Selection for and against pigmentation alleles in South Asia

Deepika Padukone

Recently some British friends were asking about what we knew about South Asian historical genetics now. I explained that it does look like there was some migration in from the Central Asian steppe and West Asia into South Asia during the Holocene. To which one friend responded, “that’s obvious though, many Indians look like brown white people.” Setting aside the semantic paradox (if you are brown, you are literally not white), it is clear what he is getting at: due to shared ancestry the facial structure of many South Asians is not that different from West Eurasians.

The Bollywood actress Deepika Padukone is an example of someone who is rather brown-skinned (naturally), but whose facial features are such that if she went with 100% skin-bleaching she would pass as white without too much trouble. For the purposes of this post, I Googled Indian albino…and came up with this family. You can make your own judgments. I don’t know what to think of that!

The reason for this post is a newly accepted paper, Ancestry-specific analyses reveal differential demographic histories and opposite selective pressures in modern South Asian populations:

Genetic variation in contemporary South Asian populations follows a northwest to southeast decreasing cline of shared West Eurasian ancestry. A growing body of ancient DNA evidence is being used to build increasingly more realistic models of demographic changes in the last few thousand years. Through high quality modern genomes, these models can be tested for gene and genome level deviations. Using local ancestry deconvolution and masking, we reconstructed population-specific surrogates of the two main ancestral components for more than 500 samples from 25 South Asian populations, and showed our approach to be robust via coalescent simulations.

Our f3 and f4 statistics based estimates reveal that the reconstructed haplotypes are good proxies for the source populations that admixed in the area and point to complex inter-population relationships within the West Eurasian component, compatible with multiple waves of arrival, as opposed to a simpler one wave scenario. Our approach also provides reliable local haplotypes for future downstream analyses. As one such example, the local ancestry deconvolution in South Asians reveals opposite selective pressures on two pigmentation genes (SLC45A2 and SLC24A5) that are common or fixed in West Eurasians, suggesting post-admixture purifying and positive selection signals, respectively.

What they did methodologically is both clever and straightforward. Basically, they managed to assign blocks of the genome to Ancient Ancestral South Indian (AASI) ancestry, and Ancestral North Indian (ANI) ancestry, which is mostly West Eurasian. This is something you would naturally do. The problem is: can you do this well? Recombination breaks apart blocks of ancestry every generation. So doing this with black Americans, who have admixed for >500 years, is relatively easy (long distinct blocks). Doing it for South Asians, whose ancestry has been recombining for at least 2,000 years, and probably more in man cases, is harder (short, less distinct blocks).

The phylogenetic graph that they infer after constructing synthetic ancestral populations, Mask_S (~AASI) and MASK_N (~ANI), is interesting in one particular way: they found that the proto-South Asians diverged before the proto-East Asians and proto-Andamanese. All this happened >40,000 years ago.

Other scholars who have looked at this see a trifurcation where the three groups diverge quickly. To a great extent, the same applies here, but they found some divergence of proto-South Asians (AASI) of Mask_S earlier. I’m not sure if this is real. It could just be errors in their masking process. Additionally, because of geography, the Andamanese may have exchanged more gene flow with the ancestors of modern Northeast Asians. I always like to point out that the Andamanese probably came from modern Burma, and so are the descendants of Southeast Asian Paleolithic people, not South Asian ones.

The researchers also found that the Mask_N population was complex in its history. We also know this, insofar as they’re probably a mix of West Asian agro-pastoralists and later migrants from the Central Asian steppe. These two groups are close to each other compared to indigenous South Asians, but they are still quite distinctive from each other.

The really interesting stuff is selection. I’ve always noticed that the derived, West Eurasian variant, of SLC24A5, was very high in South Asians, while the West Eurasian variant of SLC45A2 seemed to be lower than expected (based on ANI/ASI ratios). These authors find results which suggest that strong positive selection increased the former, and purifying (negative) selection decreased the latter. The haplotype of SLC24A5 is the same in South Asians, West Asians, and Europeans. It is also the same haplotype in “Scandinavian Hunter-Gatherers” from the Mesolithic, and “Caucasian Hunter-Gatherers” from the early Holocene/Late Pleistocene. This is an old variant and an old, but long, haplotype. It is strongly associated with skin depigmentation, but its rather high frequency in South Asia and Ethiopia suggests to me that its selected effect is not known (it is also being selected in southern Africa due to an introduction from West Eurasians via Nilotic peoples).

SLC45A2 in the derived form, unlike, SLC24A5, is restricted to high frequency within Europe, and even in Europeans it is not fixed.

And here’s the non-pigmentation stuff:

Interestingly, we report how loci that include genes involved with diabetes (SETD5), diet (ZNF) and the immune response (HLA) show West Eurasian (N) haplotypes to be significantly more represented compared to the South Asian (S) counterparts. This might be a stark contrast to what is expected, given the long term history of local adaptation of S haplotypes in local environment. We speculate that the diet-related signal may be linked with post-Neolithic dietary shifts that might have followed the arrival of the West Eurasian component in the area, while the overrepresentation of West Eurasian HLA haplotypes might have some similarity, although at a different time scale, with what has happened in Native American populations after recent colonization likely caused by European borne epidemic.

This is strongly suggestive of the fact that lifestyle and mode of production shifts occurred due to introductions from West Eurasia, rather than in situ.

There is some evidence for lots of selection in Europe in the past 2,000 years. Ancient DNA tells us Europeans have been changing in pigmentation, and the frequency of lactase persistence alleles, very recently.

Phylogenetics will eventually be solved. But selection will the big and difficult task in the future.

43 thoughts on “Selection for and against pigmentation alleles in South Asia

  1. Haven’t the Coop and Reich groups both just published eLife papers arguing that selection, if it exists, is very difficult to distinguish from population structure/stratification? Does that caveat only apply to polygenic selection, or would it also affect selection on well-defined oligogenic traits (e.g., skin color)?

  2. that particular issue is with polygenic selection. also, their papers attenuated the signature…there is still possible selection. the SDS work i think from pritchard lab on selection for pigmentation in the british isles shouldn’t be as affected by this since these are big effect loci.

  3. The deep population history of India/South Asia is one of the most interesting topics in archaeogenetics as it relates to understanding the OoA colonization of Eurasia. Modern South Asians are essentially a complicated mix of West and East Eurasians, and if we assume that “ANI” is strictly a Holocene introgression of West Asian Neolithic and Bronze Age Indo-European ancestry, that would imply the East Eurasian layer of ancestry is the base layer of the subcontinent. But I don’t think West Eurasian ancestry in South Asian will prove to be a result of strictly Holocene era population movements. Y-DNA H seems to be the modal South Asian haplogroup, per yfull its main bifurcations are between 20,000-30,000 years ago and their coalescence are all clearly rooted in India, with one notable exception being H2 which seems like it expanded out of Southwest Asia. I think these H-bearing males would have carried a West Eurasian autosomal signature with them to South Asia, where they would have come in contact with older lineages represented by C, D, and probably some sort of K2 representing an “indigenous” paternal stratum of East Eurasian ancestry in the subcontinent.

    I know there’s supposed to be some big study on the IVC coming out or whatever, but I hope we can get some Paleolithic aDNA from South Asia sometime soon. Hell, I’d be pretty excited for any ancient human DNA from any point in the late Middle Paleolithic/Upper Paleolithic time frame (so basically 100,000 to 10,000-20,000 years ago) from any part of the globe, except Europe – we already have enough WHG and older samples from the fringe of West Eurasia.

  4. R1a, yaar. Put you in a cave in Abkhazia and let you out; they’ll accept you as a long lost cousin.

  5. It never occurred to me that it wasn’t obvious that many South Asian folks look exactly like Europeans except for coloration. I thought it was obvious if you’re only looking at facial structure, nose shape, lips, cheeks, and so forth while ignoring hair and skin color. Am I weird for having thought that everyone thought this?

  6. polynices, no. it is obv. to a lot of ppl. my mother says it in bengali, but she once said “our people, whites, and arabs, we have the same countenance.” i think i know what she meant by that. sometimes when a bengali would have very asian features, my mother would say (not in a negative way), “that person looks like ‘the-other-kind'” (translating an idiom there).

  7. Re; facial shape, I’d imagine that with a combination of machine learning that can produce pseudofaces (e.g. https://thispersondoesnotexist.com/image, probably not even state of the art!) and diverse training data yoked to models of ancestry, we could produce some pretty good simulations of what we’d expect AASI to look like based on modern distribution of face shape.

    That could tell us a bit more about how much similar South Asian facial bone structure is related to actual West Eurasian ancestry (Holocene or pre-Holocene), against AASI just possibly having a more similar facial structure to West Eurasians than we might expect from other ENA groups (or at least for the elements which are salient to us – the Uyghurs look clearly half East Asian to us because we know what East Asians look like, while AASI does not really survive and hence we don’t).

    It’s possible that they were like the Jomon / Ainu groups, ““people of the same eye-socket” (as West Eurasians) despite not actually being much related to them (https://en.wikisource.org/wiki/An_Ainu–English–Japanese_Dictionary/Chapter_I/Section_IV – “It is also interesting to remark in this connection that the Ainu distinguish themselves from the Mongolian and Malay type of the human race by calling the latter Oyashikpuikotcha utara, “persons having a different class of eye-socket.” In speaking of men of their own race and cast of feature they say Shineshikpuikotcha utara, “people of the same eye-socket.”)

  8. Matt. Some Asian,especially toward the south of India (but sometimes elswhere in south Asia, and the south of course has a range of features as well) tend to have somewhat broader and sometimes flatter noses than most Western Eurasians—of course some also do not and there is much vatiation—(sometimes along with other features vaguely reminiscient of those of some Australian Aboriginals, but usually to a less prominent degree). This could be the influence of the AASI component.

  9. @Mick, agreed! Sort of surprised that the sporadic discovery of Y-haplogroup H (H2, I think) in Neolithic Near Eastern/Near Eastern-derived populations without a hint of South Asian ancestry has gone pretty much unremarked.

  10. Aryan geneflow would have increased caucasoidness, but wouldn’t ASI have a mostly caucasoid facial features? My understanding ASI = 75% iranian farmer (caucasoid)+25% andaman-like aborigine (australoid).

  11. It’s very obvious that you could cast many Hispanic actresses like Salma Hayek in an Indian movie with no problem, and vice versa.

    I understand there’s a popular actress in India who’s English, not diaspora, and who doesn’t speak a word of any Indian language, but she fits. Although there have been complaints that she “fits” according to a narrow prejudice of desirable skin color, like Hollywood actresses fit a narrow prejudice of desirable body shape.

  12. @ben-canaan

    H2 split from H1’3’4 not long after the coalescence of F; H1 and H2 are about as closely related as O and T. So it’s doubtful whether there’s any meaningful link between H2 and South Asia, or the rest of H and West Asia.

  13. Just realized now that when I posted your washed-out version I forgot to include the link to the lovely Ms. Padukone’s. https://imgur.com/a/IK9kbu6 Which was the point of doing this to begin with, as it was an answer to your original question.

    One billion hours in photoshop. Select skin, use brighten, adjust levels, adjust the tint to pinker tones.

    She looks Welsh or Italian. To be honest though she’s far hotter in brown.

  14. 1) she does look welsh! & yes, she is better-looking dark. why is that?

    2) can you lighten me up more? i’m still freaked out by how ‘central eurasian’ i look

  15. You kind of tend to get a bit of Michael Jackson-ification from banging up the brightness that probably does some weird and unattractive things to the coloration (takes outside of the natural spectra for healthy skin?).

    Another way you could do it is just morph an image by the colour contrast between a South Asian and North European eigenface – https://imgur.com/a/efz9COF.

    But you do kind of get some facial structure coming through there because its still present in the 2d face colour contrast, and some weird artefacting, so that’s still kind of imperfect.

  16. I thought pigmentation or browness in south asia is because of the onge/aboriginal ancestry and that’s why South+Middle are darker as their Onge component is high and by the time you reach the Pathans and North Pak the onge component is much lower hence lighter skin? south asians ain’t just pigmented ‘white’ eurasians primarily cuz of their aboriginal roots as far as I know..if there was no aborigine then there’d be no south asian signature and they’d just be a bunch of west asian pops. living in the subcontinent. is there really need for studies into why brown people are brown…shouldn’t it be focused on why AASI are pigmented in the first place?

  17. coolonice, it his clear for at least 10 years there has been in situ selection for pigmentation genes among south asians. it’s stupid to think it’s just ancestry. slc24a5 is too high, and slc45a2 is too low. this study is pretty neat because it assigned the region around the genome to confirm enrichment of w. eurasian and s. eurasian.

    did you bother to read the second half of the post before you left a comment?

  18. I don’t think AASI looked vaguely “Caucasoid”, like the Ainu.

    As per the recent Indian Austroasiatic paper, the Paniya of South India can be modeled as 30% West Eurasian, 70% AASI. These are some old photos of the Paniya:

    https://upload.wikimedia.org/wikipedia/commons/thumb/2/29/MPP-Pan1.jpg/220px-MPP-Pan1.jpg

    https://i.pinimg.com/736x/b6/fe/4a/b6fe4aa1a071bee2760c6683e57063da.jpg

    Despite being possibly 30% West Eurasian, they honestly look like cranio-facially “robust” Andaman islanders.

    The majority of Indo-Aryan and Dravidian South Asians do fit into the “Caucasoid” phenotype, which is probably just a reflection of West Eurasian ancestry, as Razib noted.

    For what it’s worth, the “West Asian/Iranian plateau” element of South Asian genetic heritage probably survives best among the Toda people of South India.

    https://mir-s3-cdn-cf.behance.net/project_modules/max_1200/6cc5d532414107.56816b89aaf6b.jpg

    https://mir-s3-cdn-cf.behance.net/project_modules/1400/729e0732414107.56816b89abe0c.jpg

    https://kevinstandagephotography.files.wordpress.com/2017/09/ksp_7492.jpg?w=890

    I guess South Asian phenotypes should be between the Toda and the Paniya, but with a slight skew towards northern Europeans (the IA element).

    https://connectgujarat.com/wp-content/uploads/2018/08/59704035-6438-48d9-a8ac-57ab5ca8da2d-e1535019069576.jpg

    Some recentish West Asian layers in Pakistan would further complicate.

    https://media.npr.org/assets/img/2010/08/17/03_punjab__0__86__slide-508b2fd85efa4aaf1e9ef217b770338d9d1bce63-s900-c85.jpg

    Western Pakistanis (like Pashtuns) are (strictly speaking) not South Asians, so their looks don’t count (they have substantial BMAC-related ancestry, much much heavier amounts of recentish West Asian heritage, and a slightly heavier layer of IA-related ancestry). Still, interesting to compare:

    https://c8.alamy.com/comp/B20KK7/two-pashtun-men-gather-in-the-gun-making-town-of-darra-adam-khel-pakistan-B20KK7.jpg

    https://im.indiatimes.in/content/itimes/photo/2015/Aug/27/1440675609-michael-freeman-photography-pathan-55def71450787.jpg

  19. ‘I Googled Indian albino
    They all look like Ron Howard but with hair.

    You, on the other hand look sorta Russian or maybe Armenian. https://imgur.com/a/i9JDKcO

    Razib looks more like Armenian type due to Iran_N farmer genes I suppose, I have a Turkish friend who looks 90% Razib, but with white skin of course.

    ‘I think these H-bearing males would have carried a West Eurasian autosomal signature with them to South Asia, where they would have come in contact with older lineages represented by C, D, and probably some sort of K2 representing an “indigenous” paternal stratum of East Eurasian ancestry in the subcontinent.’

    Ydna H is a pan South Asian marker, ubiquitous in every Indian caste, common in Bangladesh, in Pakistan its significant in Gandhara region; I believe H-men are the first bearer of West Eurasian autosomal signature in South Asia.

    ‘Aryan geneflow would have increased caucasoidness, but wouldn’t ASI have a mostly caucasoid facial features? My understanding ASI = 75% iranian farmer (caucasoid)+25% andaman-like aborigine (australoid).?

    As Razib said, ASI is just ~25% Iran_N, see Paniya tribals, they are also ~25% Iran_N and 75% AASI which makes them a good representative of infamous ASI. Moreover, the Caucasoid or Europid features in south Asian is mainly from Iran_N and partially from Aryans. For example, Non-brahmin South Indians have very little to none Aryan genes, but morphologically they are Europid too due to strong Iran_N. Deepika Padukone is a south Indian from Karnataka, I think.

  20. Nope. Lol. But South Asians, particularly Deepz looks nothing like a West European even non-pigmented. I went to uni in Wales too…but ya’ll can keep on dreaming I guess?

  21. “(it is also being selected in southern Africa due to an introduction from West Eurasians via Nilotic peoples)”

    I think it was via (southern) Cushitic peoples. Nilotic peoples (except for some groups in Cushitic-adjacent regions) don’t normally have West Eurasian admixture.

  22. I think Aishwarya Rai (also a South Indian) could pass for European, and Mila Kunis could pass for Indian. They could be outliers, but clearly there is a phenotype overlap.

    this is a stupid debate. especially of cool is a net-nazi (no idea if)

  23. I think it was via (southern) Cushitic peoples. Nilotic peoples (except for some groups in Cushitic-adjacent regions) don’t normally have West Eurasian admixture.

    nilotes in kenya and tanzania have west eurasian. probably from the cushitic people. just like the sandawe.

  24. 2) can you lighten me up more? i’m still freaked out by how ‘central eurasian’ i look

    Okay, I gave it a whirl. To colour you I sampled Spencer Wells photo with the colour selection tool as he’s about as white as you can get.
    I’m not actually very good at photoshop is the problem.

    https://imgur.com/a/784W6Bb

  25. @Numinous I respect your opinion but personally can’t see it particularly for Mila Kunis or Ashwariya [she’s got the archetypal indian no forehead and looks like a bunch of indian girls they just dont have the eyes]. But I see where you’re coming from.

    And Razib I dont even know what a net-nazi is lmao just a long time follower of ur blog/work…just have a diff perspective thats all.

  26. @NewGuy ‘I guess South Asian phenotypes should be between the Toda and the Paniya, but with a slight skew towards northern Europeans (the IA element).’

    That’s true for North Indians(Gangetic plains), plus I would replace Toda with Balochi type and also would add some Austroasiatic input here and there. Todas themselves look paniya influenced. South Indians are in between Balochis and Paniyas, with no northern euro influence.
    Bengalis exhibit both north Indian and south Indian phenotypes, occasionally with an East Asian influence.

    Gangetic Indian, Bihari students:
    https://media.glassdoor.com/l/639982/nit-patna-office.jpg

    South Indian, Telugu students:
    https://www.thenewsminute.com/sites/default/files/styles/news_detail/public/Naidu_Fathima_College.jpg?itok=bkMbE-v6

    Bangladesh, students from Chittagong:
    http://www.ciu.edu.bd/img/iucc/1.jpg

  27. Don’t think the latest edition of White Razib looks creepy at all; Turkish, maybe, or Greek (obviously a long lost descendant of Alexander the Great)(joke), but I prefer Brown Razib, in a totally manly way, obviously(other joke).

    I also think a lot of women look better with darker skin, but I had always assumed that was just me, given the usual narrative that males prefer pale skinned females. Maybe not. I did grow up among an excessive skin tanning culture, so maybe conditioned by the ‘brown is beautiful’ thing when I was a kid. The most beautiful girls I knew as a kid were from a neighbourhood family of Anglo-Indians who were our buddies and who used to tan to a beautiful colour, and a Dutch-Indonesian girl in my class who was somewhat dark, smelled divine and was a real knockout. So, I have always associated dark hair, eyes and skin with physical beauty. Brown Padukone is far more attractive than White Padukone, no question.

  28. @ Megalophias

    “H2 split from H1’3’4 not long after the coalescence of F; H1 and H2 are about as closely related as O and T. So it’s doubtful whether there’s any meaningful link between H2 and South Asia, or the rest of H and West Asia.”

    There is most definitely a link between H and West (Eur)Asia. H is a middle sibling of G and IJ, which are clearly West Eurasian. K is the only branch in GHIJK that could plausibly be argued to have an Eastern origin, but even that’s not clear given LT’s Western locus. When I mentioned “West Asia” initially, I wasn’t trying to imply that 30,000+ year old H men that entered South Asia were anything like Kurds or Armenians or whatever, but there is almost no chance that lineage entered South Asia from anywhere other than the West. If you’re prepared to argue it came from China or Southeast Asia instead, I would be interested in hearing your reasoning.

  29. @Mick

    Well, I don’t think they teleported there. But the TMRCA of H doesn’t differ significantly from that of K, so H1’3’4 could come from the west with K2 (leaving H2 behind with G and IJ), and it wouldn’t be genetically any more “western” than the founding population of all East Eurasians. Or if H2 back-migrated from South Asia, it need not have been there long enough to have shared South Asian-specific drift. The initial diversification of F happened quite quickly a very, very long time ago, after all.

    (The long shot model for coming from China, or even Island Southeast Asia, would be if the Toba eruption killed most of Homo sapiens in tropical Eurasia – the plume was directed northwestward, IIRC, and the TMRCA of CDEF would fit a sharp bottleneck at that time. This has other problems though.)

  30. “nilotes in kenya and tanzania have west eurasian. probably from the cushitic people. just like the sandawe.”

    They do (though core Nilotes from places like Sudan, esp. South Sudan, do not have West Eurasian admixture), but I was under the impression that the East African admixture in Khoisan groups (particularly in pastoralist northern Khoisan like the Khwe) came from early Cushitic peoples (originally from the Horn region) that migrated through (or to) Tanzania at a time before the Nilotes had migrated (from their home region of Sudan) to Kenya and Tanzania (or at least before most Nilotes had)—Cushitic groups arrived in Kenya/Tanzania there significantly earlier than the Nilotes did. The original people would likely have been hunter-gatherer groups like the Sandawe and Hadza (and perhaps also the Akie) who, especially the first group, eventually received admixture from both Nilotic and Cushitic peoples.

  31. Edit: “—i.e. (as far as I know) Cushitic peoples arrived in Kenya/Tanzania before the Nilotes. The original people of the region would likely have been hunter-gatherer groups like the Sandawe and Hadza (and perhaps also the Akie) who, income cases, eventually received admixture from both Cushitic and Nilotic peoples (and to some degree Bantu).”

    (Re: Hadza and Sandawe genetics—levels of Cushitic and especially Nilo-Saharan admixture, though present, seem to be quite low generally)
    “Genetic Ancestry of Hadza and Sandawe Peoples Reveals Ancient Population Structure in Africa”
    https://academic.oup.com/gbe/article/10/3/875/4935243

  32. “i.e. (as far as I know) Cushitic peoples arrived in Kenya/Tanzania before the Nilotes, and the Nilotic groups that migrated to that region intermixed with Cushitic groups once there (and later, in some cases, with Bantus as well).”

  33. Edit (I appologize for the multiple edits):”…intermixed with Cushitic groups after migrating there (and with local hunter-gatherers, and, in some cases, with Bantus as well).”

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