Why and when was lactase persistence selected for? Insights from Central Asian herders and ancient DNA.

Laure Segurel,Evelyne Heyer,Nina Marchi,Alexandre Fabre,Romain Laurent,Sophie Lafosse,Céline Bon,Tatyana Hegay,Perle Guarino-Vignon

doi:10.1371/journal.pbio.3000742

Abstract

The genetic adaptation of humans to the consumption of milk from dairying animals is one of the most emblematic cases of recent human evolution. While the phenotypic change under selection, lactase persistence (LP), is known, the evolutionary advantage conferred to persistent individuals remains obscure. One informative but underappreciated observation is that not all populations whose ancestors had access to milk genetically adapted to become lactase persistent. Indeed, Central Asian herders are mostly lactase nonpersistent, despite their significant dietary reliance on dairy products. Investigating the temporal dynamic of the −13.910:C>T Eurasian mutation associated with LP, we found that, after its emergence in Ukraine 5,960 before present (BP), the T allele spread between 4,000 BP and 3,500 BP throughout Eurasia, from Spain to Kazakhstan. The timing and geographical progression of the mutation coincides well with the migration of steppe populations across and outside of Europe. After 3,000 BP, the mutation strongly increased in frequency in Europe, but not in Asia. We propose that Central Asian herders have adapted to milk consumption culturally, by fermentation, and/or by colonic adaptation, rather than genetically. Given the possibility of a nongenetic adaptation to avoid intestinal symptoms when consuming dairy products, the puzzle then becomes this: why has LP been selected for at all?

Highlights

Mongol and Kazakh herders have lactase persistence (LP) phenotypic frequencies of 12% to 30% [15,16], despite 35% of the dietary energetic intake in summer deriving from dairy products in contemporary Mongols [17] and despite the evidence of mare’s milk consumption by pastoralist populations associated with the Botai culture in North Kazakhstan as early as 5,500 before present (BP) [18]
The −13.910 T allele was first seen in Central Europe 5,950 years ago
Regardless, the T allele quickly spread across Eurasia during the late Bronze Age, which is concomitant with the expansion of Yamnaya-associated cultures

Summary

Introduction

Mongol and Kazakh herders have LP phenotypic frequencies of 12% to 30% [15,16], despite 35% of the dietary energetic intake in summer deriving from dairy products in contemporary Mongols [17] and despite the evidence of mare’s milk consumption by pastoralist populations associated with the Botai culture in North Kazakhstan as early as 5,500 before present (BP) [18]. In order to clarify the situation in Central Asia, we obtained data on the prevalence of LP in modern populations with contrasted ancestral lifestyles (herders, farmers, hunter-gatherers) by genotyping a total of 963 individuals from 30 populations corresponding to 13 ethnic groups (Fig 1A, see Methods).

Results

Conclusion