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Home , Demographic history, Genetic diversity, Recent human evolution

The great expansion

Brenna M. Henna, L. L. Cavalli-Sforzaa,1, and Marcus W. Feldmanb,2 aDepartment of , Stanford University School of Medicine, Stanford, CA 94305; and bDepartment of , Stanford University, Stanford, CA 94305-5020

Edited by C. Owen Lovejoy, Kent State University, Kent, OH, and approved September 25, 2012 (received for review July 19, 2012)

Genetic and paleoanthropological evidence is in accord that today’s human population is the result of a great demic (demographic and geographic) expansion that began approximately 45,000 to 60,000 y ago in Africa and rapidly resulted in human occupation of almost all of the Earth’s habitable regions. Genomic data from contemporary suggest that this expansion was accompanied by a continuous loss of , a result of what is called the “serial founder effect.” In addition to genomic data, the serial founder effect model is now supported by the genetics of human parasites, morphology, and linguistics. This particular population history gave rise to the two defining features of in humans: from the substructured populations of Africa retain an exceptional number of unique variants, and there is a dramatic reduction in genetic diversity within populations living outside of Africa. These two patterns are relevant for medical genetic studies mapping to and for inferring the power of in human history. It should be appreciated that the initial expansion and subsequent serial founder effect were determined by demographic and sociocultural factors associated with hunter-gatherer populations. How do we reconcile this major demic expansion with the population stability that followed for thousands years until the inventions of ? We review advances in understanding the genetic diversity within Africa and the great human expansion out of Africa and offer hypotheses that can help to establish a more synthetic view of modern human .

human | hunter-gatherer demography |

enetic data indicate that, Eurasia. It is unclear what precipitated the to only 450 individuals). It is generally approximately 45 to 60 kya, tremendous population growth associated assumed that the bottleneck occurred as G a very rapid population expan- with this second occupation of the Near a small group(s) with an effective pop- sion occurred outside of Africa, East and subsequent dispersal (7); possi- ulation size of only approximately 1,000 to and spread in all directions across the bly, cultural advances accumulated to 2,500 individuals moved from the African Eurasian continents, eventually populating a “tipping point” that supported extreme continent into the Near East. It should the entire world. We dub this event the demographic growth (8), or anatomical be noted that effective population sizes Great Expansion (Fig. 1). The precise changes that are not reflected in the will generally be less than census pop- location of the exit from Africa, and the paleoanthropological record [e.g., neuro- ulation sizes, especially under relative timing of the southern coastal anatomy (9)] occurred in the ancestral and recolonization (19). migration vs. the expansion into northern population. The geographic range ex- The loss of genetic variation during Eurasia, are still under intense debate pansions of humans outside of Africa were the Great Expansion is assumed to have (1–3). However, as we discuss here, many almost certainly associated with climatic resulted from the way the world was settled parameters of the Great Expansion are fluctuations (10); however, the Great by hunter-gatherer groups that, after now well understood, including the gen- Expansion was an unprecedented demic colonizing a new habitat and expanding eral timing of the exit, the magnitude of success that occurred when the climate there, shed small groups that founded new the associated bottleneck, and the mode remained substantially colder than the colonies nearby. This genetic sampling of subsequent expansion. We review the previous interglacial. As discussed later, process led to the successive reduction of history of the Out of Africa (OOA) we know that the ancestral population for variation in the newly founded colonies, expansion, with an emphasis on recent this expansion was African, but the rate with the reduction being proportional to genomic data, and highlight future of growth and structure of the ancestral the number of founders. A set of 52 pop- avenues of research. population remain poorly understood. ulations from all continents [the Human It is important first to distinguish An enormous wealth of genetic in- Genetic Diversity Panel (20) has been between the presence of early near-modern formation about many populations has studied with two large sets of markers: humans in the Near East and the very been generated in the century since the 784 (21, 22) and 650,000 distinct OOA exit associated with the discovery of blood groups (11). The SNPs (23)]. In a single reasonably - fi Great Expansion. It is clear that anatom- de ning genetic feature of populations geneous population, genetic diversity of ically near-modern humans occupied the historically residing outside of Africa is the biparentally transmitted DNA can be Levant (4) during a warm interglacial tremendous reduction in genetic diversity assessed efficiently by counting hetero- period 130 to 80 kya, when this region was compared with populations residing in zygotes for all variants. The pattern ecologically similar to northeastern Africa sub-Saharan Africa. Recent studies of of average heterozygosities of today’s (5). However, current evidence indicates autosomal polymorphisms are remarkably populations suggest that, during the Great that this near-modern population did not consistent in demonstrating the loss of persist in the Near East and was sub- diversity in OOA populations and in esti- sequently replaced by during mates of the parameters of this bottleneck – Author contributions: B.M.H., L.L.C.-S., and M.W.F. designed the following glacial period, with little (12 17) [also demonstrated clearly in the research, performed research, analyzed data, and wrote the evidence of temporal overlap (5, 6). It is phylogenetic patterns of mtDNA and paper. not until at least 50,000 y ago that evi- Y-chromsomal variation (18)]. Resequenc- The authors declare no conflict of interest. dence of behaviorally modern humans ing studies have estimated the ancestral This article is a PNAS Direct Submission. occurs in the archaeological record in effective population size at 12,800 to 1Present address: Faculty of Philosophy, Universita Vita-Salute the Near East. Only after this point do 14,400, with a 5- to 10-fold bottleneck San Raffaele, 20132 Milano, Italy. anatomically and behaviorally modern beginning approximately 65,000 to 50,000 y 2To whom correspondence should be addressed. E-mail: human remains become widespread in ago (although see ref. 15 for a bottleneck [email protected].

17758–17764 | PNAS | October 30, 2012 | vol. 109 | no. 44 www.pnas.org/cgi/doi/10.1073/pnas.1212380109 Downloaded by guest on September 30, 2021 PERSPECTIVE

15Kya

45Kya 35-40Kya

50-60Kya

45Kya

60-100Kya Founder effect Source of founder effect Migration path

Fig. 1. Ancient dispersal patterns of modern humans during the past 100,000 y. This map highlights demic events that began with a source population in southern Africa 60 to 100 kya and conclude with the settlement of South America approximately 12 to 14 kya. Wide arrows indicate major founder events during the demographic expansion into different continental regions. Colored arcs indicate the putative source for each of these founder events. Thin arrows indicate potential migration paths. Many additional migrations occurred during the (11).

Expansion, there was a continuous de- of several genomes indicated 1% to 7% and the successful expansion of humans crease of genetic diversity with geographic differential archaic admixture among ∼100,000 y later has been the subject of distance from the place of origin in Africa populations outside of Africa (32, 33). intense paleoanthropological debate. (this takes account of the likely path of Importantly for the serial founder effect Genetic data can directly address the time migration over land). The linear correla- theory, a limited amount of archaic ad- and rate of population growth in the tion between loss of genetic diversity and mixture does not destroy our power to African ancestral population; however, geographic distance from the origin of detect a serial founder migration of the despite recent interest in this topic, cur- expansion in Africa is close to 90%. kind modeled for humans (24, 25). rent analyses are extremely limited and The Great Expansion is thus consistent Archaic admixture of 10% or greater produce conflicting results. with serial colonization and concomitant would produce a discontinuous relation- Assuming a single step model of pop- loss of genetic heterozygosity, a process ship between heterozygosity and distance ulation growth and with full called a serial founder effect (Fig. 2) and inflate long-range linkage disequilib- sequence data from one western African (21, 24, 25). A serial founder effect model rium measures (24). population (Yoruba), Gravel et al. (16) involves three explicit assumptions. First, The third assumption is that there have estimated a doubling in effective pop- migration after the initial founder expan- been no dramatic postexpansion bottle- ulation size from approximately 7,000 to sion was sufficiently limited that the pop- necks that differentially affected pop- 14,000 that occurred 150 kya. Their model, ulations in the series did not reach ulations from which the serial migration however, did not separately account for demographic equilibrium. This assump- began. If the source population for the more recent episodes of western African tion appears warranted by the detectable expansion suffered a severe bottleneck population growth that likely occur 30 to substructure among continental and sub- that reduced its genetic diversity, we should 40 kya and again at 5 kya (associated continental populations throughout the see a poorer linear fit to the decline of with the adoption of agriculture and globe (Fig. 1) (22, 23, 26–28). Second, the heterozygosity with distance from Africa, subsequent expansion of Bantu-speaking serial founder populations migrated into or erroneously assign a population with agriculturalists) (38–41). Allowing for virgin territory or had no substantial higher genetic diversity as the source multiple episodes of population growth admixture with other resident, and pre- population. It is this third assumption we in the model would likely reduce the time sumably divergent, populations. In the believe deserves additional consideration. of initial growth from 150 kya to a more context of , admixture recent estimate. In stark contrast, recent could potentially occur between humans Human Origins in Africa coalescent analysis of full genomic hap- and Neanderthals or other archaic . The African fossil record is consistent with lotypes within Yoruban individuals (17) Ancient DNA from and a gradual accumulation of anatomically estimates an effective population maxi- Denisova specimens remain subject to modern osteological features during 200 mum occurring 50 to 150 kya, followed mixed interpretations. Ancient DNA to 50 kya (34–37). By 195 to 160 kya, the by bottleneck from which they begin to sequences suggest that these hominin Omo and Herto skulls from Ethiopia recover 40 kya. Two eastern African ge- species were highly diverged from the closely anticipate the form of contemporary nomes from the Luhya and Maasai show ancestors of modern humans, more than humans, although they tend to be more an identical signal to the Yoruba, sup- 400 kya (29), and their unique haploid robust overall. Multiple near-modern pop- porting a bottleneck model for all human mtDNA and Y- signatures ulations were present across the African populations between approximately 60 to are not present among any modern continent at that time. This delay between 30 kya, whereby African populations ex- humans (30, 31). On the contrary, analysis the origin of the modern anatomical form perience a modest bottleneck and non-

Henn et al. PNAS | October 30, 2012 | vol. 109 | no. 44 | 17759 Downloaded by guest on September 30, 2021 A third analysis (49) of variation in Eastern Pygmies and farmers estimated a divergence time between these groups that was statistically similar to those found by using DNA sequence and mtDNA data. In addition to the time of population growth, population substructure within Africa is important for fully understanding the OOA migration (50). Relative to populations outside of Africa, contemporary African populations retain an enormous amount of genetic variation. Furthermore, the genetic variation varies substantially from region to region as a result of the relatively deep substructure within Africa. Studies of patterns of autosomal DNA polymorphisms in present-day African hunter-gatherers show that they maintain exceptionally high genetic diversity, and several of these groups (e.g., KhoeSan, Hadza, Sandawe, Forest Pygmies) were the first to diverge from the ancestors that Genetic Diversity went on to become the larger agricultural groups in Africa and all populations outside Africa (27, 46, 51). In particular, the speakers of southern or Fig. 2. Schematic of a serial found effect. We illustrate the effect of serial founder events on genetic diversity “ ” in the context of the OOA expansion. Colored dots indicate genetic diversity. Each new group outside of Africa click languages (sometimes referred to represents a sampling of the genetic diversity present in its founder population. The ancestral population in as bushmen) show the greatest Africa was sufficiently large to build up and retain substantial genetic diversity. diversity and the lowest association between pairs of (i.e., linkage disequi- librium) along the same chromosome. Africans a severe one (42). Coalescent of population growth and bottlenecks, in Henn et al. (51) showed a strong nega- analysis could be more sensitive to pop- part because the same populations have tive correlation within Africa of genetic ulation structure than frequency- not been surveyed for both mtDNA and diversity with distance from southwestern based estimates, which may help resolve the autosomal loci. However, it is fair to say Africa, which is also consistent with a discrepancy between the two methods (see that estimates of divergence time among serial founder effect model for African also ref. 43 for evidence of a 150-kya groups are generally more concordant. populations. The initial divergence of African bottleneck). For example, autosomal and X chromo- African populations, inferred to be the Unfortunately, genomic data from most some sequence data from five agricultural, separation between the ancestors of populations in Africa remain limited. four Western Pygmy, and three Eastern southern African KhoeSan and other Whole mtDNA genomes suggest a low Pygmy populations produced an estimate Africans, was possibly twice as old as the level of growth overall in Africa from 200 of approximately 60 kya for the divergence time of the OOA migration (52). A recent to 100 kya, but the timing of population of the farming and the hunter-gatherer study by Schlebusch et al. (53) analyzed growth estimated from mtDNA is sensi- groups and 20 kya for the separation of array data from additional sam- tive to the geographic regions sampled. the two Pygmy populations (46). The es- ples of KhoeSan populations; they find Southern Africa generally displays pop- timated size of the population ancestral to linkage disequilibrium patterns to be more ulation stability while retaining a high all 12 sampled populations was approxi- variable than reported by Henn et al. (51) estimated population size; western Africa mately 7,000 to 15,000. This analysis also and highlight the importance of recent shows multiple episodes of population inferred population bottlenecks, with demographic bottlenecks and agripastor- growth, perhaps with the 30- to 50-kya a decrease of 80% of the Western Pygmies alist migrations during the past 2,000 y. period being the most relevant; and eastern between 2.5 and 25 kya, and a later 90% Gene flow between populations within Africa also displays marked population bottleneck of the Eastern Pygmies. [Cox Africa could have important effects on growth during this time period, potentially et al. (47) obtained similar results with these estimates. However, coalescent predating that in western Africa. A dramatic a smaller data set of autosomal sequences analysis of their African dataset continue population growth signature is clearly evi- from fewer African populations.] Analysis to support a model whereby the earliest dent only in L3 mitochondrial lineages likely of mtDNA variation in a different (but population divergence is between KhoeSan originating in eastern Africa 60 to 85 kya partially overlapping) set of Pygmy and and the rest of African populations ap- (44, 45). Atkinson et al. (44) interpret this farming populations produced similar proximately 100 kya. The time depth of signature as evidence that population divergence time estimates. However, substructure within Africa has been only growth began in Africa, before the OOA estimates of the strength of population minimally explored, and it will require expansion. It should be emphasized that bottlenecks are greater with the autosomal more sophisticated methods to jointly these estimates have large error bounds and X chromosome data, and the timing estimate migration and divergence within and variation in parameter assumptions of the bottlenecks in the Eastern Pygmies a complex set of demes. That the southern such as generation time and rate is estimated from mtDNA polymorphisms African KhoeSan hunter-gatherers repre- are not fully incorporated. The mtDNA to have been earlier than that of the sent the most divergent group of Africans and (limited) autosomal data are not Western pygmies, reversing the order does not preclude an exit and subsequent perfectly congruent regarding the timing found with autosomal and X data (48). expansion from northeastern Africa by

17760 | www.pnas.org/cgi/doi/10.1073/pnas.1212380109 Henn et al. Downloaded by guest on September 30, 2021 a group that eventually spread to all terestingly, the most divergent and genet- remain very small). Even if African continents (54, 55) [although it is possible ically diverse clade was from South Africa, substructure dated back 100,000 y, most that North Africa may have been largely although Linz et al. (58) eliminated this as models indicate a single common ancestral depopulated and resettled by OOA pop- an outlier in some analyses]. Even mor- population by 150,000 y (17). As all ulations (56)]. Indeed, a serial founder phological variation of human crania sup- modern human populations maintain the model for Africa suggests a successive ports a serial founder effect model OOA ability to acquire and speak complex lan- budding of populations as they moved into (59–61). In summary, multiple in- guage, it is clear that, before the Great eastern, central, western, and eventually dependent lines of genetic evidence thus Expansion, language must have been fully northern Africa (Fig. 1). Autosomal stud- support a serial founder effect mode of developed in the ancestral population. ies that estimate the time of divergence dispersal. Additionally, another large body Although it is unknown when language between African and OOA populations of data may provide an independent test of became fully developed, the necessary have almost exclusively used data from the pattern of expansion and subsequent organs must have taken considerable time western Africans. However, a serial migrations around the globe: variation to reach the degree of complexity that is founder effect model predicts that differ- among languages. now common to the whole species. This ent populations in Africa will produce includes the capacity to learn and use com- different estimates of divergence between Concordance Between Genes and Language. plicated syntax (perhaps completed even OOA populations. The evolution of languages is rapid—in a before 100,000 y ago and certainly before An important assumption under the few hundred years, a language may change the origin of the Khoisan languages). serial founder effect model, as mentioned enough to destroy mutual understanding earlier, is that subsequent population between neighboring populations, or even Demographic Models of OOA bottlenecks do not differentially affect between ancestors and their descendants Expansion populations near the origin of the expan- 1,000 y later. Families of languages that Having established the basic pattern of the sion. It is possible that eastern African are similar enough that most linguists OOA expansion, we turn now to the local populations experienced a postexpansion recognize them as such have a common demographic processes that occurred bottleneck that decreased their diversity origin in the range of 10,000 y ago. There during the expansion: how rapidly did profile relative to other regions. The is a remarkable similarity between the population move across a geographic KhoeSan populations of southern Africa linguistic tree and the genetic tree, con- range, and what constraints on population appear not to have contracted during the firming Darwin’s speculation that, if we growth seem likely from ethnographic past 100,000 y or to have contracted knew the biological tree of humans, we studies? Deshpande et al. (25) simulated minimally compared with other pop- could predict that of their languages (62). the serial founder effect process numeri- ulations. (We note, however, that their The first attempt to connect the two trees cally, confirming that it is a good fitto present-day population numbers are was made at a time when the linguistic worldwide autosomal microsatellite data. dwindling.) Analysis of ancient DNA from tree was incomplete (63), but the similarity Archaeological information only eastern or northern African bones might was clear and later shown to be statisti- approximates the precise route of the establish that the genetic diversity was as cally real (64). As might be expected, the Great Expansion from its origin to its great as that of present-day southern geographical distribution of language conclusion 25,000 km away, over a period African KhoeSan populations. However, families and that of genetic groupings of of 50,000 y, so that the average rate of no ancient human DNA from Africa of indigenous populations are also reasonably advance of 0.5 km/y or 15 km per gener- great antiquity currently exists. From the closely related. ation on the most direct overland route currently available data, we conclude that the Beyond congruence in phylogenetic is probably an underestimate. A minimum expansion of modern humans began within topology, other aspects of genes and lan- estimate of the number of colonization southern Africa and spread to other regions guages show correlations stemming from events that took place between these two of Africa; then, a small group of humans deep population processes. A recent extremes is then calculable from the exited northeastern Africa and continued this analysis of phonemic diversity in 504 average distance between two contiguous expansion throughout Eurasia, Oceania, worldwide languages shows that this groups, which is approximately 140 km, or and eventually the Americas. diversity exhibits the same serial founder approximately 180 successive colonization effect discussed earlier for genetic varia- events between the beginning and the Independent Evidence of Out of tion, namely a loss of phonemic diversity end of the Great Expansion. With a rate of Africa Model proportional to distance from Africa (65). advance of 0.5 km/y, the time difference Human DNA variation is not the only Moreover, within Africa, the greatest di- between successive colonization events is, evidence that supports a serial founder versity is in the southern central region. on average, 280 y (approximately 10 gen- effect model OOA. Both Plasmodium Although the regression of phonemic di- erations). This gives an idea of the mini- falciparum (a malarial parasite) and versity on distance from Africa is not as mum time between one colonization and (a bacterium that oc- strong as seen with DNA polymorphisms, the next, and if we assume that, at the cupies the human digestive tract) follow this finding nevertheless suggests that the beginning of a new colony’s life, the pop- a strikingly similar pattern to the human genetic and linguistic expansion from Africa ulation doubles every generation, the rate DNA. The geographic pattern of P. falci- could have been part of the same process. of population increase must have decreased parum genetic variation was found to be Ruhlen (66, 67) has extended greatly to zero when the new colony reached the similar to that for humans, exhibiting the linguistic tree that goes back to a single stable size of 1,000 and produced a new a serial founder effect; forward simu- origin, and connects all 15 language fam- colony. The simplest assumption for this lations of the parasite’s exit from Africa ilies for which validity is fairly widely process is logistic growth, beginning with was estimated to be between 40 and 80 kya accepted. How do genetic data constrain doubling and a subsequently decreasing (depending on the assumed divergence a hypothesis of a single origin of modern rate until the stable size is approached. rate from the chimpanzee parasite Plas- language? Genetic evidence indicates that However, there is considerable room for modium reichenowi) (57). H. pylori also the vast majority of our ancestry is likely improvement of this type of simulation shows a clear decline in genetic diversity derived from a recent, common ancestral by incorporating more realistic migration, with distance from eastern Africa, with population that gave rise to modern hu- social structure, and even competition an OOA estimate of 58 kya (58). [In- mans (even estimates of archaic admixture (68) among the simulated colonies.

Henn et al. PNAS | October 30, 2012 | vol. 109 | no. 44 | 17761 Downloaded by guest on September 30, 2021 The use of contemporary human geno- limitations of the environment. When birth is very highly contaminated with all typic variation to infer the time of onset rates do not change, the change in growth sorts of potential . Most resi- and rate of expansion of the human after the population attains a stable size dents, and all Pygmies, walk with bare feet. population during the past 25,000 y has must be controlled by changes in the death In stool, urine, and other excrement of produced a wide range of estimates. Most rate. If the death rate is largely affected Pygmies and farmers, there is an extremely studies that are based on sample sizes of by , it is likely to be very low in a high load and great variety of parasites, less than 100 individuals place the onset of new environment, which is uncontaminated with some difference between the two expansion of Europeans, for example, at during the initial growth period and when ethnic groups [mostly because of many 10 to 25 kya and subsequent growth at the population density is low. We discuss parasites are acquired by Pygmies in the approximately 0.2% to 0.7% per genera- the hypothesis that, as population density forest (77)]. Pygmy camps in the forest are tion (16, 38). These small sample sizes increases, the population increasingly sometimes built in fresh areas, but old dictate that most of the variants detected contaminates its environment and has camps are often reused. Such sanitary must be at frequencies of 5% or higher. greater risk of communicable infectious conditions are not limited to the denser Recent analyses of next-generation se- disease and parasites. population described in the forest envi- quence data in large samples of Europeans ronment. Among the Dobe !Kung in the in the 2,000 to 10,000 range have detected Population Density. In a recent survey of Kalahari desert, Howell noted that in- many nucleotide variants that occur in 32 global hunter-gatherer populations, dividuals moved to a new camp site when only one or very few individuals (69–71). mean band size (i.e., the residential unit) their current site was considered contam- This distribution of rare is com- averaged only 28 individuals (73). Bands inated by insects and excrement (78). patible with explosive growth from the are organized into larger interactive and Many forms of infectious disease are also past 1,000 y at 9% per generation (69) reproductive units, sometimes referred to known to be density-dependent; as such, or the past 5,000 y at 2% per generation as tribes, among which dispersal occurs. death rates from communicable infectious (70). Ethnographic and archaeological Lee and DeVore (74) and Birdsell (75) disease would also increase as populations evidence will be useful in providing known proposed that surviving hunter-gatherer established themselves in new environ- growth rates in historic populations. From tribes have a fairly regular size of ments. The frequency of infectious genomic data, it appears safe to infer that approximately 500. The dependence of among hunter-gatherers is difficult to the human population has recently ex- population size on ecological conditions estimate by using current ethnographies panded at a much faster exponential rate imposes limits on population density. because the primary diseases often appear than was believed before the discovery of Consider, for example, the tropical forest- to be recently introduced. For example, large numbers of rare variants. dwelling central : although infectious and parasitic disease However, genetic models tend to infer population density estimated from ethno- accounted for approximately 70% to 80% minimal population growth in most regions graphic data on the Baka of Cameroon of deaths among the Dobe !Kung, tubercu- of the world between the OOA expansion is 0.47 individuals per km2 (or 35,000 losis, influenza, and sexually transmitted and the last glacial period (approximately individuals over 75,000 km2) (76). The diseases are likely to only have been recently 21 kya). Additionally, most African pop- population density of western Pygmies in introduced (78). In the Hadza of Tanzania, ulations appear to have remained relatively the Mbaiki area is even lower, 0.14 people approximately 45% of deaths from illness constant in size until the invention of per km2. A hunter-gatherer family can are ascribed to diseases that are likely agriculture in Africa and the associated travel approximately 50 km/d unloaded, and recently introduced, such as growth and bottlenecks that occurred after approximately 25 km/d loaded (estimated and (79). When the Plains Native 12 kya. How did human hunter-gatherer in a tropical forest environment). However, Americans’ primary food source, bison, was populations historically maintain stability? the effective dispersal distance between eliminated, and they were moved to We consider two models, each of which parents’ place of birth and offsprings’ reservations where the population density could explain the apparent stability [see place of birth among the Baka Pygmies is increased, huge tuberculosis epidemics Read and LeBlanc (72) for additional estimated to be only 12 to 64 km2 (76). ensued (where the TB vector was originally hypotheses]. First, as a population enters This is likely to be on the lower end of transmitted from Europeans) (80, 81). a new, pristine environment, the birth rate dispersal distances because it is derived In summary, it seems reasonable to rises as a result of the abundance of re- from a population of forest-dwelling assume that, when a new colony is founded, sources. Then, as growth occurs and the hunter-gatherers who today have extensive its environment is reasonably clean and population increases in density, epidemi- contact with farmers. largely uncontaminated by human-specific ological risks also increase until there is Although population density is often diseases. Under these conditions, death a constant death rate over short or longer thought to be so low among hunter-gath- rates are lowest and the population grows episodic time scales. Alternatively, the erers that disease played little role in early at a fairly high rate. However, as birth rate could be carefully regulated by human evolution, densities of the type parasites brought in by the colonizers cultural practices, and only allowed to observed among the central African multiply and are spread through the camp exceed replacement when resources are Pygmies still affect spread of disease. The or village environment, contamination abundant, for example, when a population epidemiologists Pampiglione and Ricciardi grows and death rates increase. We note moves into a new environment or when (77) studied African Pygmies who live in that the death rate need not be constant subsistence strategies improve. camps in the forest when they hunt but to produce apparently long-term pop- spend part of the year in farmers’ villages, ulation stability; episodic epidemiological Demography of Foragers during which they build their traditional catastrophes could also act to reduce Why should population growth that huts in inconspicuous parts of the farmers’ population sizes. occurred exponentially during the OOA villages, behind the villagers’ houses. expansion stop? The growth rate of Pygmies’ huts are usually invisible from Culturally Mediated Population Stability. So- a population is the difference between its the main road, around which farmers’ cial customs can affect birth rate in the few birth rate and its death rate; the human houses are built, often in one or a few rows hunter-gatherer groups that have been birth rate is largely determined by the on each side of the road. Even though investigated, and these may have been interaction between culturally transmitted farmers’ wives frequently sweep to keep inherited from the ancestral population. customs (as detailed later) and resource the soil in front of their houses clean, this One such custom is that women may stop

17762 | www.pnas.org/cgi/doi/10.1073/pnas.1212380109 Henn et al. Downloaded by guest on September 30, 2021 having children 10 to 12 years before In summary, we have suggested that, ulations remains a priority to address the biological menopause. At least in central during the Great Expansion, birth rate may number of African exits, the depth of African Pygmies, women stop reproducing have been more culturally regulated than substructure among African populations when their first daughter has a child (82). the death rate, which is more constrained and differential geographic pattern of This custom tends to limit the number by biological phenomena. Additionally, population bottlenecks (with implications of children born per family to six or seven, these two rates may have opposite patterns for the location of origin within Africa). and approximately two thirds of these of stability. As populations disperse into In addition, refined measures of environ- die before reproduction, so only approxi- new, abundant environments, the birth rate mental variability and its temporal/spatial mately two children per family survive to may increase initially and then eventually changes across Africa would help clarify reproduce, and population size remains stabilize if resources are limited by density. when human dispersals were likely. Com- constant. Mace and Alvergne (83) show The death rate, however, will remain low putational models incorporating multiple that a similar phenomenon occurs among after the founding of a new colony, and, episodes of growth and capable of inferring Gambian agriculturalists; as reproductive although it is smaller than the birth rate migration/divergence among more than spans overlap between mothers and at the beginning of growth, it will then three demes will need to be developed for daughters, mothers reduce their fertility increase as a result of epidemiological this next wave of genomic data. We when their daughters begin have their stresses, which can result from a contami- stress, however, that a synthesis among own children, even if the daughters are nated environment and/or increased pop- genetic, demographic, and anthropological dispersed outside their natal home. This ulation density. Therefore, after several models is important for a full under- custom of premature menopause also generations, a new colony can reach and standing of many parameters of human has the property of being elastic and re- maintain a constant population size. There prehistory, as illustrated here with pop- sponding to changes in death rates of the may be other cultural customs and bi- ulation stability. For example, studies of young. More detailed research is needed to ological constraints than those mentioned natural selection could pair selection sta- test whether this cultural menopause earlier that may help to stabilize the size tistics with current phenotypic data, fluctuates with death rates in families. of a hunter-gatherer group at its apparent and model the time of selective pressure Another custom that limits birth rates de- optimum value. The genetic studies re- based on archeological information. rives from spacing births by extending lac- ferred to here suggest that modern human Many genetic projects still ignore the rich tation over a period of 3 or 4 y. This occurs populations experienced long-term pop- background of archaeological and ethno- in part because a child can only walk ulation stability for thousands of years graphic data when testing genetic with parents during transitions from one (between 45,000 ya and 15,000 ya) with models, or tend to highlight only those territory to another after (s)he is approxi- changes in growth rate primarily linked findings that are consistent with the mately 4 y of age—otherwise (s)he has to to the adoption of agropastoralism during genetic conclusions. Information from be carried by one of the parents, who al- the Holocene (38). all of the sources mentioned here will ready have a heavy load of hunting and be necessary to constrain the com- cooking tools. Finally, we note that Conclusions plex hypotheses surrounding modern delaying the age at first marriage is an Human genetic, linguistic, and phenotypic human origins. important cultural custom, which tends data strongly support a serial founder to reduce overall fertility. We stress that effect model for the Great Expansion ACKNOWLEDGMENTS. The authors thank fertility rates among hunter-gatherer pop- OOA approximately 45 to 60 kya. Signifi- Christopher Gignoux for assistance in creat- ing the map (Fig. 1). This research was sup- ulations are not uniform, total fertility cant gaps in our knowledge of human ported in part by National Institutes of rates vary from 4.7 to 8.2 depending on the population history still exist. Additional Health Grants GM28016, HG003329, and population (79). sampling and sequencing of African pop- 3R01HG003229.

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