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. 2024 May 21;27(6):110050.
doi: 10.1016/j.isci.2024.110050. eCollection 2024 Jun 21.

Genomic imputation of ancient Asian populations contrasts local adaptation in pre- and post-agricultural Japan

Niall P Cooke  1 , Madeleine Murray  1 , Lara M Cassidy  2 , Valeria Mattiangeli  2 , Kenji Okazaki  3 , Kenji Kasai  4 , Takashi Gakuhari  5 , Daniel G Bradley  2 , Shigeki Nakagome  1   5
Affiliations

Genomic imputation of ancient Asian populations contrasts local adaptation in pre- and post-agricultural Japan

Niall P Cooke et al. iScience. .

Abstract

Early modern humans lived as hunter-gatherers for millennia before agriculture, yet the genetic adaptations of these populations remain a mystery. Here, we investigate selection in the ancient hunter-gatherer-fisher Jomon and contrast pre- and post-agricultural adaptation in the Japanese archipelago. Building on the successful validation of imputation with ancient Asian genomes, we identify selection signatures in the Jomon, particularly robust signals from KITLG variants, which may have influenced dark pigmentation evolution. The Jomon lacks well-known adaptive variants (EDAR, ADH1B, and ALDH2), marking their emergence after the advent of farming in the archipelago. Notably, the EDAR and ADH1B variants were prevalent in the archipelago 1,300 years ago, whereas the ALDH2 variant could have emerged later due to its absence in other ancient genomes. Overall, our study underpins local adaptation unique to the Jomon population, which in turn sheds light on post-farming selection that continues to shape contemporary Asian populations.

Keywords: Anthropology; Genomics.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Performance of imputing heterozygotes in five ancient individuals (A and B) The ability to impute ancient Asian individuals is assessed by two metrics: (A) the concordance measures how many of heterozygous sites in the original diploid genomes are successfully recovered from imputation, while (B) the accuracy quantifies how many of the sites that are imputed as heterozygotes are validated with the diploid data. These metrics are calculated for seven different depths of lower coverage data downsampled from the original data (i.e., 0.01, 0.05, 0.1, 0.5, 1, 2, and 5 ×). The lines with open circles represent transition mutations, while those with closed circles represent transversions. The ancient genomes included are as follows: two Jomon individuals (JpKa6904 and F23, represented by red and pink respectively), a 31,600-year-old Upper Palaeolithic North Siberian (Yana1 represented by green), and two Siberian individuals from the Baikal Region and Krasnoyarsk Krai (irk034 and kra001, represented by blue and orange, respectively).
Figure 2
Figure 2
Haplotypic analysis of 126 imputed ancient Asian individuals (A) Principal component analysis based on a matrix of identity-by-descent (IBD) sharing between all pairs of imputed ancient individuals. Different colors show different geographic or cultural backgrounds. (B) ROH profiles stratified by their total lengths of short (<1.6 Mb) and long (>1.6 Mb) fragments. Individuals with the coverage <0.5 × in their original data (i.e., pre-imputed data) are excluded due to insufficient numbers of imputed sites available for this analysis.
Figure 3
Figure 3
A genome-wide scan for positive selection in the Jomon Top: Transformed PBS represents rankings of windows (size: 80 SNPs; step between windows: 10 SNPs) by their PBS values. The dashed horizontal lines show the 99.9th (magenta) and 99.99th (purple) percentiles of the empirical distribution. Middle: Heterozygosity of Jomon (red), Han Chinese in Beijing (CHB; blue), and Utah Residents with Northern and Western European ancestry (CEU; orange) in the regions on chromosomes 2, 7, and 12. The protein-coding genes present in each region are shown by solid lines with magenta. The dashed lines mark the locations of focal SNPs in each region. Bottom: Frequencies of focal alleles in ancient populations and modern-day references. The bar plots represent the frequencies of ancestral (blue) and derived (orange) alleles for SNPs of the region on chromosomes 2, 7, and 12, respectively. The frequencies of other SNPs (rs150038188 and rs77567846 on chromosome 7; rs11495049 on chromosome 7) are shown in Figure S16.
Figure 4
Figure 4
Tracing selection within the alcohol metabolism pathway pre- and post-farming (A) Temporal changes in allele frequencies at rs1229984 and rs671 in Japanese and Chinese populations. The bar plots represent the frequencies of ancestral (blue) and derived (orange) alleles for those SNPs. Two enzymes are mainly involved in this pathway: first, ADH1B converts ethanol into acetaldehyde, and then ALDH2 digests acetaldehyde into acetate. The nonsynonymous mutation at ADH1B (rs1229984) speeds up the conversion process, while the mutation at ALDH2 (rs671) slows down the digestion. Natural selection on this pathway is directed toward the local accumulation of acetaldehyde. (B) Contrasting the recent population growth with the emergence of a novel trait that facilitates the accumulation of acetaldehyde. Top: A temporal change in effective population size estimated from IBD sharing between individuals. The estimates are obtained from five different time points: four individuals of the Odake site (Jomon; 5,979 years before present, BP), two individuals of the Kosaku site (Jomon; 4,159 years BP), two individuals of the Funadomari site (Jomon; 3,755 years BP), three individuals of the Iwade site (Kofun; 1,348 years BP), and 104 individuals of modern Japanese. Bottom: Evolution of genetic potential to retain acetaldehyde. The plots show genetic scores of alcohol consumption estimated from the two SNPs (rs1229984 and rs671) among individuals from the Jomon (n = 19), Kofun (n = 3), and modern Japanese (n = 104). The x axis represents time with the same scale as that in the top plot.
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