Journal club of one: ‘The heritability fallacy’

Public debate about genetics often seems to centre on heritability and on psychiatric and mental traits, maybe because we really care about our minds, and because for a long time heritability was all human geneticists studying quantitative traits could estimate. Here is an anti-heritabililty paper that I think articulates many of the common grievances: Moore & Shenk (2016) The heritability fallacy. The abstract gives a snappy summary of the argument:

The term ‘heritability,’ as it is used today in human behavioral genetics, is one of the most misleading in the history of science. Contrary to popular belief, the measurable heritability of a trait does not tell us how ‘genetically inheritable’ that trait is. Further, it does not inform us about what causes a trait, the relative influence of genes in the development of a trait, or the relative influence of the environment in the development of a trait. Because we already know that genetic factors have significant influence on the development of all human traits, measures of heritability are of little value, except in very rare cases. We, therefore, suggest that continued use of the term does enormous damage to the public understanding of how human beings develop their individual traits and identities.

At first glance, this paper should be a paper for me. I tend to agree that heritability estimates of human traits aren’t very useful. I also agree that geneticists need to care about the interpretations of their claims beyond the purely scientific domain. But the more I read, the less excited I became. The paper is a list of complaints about heritability coefficients. Some are more or less convincing. For example, I find it hard to worry too much about the ‘equal environments assumption’ in twin studies. But sure, it’s hard to identify variance components, and in practice, researchers sometimes restort to designs that are a lot iffier than twin studies.

But I think the main thrust of the paper is this huge overstatement:

Most important of all is a deep flaw in an assumption that many people make about biology: That genetic influences on trait development can be separated from their environmental context. However, contemporary biology has demonstrated beyond any doubt that traits are produced by interactions between genetic and nongenetic factors that occur in each moment of developmental time … That is to say, there are simply no such things as gene-only influences.

There certainly is such a thing as additive genetic variance as well as additive gene action. This passage only makes sense to me if ‘interaction’ is interpreted not as a statistical term but as describing a causal interplay. If so, it is perfectly true that all traits are the outcomes of interplay between genes and environment. It doesn’t follow that genetic variants in populations will interact with variable environments to the degree that quantitative genetic models are ‘nonsensical in most circumstances’.

They illustrate with this parable: Billy and Suzy are filling a bucket. Suzy is holding the hose and Billy turns on the tap. How much of the water is due to Billy and how much is due to Suzy? The answer is supposed to be that the question makes no sense, because they are both filling the bucket through a causal interplay. Well. If they’re filling a dozen buckets, and halfway through, Billy opens the tap half a turn more, and Suzy starts moving faster between buckets, because she’s tired of this and wants lunch … The correct level of analysis for the quantitative bucketist isn’t Billy, Suzy and the hose. It is the half-turn of the tap and Suzy’s moving of the nozzle.

The point is that quantitative genetic models describe variation between individuals. The authors know this, of course, but they write as if genetic analysis of variance is some kind of sleight of hand, as if quantitative genetics ought to be about development, and the fact that it isn’t is a deliberate obfuscation. Here is how they describe Jay Lush’s understanding of heritability:

The intention was ‘to quantify the level of predictability of passage of a biologically interesting phenotype from parent to offspring’. In this way, the new technical use of ‘heritability’ accurately reflected that period’s understanding of genetic determinism. Still, it was a curious appropriation of the term, because—even by the admission of its proponents—it was meant only to represent how variation in DNA relates to variation in traits across a population, not to be a measure of the actual influence of genes on the development of any given trait.

I have no idea what position Lush took on genetic determinism. But we can find the context of heritability by looking at the very page before in Animal breeding plans. The definition of the heritability coefficient occurs on page 87. This is how Lush starts the chapter on page 86:

In the strictest sense of the word, the question of whether a characteristic is hereditary or environmental has no meaning. Every characteristic is both hereditary and environmental, since it is the end result of a long chain of interactions of the genes with each other, with the environment and with the intermediate products at each stage of development. The genes cannot develop the characteristic unless they have the proper environment, and no amount of attention to the environment will cause the characteristc to develop unless the necessary genes are present. If either the genes or the environment are changed, the characteristic which results from their interactions may be changed.

I don’t know — maybe the way quantitative genetics has been used in human behavioural and psychiatric genetics invites genetic determinism. Or maybe genetic determinism is one of those false common-sense views that are really hard to unlearn. In any case, I don’t think it’s reasonable to put the blame on the concept of heritability for not being some general ‘measure of the biological inheritability of complex traits’ — something that it was never intended to be, and cannot possibly be.

My guess is that new debates will be about polygenic scores and genomic prediction. I hope that will be more useful.

Literature

David S. Moore & David Shenk (2016) The heritability fallacy

Jay Lush Animal breeding plans. Online at: https://archive.org/details/animalbreedingpl032391mbp/page/n99

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