The complex evolution of personality

So, apparently even sea anemones have personalities.  The idea that non-human animals can be measurably, say, bolder or shyer than others of their species may or may not be a surprising idea to you, perhaps depending on how many cats, dogs, horses, laboratory mice you have known.  But, scientists who study animal behavior are currently focusing on animal personality in a big way.  The BBC Radio 4 program Discovery discussed this the other day, and to us, the discussion raised some unintended points.

Hermit crab; Wikipedia

Presenter Adam Hart interviewed behavioral scientists studying personality in animals as diverse as songbirds and sea anemones. All agreed that variation is the norm.  Daniel Nettle, at the University of Newcastle, described five different dimensions to human personality: extroversion, neuroticism, agreeableness, conscientiousness, openness to experience.  They aren't all found in non-human animals, he said, though some seem to be, and all seem to be present in chimps.

Personality variation in the great tit, a small songbird, has been studied by many people (e.g., here and here).  For example, Samantha Patrick from the University of Gloucestershire described catching birds in the wild and releasing them into a room furnished with artificial trees, which they hadn't seen before.  Each bird's behavior upon first seeing the room is recorded, and its 'exploration score' calculated, to determine where the bird sits on a boldness/shyness range.  Fast explorers are more aggressive, and more willing to take risks than slow explorers.  And, when birds are artificially selected for parental aggression or calm, heritability of such personality traits is consistently around 50% -- that is, 50% of the behavior seems to have a genetic source.  But behavioral plasticity has been found to be common in great tits as well.

Great tit; Wikipedia, photo by Lviatour

But it's not just vertebrates that are being studied.  Mark Briffa at Plymouth University studies boldness and shyness in hermit crabs. He disturbs them by lifting them out of the water and turning them upside-down, leaves them thus for five seconds, and then replaces them in the water, and measures the time it takes for them to return to normal.  He then gives them a boldness rating.

Hart asked Briffa whether boldness in hermit crabs is at all equivalent to human extroversion.  That is, whether understanding hermit crab behavior give us any insights into human behavior.  Briffa's answer was that humans share an ancient neurobiology with other animals, including hermit crabs, and looking at that will help "simplify the problem" of human behavior.  Maybe.

So, there are conscientious crabs, those that spend a lot of time investigating empty snail shells as they make the decision about which one to move into next.  And there are bold hermit crabs, who seem to choose with little consideration.  There are evolutionary trade-offs to each of these behaviors, Briffa said.  The conscientious crabs get better shells, but waste a lot of time looking, while the bold crabs get iffier shells but saved time.  Time for what, exactly, it wasn't clear.  Can't be making more hermit crabs, because personality traits are not linked with fitness, and Briffa was not the only interviewee who said this about the animal they study.  That is, there's no individual reproductive advantage to being bold or shy, conscientious or not.  If there were, of course, there'd be a lot less variation in personality because it would have been selected out of the population in favor of the personality trait that led to more offspring.

How did these traits evolve?
This means that these traits aren't here because they were favored by natural selection, at least not in the present if these studies are any indication.  They could be here just by chance for reasons of ecology or population structure of some kind in the species' pasts.  Or, it might mean that there's a lot more plasticity in personality than is being reported, or identified by current methods, and that in some way plasticity is genetically enabled.  And indeed this would be expected, given that adaptability is so widespread that we've called it a fundamental principle of life.  A brain that can sense its circumstances, evaluate them, and plan responses may be what has evolved, but different brains, even if they were developed from the same genotype, might make different decisions.

However Hart, and interviewees, asserted that natural selection has favored a variety of personality types. But if no personality type has more offspring, gradually out reproducing the others, this can't be. It's only possible if group selection, natural selection that can see, and thus choose traits that benefit a group, is at work.

So, great tits can be shy or bold.  If an entire flock is bold, they are often on the move and able to locate new food sources, but they ignore each other, and that's bad for the cohesion of the group.  Shy birds stay together, but they don't move to new food sources, and that's bad for the health of the group.  A mix of bold and shy birds is ideal; the bold birds ensure that the flock moves to new food sources, and the shy birds follow.  Group selection would have favored a flock that includes a mix of personality traits, for the benefit of the flock rather than only a single personality trait, with its serious flaws.

But, this is a controversial issue.  Even Darwin, who himself addressed behavior including that in humans and our closer relatives, was rather mixed on this point.  The kind of mixed-flock just described could be a case of complex balanced polymorphism if the traits are genetically determined.  Too many bolds, bad for the group, too many shy, bad for the group.  The bold/shy genotypes' fitness is a function of the population in which they occur.  That would be standard genetic theory.

Group selection is coming back into fashion, being seen these days by all sorts of theoretical modelers and empirical investigators.  It has a checkered history.  The issue is that individuals shed their genes or not, and a genotype that engenders a particular behavior that is good for the group is fine -- so long as it's even better for the individuals with the genotype.  The reason this is contentious is that those strong Darwinians who are unhappy with any sort of resistance to pure individual selection argue that a genotype that favors the group cannot proliferate if that is at the relative expense of the individual with the genotype.  Otherwise, the group may do fine, but the genotype cannot become more relatively common over time.  At least not within the group.

The issues are quite mixed, and anthropomorphizing evolutionary modelers often say that an altruistic group-favoring gene variant will either be outcompeted, or that in effect it enables 'cheaters', without the good-guy genotype, to succeed at the good-guys' expense.  So the altruism-conferring variant loses out in the end.  If a group grows at the relative expense of other groups of the same species, the good-guy variants might overall increase in frequency (since the group without good guys disappears), but eventually, from a strongly deterministic Darwinian view of natural selection, the good-guy gene will get driven out.

How much does the work described above help explain behavior and the evolution of behavior in humans, where sociocultural factors clearly play a larger part in behavior than in non-humans?  The assumption, presumably, is that what's being explored here is the genetic aspect of behavior.  But, if personality is only 50% heritable in great tits, who don't share the extent of cultural influence on behavior that humans have, then it's hard to accept that we're getting at something that can be explained primarily by hard-wiring in humans.  At the very least, chance is playing a role comparable in strength to selection in determining group and individual success.  Of course, anthropomorphizing is difficult to avoid and it's difficult to tell when it's justified or not; indeed, cultural evolution has been described even in great tits, with the spread of learned behavior across a wide area.

Darwin wrote quite a lot about behavior, including altruism, aesthetics, personality and so on in Descent of Man, where he tried to show continuity between humans and other species.  His specific agenda, and even explicitly stated, was to displace religious creationism as an explanation for animal (and plant) diversity.  So he wanted humans to have traits that other animals have.  Several chapters deal with his ideas of these sorts of behavioral and communal sharing, including explanations of altruism.  He stressed behavioral continuity also in his Expression of the Emotions in Man and Animals.

Darwin was hand-waving much of the time when he did this.  And while he talked of selection, his main point was continuity and descent from common ancestry.  This is very different from observing what other species do, assessing when or how or if a trait is actually genetic in a way simple enough for selection to screen it at the gene level, and determining if, in fact, variants of the trait affect fitness.  Short term observations and risk of things like anthropomorphizing, and the likelihood that behavioral patterns for individuals may vary during their lives or in different circumstances, make the area difficult to study definitively in evolutionary terms.

But one thing is definitively clear:  animals do behave in variable ways, and that's fascinating enough.

Seasonality of cooperative behavior in a large population of juvenile primates

My Grandpa used to read this on Christmas Eve, and most years we keep up the tradition.  It's an important first-person ethnographic account of the adaptive cooperative behavior displayed seasonally by many juveniles of our species. Enjoy...


Jest 'Fore Christmas
by Eugene Field (1850-1895)

FATHER calls me William, sister calls me Will,
Mother calls me Willie but the fellers call me Bill!
Mighty glad I ain't a girl---ruther be a boy,
Without them sashes curls an' things that's worn by Fauntleroy!
Love to chawnk green apples an' go swimmin' in the lake--
Hate to take the castor-ile they give for belly-ache!
'Most all the time, the whole year round, there ain't no flies on me,
But jest'fore Christmas I'm as good as I kin be!

Got a yeller dog named Sport, sick him on the cat.
First thing she knows she doesn't know where she is at!
Got a clipper sled, an' when us kids goes out to slide,
'Long comes the grocery cart, an' we all hook a ride!
But sometimes when the grocery man is worrited an' cross,
He reaches at us with his whip, an' larrups up his hoss,
An' then I laff an' holler, "Oh, ye never teched me!"
But jest'fore Christmas I'm as good as I kin be!

Gran'ma says she hopes that when I git to be a man,
I'll be a missionarer like her oldest brother, Dan,
As was et up by the cannibals that live in Ceylon's Isle,
Where every prospeck pleases, an' only man is vile!
But gran'ma she has never been to see a Wild West show,
Nor read the life of Daniel Boone, or else I guess she'd know
That Buff'lo Bill an' cowboys is good enough for me!
Excep' jest 'fore Christmas, when I'm as good as I kin be!

And then old Sport he hangs around, so solemn-like an' still,
His eyes they seem a-sayin': "What's the matter, little Bill?"
The old cat sneaks down off her perch an' wonders what's become
Of them two enemies of hern that used to make things hum!
But I am so perlite an' tend so earnestly to biz,
That mother says to father: "How improved our Willie is!"
But father, havin' been a boy hisself, suspicions me
When, jest 'fore Christmas, I'm as good as I kin be!

For Christmas, with its lots an' lots of candies, cakes an' toys,
Was made, they say, for proper kids an' not for naughty boys;
So wash yer face an' bresh yer hair, an' mind yer p's and q's,
And don't bust out yer pantaloons, and don't wear out yer shoes;
Say "Yessum" to the ladies, and "Yessur" to the men,
An' when they's company, don'a pass yer plate for pie again;
But, thinkin' of the things yer'd like to see upon that tree,
Jest 'fore Christmas be as good as yer kin be!

**

Season's greetings 

to you and yours from me and mine...

As good as kin be.
(Photo by Juliet Dunsworth)

What if Rev Jenyns had agreed? Part III. 'Group' selection in individuals, too.

We have been using Darwin's and Wallace's somewhat different views of evolution to address some questions of evolutionary genetics and their consequences for todays attempt to understand the biological, especially genomic, basis of traits of interest. Darwin had a more particularistic individual focus and Wallace a more group-focused, ecological one, on the dynamics of evolutionary change.

HMS Beagle in the Straits of Magellan

As a foil, we noted that a friend of Darwin's, Leonard Jenyns was offered the naturalist's job on the Beagle first, but turned it down, opening the way for Darwin. We mused about how we might think today had Wallace's view of evolution, announced in the same year that Darwin's was, been the first view of the new theory. Where we'd be now if we'd had a more group than individual focus is of course not knowable, but we feel Wallace's viewpoint, at least in some senses, has been wrongly neglected.

Population genetic theory traces what happens to genetic variants in a population over time. Almost without exception the theory treats each individual as representing a single genotype. We take individual blood samples or cheek swabs, and let our "Next-Gen" sequencer grind out the nucleotide sequences as though on a proverbial assembly line. In this sense, each individual--or, rather, the individual's genotype--is taken to be the unit of evolution.

Populations were, and generally still are, seen as a mix of these individual internally non- varying homogeneous units each having a genotype. But that's an obviously inaccurate way to view life, another reflection of the difference in viewpoint about variation in life that we've been characterizing by relating them symbolically to Darwin's and Wallace's stress in their views of evolution.

There is a strong tendency to equate genotypes with the traits they cause. This derives from the tendency to reduce natural selection to screening of single genes, because if single genes cannot be detected effectively by selection, they generally won't have high predictive value for biomedicine either. It is easy to see the issue.

But individuals are populations too
Let's ask something very simple: What is your 'genotype'? You began life as a single fertilized egg with two instances of human genomes, one inherited from each parent (here, we’ll ignore the slight complication of mitochondrial DNA). Two sets of chromosomes. But that was you then, not as you are now. Now, you’re a mix of countless billions of cells. They’re countless in several ways. First, cells in most of your tissues divide and produce two daughter cells, in processes that continue from fertilization to death. Second, cells die. Third, mutations occur so that each cell division introduces numerous new DNA changes in the daughter cells. These somatic (body cell) mutations don’t pass to the next generation (unless they occur in the germline) but they do affect the cells in which they are found.

But how do we determine your genotype? This is usually done from thousands or millions of cells—say, by sequencing DNA extracted from a blood sample or cheek swab. So what is usually sequenced is an aggregate of millions of instances of each genome segment, among which there is variation. The resulting analysis picks up, essentially, the most common nucleotides at each position. This is what is then called your genotype and the assumption is that it represents your nature, that is, all your cells that in aggregate make you what you are.

In fact, however, you are not just a member of a population of different competing individuals each with their inherited genotypes. In every meaningful sense of the word each person, too, is a i of genomes. A person's cells live and/or compete with each other in a Darwinian sense, and his/her body and organs and physiology are the net result of this internal variation, in the same sense that there is an average stature or blood pressure among individuals in a population.

If we were to clone a population of individuals, each from a single identical starting cell, and house them in entirely identical environments, there would still be variation among them (we see this, imperfectly, in colonies of inbred laboratory strains such as of mice). They are mostly the same, but not entirely. That’s because they are aggregates of cells, with genomes varying around their starting genome.

Yesterday we tried to describe why the traits in individuals in populations have a central tendency: most people have pretty similar stature or glucose levels or blood pressure. The reason is a group-evolutionary phenomenon. In a population, many different genomic elements contribute to the trait, and because the population is here and hence has evolved successfully in its competitive environment, the mix of elements and their individual frequencies is such that random draws of these elements mainly generate rather similar results.

It is this distribution of random draws of all the genetic variants in the population that determines the context and hence the success of a given variant. But the process is a relativistic one, rather than absolute effects of individual variants. Gene A's success depends on B's presence and vice versa, across the genome. There is always a small number of outliers, having drawn unusual combinations, and evolution screens these in a way that results in a central tendency that may shift over time, etc.

The same explanation accounts for the traits in individuals. There would be a central tendency in our hypothetical cloned mice. That’s because the somatic mutations generate many different cells, but most are not too different from each other. As in evolution in populations, if they are dysfunctional the cell dies (or, in some instances, they doom the whole cell-population to death, as when somatic mutations cause cancer in the individual). Otherwise, they usually comprise a population near the norm.

Is somatic variation important?

An individual is a group, or population of differing cells. In terms of the contribution of genetic variation among those cells, our knowledge is incomplete to say the least. From a given variant's point of view (and here we ignore the very challenging aspect of environmental effects), there may be some average risk--that is, phenotype among all sampled individuals with that variant in their sequenced genome. But somatically acquired variation will affect that variant's effects, and generally we don't yet know how to take that into account, so it represents a source of statistical noise, or variance, around our predictions. If the variant's risk is 5% does that mean that 5% of carriers are at 100% risk and the rest zero? Or all are at 5% risk? How can we tell? Currently we have little way to tell and I think manifestly even less interest in this problem.

Cancer is a good, long-studied example of the potentially devastating nature of somatic variation, because there is what I've called 'phenotype amplification': a cell that has inherited (from the person's parents or the cell's somatic ancestors) a carcinogenic genotype will not in itself be harmful, but it will divide unconstrained so that it becomes noticeable at the level of the organism. Most somatic mutations don't lead to uncontrolled cell proliferation, but they can be important in more subtle ways that are very hard to assess at present. But we do know something about them.

Evolution is a process of accumulation of variation over time. Sequences acquire new variants by mutations in a way that generates a hierarchical relationship, a tree of sequence variation that reflects the time order of when each variant first arrived. Older variants that are still around are typically more common than newer ones. This is how the individual genomes inherited by members of a population and is part of the reason that a group perspective can be an important but neglected aspect of our desire to relate genotypes to traits, as discussed yesterday. Older variants are more common and easier to find, but are unlikely to be too harmful, or they would not still be here. Rarer variants are very numerous in our huge, recently expanded human population. They can have strong effects but their rarity makes them hard to analyze by our current statistical methods.

However, the same sort of hierarchy occurs during life as somatic mutations arise in different cells at different times in individual people. Mutations arising early in embryonic development are going to be represented in more descendant cells, perhaps even all the cells in some descendant organ system, than recent variants. But because recent variants arise when there are many cells in each organ, the organ may contain a large number of very rare, but collectively important, variants.

The mix of variants, their relative frequencies, and their distribution of resulting effects are thus a population rather than individual phenomenon, both in populations and individuals. Reductionist approaches done well are not ‘wrong’, and tell us what can be told by treating individuals as single genotypes, and enumerating them to find associations. But the reductionist approach is only one way to consider the causal nature of life.

Our society likes to enumerate things and characterize their individual effects. Group selection is controversial in the sense of explaining altruism, and some versions of group selection as an evolutionary theory have well-demonstrated failings. But properly considered, groups are real entities that are important in evolution, and that helps account for the complexity we encounter when we force hyper-reductionistic, individual thinking to the exclusion of group perspectives. The same is true of the group nature of individuals' genotypes.

We have taken Darwin and Wallace as representatives of these differing perspectives. Had Jenyns taken the boat ride he was offered, we'd have been more strongly influenced by Wallace's population perspective because we wouldn't have had Darwin's. Instead, Darwin's view won, largely because of his social position and being in the London hub of science, as has been well-documented. A consequence is that the ridicule to which group-based evolutionary arguments have been subjected is a reflection of the resulting constricted theoretical ideology of many scientists—but not of the facts that science is trying to explain.

What needs to be worked on is not, or certainly not just, increased sample size to somehow make enumerative individual prediction accurate. For reasons we've tried to suggest, retrospective fitting to the particular agglomerate of genotypes does not yield accurate individual prediction--and here we've not even considering non-genomic aspects of each genome-site's environment. Instead, we should try to develop a better population-based understanding of the mix of variants and their frequencies, and a better sense of what a given allele's 'effect' is when we know each allele's effect is not singular nor absolute, but is strictly relative to its context both in terms of its individual and population occurrences. It's not obvious (to us, at least) how to do that, or how such an understanding might relate to whether accurate individualized prediction is likely to be possible in general.

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.

On the mythology of natural selection: Part VI. Sexual and Group selection

We have been focusing in this series on forms of selection that are generally unfamiliar, and perhaps a challenge to the usual idea of evolution by natural selection.  There are a couple of rather standard types of selection that are well-known and widely discussed however, their importance or even existence sometimes debated and we wanted to acknowledge and touch upon them here.

Sexual selection
Competition in the Darwinian selective arena may not just be among individuals for food or habitat.  Males or females may have a choice of who to mate with, and this can lead to competition among them to become the chosen one.  This is called sexual selection and is a form of classic Darwinian selection.  Indeed, it was part of the title of Darwin's treatment of human evolution (The Descent of Man and Selection in Relation to Sex, 1871).  It is classically Darwinian in that it is about competition among varying individuals within a species.

From The Descent of Man and Selection in Relation to Sex; the Tufted Coquette Lophornis ornatus, female above, ornamented male below.

How, when and where sexual selection occurs, and whether it's males or females who choose, and how the competition for attention works are all variables that depend on species and situation.  For long-lived species it has been debated whether today's dominant male, for example, at the end of his lifetime really sired more offspring.  How often are both choices involved, or only males or only females, in choosing? How much manipulation is being done?  Do display characters really show genomic fitness in terms of health and the like?  These are scientific questions that can be asked about individual cases, not the general principle.  The principle need never be practiced for the idea of it to be a plausible means of differential proliferation.

However, another form of selection has been proposed, and that has been much more controversial.

Group selection
Alfred Russel Wallace, who recognized the fact of evolution more or less at the same time as Darwin did, saw selection as largely being about competition among species for limited resources in their local ecosystem, rather than simply among individuals within a species.  Species that are better at finding food than other species will proliferate at the latter's expense. This seems an unexceptionable way to view species evolution, so why would it be controversial?

The reason is at its essence rather simple.  It is individuals, not whole species, that experience mutations and reproduce successfully.  Those individuals who are better at this than their peers will proliferate and, if species are actually competing in an ecosystem, the population as a whole will do better when more of its individuals have the favored genotypes.  There need be no separate group-specific phenomenon involved.

Indeed, evolutionarily why would the favored individual even 'want' to help its group rather than just helping itself survive?  After all, most of its group-mates have different genotypes and the favored ones would be helping their inferiors to proliferate!  This relates to ideas about the evolution of altruism, and theory of when or whether an individual would help another--the formal theory (Hamilton's 'rule', for example) says that if there is any cost to you to help someone else, you'll only help a relative, because a relative is likely to have similar genotype to you.

Advocates for group selection note that there are reasons why social cooperation might benefit groups as a whole and, in the process, those whose self-interest drives them to internal competition.  If solidarity in, say, defense of food collection leads to the group's survival relative to the environment or other groups, then all its genotypes gain an edge.  This does not exclude internal classically Darwinian inter-individual competition, after all.  Various authors like EO Wilson and Martin Nowak, and David Sloane Wilson, among others have recently advanced various theories of cooperative selection or group selection.

The debate has been bitter and has taken place over decades, especially since in the early 1960s VC Wynne Edwards wrote a tome that tried to explain mating display behavior (as in peacock struts or lek behavior in birds or ungulates) that he argued was used by a species to limit its population size.  The idea was that the group uses means to suppress its overall reproduction so that, as a group, it doesn't exhaust its resources.  This argument had its flaws and it wasn't the most modest book ever written, but the sometimes-strident opposition by people like Hamilton and George Williams found many holes or objections, claiming that all the observations could be fitted into good old-fashioned Darwinian individual competitive natural selection, in the form of 'kin selection' or 'inclusive fitness'.

There's a lot of altruism in life, if you but look for it, and it is not just occurring among immediate relatives.  This has led some to defend the Darwinian axiom to say that what is (must be!) going on is 'reciprocal altruism':  you scratch my back today and I'll scratch yours tomorrow.  But that essentially is an open safety valve--a non-specific post hoc coded way to acknowledge the reality of group selection without admitting it.

In my personal view, the issues have ended up being hyper-polarized, needlessly, as the opposing view and Hamilton's rule and its many manifestations of self-sacrifice for close kin are not clearly supported in terms of empirical (as opposed to theoretical/mathematical) evolutionary importance (this finding by population ecologists who have looked for it systematically).  For example, local groups of many species (including humans during most of our evolution) consisted of kin of many complex degrees of relationship, so helping a 'random' member of the group is a way of helping your kin.

As someone who is not a very good swimmer but has had the privilege of saving a total stranger from drowning, I know from personal experience that no kinship calculus need be involved in many aspects of altruism.  Not even reciprocal altruism (the person saved was disabled and couldn't ever have saved me later!).

In any case, group selection, if, when, and where it occurs, is a variety of competitive Darwinian natural selection.  It would just have a different focus (working via the group as a whole rather than individuals), but is the same sort of essentially deterministic force for the origin of complex traits.

Selecting people

On natural selection in humans
In the Rival del Garda meeting we were happy to see Luca Cavalli-Sforza for the first time in many years. Luca, a towering figure in human genetics in the last third of the 20th century, was one of the most important conceptual leaders in uniting population (evolutionary) genetics, along with culture and language, in accounting for current human diversity. Luca, long at Stanford but who retired back home in Italy a few years ago, is well into his '80s, but still spry enough and intellectually lively. Ken had interacted with him extensively in the past, including a mid-70s sabbatical in his lab at Stanford, and subsequently in the attempt to organize a global human genome diversity project (HGDP).

Luca gave a talk at the meeting on natural selection in humans. We wondered whether, at his age and removal from Stanford he could really be up to date with the huge, rapidly emerging literature on searches of the human genome for signatures of selection. Intense, highly technical genomewide comparison of variation between humans and other primates, but especially among human continental groups, has been undertaken by many investigators using HGDP-like samples and the genetic variation in the HapMap project.

There, the idea is to find genes or genome regions in which variation is reduced in ways suggesting that specific selection has taken place--such as to produce lighter or darker skin color in various continents and/or climates, or the ability of humans to resist malaria, or of adults to digest milk (these are the classic examples).

Such searches are for classically Darwinian effects. That is, they're about who in a population has higher 'fitness'--net reproductive success because they survive better or simply have higher fertility. The search is difficult and only a few specific instances have been found, for reasons too much to go into in this post. But there is at least widespread belief that there's been quite a lot of such selection since we spread out from our African ancestral home to become a globally distributed species: how could we inhabit the globe's diversity of environments without this being the result of natural selection?

Well, Luca surprised us. His point was about culture rather than genes per se. He quite correctly noted that our having culture helped us adapt quickly to diverse environments (clothing and fire, rather than fur, to protect against cold, for example, or language to communicate among coordinated hunters or gatherers).

Non-Darwinian group selection
Luca's evidence was thus entirely unrelated to the current genomewide statistical searches, but instead related to our rapid global expansion that could not be explained by genes--except by our species' shared genes related to thinking ability, that made us capable of culture.

Humans have clearly expanded rapidly at the expense of other species. We have invaded every environment, and displaced other species where needed, advancing some such as cattle or wheat for our own use instead. Our numbers have increased in a few thousand years from a few thousand to a few billion. Nothing could be clearer as proof of natural selection in humans.

However, this is not Darwinian selection in the usual sense! Instead it is a kind of group selection, the favoring of our group vis-a-vis groups of other species that we displaced. It is closer to the version of selection and evolution proffered by Alfred Wallace (who came to his ideas independently of Darwin). Wallace gave more stress to group competition and group struggle against environments, while Darwin clearly and strongly stressed competition among individuals within groups.

The two are not incompatible at all, and both processes can be occurring at any or every time. But it's not what people have in mind these days, in their frenetic hunt for good and bad genes. So Luca may or may not be up to date in that area of work, but he certainly pointed out what is, for our species, clearly and by far the most important aspect of selection involving humans! Far more important than the rather minor kinds of selection we know about at the specific gene level--even including malaria and skin color effects.

Politically correct, if scientifically incorrect
However, in stressing this view, Luca went on to argue that because selection in humans was culture-based, there was little evidence for racial differences that could be attributed to selection. Race differences (here, let's ignore the problems with the term 'race'), he said, are superficial only. They don't reflect natural selection beyond such traits as skin color. The argument is one Luca has been making for decades, as he has been perhaps by far the leader in trying to relate human genetics to human culture, such as correlating language with geography with genetic variation. But his argument unfortunately reflected a quite out-dated view, that in some ways can even be said to be politically correct, if scientifically incorrect. To see why, let's look at the case that was made.

Luca has long pointed out that, to a considerable degree, human genetic differences are correlated with geography. The farther apart geographically that two people are (here, we refer to 'indigenous' people rather than recent intercontinental migrants), the more different they are genetically. This is called 'isolation by distance.' There is quibbling about the details, but the idea is basically accurate: French and Swedish people are genetically more like each other than French and Koreans are. This, Luca argued, shows that there cannot be much due to natural selection, because selection is related to local environmental conditions, which can be very different in nearby regions, or very similar in distant regions, would not leave such a generic pattern of differences.

But there's a subtle fallacy here. Selection of a given trait affects only the genes that produce that trait, not the whole genome. Even if selection is affecting all genes at all times, each gene is affected by different environmental conditions. And selection works not with global variation, but only with variation present in any local area. Thus, even with selection, we see isolation by distance effects.

More importantly, isolation by distance is studied by using genomewide variation. There is often a deliberate choice of genetic variants that are thought not to be involved in functionally important traits (so-called selectively neutral parts of the genome), and hence variants that are not involved in selection. Isolation by distance in the genome overall, especially at such neutral regions, is perfectly compatible with all sorts of selection going on at individual genes, but differently in different world regions.

We can see this easily in another way. Two people can have a trait, like blue eyes, diabetes, or color blindness for the same genetic reason. As a rule, the same genetic variant found in two people are descendant copies of a single original mutation that occurred sometime in the past. In that sense, they are close relatives at that particular gene. But if you look at genomewide variants, they will have no particular relationship relative to other people in the population.

So, whatever you think about the pervasiveness or importance of natural selection in the history of different human 'races', the isolation by distance argument is basically irrelevant.

Thus, while the massive global expansion of humans is overwhelming and persuasive evidence for culture-based group selection favoring humans, the global human expansion is perfectly compatible with all sorts of local selection taking place. How much of that has actually happened is a separate question requiring its own kind of evidence; and so far, that evidence has been very hard to come by.