspring. It has been proposed that humans are also a cooperatively breeding species because older daughters, grandmothers, and other kin and nonkin may provide significant childcare. Through a prospective cohort study of childrens (n = 1,700) growth and survival in the Dogon of Mali, I show that cooperative breeding theory is a poor fit to the family dynamics of this population. Rather than helping each other, siblings competed for resources, producing a tradeoff between the number of maternal siblings and growth and survival. It did not take a village to raise a child; children fared the same in nuclear as in extended families. Of critical importance was the degree of polygyny, which created conflicts associated with asymmetries in genetic relatedness. The risk of death was higher and the rate of growth was slower in polygynous than monogamous families. The hazard of death for Dogon children was twofold higher if the resident paternal grandmother was alive rather than dead. This finding may reflect the frailty of elderly grandmothers who become net consumers rather than net producers in this resource-poor society. Mothers were of overwhelming importance for child survival and could not be substituted by any category of kin or nonkin. The idea of cooperative breeding taken from animal studies is a poor fit to the complexity and diversity of kin interactions in humans.

Religion as a means to assure paternity

The sacred texts of five world religions (Buddhism, Christianity, Hinduism, Islam, and Judaism) use similar belief systems to set limits on sexual behavior. We propose that this similarity is a shared cultural solution to a biological problem: namely male uncertainty over the paternity of offspring. Furthermore, we propose the hypothesis that religious practices that more strongly regulate female sexuality should be more successful at promoting paternity certainty. Using genetic data on 1,706 father–son pairs, we tested this hypothesis in a traditional African population in which multiple religions (Islam, Christianity, and indigenous) coexist in the same families and villages. We show that the indigenous religion enables males to achieve a significantly (P = 0.019) lower probability of cuckoldry (1.3% versus 2.9%) by enforcing the honest signaling of menstruation, but that all three religions share tenets aimed at the avoidance of extrapair copulation. Our findings provide evidence for high paternity certainty in a traditional African population, and they shed light on the reproductive agendas that underlie religious patriarchy.