This analysis of South Asian adult skeletal material demonstrates that compared with a worldwide sample of terminal Pleistocene and Holocene skeletal variation, South Asians have persistently low bone breadth z-score relative to length z-score, indicating relatively low lean mass for stature. Bone breadth z-score (adjusted for length z-score and latitude) among South Asians showed statistically significant increase through time, albeit of very small magnitude and explaining less than 1% of the variation, so relative low lean mass appears to have been a constant characteristic of South Asians across the last 11,000 years. Adjusted for latitude, South Asian bone length z-scores decreased between the Mesolithic and later periods by 1.2 z-scores, indicating a marked fall in stature with the adoption of agriculture, followed by a more gradual decline in stature through to the 20th century.

Our finding that South Asian low lean mass has ancient origins would be most consistent with long-term adaptations to ecological pressures, rather than more recent dietary change or the impacts of 19th–20th century famines exacerbated by British colonial policy. The lack of well-preserved postcranial remains predating 11,000 years BP prevents us from examining earlier trends in South Asian lean mass. Other researchers have noted the relatively “gracile” bones (narrow relative to their length) of Mesolithic South Asians compared with more robust hunter-gatherers34,35,36 and have also attributed this slight build to climatic adaptation35,36. Our data show that this characteristic persists into recent times.

Interestingly, skeletal remains of East Africans and native Australians show similar patterns of low bone breadth relative to length, and by inference low lean mass35. Like South Asians, native Australians have an elevated incidence of NCDs37, relatively low lean mass, a higher proportion of body fat for a given BMI, and a tendency towards abdominal obesity38,39, although their relatively long limbs attenuate some of these contrasts40. South Asia and Australia were both colonised relatively early by dispersals of modern humans, and both subsequently had long periods (tens of thousands of years) for in situ development with relatively low levels of gene flow41,42,43. Whether there is a similar link between low lean mass and T2D susceptibility among South Asians and native Australians, and whether such phenotypic similarities reflect common ecological factors (equatorial climates susceptible to ENSO effects) or potentially neutral processes/shared ancestry could not be addressed here and are questions for future investigation.

Evidence that South Asian low lean mass is strongly heritable might indicate a still-unidentified genetic basis. There is evidence for natural selection near the Myostatin (MSTN or GDF-8) gene among South Asians44, which decreases skeletal muscle mass in fetal and postnatal life, but the nature and effect of any changes to this gene in South Asians remain to be clarified. In a sample of north Indian adults, variants at this locus were associated with variability in lean mass and (abdominal) obesity45. Alternatively, the heritability of low lean mass may originate from an intense cycle of inter-generational plasticity that is hard to break: low maternal lean mass may be the strongest predictor of low offspring lean mass at birth46, and low birth weight (associated with lower lean mass) predicts low adult lean mass47. Fifty generations of undernutrition in a rat model led to the development of a similar phenotype (including low birth weight, central adiposity, insulin resistance, and vitamin B12 and folate deficiency) in the absence of genetic change48. The phenotype largely persisted for 2 generations after returning the offspring to a standard diet (although birth weight and fat mass did show partial recovery), indicating that the South Asian phenotype might plausibly result from multigenerational undernutrition. Our study is unable to shed light on the heritable basis of low lean mass of South Asians but does indicate that it is a longstanding characteristic.

Other factors are also likely to contribute to elevated NCD susceptibility among South Asians. Genetic loci associated with obesity and/or T2Ds have been identified among South Asians49,50, while the impacts of early life environment on later growth and metabolic function may also be partly responsible51,52. Low birth weight is particularly common in India53 and is associated with reduced ‘metabolic capacity’ in adulthood (including muscle mass, pancreatic beta cell mass, and renal nephron number)54,55. Especially under conditions of elevated ‘metabolic load’ (high sugar and fat diets in a context of low activity levels) individuals with lower capacity are more susceptible to obesity and associated NCDs56. All these factors appear to link low lean mass and excess adiposity to NCD risk, and differ on the timescales on which they operate15.

A key component of NCD susceptibility is excess adiposity. Unfortunately, at present there are no methods to reliably estimate body fat from skeletal dimensions57,58,59 so we were unable to investigate temporal trends in fat mass alongside lean mass. Since fat mass is highly plastic, contingent on local environment, age, diet and activity, and largely a result of modernisation, this component of NCD risk is a distinct phenomenon. Lean mass is low in South Asians compared with other populations across the range of BMI8,60 i.e., regardless of obesity status, and thus patterns of lean mass variation are of greater importance for understanding the origin of baseline disease susceptibility.

Unlike the temporal stability in relative lean mass, the marked decrease in mean long bone length z-scores (proxies for stature) between the Mesolithic and subsequent periods coincides with changing patterns of niche construction associated with agriculture, and echoes other studies of South Asia25,26 and other parts of the world23,24. This decline in stature in South Asia following the adoption of food production is estimated elsewhere to be ~9 cm in males26, similar to our results. The decline in stature with the adoption of agriculture appears to have been particularly marked in South Asia (e.g., compare24), although uneven spatial and temporal distribution of the data in different world regions complicates any direct comparison. Decreased stature may indicate an additional increase in underlying NCD susceptibility among South Asians on top of that resulting from low lean mass. Short stature is thought to be associated with T2D susceptibility because, like low lean mass, it is linked to poor early life conditions (potentially across multiple generations), which are also known to increase NCD susceptibility18,61. Interestingly, the relationship between T2D risk and stature is reportedly strongest in Asians and native Australians compared to other populations62.

Although Mesolithic South Asians were generally tall, 4 out of the 5 Sri Lankans, one individual from Damdama and one from Deulga Hills, India63 (the latter could not be included in this study due to poor preservation), had very low bone length z-scores before latitude adjustment. This may indicate some interesting variation in hunter-gatherer body size within South Asia, whereby some populations were extremely short while others very tall. The potential causes of this variation require future investigation.

The continued gradual decline since agriculture was adopted is consistent with previous analyses of skeletal and anthropometric data25,64 and may reflect the ongoing impact of agriculture, exacerbated by more recent societal pressures in a context of severe famines. The limited size and diversity in geography and social status of available skeletal samples for South Asia means there may have been more recent, shorter-term variation in stature and lean mass that we were unable to detect. Therefore the transition to food production or repeated famines may still have influenced relative lean mass in South Asian populations. Nonetheless, unlike the clear decrease in stature with the adoption of food production, relative lean mass does not appear to have altered significantly over the last 11,000 years. This pattern, whereby stature appears to relate more to nutritional factors, while physique (bone breadth and body mass) appears to reflect ecological (climatic) pressures, is consistent with theoretical models and empirical data concerning variation in human skeletal size and proportions65,66.

A limitation of our analyses is that we could not investigate and control for genetic, environmental and other sources of variation across the extensive geographic region of South Asia, which is widely recognised for its genetic, morphological, linguistic and cultural diversity67. Recent studies evaluating large-scale geographic variation in human morphology have incorporated genetic and morphological data to tease apart neutral and adaptive influences on phenotype (e.g.68,69). In the case of South Asia, ancient DNA studies have generally failed due to unfavourable preservation conditions, making links between ancient and modern populations in the region uncertain. Therefore any attempt to replicate combined genetic and skeletal morphological approaches, especially in the light of the small and fragmentary archaeological skeletal samples available, is problematic at present. While variation in T2D rates70, stature25,71 and obesity72 across contemporary South Asia has been documented in association with environmental factors (e.g. urban vs. rural location), the contributions of genetic and geographic influences on this variation are not well understood, and variation in low lean mass in this region is poorly documented. Thus, any attempt to relate the archaeological data with this modern variation would be speculative and has not been attempted here. In vivo body composition data confirm that low lean mass is widespread across the region today, and as South Asians do share a deep common ancestry (see above), a large scale regional approach is justified. We look forward to the time when improved data will facilitate a more nuanced and detailed analysis of intra-regional variation and its causes.

The use of proxies for stature and lean mass is clearly another source of potential error in the dataset, but one that cannot be avoided given that skeletal remains are our only available data source for prehistoric South Asian phenotypes. The proxies we used are well established (as discussed in the Methods), and the use of z-scores rather than estimation equations avoid adding a further step that could introduce further error. Another limitation of the study is that we combined published and novel data because of limited availability of archaeological collections for new study. While this may have added noise to the data due to inter-observer error in the skeletal measurements, we selected only published data collected using methods comparable to our own to limit this effect. Furthermore, inter-observer error in such measurements is generally low73. The preponderance of males in our South Asian samples may have affected the outcomes if any changes in stature or lean mass were stronger in one sex than the other. The use of sex-specific z scores accounts for differences in body size between males and females, and we are not aware of any evidence for sex differences in the relationship between lean mass and type 2 diabetes. Low lean mass characterises contemporary South Asians regardless of sex. It remains possible that patterns of change in lean mass may have differed between the sexes, but the size of the available skeletal sample does not permit us to investigate this question at present. Finally, there are limitations to the accuracy of the sample chronology, as few samples have been directly dated with modern radiometric methods and many rely on older radiocarbon dates calibrated by various methods, or by relative dating using established regional cultural sequences (see Methods for more detail). Again, while this may lead to some noise in the data, the relative age of the different skeletal samples should be robust. All the above factors may have led to more conservative results, but we would not expect them to be sufficient to invalidate our findings (see Methods for further discussion).

In conclusion, our analyses suggest that the low lean mass phenotype characteristic of contemporary people of South Asian ancestry has existed for at least 11,000 years. The available data have insufficient resolution to show whether or not there were further small changes in proportional lean mass since the adoption of food production, or as a consequence of more recent famines. Given the antiquity of this phenotype, the most likely explanations for low lean mass in South Asia appears to be either climatic adaptation or neutral evolutionary processes, but the available data do not allow us to distinguish between these hypotheses at present. Consistent with previous work, our data indicate that stature, which is also associated with elevated T2D susceptibility, fell sharply with the transition to food production, and continued to decline more slowly until the 20th century. The implication of our results is that South Asian low lean mass, and associated NCD susceptibility, may have a genetic basis and is unlikely to change in the short term, so that other strategies (such as behavioural and/or dietary intervention) are required to address the epidemic of NCDs that is particularly acute in South Asia.