Luke Matthews, PhD
  • Home
  • Publications and Research
  • Blog

If selection is on individuals, why aren't the selfish mutants taking over?

9/26/2012

8 Comments

 
I've followed the literature and debates on the evolution of cooperation since the beginning of my graduate schooling.  Central to these debates is the role played by group structure in allowing altruistic cooperation to evolve, and whether it deserves to be called group selection.  What we call it is a semantic issue, but in their take-down of group selection, people like Richard Dawkins and Steven Pinker have misrepresented the evolutionary mechanisms for group selection.  The key misrepresentation is that selection only acts on individuals or genes, and that there is no value added to thinking about groups.

First, we have to be clear what this debate is about.  The only type of cooperation that matters in this debate is classically called 'evolutionary altruism.'  This means a behavior that has a real fitness cost to the actor who performs the behavior.  Doing the behavior itself is costly, such that it would be eliminated by natural selection if not for direct fitness benefits acquired by the recipient.  However, for any behavior to evolve that benefits only the recipient and not the actor, then there has to be a mechanism by which the recipients of the behavior also tend to be those who perform the behavior as well.  Otherwise there will be 'freeriders' who game the system by collecting benefits as recipients, but because they never perform the behavior they will never pay the costs.  Essentially all models for how evolutionary altruism can evolve are just mechanisms that effectively cut these freeriders out of being recipients, such that recipients are more likely to be also performers of the behavior.  The equation that formalizes the rigor with which the mechanism must exclude freeriders is W.D. Hamilton's famous formulation for inclusive fitness, which describes how the relatedness must exceed the ratio of the cost of performing the behavior over the benefit of receiving it.  r > c/b (see Nowak 2006).  r measures recent genealogical relatedness, in this case, and is one mechanism to ensure that the recipient has at least  probability = r of having the genes that cause the individual to perform the altruistic behavior.

That's the mathematical kernal - now enter decades of semantic nutshells around this.  Does altruism evolve because of group selection, or is it because individuals are gaining 'indirect' fitness benefits for themselves, or is it really genes promoting copies of themselves residing in the bodies of other individuals?  People like Dr. Dawkins and Dr. Pinker have been consistent and vociferous in their denial of any group selection going on in the evolution of altruism.  Here are some thought experiments that are troubling for this assertion:

1.  Consider an evolutionarily altruistic behavior that has evolved by kin selection.  For this behaivor, individuals recognize siblings and then perform a fitness-costly behavior that benefits the sibling.  Siblings have an r=0.5, which satisfies Hamilton's equation for this particular behavior, but assume relatedness lower than 0.4 does not.  So far so good.  Now, our individual selectionists will point to the benefits being given to relatives and say 'see - indirect benefits to the actors - ergo, no group selection effects.'  But what happens when a freerider mutant who never performs the behavior is born into an altruist family?  There is no reciprocity in this system, meaning the mutant's siblings just detect that he is their sibling and thus donates the benefits to him.  What happens?  The freerider mutant always will have a higher fitness than his siblings, because he never pays the cost of the behavior and he receives just as many benefits.  If the only thing we need to think about is the relative fitness of individuals, then kin selection cannot evolve altruistic behaviors because freerider mutants always have higher fitness than their altruistic siblings.  How can the gene for the altuistic behavior ever prosper?  Clearly within their own families, altruists always lose to freeriders.
    If you are a scientist whose thinking has been dogmatized against group selection, don't worry, there's hope.  Just each morning keep repeating the freerider (saying selfish is more fun) mutant scenario, and it will help to deprogram you.  This is what I had to go through to really understand this after years of programming.  Just keep saying, but what about the fact that freerider (selfish) mutants always have to have higher fitnesses within their own families?! 
    The reason Hamilton's equation actually works is because freerider mutants go on to have families that are dominated by sets of freeriders.  That's the only way it can work.  Once this happens, the payoff to selfishness drops below altruism because now the selfish individuals get none of the benefits of the behavior (none of their siblings perform the behavior).  Hamilton himself identified this very clearly in his 1975 book chapter in the volume "Biosocial Anthropology".  Try reading it in addition to Hamilton's 1964 (here is the first one of the pair).
    David S. Wilson has argued, and I agree, that the best way to think about and phrase this insight is that evolutionary altruism evolves because of across-group fitness differentials.  The reason Hamilton's equation works is because a sufficient level of recent genealogical inheritance will create enough across group fitness differential to overcome the invasion of freerider mutants.  Should we call this group selection?  Seems reasonable to me, but we could call it other things.  It differs from traits that we could properly say are selected only at the individual level because the fitness differential that causes the gene to increase in frequency only occurs across some sets of individuals in the population (in my scenario these sets are individuals across different kin groups).  Indeed, this is why Hamilton himself suggested in 1975 that it would be clearer to call some inclusive fitness effects as kin-group selection.  I like this term a lot actually.  We could also make the distinction by talking about selection that is within-group and within-population as different from selection that is within-population only.  That might be most pleasing to the likes of Drs. Dawkins and Pinker, as now we would only by implication be saying something happens at a group level.  It's completely correct - kin selected evolutionary altruism is not selectively favored within groups of kin.  Any claim that it is so selected is demonstrably, devastatingly, false.  Hamilton shows this very clearly in his 1975 chapter.  Within-group within-population is a bit wordy though, so we would have to make acronyms out of them and distinguish between WGWP and WP forms of selection.  Seems cumbersome, but again, we humans make up these semantics so we can call it what ever we like.


2.  OK, so after thought experiment 1 a now wavering anti-group-selectionist might be thinking 'well fine, but that scenario didn't change any of the actual predictions of my incorrect individual selection verbiage.  So, even if I was right for the wrong reasons, I still got the right predictions, which is what matters in science.'  That's quite fair, and I agree wholeheartedly that getting the right predictions is what matters in science.  Once we give up on this we become philosophers, and we had those for thousands of years and never figured out anything. 
    But individual selection thinking does get predictions wrong.  One prediction that gets missed every time without thinking about groups is the distinction between an altruistic behavior that by its nature is a public good (perhaps an alarm call to my whole group) from one that relies on kin recognition mechanisms.  In the former, there is no point in evolving kin recognition and the r that matters is the average r of the group.  The fact that the alarm call warns siblings, for example, has to be discounted by the fact that it warns nonrelated individuals, and the discounting comes out to exactly the mean r across the group that hears the alarm call.  This is a serious prediction that in my experience with students and colleagues gets missed all the time and, again, is very well laid out in Hamilton's 1975 paper (and also by the way it is in the 1964 paper).  Sure, you can rephrase how kin selection works on public good in inclusive fitness terms if you want, but the correct predictions do not flow naturally from this logic and I think are frequently missed by empirical researchers.

3.    Let's continue to where things continue to get worse for anti-group-selection views when we think more about gene-eye-views of the world.
    Are genes the unit of selection?  I have no doubt they are a unit of inheritance, but selection?  The only way they can be a unit of selection is if you adopt a very contorted notion of what a gene is.  Let me illustrate.  Imagine two villages of humans that each are involved in reciprocal altruism within the village - you scratch my back and I'll scratch yours.  So, now the individuals stop giving benefits to freeriders after they discover through their interactions who is a freerider.  Let's suppose one village all have the same gene variants (alleles) that cause them to behave with altuistic reciprocity, but the other village is like a UN training camp with people from all over the world.  Just by chance, the UN village has different alleles that have different base pair sequences.  They all equally produce the same altruistic reciprocity behavior, but they are different sequences, and they have different evolutionary origins.  Maybe some of them even differ in functional parts of the allele that contribute to reciprocal altruism, and maybe in fact some people's reciprocity behavior is influence by different sections of DNA that are not even orthologous to the sections that affect another's reciprocity.  Even though they create the same phenotype, would anyone really call these the same 'genes'?  With their different origins and different sequences can they be said to be the same 'entities' selfishly advancing 'their' own replication?  It seems to me they are not, and remember the village with all the same homologous reciprocity inducing alleles with the exact same base pair sequences!  Any natural interpretation of the English language would conclude that there is more successfully selfish genic selection for reciprocity happening in the homogenous village.  I mean, the UN village is benefiting copies of other genes that aren't even remotely related to each other. 
    The point is none of this 'gene's eye view' and 'selfishly replicating genes' stuff matters.  Evolution, remember, is just a set of mundane mechanistic interactions that stack up to produce algorithmic effects over time.  Think of it like a set of billiard balls being hit ever so deterministically on a table, but instead of the balls moving across space the chains of causal collisions are moving through time.  It doesn't matter whether these alleles had the same origin, different origin, or even if they are in the same places on chromosomes or code for the same protein products.  All that matters is they cause the individuals to do this reciprocal behavior with other reciprocal individuals, so all these diverse genes involved in such a system can rise with the other's tides.  I think somewhere Dr. Dawkins tried to redefine individual selfish genes as just this highly abstract entity, such that we would call different nonorthologous stretches of DNA and different nonhomologous alleles all one 'gene' if they were all related to a single phenotype.  But no one actually defines 'a gene' this way because it would make doing human genomes, and biochemistry, and most of biology impossible. 

After these thought experiments hopefully you have loosened up to see the key to evolutionary altruism is just to find any mechanism where the benefits of altruistic action keep getting to other altruists and freeriders are excluded.  Any mechanism that reliably establishes a correlation between being an altruist and receiving benefits from other altruists will do - it doesn't have to achieve this at every grouping level of society, and it doesn't have to do it through homologous genes that selfishly replicate themselves.  In fact, it doesn't need genes at all, just inherited stuff.  Now the predictions really start to diverge from typical gene and individual selectionist theory.  Because if you just need inherited stuff, then evolution can use cultural variants as well to create evolutionarily altruistic adaptations.  That's a topic for another blog (here is my recent paper on it), and I hate to say this one more time, but yes, W.D. Hamilton already identified how cultural evolution would work equally well for all this in his 1975 chapter.   
8 Comments
Brett Austin
11/11/2012 07:35:21 pm

Hi Luke. Thanks for an interesting post!

I'm sorry that this question is not directly related to the thesis of your blog post, but you clearly know more about kin selection than I do. I wonder if you'd be able to take a minute to shed some light on a question I have?

I've been reading a lot about kin selection on the internet, but I still can't find any comment on the origin/spread of an kin-altruistic genetic mutation. I hear a lot about how altruism is advantageous in groups or families where the trait is already widespread, but how does it spread from the initial mutation in a single individual, to the whole family? All the explanations I have read seem to assume that the gene is already present in a majority, if not all, of the kin, which is why altruism is selected for. But surely there is no advantage to being kin-altruistic when you are the original mutant and the only member of the family with the gene, and the gene will die when you starve after giving your last piece of your cake to your sister.

What am I missing?

(Sorry for my high-school understanding of Biology, and the consequent imprecise use of terms like 'gene' and 'trait'. If the answer is out of my league, just say so, I won't be offended. But if it's not too hard to explain, I'd be really grateful for an answer!)

You could consider it an act of genuine, non-kin altruism!

Reply
Luke link
11/12/2012 11:32:28 am

Hi Brett,
No need to apologize - you have a great question that is very directly related to the post! Your question is essentially the reciprocal condition of my explanation of why selfish mutants always have higher fitness in the first generations and in the first families into which they are born. You are asking about the flip side of this, when the whole population is selfish and an evolutionary-altruist-toward-kin mutant is born. How does it invade the population since this altruist mutant will have lower fitness by paying costs but receiving no benefits from its selfish kin?

The answer is drift. Kin selection does not account for that very first invasion of of the altruistic gene. It can't because what kin selection is at a mechanistic level is a way that genetic inheritance happens to produce the sufficient guarantee that the benefits of altruism go to other altruists, but in the generation of the original mutant altruist this guarantee of course cannot exist. There needs to be at least a little drift initially such that the altruist mutants survive and become structured into families of altruists. The same actually applies to reciprocal altruism - the first mutant tit for tat players are selectively disadvantaged in an all selfish population - you need a group of tit for tat players before it becomes a selectively advantaged strategy. This is one of the quirky features of all mechanisms for evolutionary altruism that makes it somewhat different from individually selected traits that do not depend on receiving benefits from others for their selective increase in frequency.

Hamilton implied as much in his original 1964 article. I included a link in my post to the first his full article. On page 14 you will find the following section, which shows Hamilton recognized altruism was always selectively disadvantageous in the initial mutants:

"Finally, it must be pointed out that the model is not applicable to the selection of new mutations. Sibs might or might not carry the mutation depending on the point in the germ-line of the parent at which it had occurred, but for relatives in general a definite number of generations must pass before the coefficients give the true - or, under selection, the approximate - expectations of replicas. This point is favourable to the establishment of taking-traits and slightly against giving-traits."

Reply
Brett Austin
11/12/2012 07:37:03 pm

Great, thanks for that! I do appreciate your time.

I don't know why I couldn't find the answer anywhere else - I think perhaps I was asking the wrong question.

The more I think about it, you did actually answer my question in the original post, just in reverse :)

Also, the more I think about it, this stuff does my head in - I think I'll leave it to the experts to solve the kin-selection vs. group-selection debate. After all, I'm a philosopher, and us lot have never solved anything! (no offense taken) ;)

Thanks again!

Reply
Luke link
11/15/2012 01:02:37 pm

My opinion is you were not asking the wrong question at all. I think you had trouble finding the answers to your excellent questions because we evolutionists have been doing a poor job of presenting this material. There is a lot of misinformation of the public going on in part because much of the discussion by the most prominent people is focused on debating which are the best metaphorical words to use to describe evolutionary processes rather than explaining the processes.

As for this stuff doing you head in, I remember reading a similar comment by Daniel Dennet in an article he wrote reviewing Wilson and Sober's book "Unto Others". Dr. Dennet commented on these issues being 'slippery' as I recall. I really think they aren't, so long as you let go of the idea that evolution has to be understood as some kind of entities (genes, individuals, etc.) acting to maximize a utility function for fitness. That is what drives the confusion about how kin selection requires drift at first and selfish mutants are always favored in their own families, because those are examples of how the evolutionary processes that result in adaptation do not intuitively behave like agents maximizing fitness. It is the last vestiges of vitalism in my view that biological scientists insist on conceptualizing evolutionary selection processes as the working out of the 'interests' of evolving entities. If you just think of the mechanics like the way we study billiard ball collisions or molecules it all becomes more clear. Sure, we use metaphors in physics and chemistry about physical things like gases 'wanting' to do this or that, but physicists and chemists don't insist that processes they study must be expressible and expressed in such a way. Many evolutionists seem to insist that any process of natural selection must be expressible in terms of agents maximizing outcomes, but Darwin's insight was that this isn't really what is happening out there in the world. There is just this repetitive algorithm (we metaphorically call it natural selection) that has to happen due to the way physical stuff (chemicals, individuals, groups, whatever) interact and replicate. A lot of time that looks to us to create the same observed patterns as entities actively trying to maximize Darwinian fitness, but fundamentally that isn't what is going on.

As for my jab at philosophy in the post, I'm glad you take no offense. I must confess when I wrote that line I recognized I was stooping a bit into rhetoric for rhetoric's sake. More accurately my view is that philosophy never gets us much of anywhere in scientific understanding, which is by definition predictive and testable. Abstract rational argument that is neither predictive nor testable cannot yield scientific understandings, although on other epistemological grounds many of us, myself included, may accept that such philosophical discourse can arrive at justified beliefs.

Reply
Jason Hodgson
1/26/2013 09:10:46 am

This takes me back to whiskey arguments in computer room!

Of course the gene is the unit of selection and not the individual! There is a reason population genetics is not written from the perspective of individuals. Individuals (as the name implies) only occur once. Try incorporating individuals into your math!

Extend your first thought experiment.

Scenario 1: The mutant cheater gets run over by a bus prior to reproductive age.

Senario 2: The mutant cheater also has a second independent mutation that renders her sterile.

Scenario 3: The mutant cheater has a myriad of other alleles that quantitatively result in low fitness despite the within family advantage afforded by the cheating allele.

If selection is at the level of the individual, you'd conclude that the cheater mutation had zero or low fitness, even within the gullible family of altruists. But it's not at the level of the individual. Selection is the average excess or deficit of reproduction of alleles within populations.

From this perspective, it does not matter whether a cheater has an advantage within his own family, it matters if, on average, the allele has an advantage within the population. This particular problem is one of frequency-dependent selection as Hamilton and you point out.

I think we can conceive of ways that selection for an allele would result in individual altruism towards kin and altruism towards groups. Testing whether these exist in the real world is pretty tough though!

Reply
Luke link
1/28/2013 11:14:45 am

Hey Jason,
Great to have your comments on my blog! What you are proposing "Selection is the average excess or deficit of reproduction of alleles within populations." is a classic example of the averaging fallacy. This is explained well by D.S. Wilson and Eliot Sober in their book Unto Others, but there are other articles and such where you can find it. The fact of an average increase or decrease in alleles does not tell us the locus of selection, even if we were to have some convincing work with nonsynonymous:synonymous and the like to show it is selection and not drift. There is nothing we will ever observe about genes alone that will tell us what a selection pressure is, because selection is a result of interactions of phenotypes and physical, biotic, and social ecologies.

Think for a minute about the metaphor. Darwin said the algorithm of differential survival and reproduction had a similar net effect to the effect of a selective breeder who culled and bred his animals - hence the metaphor Natural Selection - it's as if Nature were like a selective breeder. The breeder clearly literally selects animals - let's say the fattest cows. Ecological interactions, Darwin pointed out, have a similar aggregate effect over time by favoring cows with some traits more than others, etc. But, according to your logic, because the human breeder effectively causes a rise in the average frequency of alleles related to fatness, that he is actually selecting for genes. That makes no sense, and it makes Darwin's metaphor make no sense, because human breeders don't need to know anything about genes, they just need to know about cows, and they clearly consciously select for cows.

All of your counter arguments are erroneous confusions about narrowing my scenarios to particular idiosyncratic events for individuals, but Natural Selection and selective breeders obviously only work because of the overall effect averaging out idiosyncracies. You don't need to invoke gene selectionism to invoke what statistical average effects will occur. I could issue the same exact counters as you have about each particular copy of a gene. Oops, but 1). this copy got hit with a nonsense mutation - ha ha., 2). This copy of a gene landed in an in-viable fetus, 3) this copy of a gene got nullified by a more dominant allele.

This is not a semantic argument either. Think outside of altruism theory for a minute, and think of all the times we have told our students that Natural Selection causes certain things because it can't 'see' genes. That's why, for example, Natural Selection can produce crazy inefficient gene interactions, or favor evolutionarily unrelated alleles for sickle cell because they end up having the same phenotypic effect on individuals. That's because Natural Selection can't (metaphorically) see genes so it can't select for specific genes.

What we conclude about all this has big consequences. If you are right, then there de facto cannot be Natural Selection of cultural traits, because they are encoded through socially learned information rather than genes - so if selection acts only on genes then it cannot act on culture. Similarly, Natural Selection, according to you, cannot act on maternal effects or the results of DNA methylation. Those are not true allelic variations so, according to your viewpoint, cannot be acted on by Natural Selection. I think these conclusions are obviously false. Remember my cows. It's very clear that maternal effects have a substantial influence on body fatness and condition. The selective breeder can change the characteristics of his cow population by selecting individuals for fatness, and even if the only mechanism of that inherited variation is maternal effect then he will still get a shift in the trait mean over time.

As for frequency dependent selection - that does play a role in some group selection (aka multilevel selection) models but not in this case. First, frequency dependent selection applies to many things that have nothing to do with altruism. The classic hawk-dove game is one such example, and so is the advantage of rare blood types. Second, Hamilton's classic formulation of kin selection does not result in frequency dependent selection. Consider the blood type case. Rare blood types are favored by selection because they render individuals less likely to contract certain diseases. The blood type so favored then increases in frequency and at some point become the most common, at which point rarer blood types are favored. The point is intermediate population frequencies are favored. This is not what Hamilton said at all. If his equation is met, then the altruism allele according to his theory will be driven to fixation and selfishness will only occur at the mutation rate. You are confusing frequency dependence with the multilevel character of this selection - that the fitness differentials favor the altruism only across particular sets of individuals in the po

Reply
Luke link
1/28/2013 11:27:31 am

(previous comment cut short) ...
... sets of individuals in the population. To say the actual mechanism of selection doesn't matter because allele frequencies changed is the averaging fallacy.

Jason Hodgson
1/29/2013 03:56:44 pm

Hi Luke,

Thanks for the careful response!

I'm not proposing that definition of selection. That is just the standard understanding in population genetics. In population genetics we track allele frequencies in populations. If you want to describe selection on an allele you describe it relative to the other alleles in the population, and that means averaging, fallacy or not.

"But, according to your logic, because the human breeder effectively causes a rise in the average frequency of alleles related to fatness, that he is actually selecting for genes."

Yes, that is precisely what happens. He selects for the genes that are involved in fatness and ignores all the other genes that the cow has (except ones tightly linked to the fatness genes). He may not know he's doing this, but that is what he is doing. If you look through the genomes of the population of cows you will see signatures of selection restricted to the fatness genes, and all of the other genes will be unaffected.

"All of your counter arguments are erroneous confusions about narrowing my scenarios to particular idiosyncratic events for individuals,"

Well, in non-clonal taxa, individuals are definitionally idiosyncratic. That's the problem.

"but Natural Selection and selective breeders obviously only work because of the overall effect averaging out idiosyncracies."

Wait, now I'm confused. In my mind, this is the standard population genetic understanding of selection that you object to above. I'm sure I'm missing something.

"Oops, but 1). this copy got hit with a nonsense mutation - ha ha., 2). This copy of a gene landed in an in-viable fetus, 3) this copy of a gene got nullified by a more dominant allele."

But these are no problem at all when you understand that the fate of an allele in any individual genome is not important, rather the fate of the allele in the population (again the standard pop-gen understanding).

"That's why, for example, Natural Selection can produce crazy inefficient gene interactions, or favor evolutionarily unrelated alleles for sickle cell because they end up having the same phenotypic effect on individuals. That's because Natural Selection can't (metaphorically) see genes so it can't select for specific genes."

Selection on genes predicts these things. If two unrelated alleles have the same selection coefficient they will be neutral relative to each other and both increase in frequency relative to alleles with lower selection coefficients.

"If you are right, then there de facto cannot be Natural Selection of cultural traits, because they are encoded through socially learned information rather than genes - so if selection acts only on genes then it cannot act on culture."

I don't think this at all. I fully accept that there can be (and are) other evolutionary processes in addition to genetics. Language and culture are probably examples.

I'm convinced we are talking past each other. I actually suspect this is just semantics. I'm pretty sure our fundamental understanding of evolution is pretty similar. I think the test is would we go about any particular analysis differently? I suspect not.




Leave a Reply.

    Author

    This is my personal blog.  The views expressed on this page are my own.  My views should not be taken to represent the views of my mentors, employer, or any person or group other than myself. 

    Archives

    November 2022
    May 2022
    March 2022
    April 2019
    March 2017
    June 2015
    June 2014
    December 2013
    October 2012
    September 2012

    Categories

    All
    Cultural Diffusion
    Cultural Phylogenetics
    Group Selection
    History Of Anthropology
    Kin Selection
    Multilevel Selection
    Neanderthal
    Out Of Africa
    Social Science
    Statistics

    RSS Feed

Powered by Create your own unique website with customizable templates.