Email to Dennis Venema about human population bottlenecks


Posted 29th September 2017

A few months ago, I was reading a new book by Dennis Venema and Scot McKnight entitled Adam and the Genome. I was surprised to find a claim within the book that the past effective population size of humans has definitely never dropped below 10,000 individuals and that this is a fact of comparable scientific certainty to heliocentrism. I emailed Dennis Venema, the biologist author of the book, to query this. Unfortunately, he has not yet responded. I therefore remain unconvinced that it is a scientific impossibility for human beings to have all descended from a single couple. If I am wrong, though, I would like to know. I therefore post my email here, in hopes of garnering responses to my objections. When I have time, I may post a blog on this topic, which would be more polished and tie up some of the loose ends [Note added on 28th October 2017: I have now blogged about this here].
From: Richard Buggs
Subject: Human population bottlenecks
Date: 10 May 2017 at 19:05:18 BST
To: Dennis Venema

Dear Dennis,

I hope you don’t mind me emailing you out of the blue. I am a biologist and a Christian. I have recently been asked by a couple of friends from my church in London about the issue of a historical Adam and Eve. They are studying for ordination at a local Church of England theological college, and were set an essay on the topic by one of their lecturers. In this context, I have been reading your recent book "Adam and the genome”.

Whilst I very much sympathise with your desire to bring science and the bible together, and help Christians not to be alienated from science, I have a few concerns about the parts of chapter three in your book on past effective population sizes. This is an areas that I have had a fair bit of exposure to over the past few years, having, for example published PSMC analyses in my research (see Nature 541: 212–216). [I then mentioned a couple of my MSS in preparation.]

I was a bit surprised that you categorically state in your book that the past human effective population size has definitely never dropped below 10,000 individuals and say that this is a fact of comparable scientific certainty to heliocentrism. Most people working in the field take reconstructions of effective population size with a pinch of salt. I well remember my surprise as a newly graduated PhD student attending a summer school on molecular evolution at Edinburgh University in 2005 on hearing Gil McVean from Oxford say over breakfast that effective population size is a nebulous concept. As I am sure you know, effective population size is a measure of a population’s susceptibility to drift, rather than an attempt to measure census population size. I would be very hesitant to rely too heavily on any estimate of past effective population size.

To get more specific, I think you are mistaken when you say this:

"If a species were formed through such an event [by a single ancestral breeding pair] or if a species were reduced in numbers to a single breeding pair at some point in its history, it would leave a telltale mark on its genome that would persist for hundreds of thousands of years— a severe reduction in genetic variability for the species as a whole”

It is easy to have misleading intuitions about the population genetic effects of a short, sudden bottleneck. For example, Ernst Mayr suggested that many species had passed through extreme bottlenecks in founder events. He argued that extreme loss of diversity in such events would promote evolutionary change. His intuition about loss of diversity in bottlenecks was wrong, though, and his argument lost much of its force when population geneticists (M. Nei, T. Maruyama and R. Chakraborty 1975 Evolution, 29(1):1-10) showed that even a bottleneck of a single pair would not lead to massive decreases in genetic diversity, if followed by rapid population growth. When two individuals are taken at random from an existing large population, they will on average carry 75% of its heterozygosity (M. Slatkin and L. Excoffier 2012 Genetics 191:171–181). From a bottleneck of a single fertilised female, if population size doubles every generation, after many generations the population will have over half of the heterozygosity of the population before the bottleneck (Barton and Charlesworth 1984, Ann. Rev. Ecol. Syst. 15:133-64). If population growth is faster than this, the proportion of heterozygosity maintained will be higher.

This means that a single pair of individuals can carry a great deal of heterozygosity with them through a bottleneck, if they come from an ancestral population with high diversity, and they will pass that on to the population they found, so long as it grows rapidly.

As you will know, it is a feature of humans that despite our current census population size of over seven billion individuals, we have lower genetic diversity than the world’s much smaller current day population of chimpanzees. The average human has 3.1 million single nucleotide variants (SNVs), but the average chimp has 5.7 million (Prado-Martinez et al 2013 Nature). African humans approximately 1.1 heterozygous SNVs in every 1000bp, whereas central chimpanzees have approximately 1.75 (Prado-Martinez et al 2013 Nature). Thus, if two central African chimpanzees were taken today and used to found an isolated population that experienced explosive population growth, the new population would have similar levels of genetic variability to modern humans.

I am not stating these figures because existing populations of chimpanzee gave rise to modern humans, but simply to show that it is hard to see how overall levels of SNP diversity and heterozygosity in modern humans could exclude the possibility of a past bottleneck of two individuals.

On top of this, we need to add in the fact that explosive population growth in humans has allowed many new mutations to rapidly accumulate in human populations, accounting for many SNPs with low minor allele frequencies (A. Keinan and A. G. Clark (2012) Science 336 (6082): 740-743).

I am also concerned about your interpretation of PSMC analysis. I do not think that a PSMC analysis that never drops below an Ne of 10,000 can be used to prove that a sudden, short bottleneck never happened. Because a single couple can carry with them 0.75 of the heterozygosity of their ancestral population, we would not expect a huge number of coalescence events at the bottleneck, and those that are there were would be smeared out over a long period of time around the bottleneck, as within the orginal Li and Durbin 2011 paper, the authors note:

“The simulations did, however, reveal a limitation of PSMC in recovering sudden changes in effective population size. For example, the instantaneous reduction from 12,000 to 1,200 at 100 kyr ago in the simulation was spread over several preceding tens of thousands of years in the PSMC reconstruction.” (Li and Durbin 2011).

Work by a graduate student in Beth Shapiro’s lab has shown that the PSMC method cannot accurately reconstruct sharp bottlenecks (https://users.soe.ucsc.edu/~chkcole/Shapiro.html).

In general, I am concerned that the studies you cite did not set out to test the hypothesis that humans have passed through a single-couple bottleneck. They are simply trying to reconstruct the most probable past effective population sizes of humans given the standard assumptions of population genetic models. I personally would feel ill at ease claiming that they prove that a short sudden bottleneck is impossible.

Sorry to send an email of such length, but I wanted to let you know that in my view you seem to be on very shaky ground here, and in danger of alienating Christians from science on the basis of a wrong interpretation of the current literature. In this case, I think you are being a bit over-zealous for science, and insisting on an overly literal interpretation of the past Ne literature. I would encourage you to step back a bit from the strong claims you are making that a two person bottleneck is disproven. Maybe you could write a blog dialing back on this a bit?

With best regards,

Richard