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Breakdown of Lactase Persistence Paper
Dairying, diseases and the evolution of lactase persistence in Europe - Evershed et al 2022
A huge paper was published in Nature on July 27th looking at the evolution of lactase persistence in Europe. The aim was to try and resolve an old problem - how and why did certain populations become tolerant of dairy in prehistory. Lactase persistence (LP) - the genetic adaptation which allows adults to produce the lactase enzyme post-childhood - is a confusing phenomenon. It seems that it should map one-to-one with dairy consuming peoples, ie those populations in the world who consume dairy should show lactase persistence and those who do not should not have this adaptation. But this is not the case and even pastoralists such as the Nilotic Dinka, who have consumed dairy for millennia, do not show genetic lactase persistence. Therefore the question stands - how and why did some people come to drink milk?
The paper takes two approaches: to map the spread of dairy consumption in Europe and match it to known LP markers, and to investigate a modern population to see what benefits LP offers.
Modelling the spread of dairy in Europe
In order to map the origins and spread of dairy consumption the researchers turned to lipid residue analysis. Put simply, pottery can absorb fats and other molecules which are protected from microbes and the elements. This means archaeologists can extract the fats and proteins and examine them to determine what foods or liquids the pottery may have held or what may have been cooked in them. This isn’t a straightforward process since there are very few molecules which can be definitively matched to one substance, so a complex set of methods looking at isotope ratios and other techniques are used to infer the contents of the pots.
For this paper the researchers took already published datasets:
Overall, we used 6,899 animal fat residues derived from 13,181 potsherds from 826 phases from 554 sites, with associated georeferences and phase chronology including more than 1,000 radiocarbon dates. These data were used to generate time series depicting the frequency of milk use across prehistoric continental Europe from 7000 BC to AD 1500 and regional time series
From these huge collections they were able to build a spatio-temporal map of dairy use in prehistoric Europe. A few key points jump out:
Early Greek Neolithic communities appear to be dairy-free, based on pottery analysis. This is something of a mystery but may simply be that Greek communities used different, non-ceramic, containers for their dairy.
The prehistoric Balkans was the core region for the early intensification of milk use, which is consistent with the rise of cattle exploitation there.
Dairy consumption was NOT consistent across the Neolithic and Bronze Age periods, there are substantial levels of fluctuation, probably reflecting the farming boom and busts across the millennia.
This second map certainly surprised me, the early dairy dates in Belarus and the Baltics seem far too early. This seems to suggest that hunter-gatherers were consuming dairy in northern Europe as soon as the first Neolithic farmers appeared in Europe. This paper looking specifically at Baltic, Polish and Belarusian ceramic analysis shows the earliest dates for Estonian pottery to be 5500 BC, but these were certainly not used for dairy, but for fish. I suspect the authors of this dairy paper have made a mistake in their dating here.
Origins of LP
To look at the genetic origins of LP the researchers looked at the genetic marker for LP in 1,786 prehistoric European and Asian individuals. The earliest appears around 4600 BC and becomes appreciable in a population around 2000 BC. The researchers attempted to match LP markers to frequency of pottery evidence for dairy but this yielded no pattern at all. Finally they looked at LP incidence against latitude, which showed higher frequencies of the LP allele in more northern regions (UK and Scandinavia) which supports the traditional idea that dairy assists in vitamin-D and calcium assimilation at higher latitudes.
The boom and bust fluctuations of dairy use in the Neolithic and the use of dairy long before LP was stable in European populations prompted the researchers to look at modern populations to see what health benefits are evident from dairy consumption, to help understand if this drove LP adaptation.
The UK Biobank includes genotypic and phenotypic data from about 500,000 people aged between 37 and 73 years, recruited between 2006 and 2010 (http://biobank.ndph.ox.ac.uk/showcase). In a subset of approximately 337,000 unrelated participants who classified themselves as ‘white, British’ and have similar genetic ancestry.
Looking at this modern UK population of white British people, the researchers found the following surprising results:
There was no association between lactose tolerance and dairy in the diet. Lactose intolerant people still consumed dairy in similar quantities to LP people: “Around 92% (95% confidence interval (CI) 91.5–92.2%) of genetically LNP participants mainly use fresh cows’ milk instead of soya or no milk and only 2.5% of milk consumers reported following a lactose-free diet (95% CI 2.4–2.7%). This suggests that LP has only a small effect on milk consumption and use of lactose-free products is not an explanation”
LP individuals had a higher BMI but showed no difference in height between themselves and lactose intolerant people.
No difference in vitamin D and calcium levels between LP and non LP individuals.
LP allele association with all-cause mortality, mother’s age of death and father's age of death, were all close to the null. These results suggest that milk has little or no adverse health effect when consumed by lactose intolerant adults in a contemporary population
There was no difference in fertility, measured by number of children, between LP and non LP individuals.
While this seems to contradict the theory that milk offered nutritional and health advantages to prehistoric populations, this seems to me to be very weak evidence. Firstly modern populations do not consume dairy in anything like the amounts that even our recent ancestors did. According to the DEFRA Family Food Survey, UK families have halved their liquid milk consumption since 1974, from 140 to 70 litres per year per person. Secondly modern populations are buffered from the effects of malnutrition and ill health through extensive food fortifications, childhood vaccinations and antibiotics, making any comparison of health between two population subsets very difficult, let alone comparing them to prehistoric populations. Third the quality of milk is difficult to compare between prehistoric and modern consumers. Personally I think this kind of analysis does little to shed light on the advantages of dairy to a Neolithic community, in almost every way we are different and protected against disease, flattening the health benefits of almost any one foodstuff in a large dataset. Vitamin D supplements and calcium fortification in beverages, including non-dairy plant milks, would obscure the prehistoric differences and the advantages of dairy.
However, what this data does seem to support is the hypothesis that lactose intolerance is not detrimental to one’s health, even when consuming dairy. The authors point to the huge recent growth in Chinese milk consumption to support this proposal.
The Chronic and Crisis Mechanism of LP Evolution
The authors are convinced from their data on modern populations that dairy offers little health advantage to a population, so they turn to alternative explanations to understand LP evolution. Rather than look at the health benefits, they look instead at what advantages dairy offers to a population in crisis.
Following their argument so far:
Dairy use was widespread from the onset of the European Neolithic
Dairy use fluctuated, likely with the boom and bust of early farming communities
Lactase persistence offers no clear benefits over lactose intolerance
Being lactose intolerant does not appear to have any negative health consequences
From these points the researchers highlight two key scenarios where LP might have been selected for: famine and disease.
Given the widespread prehistoric exploitation of milk shown here (Fig. 2) and its relatively benign effects in healthy LNP individuals today, we propose two related mechanisms for the evolution of LP. First, the detrimental health consequences of high-lactose food consumption by LNP individuals would be acutely manifested during famines, leading to high but episodic selection favouring LP. This is because lactose-induced diarrhoea can shift from an inconvenient to a fatal condition in severely malnourished individuals and high-lactose (unfermented) milk products are more likely to be consumed when other food sources have been exhausted. This we name the ‘crisis mechanism’, which predicts that LP selection pressures would have been greater during times of subsistence instability. A second mechanism relates to the increased pathogen loads—especially zoonoses—associated with farming and increased population density and mobility. Mortality and morbidity due to pathogen exposure would have been amplified by the otherwise minor health effects of LNP in individuals consuming milk—particularly diarrhoea—due to fluid loss and other gut disturbances, leading to enhanced selection for LP. We name this the ‘chronic mechanism’, which predicts that LP selection pressures would have increased with greater pathogen exposure
This is a neat theory, essentially pointing to the two events which would would differentiate LP and non LP individuals, where otherwise they would be indistinguishable. This, combined with the increasing frequency of LP at higher latitudes, paints a picture of LP evolution through a combination of health benefits and periods of famine and disease, selectively sweeping through communities and promoting LP in surviving generations.
However, this scenario doesn’t explain why Neolithic communities chose to consume milk to begin with, if there really are no health advantages. The authors concede that many other scenarios are plausible, if harder to test empirically:
Other plausible proposals for selection favouring LP in Europe, such as milk as a relatively pathogen-free fluid, milk allowing earlier weaning and thus increased fertility, milk galacto-oligosaccharide benefits for the colonic microbiome or higher efficiencies of calorie production from dairy farming are more difficult to assess.
Overall this is the kind of paper we need and are seeing more of. Big scientific and genetic datasets providing spatio-temporal stories about human evolution integrated with traditional archaeological work. However this can come at a cost, as I suspect we might be seeing with the dating on the pottery work here. The hypothesis of LP evolution is compelling, although claims about the lack of any benefits to dairy consumption seem based on a poor analogy with modern populations. The map of dairy consumption through the Neolithic is fascinating, as it seems more like a fluctuating patchwork rather than a consistent feature of life. Someone may be able to match up these periods with fine scaled local archaeological data to tell smaller stories of famine and disease amongst early farming communities. What is left to explore here is how this theory matches up with LP evolution across the world, and whether the crisis and chronic mechanisms have any parallel on the Eurasian steppe, East Africa and the Middle East for instance.
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