Genetic signature of natural selection in first Americans

Abstract

When humans moved from Asia toward the Americas over 18,000 y ago and eventually peopled the New World they encountered a new environment with extreme climate conditions and distinct dietary resources. These environmental and dietary pressures may have led to instances of genetic adaptation with the potential to influence the phenotypic variation in extant Native American populations. An example of such an event is the evolution of the fatty acid desaturases (FADS) genes, which have been claimed to harbor signals of positive selection in Inuit populations due to adaptation to the cold Greenland Arctic climate and to a protein-rich diet. Because there was evidence of intercontinental variation in this genetic region, with indications of positive selection for its variants, we decided to compare the Inuit findings with other Native American data. Here, we use several lines of evidence to show that the signal of FADS-positive selection is not restricted to the Arctic but instead is broadly observed throughout the Americas. The shared signature of selection among populations living in such a diverse range of environments is likely due to a single and strong instance of local adaptation that took place in the common ancestral population before their entrance into the New World. These first Americans peopled the whole continent and spread this adaptive variant across a diverse set of environments.

Keywords: first Americans; genetics; natural selection; peopling of America.

Fig. 1.

Significant SNPs found in Native American populations compared with other continental populations (Africans, Asians, and Europeans). The comparison was tested using Fisher’s exact test with Bonferroni correction. We found three significant SNPs, two within FADS2 (rs174570, P < 0.0001 and rs174556, P < 0.001) and another located on chromosome 22 (rs13054099, P < 0.0000001) in SLC25A17.

Fig. S1.

(A and B) Distribution of the PBS statistics (99.9th and 99.5th percentiles) for the Native American branch across the extension of chromosome 11 (on the x axis) in each dataset (1 and 2, respectively). (C and D) F_ST outlier detection from BayeScan across the extension of chromosome 11 (on the x axis) in both datasets. With a false discovery rate of 0.05 (dashed line), SNPs that reach a significant log-transformed q-value (y axis) in the Native American population are shown in red. The dashed lines indicate the sliding-window q-value.

Fig. S2.

Distribution of 10,000 simulated PBS values under a neutral coalescent model. The dashed line represents the top observed PBS SNP values in the empirical datasets. (A) Dataset 1. (B) Dataset 2.

Fig. 2.

The geographic distribution of the putatively selected FADS haplotype that presents a signal of natural selection in Native American populations.