The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists

Patin, Étienne; Siddle, Katherine J.; Laval, Guillaume; Quach, Hélène; Harmant, Christine; Becker, Noémie S.; Froment, Alain; Regnault, Béatrice; Lemée, Laure; Gravel, Simon; Hombert, Jean Marie; Veen, Lolke van der; Dominy, Nathaniel J.; Perry, George H.; Barreiro, Luis B.; Verdu, Paul; Heyer, Évelyne; Quintana-Murci, Lluı́s

doi:10.1038/ncomms4163

Cited by 113 publications

(144 citation statements)

References 56 publications

Supporting

Mentioning

119

Contrasting

Unclassified

Order By: Relevance

“…2A) revealed variable but considerable levels of Bakiga ancestry among the Batwa individuals (mean = 14.2%; range = 0-93%). Conversely, the estimated levels of Batwa ancestry among the Bakiga were much lower (mean = 5.3%; range = 0-10.4%), consistent with previous findings (11).…”

Section: Significancesupporting

confidence: 80%

“…Moreover, if our inference of within-Africa convergent evolution is correct, then this means that the pygmy phenotype evolved (at least in part) more recently than ∼20-30 kya, which is the estimated time of divergence between east central and west central African rainforest hunter-gatherers (11,34). This insight potentially informs competing hypotheses concerning the antiquity of rainforest hunter-gatherer behavior (40,41).…”

Section: Discussionmentioning

confidence: 96%

“…All samples were genotyped on the Illumina HumanOmni1-Quad genotyping array (Illumina). The 1M SNP genotype data for the Baka, Nzebi, and Nzime and for 40 Batwa and 40 Bakiga individuals were reported in Patin et al (11). Genotypes of 928,705 SNPs were called in all samples using the Illumina Genome Studio v2010.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers

Perry

Foll

Grenier

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

108

View full text Add to dashboard Cite

The evolutionary history of the human pygmy phenotype (small body size), a characteristic of African and Southeast Asian rainforest hunter-gatherers, is largely unknown. Here we use a genome-wide admixture mapping analysis to identify 16 genomic regions that are significantly associated with the pygmy phenotype in the Batwa, a rainforest hunter-gatherer population from Uganda (east central Africa). The identified genomic regions have multiple attributes that provide supporting evidence of genuine association with the pygmy phenotype, including enrichments for SNPs previously associated with stature variation in Europeans and for genes with growth hormone receptor and regulation functions. To test adaptive evolutionary hypotheses, we computed the haplotypebased integrated haplotype score (iHS) statistic and the level of population differentiation (F ST ) between the Batwa and their agricultural neighbors, the Bakiga, for each genomic SNP. Both jiHSj and F ST values were significantly higher for SNPs within the Batwa pygmy phenotype-associated regions than the remainder of the genome, a signature of polygenic adaptation. In contrast, when we expanded our analysis to include Baka rainforest hunter-gatherers from Cameroon and Gabon (west central Africa) and Nzebi and Nzime neighboring agriculturalists, we did not observe elevated jiHSj or F ST values in these genomic regions. Together, these results suggest adaptive and at least partially convergent origins of the pygmy phenotype even within Africa, supporting the hypothesis that small body size confers a selective advantage for tropical rainforest hunter-gatherers but raising questions about the antiquity of this behavior.human evolutionary ecology | human hunter-gatherers | population genomics | convergent evolution

show abstract

Section: Significancesupporting

confidence: 80%

Section: Discussionmentioning

confidence: 96%

See 1 more Smart Citation

Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers

Perry

Foll

Grenier

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

108

View full text Add to dashboard Cite

show abstract

“…This is relevant because Baka and Mbuti are hunter-gatherer populations that diverged a long time ago from Bantu African populations (50-65 kya) as well as from each other (20-30 kya) [47,[65][66][67][68]. Secondly, we observe low levels of admixture between these groups (Bantu admixture in Mbuti: 0-16%, Bantu admixture in Baka: 6.5-9.4%) [69,70]. However as many individuals were estimated to have no Bantu admixture and FY Ã O is nearly fixed in these hunter-gatherer populations, these identical haplotypes are unlikely to be due to recent gene flow.…”

Section: Discussionmentioning

confidence: 84%

Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

McManus

Taravella

Henn

et al. 2016

Preprint

View full text Add to dashboard Cite

The human DARC (Duffy antigen receptor for chemokines) gene encodes a membranebound chemokine receptor crucial for the infection of red blood cells by Plasmodium vivax, a major causative agent of malaria. Of the three major allelic classes segregating in human populations, the FY*O allele has been shown to protect against P. vivax infection and is at near fixation in sub-Saharan Africa, while FY*B and FY*A are common in Europe and Asia, respectively. Due to the combination of strong geographic differentiation and association with malaria resistance, DARC is considered a canonical example of positive selection in humans. Despite this, details of the timing and mode of selection at DARC remain poorly understood. Here, we use sequencing data from over 1,000 individuals in twenty-one human populations, as well as ancient human genomes, to perform a fine-scale investigation of the evolutionary history of DARC. We estimate the time to most recent common ancestor (T MRCA ) of the most common FY*O haplotype to be 42 kya (95% CI: 34-49 kya). We infer the FY*O null mutation swept to fixation in Africa from standing variation with very low initial frequency (0.1%) and a selection coefficient of 0.043 (95% CI:0.011-0.18), which is among the strongest estimated in the human genome. We estimate the T MRCA of the FY*A mutation in non-Africans to be 57 kya (95% CI: 48-65 kya) and infer that, prior to the sweep of FY*O, all three alleles were segregating in Africa, as highly diverged populations from Asia and 6 ¼Khomani San hunter-gatherers share the same FY*A haplotypes. We test multiple models of admixture that may account for this observation and reject recent Asian or European admixture as the cause.

show abstract

“…Cold Spring Harbor Laboratory Press on May 12, 2018 -Published by genome.cshlp.org Downloaded from farmers from West Africa ∼5 kya (Cavalli-Sforza 1986;Tishkoff et al 2009;Patin et al 2014). Indeed, our inferred time of admixture coincides with the time of Neolithic agricultural development in Africa ∼5-10 kya (Phillipson 2005), as well as with the estimated times of agriculturalist expansion for both Bantu-speaking (5.6 kya, 95% C.I.…”

Section: Demography and Selection In African Pygmiesmentioning

confidence: 78%

Whole-genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection

et al. 2016

View full text Add to dashboard Cite

African Pygmies practicing a mobile hunter-gatherer lifestyle are phenotypically and genetically diverged from other anatomically modern humans, and they likely experienced strong selective pressures due to their unique lifestyle in the Central African rainforest. To identify genomic targets of adaptation, we sequenced the genomes of four Biaka Pygmies from the Central African Republic and jointly analyzed these data with the genome sequences of three Baka Pygmies from Cameroon and nine Yoruba famers. To account for the complex demographic history of these populations that includes both isolation and gene flow, we fit models using the joint allele frequency spectrum and validated them using independent approaches. Our two best-fit models both suggest ancient divergence between the ancestors of the farmers and Pygmies, 90,000 or 150,000 yr ago. We also find that bidirectional asymmetric gene flow is statistically better supported than a single pulse of unidirectional gene flow from farmers to Pygmies, as previously suggested. We then applied complementary statistics to scan the genome for evidence of selective sweeps and polygenic selection. We found that conventional statistical outlier approaches were biased toward identifying candidates in regions of high mutation or low recombination rate. To avoid this bias, we assigned P-values for candidates using whole-genome simulations incorporating demography and variation in both recombination and mutation rates. We found that genes and gene sets involved in muscle development, bone synthesis, immunity, reproduction, cell signaling and development, and energy metabolism are likely to be targets of positive natural selection in Western African Pygmies or their recent ancestors.

show abstract

The impact of agricultural emergence on the genetic history of African rainforest hunter-gatherers and agriculturalists

Cited by 113 publications

References 56 publications

Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers

Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers

Population Genetic Analysis of the DARC Locus (Duffy) Reveals Adaptation from Standing Variation Associated with Malaria Resistance in Humans

Whole-genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection

Contact Info

Product

Resources

About