Remarkably Low KIR and HLA Diversity in Amerindians Reveals Signatures of Strong Purifying Selection Shaping the Centromeric KIR Region.

The killer-cell immunoglobulin-like receptors (KIR) recognize human leukocyte antigen (HLA) molecules to regulate the cytotoxic and inflammatory responses of natural killer cells. KIR genes are encoded by a rapidly evolving gene family on chromosome 19 and present an unusual variation of presence and absence of genes and high allelic diversity. Although many studies have associated KIR polymorphism with susceptibility to several diseases over the last decades, the high-resolution allele-level haplotypes have only recently started to be described in populations. Here, we use a highly innovative custom next-generation sequencing method that provides a state-of-art characterization of KIR and HLA diversity in 706 individuals from eight unique South American populations: five Amerindian populations from Brazil (three Guarani and two Kaingang); one Amerindian population from Paraguay (Aché); and two urban populations from Southern Brazil (European and Japanese descendants from Curitiba). For the first time, we describe complete high-resolution KIR haplotypes in South American populations, exploring copy number, linkage disequilibrium, and KIR-HLA interactions. We show that all Amerindians analyzed to date exhibit the lowest numbers of KIR-HLA interactions among all described worldwide populations, and that 83-97% of their KIR-HLA interactions rely on a few HLA-C molecules. Using multiple approaches, we found signatures of strong purifying selection on the KIR centromeric region, which codes for the strongest NK cell educator receptors, possibly driven by the limited HLA diversity in these populations. Our study expands the current knowledge of KIR genetic diversity in populations to understand KIR-HLA coevolution and its impact on human health and survival.

Microdemographic Determinants of Population Recovery among the Northern Aché.

A pattern of population crash and rapid recovery is a common feature of the pacification and settlement experience of the indigenous peoples of tropical South America. Despite the obvious importance of these events to the demographic and anthropological sciences as a whole, as well as their significant practical implications, little is known about the microdemographic determinants of these paired phenomena. Using methods of asymptotic and stochastic demographic analysis, we reconstructed the microdemographic drivers of this history among one indigenous population: the Northern Aché of eastern Paraguay. This article explores the implications of these relationships for understanding the overall demographic turnaround observed within similar groups, as well as for the future trajectory of the Northern Aché in particular.

Cooperative breeding in South American hunter-gatherers.

Evolutionary researchers have recently suggested that pre-modern human societies habitually practised cooperative breeding and that this feature helps explain human prosocial tendencies. Despite circumstantial evidence that post-reproductive females and extra-pair males both provide resources required for successful reproduction by mated pairs, no study has yet provided details about the flow of food resources by different age and sex categories to breeders and offspring, nor documented the ratio of helpers to breeders. Here, we show in two hunter-gatherer societies of South America that each breeding pair with dependent offspring on average obtained help from approximately 1.3 non-reproductive adults. Young married males and unmarried males of all ages were the main food providers, accounting for 93-100% of all excess food production available to breeding pairs and their offspring. Thus, each breeding pair with dependants was provisioned on average by 0.8 adult male helpers. The data provide no support for the hypothesis that post-reproductive females are the main provisioners of younger reproductive-aged kin in hunter-gatherer societies. Demographic and food acquisition data show that most breeding pairs can expect food deficits owing to foraging luck, health disabilities and accumulating dependency ratio of offspring in middle age, and that extra-pair provisioning may be essential to the evolved human life history.

Genetic clues about the origin of Aché hunter-gatherers of Paraguay.

Seventeen genetic studies performed among the until recently hunter-gatherer Aché were reviewed and the corresponding data integrated to general information about this group, and to statistical tests of hypothesis concerning its origin(s). Two features of the Aché gene pool emerge: (a) the distinctiveness in relation to the general pattern of Amerindian genetic data; and (b) the reduced within population genetic variability. As for the origin of this people, the evidence suggests a general Tupian background with considerable introgression of Jê genetic material, which could be explained by the Tupi warfare habit of absorption instead of extermination of defeated individuals.

The public health implications of maternal care trade-offs.

The socioeconomic and ethnic characteristics of parents are some of the most important correlates of adverse health outcomes in childhood. However, the relationships between ethnic, economic, and behavioral factors and the health outcomes responsible for this pervasive finding have not been specified in child health epidemiology. The general objective of this paper is to propose a theoretical approach to the study of maternal behaviors and child health in diverse ethnic and socioeconomic environments. The specific aims are: (a) to describe a causal pathway between the utility that women obtain through work outside the home and through child care and disease hazard rates in childhood using an optimization model; (b) to specify the influence of ethnic and socioeconomic factors on model constraints; (c) to use the model as a tool to learn about how different combinations of maternal wage labor and child care time might influence child health outcomes in diverse social contexts; (d) to identify parameters that will require measurement in future research; (e) to discuss research strategies that will enable us to obtain these measurements; and (f) to discuss the implications of the model for biostatistical modeling and public health intervention. Optimization models are powerful heuristic tools for understanding how ethnic, environmental, family, and personal characteristics can place important constraints on both the quality and quantity of care that women can provide to their children. They provide a quantitative appreciation for the difficult trade-offs that most women face between working in order to purchase basic goods that children cannot do without (e.g., food, clothing, shelter, health insurance), and increasing offspring well-being through child care (e.g., training in social skills, affection, protection from environmental hazards, help with homework).

Distribution of CGG repeats and FRAXAC1/DXS548 alleles in South American populations.

In order to assess the molecular variability related to fragile X (FMR1 locus), we investigated the distribution of CGG repeats and DXS548/FRAXAC1 haplotypes in normal South American populations of different ethnic backgrounds. Special attention was given to Amerindian Wai-Wai (Northern Brazil) and Ache (Paraguay), as well as to Brazilian isolated communities of African ancestry, the remnants of quilombos. Comparison of samples from quilombos, Amerindians, and the ethnically mixed, but mainly European-derived population of São Paulo revealed that the 30-copy allele of the fragile X gene is the most frequent in all groups. A second peak at 20 repeats was present in the population of São Paulo only, confirming this as a European peculiarity. The distribution of DXS548 and FRAXAC1 alleles led to a high expected heterozygosity in African Brazilians, followed by that observed in the population of São Paulo. Amerindians showed the lowest diversity in CGG repeats and DXS548/FRAXAC1 haplotypes. Some rare alleles, for example, the 148-bp (FRAXAC1) or 200-bp (DXS548) variants, which seem to be almost absent in Europe, occurred in higher frequencies among African Brazilians. This suggests a general trend for higher genetic diversity among Africans; these rarer alleles could be African in origin and would have been lost or possibly were not present in the groups that gave rise to the Europeans.

Hunter-gatherer inter-band interaction rates: implications for cumulative culture.

Our species exhibits spectacular success due to cumulative culture. While cognitive evolution of social learning mechanisms may be partially responsible for adaptive human culture, features of early human social structure may also play a role by increasing the number potential models from which to learn innovations. We present interview data on interactions between same-sex adult dyads of Ache and Hadza hunter-gatherers living in multiple distinct residential bands (20 Ache bands; 42 Hadza bands; 1201 dyads) throughout a tribal home range. Results show high probabilities (5%-29% per year) of cultural and cooperative interactions between randomly chosen adults. Multiple regression suggests that ritual relationships increase interaction rates more than kinship, and that affinal kin interact more often than dyads with no relationship. These may be important features of human sociality. Finally, yearly interaction rates along with survival data allow us to estimate expected lifetime partners for a variety of social activities, and compare those to chimpanzees. Hadza and Ache men are estimated to observe over 300 men making tools in a lifetime, whereas male chimpanzees interact with only about 20 other males in a lifetime. High intergroup interaction rates in ancestral humans may have promoted the evolution of cumulative culture.

Heritability and fitness correlates of personality in the Ache, a natural-fertility population in Paraguay.

The current study assessed the heritability of personality in a traditional natural-fertility population, the Ache of eastern Paraguay. Self-reports (n = 110) and other-reports (n = 66) on the commonly used Big Five Personality Inventory (i.e., extraversion, agreeableness, conscientiousness, neuroticism, openness) were collected. Self-reports did not support the Five Factor Model developed with Western samples, and did not correlate with other-reports for three of the five measured personality factors. Heritability was assessed using factors that were consistent across self- and other-reports and factors assessed using other-reports that showed reliabilities similar to those found in Western samples. Analyses of these items in combination with a multi-generation pedigree (n = 2,132) revealed heritability estimates similar to those found in most Western samples, although we were not able to separately estimate the influence of the common environment on these traits. We also assessed relations between personality and reproductive success (RS), allowing for a test of several mechanisms that might be maintaining heritable variation in personality. Phenotypic analyses, based largely on other-reports, revealed that extraverted men had higher RS than other men, but no other dimensions of personality predicted RS in either sex. Mothers with more agreeable children had more children, and parents mated assortatively on personality. Of the evolutionary processes proposed to maintain variation in personality, assortative mating, selective neutrality, and temporal variation in selection pressures received the most support. However, the current study does not rule out other processes affecting the evolution and maintenance of individual differences in human personality.

Co-residence patterns in hunter-gatherer societies show unique human social structure.

Contemporary humans exhibit spectacular biological success derived from cumulative culture and cooperation. The origins of these traits may be related to our ancestral group structure. Because humans lived as foragers for 95% of our species' history, we analyzed co-residence patterns among 32 present-day foraging societies (total n = 5067 individuals, mean experienced band size = 28.2 adults). We found that hunter-gatherers display a unique social structure where (i) either sex may disperse or remain in their natal group, (ii) adult brothers and sisters often co-reside, and (iii) most individuals in residential groups are genetically unrelated. These patterns produce large interaction networks of unrelated adults and suggest that inclusive fitness cannot explain extensive cooperation in hunter-gatherer bands. However, large social networks may help to explain why humans evolved capacities for social learning that resulted in cumulative culture.

The beta-globin gene cluster distribution revisited-patterns in Native American populations.

New frequencies for the beta-globin gene cluster haplotypes are presented for the Aché (N = 82 individuals), Guarani (N = 76), and Kaingang (N = 54), three Native South American populations that live in an area between parallels 20 degrees S and 30 degrees S not covered by previous studies at this locus. The haplotype frequencies obtained for the three populations are within the interval observed for 28 other Native American populations. The Aché show much less haplotypes (five) than the other two populations (9-10), the haplotype prevalences being more similar to those of the Guarani than to the Kaingang. The Native American total heterozygosity was about half (0.41) that obtained for the African populations (0.71), but was not much different from those obtained for other continents. A geographical pattern was disclosed in South America by mapping the frequencies of the most common haplotype (haplotype 2), and by means of spatial correlation analysis. The analysis of molecular variance (AMOVA) and pairwise F(ST) data suggest three distinct sectors for the genetic landscape of Native South America: the Andes, the Center/Southeast region, and the Amazon.

Life in the slow lane revisited: ontogenetic separation between chimpanzees and humans.

This study investigates the evolution of human growth by analyzing differences in body mass growth trajectories among three populations: the Ache of eastern Paraguay, the US (NHANES, 1999-2000), and captive chimpanzees. The relative growth statistic "A" from the mammalian growth law is allowed to vary with age and proves useful for comparing growth across different ages, populations, and species. We demonstrate ontogenetic separation between chimpanzees and humans, and show that interspecific differences are robust to variable environmental conditions. The human pattern of slow growth during the lengthened period from weaning to the beginning of the adolescent growth spurt is found among the Ache (low energy availability and high disease load) and also in the US (high energy availability and low disease load). The human growth pattern contrasts with that of the chimpanzee, where absolute growth rates and relative "A" values are faster and less prolonged. We suggest that selection has acted to decrease human growth rates to allow more time for increased cognitive development with lower body-maintenance costs.

Growth rates and life histories in twenty-two small-scale societies.

This study investigates variation in body growth (cross-sectional height and weight velocity) among a sample of 22 small-scale societies. Considerable variation in growth exists among hunter-gatherers that overlaps heavily with growth trajectories present in groups focusing more on horticulture. Intergroup variation tends to track environmental conditions, with societies under more favorable conditions displaying faster growth and earlier puberty. In addition, faster/earlier development in females is correlated with higher mortality. For example, African "Pygmies," Philippine "Negritos," and the Hiwi of Venezuela are characterized by relatively fast child-juvenile growth for their adult body size (used as a proxy for energetic availability). In these societies, subadult survival is low, and puberty, menarche, and first reproduction are relatively early (given their adult body size), suggesting selective pressure for accelerated development in the face of higher mortality. In sum, the origin and maintenance of different human ontogenies may require explanations invoking both environmental constraints and selective pressures.

Geography influences microsatellite polymorphism diversity in Amerindians.

Data related to 15 short tandem repeat polymorphisms (STRPs) are reported for four South American Indian populations, and integrated with previous Brazilian Indian results. Overall heterozygosities varied significantly among groups (Kruskal-Wallis test, P = 0.002). The lowest levels of heterozygosity were observed in the Ache, Ayoreo, and Surui, an expected finding considering their isolation and ethnohistory. Genetic distance and gene diversity analyses suggested that geography was a good predictor of genetic affinity among these Native Americans. New evidence from this study supports the hypothesis that the Ache population descends from a Ge group that preceded the Guarani colonization of Paraguay.

T-cell and chemokine receptor variation in south Amerindian populations.

The immune response of relatively small, endogamous populations is of special interest, because they may differ from those of large, ethnically diverse, urban groups. As a contribution to this area of investigation, we tested 99 individuals from two Brazilian native populations for two T-cell receptor gene segments (TCRBV3S1 and TCRBV18) and 241 subjects from eight tribes of this ethnic group in relation to the chemokine receptor CCR5delta32 allele. Differences in TCRBV3S1 and TCRBV18 prevalences of the Amerindians in relation to European- and African-derived individuals were not marked. We confirmed the absence of the CCR5delta32 allele in most groups, its presence in the Mura and Kaingang, probably because of European gene introgression.

Longitudinal study of tuberculosis outcomes among immunologically naive Aché natives of Paraguay.

This study documents the course of a tuberculosis epidemic in an immunologically naive group of South American Indians within fewer than 20 years after first sustained contact with outsiders. Groups of Northern Aché (ah-CHAY) of eastern Paraguay were contacted and settled on reservations between 1971-1979. Not surprisingly, the Aché are very susceptible to tuberculosis, and the epidemiological characteristics of the disease are quite different from those of populations that have had tuberculosis for centuries. Within 6 years of the first detected case of tuberculosis among the Aché, the prevalence rate of active tuberculosis cases reached 18.2%, and of infected cases among adults, 64.6%, some of the highest rates ever reported for any human group. Remarkably, males and females are equally likely to have been diagnosed with active tuberculosis, Aché children between birth and 5 years of age are least vulnerable to tuberculosis, high nutritional and socioeconomic status do not decrease the risk of disease or infection, and children immunized with BCG are less responsive to tuberculin challenge than are other children. Moreover, similar to the Yanomamö, but unlike populations of European or African descent, a high percentage of Aché with active disease test negative on tuberculin challenge tests (purified protein derivative; PPD). These differences may be due to a high prevalence of diminished cell-mediated immunity, and T-helper 2 dominance. We also hypothesize that these immunological characteristics, low genetic diversity, hostile intergroup interactions, and behavioral noncompliance to treatment protocols together contribute to the high rates of active disease observed. Existing tuberculosis control programs are poorly equipped to handle the impact of these causal complexities on the course of recent tuberculosis epidemics that have quickly spread throughout native communities of Latin America during the last decade.

Polymorphisms of CYP1a1, CYP2e1, GSTM1, GSTT1, and TP53 genes in Amerindians.

Polymorphisms at the TP53, cytochrome P-450 (CYP), and glutathione S-transferase (GST) genes are related to cancer susceptibility and present high diversity in allele frequencies among ethnic groups. This study concerns the CYP2E1, GSTM1, and GSTT1 polymorphisms in seven Amerindian populations (Xavante, Guarani, Aché, Wai Wai, Zoró, Surui, and Gavião). Polymorphic sites at CYP1A1 and TP53 were also studied in the Aché and Guarani tribes and compared with previous results about these systems already obtained in the other populations. The CYP2E1*5B haplotype showed, respectively, the highest and the lowest frequencies already observed in human groups. High frequencies of CYP1A1*2A and CYP1A1*2C alleles and mostly low values of GSTM1*0/*0 and GSTT1*0/*0 genotypes were observed. These data may be interpreted as being due to genetic drift or selection for these high-frequency CYP1A1 alleles and against GST null genotypes during America's colonization. Intrapopulation diversity varied from 0.19 (Guarani) to 0.38 (Surui), and 90% of the total diversity was due to the variability within populations. The relationships between these Amerindians and with other ethnic groups were evaluated based on D(A) distances and the neighbor-joining method. Low correlation was observed between genetic relationships and geographic distances or linguistic groups. In the TP53 comparison with other ethnic groups, Amerindians clustered together and then joined Chinese populations. The cluster analysis seems to indicate that the Aché tribe might descend from a Gê group that could have first colonized that Paraguayan region, but had also assimilated some amount of the Guarani gene pool, maybe through intertribal admixture.