Haplogroup R2 - Highlights from various studies

• The most frequent haplogroups among the Indian upper castes belonged to R subclades (R*, R1 and R2) and that among the lower castes and tribal populations to haplogroup H and the distribution pattern of the major Y-lineages was observed to be similar in tribal and lower caste populations, and distinct from the upper castes thereby suggesting a tribal origin for the Indian lower castes, unaffected by geography.
• The presence of west/central Asian lineages (J2, R1 and R2) and its higher STR diversity in most of the tribes suggested its presence in India much before the arrival of Indo-European pastoralists.
• With regard to the caste populations, a South Asian origin for the Indian caste communities with minimal Central Asian influence was proposed based on the absence of certain haplogroups in Indian samples (C3, DE, J*, I, G, N and O) which covers almost half of the Central Asian Y- chromosomes and the presence of some haplogroups in Indian Y-chromosomes (C*, F*, H, L and R2) that is poor in Central Asia.
• The claims for the association of haplogroups J2, L, R1a and R2 with the origin of majority of the caste’s paternal lineage from outside India, was rejected.
• Indians showed the presence of diverse lineages of three major Eurasian Y-chromosomal haplogroups, C, F and K and the exclusive presence of several subclusters of F and K (H, L, R2 and F*) in the Indian subcontinent (especially H, L and R2) was consistent with the scenario that the southern route migration from Africa carried the ancestral Eurasian lineages to the Indian subcontinent.

Molecular Genetic Perspective of Indian Populations: A Y-Chromosome Scenario
S. Krithika, Suvendu Maji and T.S. Vasulu

• Our analysis revealed that haplogroup R2 characterizes 13.5% of the Indian Y-chromosomes and its frequency among Dravidian speakers was comparable to that of haplogroup H (20.9%) and significantly different from Indo-European and Austro-Asiatic speakers (?2= 16.2, d=3, p<0.05). While the distribution across various geographic regions was almost uniform, significant differentiation was observed along the social groups (?2= 18.7, d=3, p<0.05); a decreasing gradient was discernible as one moved up the caste hierarchy. Although tribes contributed only 7.4% of the total R2 lineage, it was proportionately distributed between the Austro-Asiatic and Dravidian tribes. Extensive analysis of its distribution between north and south Indian populations showed that while there was marginal difference among middle and lower caste groups of north India (17.1 and 17.4 % respectively), a clear gradient was observed among south Indians, where the frequency declined by more than one-half from lower to upper caste groups. Analysis of 20-Y-STRs within the R2 lineage revealed that three haplotypes were shared; one between Kamma Chaudhary and Kappu Naidu, both lower caste Dravidian speakers from Andhra Pradesh and two within Karmali and Pallar populations.
• Four haplogroups; H= 23%; R1a1=17.5%; O2a=15% and R2=13.5%, form major paternal lineage of Indians and together account for ~70% of their Y-chromosomes.
• The observed high frequency of R2 Y-chromosomes in Indians, which is equivalent to that of haplogroup H among Dravidian speakers, corroborates previous reports suggesting its Indian origin (Cordaux et al., 2004). The deep coalescence time for R2 lineages, dating back to Late Pleistocene, supports its indigenous origin. Outside India, it is found in Iran and Central Asia (3.3%) and among Roma Gypsies of Europe, known to have historical evidence of their migration from India (Wells et al., 2001). Within India, while it is predominant in both eastern and southern regions, its distribution pattern is rather patchy in east (Sahoo et al., 2006). It is most likely that genetic drift or bottleneck has reduced the paternal diversity of Karmali, which contributes 28% of the eastern R2 lineages. This population although considered to be Austro-Asiatic speak- er, does not present any evidence of O2a Y- chromosome lineage, portraying a distinctly different history.
• Further, deeper coalescence age for the Y-chromosome haplogroups C, H, R2 compared to O2a is consistent with hypothesis that Austro-Asiatic speakers cannot be considered as the earliest settlers of South Asia.
• Based on deep coalescence age estimates of H, R2 and C Y-chromosome lineages, their diversity and distribution pattern, our data suggests an early Pleistocene settlement of South Asia by Dravidian speaking south Indian populations; the Austro-Asiatic speakers migrated much later from SE Asia and probably contributed only paternal lineages while amalgamating with the aboriginal populations of the region.

High Resolution Phylogeographic Map of Y-Chromosomes Reveal the Genetic Signatures of Pleistocene Origin of Indian Populations
R. Trivedi, Sanghamitra Sahoo, Anamika Singh, G. Hima Bindu, Jheelam Banerjee, Manuj Tandon, Sonali Gaikwad, Revathi Rajkumar, T Sitalaximi, Richa Ashma, G. B. N. Chainy and V. K. Kashyap

• The high frequency and STR diversity of haplogroup R2 in Indians corroborates its Indian origin.
• It has also been reported in Iran and Central Asia with marginal frequency, which more likely suggests a recent migration from India. It is present at high frequency (53%) among Gypsies of Uzbekistan, known to have historically migrated out from India. Interestingly, this haplogroup is absent or infrequent among Gypsies of Europe whose predominant Y chromosome haplogroup is H.
• “The proposition that a high frequency of R1a in India is caused by admixture with populations of Central Asian origin is difficult to substantiate, as the proposed source region does not meet the expectation of containing high frequencies of the other components of haplogroup R, with no examples of R* and generally low incidence of R2, which, unlike J2, does not show evidence of a recent diffusion throughout India from the northwest.  The distribution of  R2, with its concentration in Eastern and Southern India, is not consistent with a recent demographic movement from the northwest. Instead, its prevalence among castes in these regions might   represent a recent population expansion, perhaps associated with the transition to agriculture, which may have occurred independently in South Asia.”
• Departing from the ‘‘one haplogroup equals one migration’’ scenario, Cordaux et al. defined, heuristically, a package of haplogroups (J2, R1a, R2, and L) to be associated with the migration of IE people and the introduction of the caste system to India, again from Central Asia, because they had been observed at significantly lower proportions in South Indian tribal groups, with the high frequency of R1a among Chenchus of Andhra Pradesh considered as an aberrant phenomenon. Conversely, haplogroups H, F*, and O2a, which were observed at significantly higher proportions among tribal groups of South India, led the same authors to single them out as having an indigenous Indian origin.

Gyaneshwer Chaubey et al., “Peopling of South Asia: investigating the caste-tribe continuum in India,” BioEssays 29, no. 1 (2007): 91-100. 

• Similarly, the proposition that a high frequency of R1a in India is caused by admixture with populations of Central Asian origin is difficult to substantiate, as the proposed source region does not meet the expectation of containing high frequencies of the other components of haplogroup R, with no examples of R* and generally low incidence of R2, which, unlike J2, does not show evidence of a recent diffusion throughout India from the north- west.
• Second, it is notable that the results from the ADMIX2 program gave relatively high reciprocal admixture (0.3–0.35) proportions for Northwest Indian and Central Asian populations, despite the incompatibility of the respective haplogroup frequency pools; our Northwest Indian sample totally lacks haplogroups C3, DE, J*, I, G, N, and O, which cover almost half of the Central Asian Y chromosomes, whereas the Central Asian sample is poor in haplogroups C*, F*, H, L, and R2 (with a combined frequency of 10%). Hence, the admixture proportions are driven solely by the shared high frequency of R1a. In other words, if the source of R1a variation in India comes from Central Asia, as claimed by Wells et al. and Cordaux et al., then, under a recent gene flow scenario, one would expect to find the other Central Asian-derived NRY haplogroups (C3, DE, J*, I, G, N, O) in Northwest India at similarly elevated frequencies, but that is not the case.
• Alternatively, although the simple admixture scenario does not hold, one could nevertheless argue that the other haplogroups were lost during a hypothetical bottleneck (lineage sorting among the early Indo-Aryans arriving to India). But in line with this scenario, one should expect to observe dramatically lower genetic variation among Indian R1a lineages. In fact, the opposite is true: the STR haplotype diversity on the background of R1a in Central Asia (and also in Eastern Europe) has already been shown to be lower than that in India. Rather, the high incidence of R1* and R1a throughout Central Asian and East European populations (without R2 and R* in most cases) is more parsimoniously explained by gene flow in the opposite direction, possibly with an early founder effect in South or West Asia.
• Rather, taken together with the evidence from Fst values, the elements discussed so far (i.e., admixture, factor analysis, and frequency distributions) are more parsimoniously explained by a predominantly pre-IE, pre-Neolithic presence in India, for the majority of those Y lineages considered here (R1a, R2, L1), which occur together with strictly Indian-specific haplogroups and paragroups (C*, F*, H) among both caste and tribal groups. The distribution of R2, with its concentration in Eastern and Southern India, is not consistent with a recent demographic movement from the northwest. Instead, its prevalence among castes in these regions might represent a recent population expansion, perhaps associated with the transition to agriculture, which may have occurred independently in South Asia (23). A pre-Neolithic chronology for the origins of Indian Y chromo- somes is also supported by the lack of a clear delineation between DR and IE speakers. Again, although appeals to language change are plausible for explaining the appearance of supposedly tribe-specific Y lineages among incoming IE speakers, it is much harder to conceive of a systematic movement of external Y- chromosome types in the opposite direction, via the uptake of DR languages. The near absence of L lineages within the IE speakers from Bihar (0%), Orissa (0%), and West Bengal (1.5%) further suggests that the current distribution of Y haplogroups in India is associated primarily with geographic rather than linguistic or cultural determinants.
• It is not necessary, based on the current evidence, to look beyond South Asia for the origins of the paternal heritage of the majority of Indians at the time of the onset of settled agriculture. The perennial concept of people, language, and agriculture arriving to India together through the northwest corridor does not hold up to close scrutiny. Recent claims for a linkage of haplogroups J2, L, R1a, and R2 with a contemporaneous origin for the majority of the Indian castes’ paternal lineages from outside the subcontinent are rejected, although our findings do support a local origin of haplogroups F* and H. Of the others, only J2 indicates an unambiguous recent external contribution, from West Asia rather than Central Asia. The current distributions of haplogroup frequencies are, with the exception of theO lineages, predominantly driven by geographical, rather than cultural determinants. Ironically, it is in the northeast of India, among the TB groups that there is clear-cut evidence for large-scale demic diffusion traceable by genes, culture, and language, but apparently not by agriculture.

A Prehistory of Indian Y-Chromosomes: Evaluating Demic Diffusion Scenarios
Sanghamitra Sahoo et al, 2006, The National Academy of Sciences of the USA

• H, L, and R2 are the major Indian Y-chromosomal haplogroups that occur both in castes and in tribal populations and are rarely found outside the subcontinent. Haplogroup R1a, previously associated with the putative Indo-Aryan invasion, was found at its highest frequency in Punjab but also at a relatively high frequency (26%) in the Chenchu tribe.
• Altogether, three clades—H, L, and R2—account for more than one- third of Indian Y chromosomes. They are also found in decreasing frequencies in central Asians to the north and in Middle Eastern populations to the west. Unclassified derivatives of the general Eurasian clade F were observed most frequently (27%) in the Koyas.
• The presence of several subclusters of F and K (H, L, R2, and F*) that are largely restricted to the Indian subcontinent is consistent with the scenario that the coastal (southern route) migration(s) from Africa carried the ancestral Eurasian lineages first to the coast of Indian subcontinent (or that some of them originated there). Next, the reduction of this general package of three mtDNA (M, N, and R) and four Y-chromosomal (C, D, F, and K) founders to two mtDNA (N and R) and two Y-chromosomal (F and K) founders occurred during the westward migration to western Asia and Europe. After this initial settlement process, each continental region (including the Indian subcontinent) developed its region-specific branches of these founders, some of which (e.g., the western Asian HV and TJ lineages) have, via continuous or episodic low-level gene flow, reached back to India. Western Asia and Europe have thereafter received an additional wave of genes from Africa, likely via the Levantine corridor, bringing forth lineages of Y-chromosomal haplogroup E, for example (Underhill et al. 2001b), which is absent in India.
• Given the geographic spread and STR diversities of sister clades R1 and R2, the latter of which is restricted to India, Pakistan, Iran, and southern central Asia, it is possible that southern and western Asia were the source for R1 and R1a differentiation. Compared with western Asian populations, Indians show lower STR diversities at the haplogroup J background (Quintana-Murci et al. 2001; Nebel et al. 2002) and virtually lack J*, which seems to have higher frequencies in the Middle East and East Africa (Eu10 [Ne- bel et al. 2001]; Ht25 [Semino et al. 2002]) and is common also in Europe (Underhill et al. 2001b). Therefore, J2 could have been introduced to northwestern India from a western Asian source relatively recently and, subsequently, after co-mingling in Punjab with R1a, spread to other parts of India, perhaps associated with the spread of the Neolithic and the development of the Indus Valley civilization. This spread could then have also taken with it mtDNA lineages of haplogroup U, which are more abundant in the northwest of India, and the western Eurasian lineages of haplogroups H, J, and T.

The Genetic Heritage of the Earliest Settlers Persists Both in Indian Tribal and Caste Populations
T. Kivisild et al, 2003

• …..the occurrence of Y- chromosome haplogroups L, H, R2, and R1a in both caste and isolated tribal populations suggests much of the existing Indian population structure is very old. Additionally, the high diversity of Y haplogroups R1a1 and R2 in both South Indian and Indus valley populations has led to the suggestion that there is little, if any, genetic influence from other Eurasians on the castes of South India.
• The antiquity and complex geographic distribution of the R1a1 and R2 haplogroups led these authors to conclude that the majority of the subcontinent Y-chromosomes arrived in or before the early Holocene (10,000 years ago) rather than in a later Indo-European expansion. Likewise, and concordant with other studies of tribal Indian populations, we observe Y-chromosome R1a1 lineages in South Indian tribal Irula (unpublished data), a population substantially differentiated from South Indian castes.
• Yet, the occurrence of Y- chromosome haplogroups L, H, R2, and R1a in both caste and isolated tribal populations suggests much of the existing Indian population structure is very old. Additionally, the high diversity of Y haplogroups R1a1 and R2 in both South Indian and Indus valley populations has led to the suggestion that there is little, if any, genetic influence from other Eurasians on the castes of South India.

WS Watkins et al., “Genetic variation in South Indian castes: evidence from Y-chromosome, mitochondrial, and autosomal polymorphisms,” BMC Genetics 9, no. 1 (2008): 86.

• On the basis of the combined phylogeographic distributions of haplotypes observed among populations defined by social and linguistic criteria, candidate HGs that most plausibly arose in situ within the boundaries of present-day India include C5-M356, F*-M89, H-M69* (and its sub-clades H1-M52 and H2-APT), R2-M124, and L1-M76. The congruent geographic distribution of H-M69* and potentially paraphyletic F*-M89 Y chromosomes in India suggests that they might share a common demographic history.
• The decreasing frequency of R2—from 7.4% in Pakistan to 3.8% in Central Asia (Wells et al. 2001) to 1% in Turkey (Cinnioglu et al. 2004)—is consistent with the pattern observed for the autochthonous Indian H1-M52 HG.
• On the basis of a broad distribution—involving all social and linguistic categories in India—and relatively high diversification patterns, it can be concluded that representatives of HGs C5-M356 H-M69*, F*, L1, and R2 have ancestry indigenous to the Asian subcontinent.
• In HGs R1a1 and R2, the associated mean microsatellite variance is highest in tribes, not castes. This is a clear contradiction of what would be expected from an explanation involving a model of recent occasional admixture. Beyond taking advantage of highly resolved phylogenetic hierarchy as just an efficient genotyping convenience, a comprehensive approach that leverages the phylogeography of Y-chromosome diversification by using a combination of HG diversification with geography and expansion-time estimates provides a more insightful and accurate perspective to the complex human history of South Asia.
• When considered at the general HG level, L, R1a, and R2 all display approximate similarity with respect to population-category apportionment and frequency (Cordaux et al. 2004).
• Although it would be convenient to assume that R1a1 and R2 representatives reflect a recent common demography (Cordaux et al. 2004), it is entirely plausible that they harbor as-yet-undiscovered subsequent haplogroup diversification that approximates the phylogeographic patterns revealed for HG L.
• The phylogeography and the similarity of microsatellite variation of HGs R1a1 and R2 to L1-M76 in South Asian tribes argues that they likely share a common demographic history.
• The distribution of HG R2-M124 is more circumscribed relative to R1a1, but it has been observed at informative levels in Central Asia, Turkey, Pakistan, and India. The distribution of R1a1 and R2 within India is similar, as are the levels of associated microsatellite variance. The ages of the Y-microsatellite variation for R1a1 and R2 in India suggest that the prehistoric context of these HGs will likely be complex.
• .... there is no evidence whatsoever to conclude that Central Asia has been necessarily the recent donor and not the receptor of the R1a lineages. The current absence of additional informative binary subdivision within this HG obfuscates potential different histories hidden within this HG, making such interpretations as the sole and recent source area overly simplistic. The same can be said in respect to HG R2-M124.

Sanghamitra Sengupta et al., “Polarity and Temporality of High-Resolution Y-Chromosome Distributions in India Identify Both Indigenous and Exogenous Expansions and Reveal Minor Genetic Influence of Central Asian Pastoralists,” American Journal of Human Genetics 78, no. 2 (February 2006): 202–221.

• The most frequent haplogroup among the Indian upper castes belongs to R lineages (R*, R1 and R2); together, these account for 44% of the upper caste Y-chromosomes. Haplogroup H was the most frequent Y lineage in both the lower castes and tribal populations, with frequencies of 0.25 and 0.30, respectively. The Indian Y-SNP tree (Figure 3) shows that the distribution pattern of the major Y lineages is similar in tribal and lower caste populations, and is distinct from the upper castes.
• The sister clades; R1a1 (M17) and R2 (M124) of the M207 lineage together form the largest Y haplogroup lineage in India, with a frequency of 0.32. They are present in substantial frequencies throughout the subcontinent, irrespective of the regional and linguistic barriers. The haplogroup R-M17 also has a wide geographic distribution in Europe, West Asia and the Middle East, with highest frequencies in Eastern European populations [23]. It is proposed to be originated in the Eurasian Steppes, north of the Black and Caspian seas, in a population of the Kurgan culture known for the domestication of horse, ~3500 ybp [23], and widely been regarded as a marker for the male-mediated Indo-Aryan invasion of Indian subcontinent. However, these observations were contradicted by the higher STR variations observed in the Indian M17 and M124 samples, compared with the European and Central Asian populations, suggesting a much deeper time depth for the origin of the Indian M17 lineages. In the present study, it was observed that the R lineages were successfully penetrated to high frequencies (0.26) in the South Indian tribal populations, a testimony for its arrival in the peninsula much before the recent migrations of Indo-European pastoralists from Central Asia. In a recent study, Sengupta et al [24] observed higher microsatellite variance, and clustering together of Indian M17 lineages compared with the Middle East and Europe. They proposed that it is an early invasion of M17 during the Holocene expansion that contributed to the tribal gene pool in India, than a recent gene flow from Indo-European nomads. However, we found that its frequency is much higher in upper castes (0.44) compared to that of the lower caste (0.22) and tribal groups (0.26). This uneven distribution pattern shows that the recent immigrations from Central Asia also contributed undoubtedly to a pre-existing gene pool.
• The presence of the so called west/central Asian lineages like J2, R1 and R2 in most of the endogamous tribal populations, and its higher STR diversity indicates its presence in the sub-continent much before the arrival of the Indo-European pastoralists. In short, the impact of their arrival in the Indian sub-continent is rather social and political, than genetic.

Ismail Thanseem et al., “Genetic affinities among the lower castes and tribal groups of India: inference from Y chromosome and mitochondrial DNA,” BMC Genetics 7, no. 1 (2006): 42.

• .....it was suggested that a package of Y-HGs (J2, R1a, R2 and L) was associated with the migration of Indo-European people from Central Asia.7 Although our study observed a high frequency of Y-HGs, R1a1, J*/J2, R2 and L, it was not exclusively restricted to any region or population (Table 1). Moreover, most of the population groups from the studied regions showed a less frequency of the highly frequent haplogroups of Central Asia: C3, DE, I, G, J*, N and O, except for some population-specific distributions.
• The percentage distribution of haplogroups in Brahmins (n=256) showed a total of six most frequent (percentage >5%) haplogroups: R1a1* (40.63%), J2 (12.5%), R2 (8.59%), L (7.81%), H1 (6.25%) and R1* (5.47%), contributing to 81.25% of the total distribution in Brahmins. Tribals and scheduled castes (n=254) also showed six haplogroups: H1 (31.10%), R1a1* (20.47%), J2 (10.24%), L (7.87%), H* (7.87%) and O (6.69%), contributing in total to 84.25%.
• All together (Brahmins, schedule castes and tribals), 22 Y-haplogroups were observed. The percentages of seven of these haplogroups (with percentage >5%) accounted for 85.5% of the total number of Y-chromosomes (n=2809). The haplogroups with their percentages in descending order were: R1a1* (21.1%), H1 (19.1%), R2 (10.5%), O (10.1%), L (9.5%), J*/J2 (8.3%) and F* (6.9%).
• Five haplogroups out of 18 were found to be most frequent (>5%) in Brahmins (R1a1* (35.7%), J*/J2 (12.4%), L (11.3%), R2 (10.8%) and H1 (8.0%)) and represented 78.2% of the total number of samples (n =767), whereas haplogroup O was found to be very less frequent (0.7%) in Brahmin Y-chromosomes. Seven out of 14 haplogroups (with percentage >5%) (H1 (24.2%), R1a1* (17.2%), R2 (14.2%), L (12.2%), F* (9.8%), J*/J2 (6.4%) and K* (5.3%)) represented 89.3% of the total number of Dalit Y-chromosomes (n =674). Tribal Y-chromosomes represented by seven out of 20 haplogroups displayed percentages >5%: O (25.5%), H1 (25.3%), R1a1* (10.2%), F* (7.5%), R2 (6.4%), J*/J2 (6.1%) and L (5%) (86% of the total number of samples (n=1368)).

Swarkar Sharma et al., “The Indian origin of paternal haplogroup R1a1* substantiates the autochthonous origin of Brahmins and the caste system,” J Hum Genet 54, no. 1 (January 9, 2009): 47-55.

(Y Haplogroups and Aggressive Behavior in a Pakistani Ethnic Group)

• Five Y haplogroups that are commonly found in Eurasia and Pakistan comprised 87% (n=136) of the population sample, with one haplogroup, R1a1, constituting 55% of the sampled population. A comparison of the total and four sub-scale mean scores across the five common Y haplogroups that were present at a frequency >=3% in this ethnic group revealed no overall significant differences. However, effect-size comparisons allowed us to detect an association of the haplogroups R2 (Cohen’s d statistic5.448–.732) and R1a1 (d5.107–.448) with lower self reported aggression mean scores in this population.
• Mean scores were lowest for haplogroup R2 (58.83) and highest for J2a2 (74.60).
• Using measures that are independent of sample size, we were able to detect an effect-size association of haplogroups R2 and R1a1, with lower mean scores indicating that the male-specific regions of the Y chromosome may contribute to self-reported human aggressive behavior. Both R1a1 and R2 share a common ancestor on the Y phylogenetic tree [Karafet et al., 2008] and membership in haplogroup R defined by the M207 mutation accounts for a small effect size (Cohen’s d statistic=.120) and 6% of the variance in the mean scores (r =241). This association of haplogroup R, which is a frequent haplogroup found in extant Indo-European populations, raises an intriguing possibility that behavior could have played a role in its evolutionary selection.

S. Shoaib Shah et al., “Y haplogroups and aggressive behavior in a Pakistani ethnic group,” Aggressive Behavior 35, no. 1 (2009): 68-74.