Genetic connections and convergent evolution of tropical indigenous peoples in Asia.

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Abstract

Tropical indigenous peoples in Asia (TIA) attract much attention for their unique appearance, whereas their genetic history and adaptive evolution remain mysteries. We conducted a comprehensive study to characterize the genetic distinction and connection of broad geographical TIAs. Despite the diverse genetic makeup and large interarea genetic differentiation between the TIA groups, we identified a basal Asian ancestry (bASN) specifically shared by these populations. The bASN ancestry was relatively enriched in ancient Asian human genomes dated as early as ∼50,000 years before the present and diminished in more recent history. Notably, the bASN ancestry is unlikely to be derived from archaic hominins. Instead, we suggest it may be better modeled as a survived lineage of the initial peopling of Asia. Shared adaptations inherited from the ancient Asian ancestry were detected among the TIA groups (e.g., LIMS1 for hair morphology, and COL24A1 for bone formation), and they are enriched in neurological functions either at an identical locus (e.g., NKAIN3), or different loci in an identical gene (e.g., TENM4). The bASN ancestry could also have formed the substrate of the genetic architecture of the dark pigmentation observed in the TIA peoples. We hypothesize that phenotypic convergence of the dark pigmentation in TIAs could have resulted from parallel (e.g., DDB1/DAK) or genetic convergence driven by admixture (e.g., MTHFD1 and RAD18), new mutations (e.g., STK11), or notably purifying selection (e.g., MC1R). Our results provide new insights into the initial peopling of Asia and an advanced understanding of the phenotypic convergence of the TIA peoples.

https://academic.oup.com/mbe/article/39/2/msab361/6481554?login=false


One question that has long been debated is whether the distinctive physical features (e.g., small body size, dark skin, curly hair, and broad nose, collectively known as “Negrito-like” phenotypes) shared by the tropical hunter-gatherers are ancestral or derived as a result of genetic convergence. Migliano et al. (2013) identified various signals of growth-related positive selection in different tropical indigenous populations, whereas Bergey et al. (2018) reported shared natural selections on height-related pathways in African and Asian rainforest hunter-gatherers. Relatively more analyses were carried out in single tropical indigenous populations or geographically related indigenous groups. Novel adaptive signals of height, hair, nasal morphology, and those in response to some extreme environmental stresses have been reported in each of these populations or groups (Liu et al. 2015; Lopez et al. 2019; Zhang et al. 2021). However, the current understanding of the genetic basis of the dark skin phenotype is rather limited. Over the past few decades, tremendous advances have been made in our understanding of the evolutionary history of light skin in Europeans and East Asians, whereas only a few recent studies revealed the skin color variations and related loci in populations of African ancestry (Bonilla et al. 2005; Beleza et al. 2013; Crawford et al. 2017; Hernandez-Pacheco et al. 2017; Lloyd-Jones et al. 2017; Martin et al. 2017). Interestingly, some of the dark pigmentation-associated variants could have been under parallel evolution in different continents (Crawford et al. 2017). An alternative argument is that dark skin, as well as other “Negrito-like” phenotypes, are probably products of convergent adaptations, as evidenced by extensive genetic differentiation among these populations (Endicott et al. 2003; GenomeAsia100K Consortium 2019). Although exposed to intensive ultraviolet (UV) radiation all year round at similar latitudes, the indigenous populations are more darkly pigmented than their counterparts. This was evidenced by visual impressions and reported melanin measures (demonstrated in supplementary note S1, Supplementary Material online). The long history and simple modes of subsistence (e.g., foraging, pastoralism, and horticulture) of these populations would give special insights into the genetic mechanism of human pigmentation evolution.

 
If there was a convergent evolution between the populations of sub-Saharan Africa and those of Southeast Asia, in addition to similar environmental conditions, the time factor must be important. Because if it were only for the environment, the Amerindians of the Amazon region and other areas of the American continent with tropical jungle should have very dark skin and very curly hair, and we know that this is not the case.
 
If there was a convergent evolution between the populations of sub-Saharan Africa and those of Southeast Asia, in addition to similar environmental conditions, the time factor must be important. Because if it were only for the environment, the Amerindians of the Amazon region and other areas of the American continent with tropical jungle should have very dark skin and very curly hair, and we know that this is not the case.



The current leading theory is that Negritos, Melanesians/ Papuans, and to a degree Aboriginal Australians resemble "black Africans" because they have retained the physical traits of the first humans who left Africa. The alternative that the distinctive phenotype of the Negritos results from convergent evolution can't be excluded though.

Convergent Evolution and Life History An alternative explanation for the negrito phenotype is that of convergent evolution, whereby similar physical traits developed independently among multiple populations. The traditional explanation for dark complexion is a need to dissipate heat, but this is not convincing because dark-bodied radiation is similar for all colors. Protection from ultraviolet light is another reason evinced for dark skin, yet tropical sunlight requires only a light brown skin color to be an effective prophylactic in this respect, and life in the rainforest reduces the need still further. Living in tropical rainforests is also suggested to contribute to a reduction in stature due to locomotory adaptation to the environment. One such adaptation—typical of both negrito and African pygmy populations—is aboreal foraging, which leads to considerable stresses on the lower limb joints. Although the ankle morphology of nonhuman primates in the wild and captivity accurately predicts the amount of climbing they engage in, the same plasticity is not detected among human climbing populations (Venkataraman et al. this issue). If aboreal foraging has been significant throughout prehistory, it is also possible that tree climbing itself favors a short stature, by way of reduced mortality rates. A related explanation for the existence of short stature is that it evolved as a life-history trade-off favoring early reproduction and cessation of adult growth in the face of high mortality rates, but this hypothesis is as yet unproven (Migliano et al. 2007). Genome-wide scans of genotype data on African, Philippine, and Papuan populations of short stature indicate recent positive selection at different loci associated with growth and sexual development (Migliano et al. this issue). There is, however, no evidence for direct selection acting on genes associated with height regulation, which might be expected in the case of locomotory adaptation. Although these results can be interpreted as supporting the hypothesis of convergent evolution for some aspects of phenotype in the recent past, this analysis would not necessarily be able to detect selection associated with short stature if it was the ancestral condition of all populations in the region. .........
https://digitalcommons.wayne.edu/cgi/viewcontent.cgi?article=2049&context=humbiol


Here's the thing by the time humans spread farther North and were ready to move into North America, they had time to evolve into physical characteristics better suited to colder climates. Negritos came from Southeast Asia close to the equator whereas the Native Americans came from Northeast Asia. Since Negritos and Native Americans came from different populations and very different regions and latitudes, they look different. It appears that Eurasians like the Negritos in the lower latitudes near the equator either have retained or developed their dark coloring and tropical features while those in the higher latitudes developed different traits that were suited to their environments.

 
“Negrito-like” phenotypes of tropical indigenous peoples in Asia could be associated with Denisovan admixture common in Australia and Southeast Asia. The ancient hominins known as the Denisovans interbred with modern humans in Southeast Asia. Philippine Negritos retained most of their inherited Denisovan archaic tracts and were left with the highest level of Denisovan ancestry in the world. Philippine Negritos were recently admixed with East Asian-related groups, who carry little Denisovan ancestry, and which consequently diluted their levels of Denisovan ancestry.

The study by Larena et al. (2021) shows that Ayta Magbukon possess the highest level of Denisovan ancestry in the world, ∼30%–40% greater than that of Australians and Papuans, consistent with an independent admixture event into Negritos from Denisovans.


Summary
Multiple lines of evidence show that modern humans interbred with archaic Denisovans. Here, we report an account of shared demographic history between Australasians and Denisovans distinctively in Island Southeast Asia. Our analyses are based on ∼2.3 million genotypes from 118 ethnic groups of the Philippines, including 25 diverse self-identified Negrito populations, along with high-coverage genomes of Australopapuans and Ayta Magbukon Negritos. We show that Ayta Magbukon possess the highest level of Denisovan ancestry in the world—∼30%–40% greater than that of Australians and Papuans—consistent with an independent admixture event into Negritos from Denisovans. Together with the recently described Homo luzonensis, we suggest that there were multiple archaic species that inhabited the Philippines prior to the arrival of modern humans and that these archaic groups may have been genetically related. Altogether, our findings unveil a complex intertwined history of modern and archaic humans in the Asia-Pacific region, where distinct Islander Denisovan populations differentially admixed with incoming Australasians across multiple locations and at various points in time.

https://www.cell.com/current-biology/fulltext/S0960-9822(21)00977-5
 

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