No evidence for positive selection for human height

Have humans gotten taller? Yes, there is evidence that contemporary people are much taller than their ancestors. This phenomeon is known as secular trend in height and has been particularly marked in the 20th century in Western countries, possibly as a result of improved health care and access to food (https://en.wikipedia.org/wiki/Human_height). Such a fast increase in height is usually taken to show the importance of the environment in physical growth because the timescale of DNA evolution is much larger and cannot take place in a few decades.

However, there is evidence for a reduced mating and reproductive success of shorter males, together with a preference for average height and tall men (Stulp et al., 2014), indicating that sexual selection is at work. This fact would lead us to think that there has been (sexual) selective pressure for taller stature, hence leading to an increase of height-increasing allele frequencies in contemporary human populations.

In a recently published paper, my colleagues and I (Woodley et al., 2017) found a higher frequency of IQ/educational attainment-increasing alleles in contemporary European individuals than in a sample of Bronze Age people from Europe and Western Asia, with odds ratios (for proportion of alleles in ancient vs modern) ranging from 0.8 to 0.9.

Wood et al. (2014) discovered 697 SNPs that were significantly associated with human height. I decided to look up the counts of these SNPs in modern and ancient populations using the same sample of Bronze Age people that was employed for the IQ/educational attainment study.  A 2 x 2 contingency table shows the counts of positive and negative alleles for ancient and contemporary genomes.

Table 1. 2 x 2 contingency table with Positive and Negative GWAS Effect Allele Counts for Ancient and Modern Genomes.

Positive allele count Negative allele count
Ancient Genomes 19283 19277
Modern Genomes 324781 332137

It can be seen that the counts are equally distributed among contemporary and ancient populations. An odds ratio was computed, yielding a null effect (O.R.= 1.022). Fisher’s exact test yielded significance, but this is due to the huge sample size as over 600 SNPs were employed. The magnitude of the effect is very small (and actually favoring ancient populations).

This null finding is paradoxical and hard to interpret in light of the evidence for lower mating reproductive success of shorter males in contemporary populations. It is possible that human stature did not affect reproductive success in traditional societies where female choice was very limited and marriages were arranged by families. Hence the higher attractiveness of taller males (or lower attractiveness of shorter men) might not have translated into different fitness levels.

Indirectly, this finding also strengthens the effect that my colleagues and I found for the educational attainment/IQ alleles because it shows that the method we employed does not have a systematic bias towards modern populations for alleles that have positive GWAS beta. In other words, this finding rules out the possibility that our results were due to an artifact.

All we are left with is a very puzzling finding. One possible explanation is balancing selection, where average height men enjoy higher reproductive success than short or very tall men, as suggested by Stulp et al. (2014). Another balancing force could be male preference for shorter females, counterbalancing the female preference for taller males. Finally, an advantage in times of resource scarcity for smaller bodies requiring less food might have also played a role in producing balancing selection. I am sure endless other interpretations are possible you are welcome to offer yours.

Update: A paper was published in Nature Genetics last week (Capellini et al., 2017) showing selection on alleles reducing height among Eurasians around the GDF5 gene. Hence, whatever sexual selection pressure for larger height might have been counterbalanced by other selective pressures.

References:

Capellini, T.D. et al. Ancient selection for derived alleles at a GDF5 enhancer influencing human growth and osteoarthritis risk. Nature Genetics (2017) doi:10.1038/ng.3911

Stulp, Mills, Pollet, Barrett (2014). Non-linear associations between stature and mate choice characteristics for American men and their spouses. Am J Hum Biol. 2014 Jul-Aug;26(4):530-7. doi: 10.1002/ajhb.22559.

Michael A. Woodley of Menie,1,2 Shameem Younuskunju,3 Bipin Balan,4 and Davide Piffer (2017).  Holocene Selection for Variants Associated With General Cognitive Ability: Comparing Ancient and Modern Genomes. Twin Research and Human Genetics Volume 20, Number 4, doi:10.1017/thg.2017.37

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2 thoughts on “No evidence for positive selection for human height

  1. There may be a simple explanation: in a famine-prone society, the advantage of height (size) for sexual selection is balanced by the disadvantage for avoiding starvation.

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