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Males were saved by agriculture

Science China Press

Once upon a time, settlers in the Fertile Crescent of West Asia domesticated few wild plant and animal species. To be precise, it was about 11-12 thousand years ago (kya), and nowadays we name this behavior as, agriculture.

The emergence of agriculture is suggested to have driven extensive human population growths, because food production by agriculture can support far higher population densities compared to hunting and foraging. Nevertheless, like the famous question "chicken or the egg", dispute between agriculture and initial population expansion in Neolithic Time exists for long.

Despite historical and archaeological efforts, previous genetic work such as mitochondrial DNA analysis in worldwide populations found that most major maternal lineage expansions began after Last Glacial Maximum (LGM, about 15 kya) but before the first appearance of agriculture, and the increase of population size was likely the driving force that led to the advent of agriculture. There are also numerous studies on population expansion using paternal Y chromosome single nucleotide polymorphism (SNPs) in the genealogical tree and rapidly mutating short tandem repeats (STRs) yet without an convincing result, owning to the fact that nonrandom sampling of SNPs can result in an ascertainment bias, and to choose whether the evolutionary rate or the genealogical rate of STRs in Y chromosome dating is controversial, since the result can be almost three-fold difference.

As science and technology update rapidly, entirely sequenced Y chromosomes in numerous human individuals have only recently become available. With the next-generation sequencing technology, the 1000 Genomes Project has sequenced whole Y chromosomes from more than 500 males, which provides a wonderful chance to estimate population sizes through time from a set of globally distributed populations without ascertainment bias.

To resolve the long dispute, researchers in Fudan University analyzed about 8.9 mega-base pairs on the unique regions of Y chromosome and whole mitochondrial genomes of 526 male individuals from three African, five European, three Asian and three American populations sequenced in the 1000 Genome Project.

A maximum likelihood tree was constructed using Y chromosomal SNPs. Containing samples from haplogroup A, B, C, D, E, G, I, J, N, O, Q, R, and T, the tree is a good representation of geographical paternal lineages. To infer the expansion time, researchers calculated the date of each divergence event throughout the tree using Bayesian method with a constant mutation rate. The outcome demonstrates that most major paternal lineage expansions coalesced in Neolithic Time. In other words, these Neolithic expanding clades comprise a large proportion of current population.

Researchers then estimated effective population size through time via coalescent Bayesian Skyline plots to infer population size changes during the LGM and the advent of agriculture. Rapid, roughly exponential population growth in most European and Asian maternal lineages occurred right after the LGM (12-8 kya), followed by a long period of very slow growth (since 8-7 kya). However, at the paternal side, all the populations show the most pronounced expansion from 6.5 kya to 2 kya, with a 10- to 100-fold increase in population size. The fastest growth intervals for global male populations range from 1.5-3.3 kya, which are 1-3 ky later than the advent of agriculture.

The correspondence between the coalescence age of most paternal lineages and the population growing periods observed in skyline plots suggested that the initial male population expansion began within the Neolithic Time, probably due to the advent and spread of agriculture. "Agriculture has provided a much more stable food supply than hunting and foraging, leading to higher population fertility and infant survival rate, more importantly, as agriculture has kept male away from dangerous hunting, the reduction in hunting-related mortality of males might contribute most to this sex-biased Neolithic expansion," they supposed.

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This research was funded by the National Excellent Youth Science Foundation of China (31222030), National Natural Science Foundation of China (91131002), MOE Scientific Research Project (113022A), and Shanghai Shuguang Project (14SG05).

See the article: Wang C C, Huang Y Z, Yu X E, et al. Agriculture driving male expansion in neolithic time. Sci Sin Vitae, 2016, 46: 468-474, doi:10.1360/N052016-00126 http://engine.scichina.com/publisher/scp/journal/SSV/46/4/10.1360/N052016-00126?slug=abstract

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