What if Rev Jenyns had agreed? Part II. Would evolutionary theory be different from a population perspective?

In yesterday's post I noted some general differences between Darwin's individual-centered theory of evolution, and AR Wallace's more population-focused ideas.  Of course they both developed their ideas with the kinds of knowledge and technology then available, so we can use them to represent differing points of view we might hold today, but must realize that that is symbolic rather than literal. They were who they were, both skilled and perceptive, but their ideas were subject to modification with subsequent knowledge. One major piece of knowledge that emerged after their time was that genes are point causes of biological function, that is, single locations in DNA with distinct activity.
But that knowledge was derived from Mendel, Morgan, Watson, Crick and a host of others, who, following Mendel, pursued genetic function with independent point causation as the assumed starting point that drove their study designs.  DNA may be atoms on a string, but the assumption was misleading then, and still is today.

Alfred Russel Wallace

The modern theory of evolution, population genetics, is based on genes as point causes, and it recognizes the local nature of evolution in time and space.  A genetic variant's chances of spreading in a population are, naturally enough, seen in population perspective.  But by and large that perspective is about a genetic variant, and indeed attempts to explain functional and adaptive evolution from a single gene's point of view.  The variant's success depends on the relative success of other variants at the same locus--competition.  Of course that success depends on many things, but this perspective basically just 'integrates' away all factors other than the gene itself, computing a net-result picture.  It is very 'Darwinian' in the sense of being strongly deterministic and considering genes as points individually competing with each other for success.

This is not a fallacious picture, but I think it's not terribly relevant to the kinds of questions most people are asking these days, both in evolution and in biomedical genetics.  One needn't deny that individual genetic variants don't have their differential success over time, or that we can't or shouldn't be aware of nucleotide differences.  To do so would be something like denying that a house is made of bricks, the bricks can be identified and enumerated, and they have something to do with the nature of the house.  The question is the degree to which you can explain or predict the house from the enumeration of the bricks.

There are those who suggest that evolution is more about interaction at the genome level than it is about single alleles; enumerating bricks is not enough. However, the allele-focused view would have it that it is only the 'additive' aspect of each individual allele's effect on its own, that is transmitted. The idea is that even if the combination of alleles at and among loci affect an individual's traits (roughly, this is called 'epistasis'), s/he only transmits a roughly random half of those to each offspring.  Thus, the combination effect is not inherited.  Epistatic holism is an evolutionary hoax.

This venerable riposte to those arguing for a more 'holistic' or complex genomic viewpoint may be mathematically true in the abstract, but misses an important point.  In fact, the fitness (reproductive success) of a given allele entirely depends on the rest of the genome and the external environment.  If you just think about how life works (that is, metabolism, morphology, and many other complex interactions), the dependency is very unlikely to be simply additive. Things work, things adapt in combinations.  But we'll see below how this squares with the additive-only view.

In fact, the collective context-dependency of each allele's functional effects means that the evolution of a population is dependent on its mix of genomic variation--which brings us back to Wallace, and is what group selection is properly about.

Group selection: why a bad reputation?
Group selection got a bad reputation in part when a book by VC Wynne-Edwards was published in 1964 that claimed that in many species, individuals restrained their reproduction essentially for the good of the group (whether or not this was done knowingly for that purpose).  This was a kind of fitness-related altruism that was ridiculed on the grounds that if I restrain my reproduction for the good of the group, others may not be so restrained and any genetic variant that led me to do what I did would thus be out-competed.  So group selection was out, but WD Hamilton introduced concepts of extended kinship to explain altruistic behavior, such as why I might help someone at a cost to myself--if that someone were a relative, for example.  Hamilton's rule became dogma and explains much of the sociobiology of our era still today (though the rule doesn't really work very well when closely tested).

In this sense, group selection was viewed or modeled as driven by single genes and the argument was how an individual 'altruism' gene could possibly sacrifice itself and still get ahead, the one coin of the realm recognized by the most strident of Darwinists.  In recent years, various defenses of the idea and proposed mechanisms have been offered, usually with no reference to Wallace's more ecological concept.  The reason his views might be relevant is not that he thought about this in modern terms, but because he recognized that the collective qualities of the group--its overall members' traits--are what affects the group's chances of confronting the environment or other populations that it faces.

But in fact I think that while the evolution of altruism is an interesting question, it is a red herring that has given group selection a bad name.  Because there is a lot more about group selection than that gene-centered, restricted argument would suggest, and it's fundamental to life.  Indeed, it is possible that Wallace's idea, that the properties of the group determine its success, is more cogent than the gene-focused version--but for different, wholly non-mystical reasons.

Group selection, more properly conceived
The answer in brief is not a new fact but a different way of weighing the facts.  It is based on the indisputable fact that DNA is, by itself, quite an inert molecule. Anything it does is only in context.  The chance of an allele being successful depends on what else it finds itself combined with.  If in that context, the allele's effects are harmful, it has reduced prospects.  But if it finds itself in genomic and environmental circumstances in which it functions well, it can proliferate.

But what determines those genomes?  It's the relative frequency of their alleles in the population.  This is the result of the genomic history of the population as a reproducing unit.  Unless quickly removed, our new allele will see itself, probabilistically, in the company of other variants in the individuals who carry it.  If the number of those variants, and/or their frequencies, in which it can have positive effect is high enough, it has an increased chance of proliferating.  This is, in a legitimate sense group selection, because genomewide the success of the group depends on its collective distribution of alleles.  (Here we're not considering how that collective success operates, whether in terms of mating, avoiding predators, finding food, dealing with local climate, etc.).

The same variant that does very well in one genomic or environmental setting may do very poorly in another.  This is another manifestation of the central fact that a variant has no predetermined effect on its own.  It's why personalized medicine, based on predicting disease from genotypes, has a long way to go, at best, for other than very severe, largely early onset traits.

It is not that the individual variant, or the individual person, isn't important, or that we can't trace the frequency change of the variant, just as has been done for decades by population genetics theory.   But it misses the important collective aspect of an allele's success.  It's like the fact that we can count the bricks that make up our building, but we are hard-pressed to understand the building that way.

Over time, a successful population accumulates enough variants in enough genes that enough newly arising alleles are in favorable 'soil' to confer viable effects on individuals who bear them.  A population depauperate of enough of an allelic mix, genomewide, dies out.  This is, in every meaningful and non-mystical sense, a group phenomenon and if the term hadn't already been abused, group selection.  If a population perspective is really the most important one for understanding genome dynamics, then our usual genetic reductionism is misplaced.  

The Normal (bell-shaped) distribution of so many traits, like stature; UConn WWI recruits

Everyone in a population differs a bit but most people, for most traits, are rather near the middle.  The roughly Normal (bell-shaped) distribution of traits like human stature is a reflection of this.  There are those in the high- or low-end tails (very tall or very short), but most are near the middle.  There is a strong 'central tendency'.  Where does that come from?  It is a direct reflection of an evolution that makes most people inherit what in their collective ancestry has evolved as a 'fit' state for that population's circumstances.  There are always new mutational variants arising, and if the population--the 'group'--had not evolved this central tendency, it would not be a healthy one, and that would affect the likely fate of new mutations.  There are exceptions, but the restricted variance of natural populations, the tendency of most individuals to be quite similar, reflects what is, in fact, a form of group-selection history.

A major way in which this can arise, given that we have genomes made of multiple chromosomes and there is recombination and we are diploid but pass on only half our genome complement, is for many different genomic factors to affect a trait--for it to be 'polygenic'.   I think that it is the assembly of many more or less equivalent parts, independently segregating, that enables most individuals to inherit what the population's previous history has proved viable, that is, multiple independent contributors is why such central-tendency, limited-variance characteristics are so widespread.  Gene duplication and other processes help generate this state of affairs.  It's the way molecular interaction works; if things had been too genetically unitary, survival would have been more precarious.

From this perspective, the standard 'selfish gene' viewpoint's denial of the importance of epistasis and other contextual elements of gene function is off the mark.  It misperceives the nature and vital importance of the population in which these combinations exist, and the necessity that those factors be there, in enough numbers and/or with high enough frequency.

So, Wallace again?  But wait--isn't it individuals who reproduce or not?
But what about those individuals, on whom a century of population geneticists and countless popular science writers, have placed their hyper-competitive hyper-individualized stress?  The individual, driven by some critical genetic variant survives or not.  Individuals as wholes are viewed (or should we say dismissed), essentially, as mere carriers of the gene whose evolution is being tracked.  The context of population may be real, as discussed above, but the individual, basically a manifestation if its genotype, is what selfishly acts and determines success. No?

Sure, in a sense.  But the variant's prospects depend on the collective, and it's mutual, or relative.  Variant One is affected by Variant Two--but Variant Two is affected by Variant One, and so on.  The individual, or worse, individual gene focus is something one can compute, but it is misleading.  And, in fact, the situation is even more problematic in respect to what individuals actually are, genomically.

In Part III, I'll discuss how individuals, too, are being misperceived as the ultimate functional units based on their individual genotypes, either as wholes or in terms of specific genes.  Again a group or population perspective has an important, largely unrecognized role to play in individuals' and hence groups' success.

Wallace was onto something that's rather absent in Darwin, and still absent today as a result of the fact that the particularist aspect of Darwin's and Mendel's view prevailed.