Thursday, July 24, 2014

On the mythology of natural selection. Part VIII: Complex evolution without selection?

The default and sometimes only explanation for the origin of complex biological traits is an often barely-altered invocation of Darwin's notion of an all-seeing force-like natural selection.  As we have said earlier in this series, when conditions are suitable, natural selection will follow essentially by definition of 'suitable'.  Natural selection is about the proliferation of better traits at the expense of lesser traits in a given environment.  But we have tried to suggest that there are many ways in which adaptive evolution can occur without that sort of selection.

In the processes we've discussed so far, we have largely avoided the notion of chance as anything but a blurring factor of purely deterministic notions.  Persistent genotype-based advantage will, depending on how strong the difference is, often proliferate even in the face of chance (genetic drift).  Theoretically, the fate depends (statistically) on the relative strength of the selective advantage of one state over its competitors, and the size of the population (which affects the chance aspects of reproduction).  In this situation, the success of the favored is to some extent, if not completely, largely like that of a steady force.  In fact, the models that show this largely assume a steady state (e.g., similar selective advantage of the allele in question over long time periods).  It is important in this theory, which is mathematical and not questioned, that selectively neutral or even somewhat harmful variants can also, if with less probability, proliferate at the expense of competing variants.  Overall, however, one can fiddle with the details of such a model to make of drift a fly, but not a fatal flaw, in the classical selectionist ointment.

But let us see how far we can go by considering that context changes all the time, sometimes more, sometimes less.  And if context changes all the time, selective value will change.  That makes things much less predictive over very long time periods, if these fitness differences are small.  We have to note this because as entrenched as deterministic selection is in the theory of evolution, the idea that evolution creeps along at usually a literally imperceptibly slow pace is equally entrenched.

What if we assume that there is no natural selection relative to some trait we wish to follow? To what extent could chance (drift) alone lead to adaptive traits?  We illustrate this notion with an example of we called receptor-mediated evolution in Chapter 10 of our book The Mermaid's Tale.   We schematically illustrate the evolution of a complex trait without any natural selection.  The legend is below the figure:

A.  Free-floating cells with environment-sensing surface proteins.  B, C. These experience mutation that make them able to adhere to copies of the same receptor on other cells (mutation-bearing cells are differentially shaded). This leads to aggregations of cells.  We can call it an ‘organism’ at some stage.  D, E.  Receptor-based aggregates sequester cells of specific mutational types or ‘species.’  The cells within a cluster can differentiate by gene expression, depending on whether they detect contact with the outer environment or not, forming specialized subsets (eventually leading to organs).  F.  A cluster can shed individual cells that will then divide to form new clusters of the same kind as their parents.  G. Mutations leading to the release of just the extracellular part of the receptor can bind to related cells elsewhere, triggering them to differentiate into new clusters—an early form of signaling.

Starting small and in some local area, there need be no serious competition for resources and hence no natural selection against (or for) the modified receptors that evolve by mutation in this little story.  Cells with like properties encounter each other randomly or locally because that's where they were formed.

This is of course schematic and hypothetical. But it shows, we think, that complexity can in principle arise slowly, element by element, without the need for competition for resources or overpopulation and so on.  What is required is that over time in some location, a variety of mutations arise among countless individuals (here, starting with cells).  Unless or until they do arise, evolution doesn't of course occur! This doesn't preclude the new evolving forms experiencing selection in some way or at some time, but the point is that it need not be a necessary part of the dynamics.  If chance combinations of non-harmful genotypes arise, and environments change, or a randomly arisen combination happens now to offer a viable function, can that continue to improve (very slowly) over time?

When, whether, where, or how often this sort of phenomenon accounts for adaptive change, very slowly and locally, is a matter to think about and perhaps there would be ways to test its credibility.  The slower evolution works, the greater is the plausibility that such phenomena can be a part of adaptive evolution--by drift and without the need for natural selection.

Drift?  Maybe--but is it, too, a mythological concept?
We have argued that chance in the form of what is called genetic drift must play a role in evolution. The course of evolution involves elements of competition but inevitably also of chance.  Chance has at least two relevant meanings here.

First, we might say that two foxes have somewhat different bodies, but are the same when it comes to catching rabbits.  The chance of a successful chase is the same.

Second,  genetic mutations in DNA sequence certainly happen sometimes by what is essentially chance: a cosmic ray from the sun zaps your DNA somewhere in a way totally unpredictable and, most important to evolution, that has no relationship to a trait that may affect the fitness of the victim.  When it comes to reproductive success, there is no selective difference between the new and competing existing genotypes.  For each genotype, the chance of reproducing is the same.

Now, how can we tell if the two foxes, or the two genotypes, have the 'same chance' of success?  What does 'same' mean here and how on earth could we possibly tell?

In this sense, one can never prove, essentially not even in principle, that two functional states are identical--that the difference is exactly zero.  By this criterion even drift becomes a mythological if not mystical notion.  Or you can take the position of a physicist who believes in deterministic laws of nature, then certainly at some level, even if you can't see it, there is a fitness difference. But as we have seen repeatedly in this series, that then is an assumption and defines all evolutionary change as being due to natural selection: If it survived it was selected for, end of story.

That is, as we have repeatedly said, a definition not a scientific statement.  But there's more than that.

Too small to detect, yet treated as if so important?
Let us suppose for the sake of argument that selection of a purely deterministic sort (steady, fixed selective difference between alternatives, no chance element, etc.) is taking place.   Let's say one state has a 1% advantage over its competitor.  Does this sound small?  Well, for evolutionarily relevant natural selection that would be considered quite unusually strong (remember, we're not here discussing artificial selection or selections such as antibiotic resistance which can be extremely strong).  Most selection in real-live Nature is probably at least ten times weaker--differences on the order of one part in a thousand or less.

But let's stick with the strong 1% advantage.  That means that if you have 101 offspring to my mere 100.  Here again we're letting it be deterministic not just a long-term average over a species' populations and countless generations.  Such a difference would be exceedingly difficult, or sometimes statistically impossible, to document from actual samples of completed fitness in a natural population.  Even if such a difference persisted for the thousands or more generations required for a major trait adaptation, it could not reliably be estimated at any given time, and that means for every given time (because even in generations when you did detect it, by some statistical criterion, you could not reliably know that this wasn't a fluke of sampling.

This in no way implies that slow, even steady and deterministic selection, the usual image, does not occur.  But it does mean that the image of great advantage in the raw competition of Nature is an exaggeration of large proportions.  It essentially gives an image that equates the carnage in the backyard as mainly about adaptive selection, rather than mainly about just plain carnage of everyone seeking its dinner.

Here the importance has serious implications for humans and those who seek Darwinian explanations for every little human trait, physical or especially behavioral.  The fact is that adaptive differences are essentially so trivial that they have no real import at any given time.   That is, they should not be used as tools to justify discrimination or inequality and so on.  How and whether such policies based on different traits, talents, and the like should be implemented cannot usually be justified on evolutionary grounds.  Evolutionary grounds are about net reproductive success, not human cultural values (in another post we noted that contrary scenarios from the usual are easy to construct!).

Tempering excessive invocation about natural selection is an important reason that we decided to do this long series about the nature of evolutionary adaptations and change.  That is because we see a sometimes rather fervent eagerness to revive evolutionary value judgments about people as individuals or as labeled groups.

Of course, many genetic variants lead to serious disease and clearly may impair reproductive success in a huge way.  But we treat disease for its own sake, not because of its evolutionary import.  Mixing sociological judgments with evolutionary theory is to dabble in the Devil's game, as history has shown.

If a trait is so adaptively important, why is so much variation still around?
If selection were strong because a trait were being refined or fine-tuned by selection, and selective differences were strong enough to make a contemporary mountain rather than molehill of, why is there then still so much variation?  Why hasn't selection made everyone almost alike?

For example, if intelligence (as in IQ scores, say) were so vital to the human place in Nature, why is there such a range between the very smart and the very not-so?  Here, we are not referring to pathological mental impairment.

The answer is that either trait differences aren't actually that relevant to evolution--that is make little difference to net reproductive success, or there is a balance between lowered reproduction due to selection, the blurring effects of chance, and the input of new variation by mutation and recombination. This would probably be the preferred explanation for most theoretical population geneticists.  But if true, it implies that selection really is not that strong after all, possibly because so many genes are contributing to the trait that individual differences simply cannot be tightly purged by selection.  Maybe this is in part because the many genes each have other roles to play as well, and can't be purged too tightly without affecting those traits.

Further, even if selection of a classical deterministic kind is at work, it could be that only the very fastest relative to the slowest fox has an advantage.  That will move the average chasing speed of foxes towards being faster, but other than the rare outliers, there need be no fitness-related differences.  This again is a very different idea from that of eagle-eyed, ever-vigilant, fine-tuned selection.

One should also realize that it isn't that foxes today are somehow more 'fit' than their distant ancestors were--that they have been struggling for eons of doing poorly to evolve being OK today.  At every age they were, as a population perfectly fit, for that particular time, as one would say if one were observing them at the time.

There are many issues here, but the bottom line is that at the level of individual genes, and probably at the trait level itself, selection is just not very precise and/or that the species does perfectly well with its broad trait variation.  Again, too big of a deal should not be made, on evolutionary grounds, for the range of differences we see.

In sum
We risk reductio ad absurdum by taking too strong a stand in any direction when it comes to the evolution of complex traits.  In any discussion of evolutionary factors, call them what you will, we face a major challenge in determining the reason for evolutionary success--or even, one might say, the meaning of 'reason' in this context.  We are stuck in a profound way with statistical statements based on empirical, and inherently limited samples, imperfect measurements, unobservable past events, and essentially subjective testing and decision-making criterion (a subject we've discussed before).

Tiny differences, be they 'due' to chance or some very weak force, can be imperceptible by such criteria but can accumulate.  They can lead over eons to something useful, and even if now and then nudged by other forms of selection, differential proliferation can occur essentially by what is reasonable to call chance.

Gene duplication is a form of drift that in principle can lead to redundancy that can buffer the organism against future mutations that generate function in one of the copies.  Most of our genomes have arisen, from early days, via duplication and rearrangement of existing bits of DNA (exon shuffling, in exact recombination, translocations, transpositions and the like).  Even standard genome evolutionary theory and explanations recognize this.  Relative to future function, gene duplication is a form of random event, like point mutation.  But duplication of existing functional elements provides a potential source of new function, usually related to current function--some of which can serve as fortunate 'pre-adaptations' for the organism's niche at that or later times.

Even more than that, as I have recently discussed in one of my regular column installments in Evolutionary Anthropology*** (with references to others' work), a random DNA sequence long enough to code for a protein of a respectable 50 or more amino acids is not trivial, if mutation or translocation or duplication generated a promoter sequence.  Since all nucleotide triplets can be used as codons, and only 3 of 64 possible codons are STOPs and there are 6 possible reading frames, etc. Other elements (polyA site, ATG, etc.) may also be needed, but genomes are big, organism numbers huge, and earth history very very long long.  What is transcribed need not be translated to be functional, as in the plethora of noncoding RNAs.  And the protein need not have a function right away so long as it doesn't get in the way of what a cell is doing.

A function can arise later.  Or not.  In the long history of life and the diverse functions, choices, and opportunities of species, the various forms of adaptive response discussed in this series may apply even to essentially randomly arisen genes.  When we dismiss anything but classical natural selection as our explanation, we close off other possible accounts for traits that we see here today.

We hope, at least, to have provided some food for thought on this fundamental aspect of causation in life and its genomes.

For discussions of ways chance and selection can mold what we see in genomes, work by Michael Lynch makes good reading (e.g., The frailty of adaptive hypotheses for the origins of organismal complexityPNAS, 2007 and his book The Origin of Genome Architecture); of course, he may not agree with what we say here.

***Weiss, K  Little Orphan's Nanny: Where do genes come from and who takes care of them?  Evol. Anthropol. 22: 4-8, 2013 (paywalled--email me for pdf)

Wednesday, July 23, 2014

On the mythology of natural selection: Part VII. Phenogenetic drift

We are trying in this series of posts (see this week and last, beginning with Part I here) to enumerate a few ways in which organized traits can arise without the usual canonical view of natural selection as the complete, force-like causal process.  We do this to temper what we see as an often unquestioning belief in natural selection.  We do this because such a belief leads to what we think is extreme, and unwarranted, genomic determinism and belief in inborn inherency that leads both to potentially disastrous societal consequences and false hopes in regard to promises for health and well-being.

Also, mistaken reliance on simplistic explanations impedes the effort to understand the truth rather than mythology about the truth--because mythology removes a sense that we must work harder to understand the actual truth.

Today, we wish to note an important aspect of the relationship between genes and traits, even if one were to accept a purely "Newtonian" law- or force-like version of ubiquitous natural selection as the, that is the, cause of traits in organisms.

The point is that even then, and even if genes (broadly defined, without quibbling about what a 'gene' is) worked in a perfectly force-like deterministic causal way, even ignoring all the obvious probabilistic aspects or environmental components, even then, genetic determinism is not the simple story as is often portrayed.

"Survival of the fittest"?  A non-sensical notion too widely adopted
It is blatantly clear to anyone wishing to make even the most casual observation of nature rather than a book of slogans, that 'survival of the fittest' is at the very best a misleading term.  What does 'the' mean? The one and only most-fit individual?  Clearly not!  All those who are fit (here 'fit' refers to success in the evolutionary screen of natural selection)?  Or somewhat fit?  If that, then what does 'fittest' mean?  All those 'equally' best or only the very best survive?  That is an untestable definition.

Darwin should not have adopted this phrase, which he borrowed from Herbert Spencer to clarify, one might say, his term 'natural selection' to make sure that no one would think he (Darwin) was imagining God as nature's selector. The plain and manifest truth is that 'survival' is not exactly the right term so Darwin mis-spoke or spoke metaphorically, because it is both survival and reproduction that are important, and for most species not just survival per se but length or timing of survival, etc.  What Darwin probably meant was 'survival' in the sense of being represented in the next generation.  In any case, semantics aside, in the hurly-burly of real life, evolutionary success is a problematic, quantitative rather than simple qualitative yes-no phenomenon.

It is common if not typical or even necessary that biological traits are produced by the action of many functional elements of an organism's genome, not just one.  Traits themselves usually have at least some variation among individuals within and between species (and during each one's life).  Here we ignore environmental factors, but their variation is of course often an important additional contributor to trait variation. Essentially, life is causally a many-to-many phenomenon.

This fact has profound implications for our understanding of phenogenetic relationships, that is, relationships between genes and the traits to which they contribute.  To show this clearly, in what follows, we will for the sake of argument just assume the force-like universal view of simplistic natural selection.

Divergence of primordial EMP (enamel) gene. Phenogenetic drift. Source: Kawasaki and Weiss, 2003

Phenogenetic drift
With traits that are affected by many different genes (often called 'polygenic' as a short-hand term), many different genotypes can yield essentially the same phenotype.  This is we have called 'phenogenetic equivalence'.  In the Darwinian arena, individuals with the same trait will have similar fitness prospects--they'll be treated similarly by natural selection--even if their trait is due to different genotypes.  That means that the contributing genetic variants are equally 'fit': they proliferate equally well. Different individuals in a population, or individuals from different populations, or individuals from the same population over different time periods, will have the same traits for different genomic reasons. This kind of causation is essentially the definition or essence of polygenic or causally complex traits.

When this occurs, along with the chance elements in life itself, the chance elements in recombination among genes in genomes and between parents and the gametes they provide to each offspring, the relative frequency of the contributing genomic variants will vary over place and time essentially by chance--they will drift as the term has it. This is the case even when selection of the classical kind is at work, even when the selection is strong. This is phenogenetic drift, or chance changes in the relationship between phenotypes and genotypes. (The phenomenon was discussed in the reference below***, and elsewhere in my work, and see Kawasaki on SCPP genes and mineralization, or Wagner on avian digits, e.g.)

With phenogenetic drift there is no reason to expect that a given gene or genetic variant is necessary or sufficient for the trait.  Genetic determinism has a different kind of meaning than the usual 'marginal' (statistically, on-its-own) view of genetic causation.  One could say that the Predictance, the probability of a given phenotype for a given genotype, was very high, but the Detectance, the probability of a given genotype underlying a given phenotype, was low.

But the common reality, based on countless GWAS and other types of genomewide enumeration studies to relate phenotypes to genotypes, is that such prediction is usually small, trivially so for each individual variant and even if all statistically detected genetic variants are taken into account.  Now and then a strong-effect variant at a specific gene is identified, and one might find evidence that fitness--health or actual survival--is predictable from the genotype at that specific gene.  But that is the exception, the Mendelian tease, the first taste of a drug that leads to the hyper-Darwinian addiction.

The Mendelian tease: peas that followed rules; Ernst Benery Erfurt, 1867.

In sum
For rhetorical purposes we have assumed here that the world is a deterministic Darwinian one, but in fact environments are at least as complex as genomes, the interactions among genes are complex, and probabilistic elements are involved all along the way.  We cannot escape a certain amount of probabilism, either because that is the true essence of biological causation, or at least because our measurements are imperfect. Worse, we don't know all the factors to measure, and when it comes to environments they are always changing and in directions we simply cannot predict.  This is particularly true in the case of humans, because our behavior is based on all sorts of unpredictable cultural elements, so that, for example, disease risks are inherently estimated from past exposures, and our future exposures (diet, environmental chemicals, climate, etc. simply cannot be predicted).  All these factors introduce slippage between genotype and phenotype at any given time, and hence over evolutionary time.

Again: the bottom line is that when many genetic factors contribute to a trait's variation, the combination underlying any given individual's trait can be unique to that individual.  It can be problematic to predict the trait from the genotype (as in 'personalized genomic medicine') or to predict the underlying genotype of an individual's phenotype.  Genetic causation is typically not as deterministic as its widespread, if often implicit, image.

Phenogenetic drift is an obvious fact of life, and it raises important questions related to the DNA sequence conservation issue we considered in the context of functional selection earlier in this series. That's because when contributing factors are experiencing phenogenetic drift, specific genes or variants need not be particularly conserved.  So how is it that when phenogenetic drift is part of life and evolution, there is so much evidence at the gene-by-gene sequence level, for purifying selection, for sequence conservation?  Here is a serious subject for study, though it poses no sort of controversy about adaptive evolution except by showing why simplified views of natural selection are inaccurate and at best incomplete.

The so-called Modern Evolutionary Synthesis, formulated in the 1930s and 40s, united paleontology, Darwinian gradualism, and Mendelian inheritance into a single gene-based view of life and its evolution.  It was, essentially and at least implicitly, focused on the effects of variants at single genes, screened by natural selection.  The theory of population genetics was its mathematical basis, and is usually presented for simplicity's sake in textbooks and classes as focused on single 'Mendelian' (two-allele) models, just like green and yellow peas.  But this almost cartoon-like simplification has widely been implicitly or or even explicitly accepted as the reality, even in current medical school curricula (and widely in 'gene-for' research, a topic we often write about). This view in practice often treats individual genes as having inherent deterministic (causal) value, on their own, free of much recognition of context.

Phenogenetic drift, like other not-Darwinian aspects of genotype-phenotype relationships and their evolution, is simply observable, not mystical, perverse, or in any way arcane or secret.  It belongs in the panoply of tools we have to attempt to understand biological causation and its evolution, fleshing out the skeleton of the process that Darwin was able to intuit with the tools available in his time, and as a corrective to the caricature-like simplism that is so widespread today, even in many professional circles and in the public media.  Of course, nobody admits to being simplistic--but pay attention to what they actually say and how they say it, to see whether you think our impressions are accurate nor not.

***Weiss, K, Fullerton, SM  Phenogenetic Drift and the evolution of genotype-phenotype relationships.  Theoretical  Population Biology, 57: 187-195, 2000.

Tuesday, July 22, 2014

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.

Monday, July 21, 2014

On the mythology of natural selection: Part V. Niche construction

The usual Darwinian presentation of adaptive life assigns essentially all of it to natural selection, in which, going back essentially unaltered to Darwin, constraints of the environment (including overpopulation relative to resources, and competition for those resources, and predators, and competition for mates and territory) screen contending alternatives and allow some to reproduce more and others less.  We model this traditionally in terms of relative success within a local population with its local ecological circumstance, rather than in absolute terms.  And while competition is among organisms, the usual theory is that it really is all about genes and their  proliferative success.

We have pointed out that many conditions must persist well enough, and long enough for this to be a helpful explanation for complex traits.  Not that it is wrong per se but that it is usually offered without much qualification or reservation yet is quite difficult to prove and verges on tautology.  One can, of course, define as 'natural selection' any change in relative frequency of some genetic variant.  But that is then just a description, not a scientific statement--even though it seems by far to be the normal practice, especially among those not formally trained or knowledgeable in evolutionary theory (such as many if not most human geneticists).

We have described two means of differential proliferation of genetic variants, organismal and functional selection, which are completely consistent with evolutionary history as the basis of the origin of biological traits, but are different from classical Darwinian natural selection.  In organismal selection, organisms explore and choose 'niches' as they are called, or ways to live.  Functional selection simply refers to failed development or function if some contributing molecule just doesn't work in a satisfactory way.  In organismal selection, organisms are proactive rather than passive, and there is another way this can happen as well.

Niche construction
Organisms, even plants, explore their environment and where possible go where they can do well.  They choose or 'select' their environment.  This can have a genetic basis and serve as a source of evolution of complex traits that are not just the product of competitive natural selection.  But organisms can also alter their environment to make it, in a sense, the way they'd like it to be.  This is known as nice construction.   The term was first used, to our knowledge, by Olding-Smee, Layland, and Feldman in the 1990s; if there was a former coining of the term, we are not aware of it.  You can see more at the Wikipedia entry by the same name, which gives examples.

Beavers constructing their niche in Tierra del Fuego. Wikimedia.

The idea is that individuals in a species modify their environment, and that in turn makes the environment suitable for the species.  Earthworms modify the soil which is then good for earthworms (Darwin, who wrote an interesting book on earthworms, knew about this!). Earthworms have genes 'for', that is genomes whose effects function well in, the particular environment.  This alteration of the environment is not the same as an 'autonomous' environment screening competing organisms.  In that sense, the evolution of niche constructors and their niches is not the same as passive natural selection.

Harlaxton Manor, England. Wikimedia

Niche constructors extroadinaires: you and me!
Of course we humans are the pinnacle of niche construction today--though bees, ants, and even earthworms and perhaps even such species as corals and bacterial biofilm makers do this very well at their own scale and pace.  That makes one wonder what ulterior motive lurks in the minds of those who are obsessed with finding genetic reasons for every little facet of our normal behavior, including sociocultural traits.

That point aside, not all niche construction is 'intentional' the way beavers intentionally build their dams or we build manor homes.  But to the apparent great extent by which evolution proceeds very slowly in assembling complex traits, including behaviors, it is not clear how much good old-fashioned natural selection is responsible or required for the ability to modify the environment.  Likewise, organismal selection may be an important part of the gradual accretion of such powers, with those who bore appropriate genotypes finding the modified environment and modifying it further.  A tiny beginning could make it such that most of the evolution is by non-'Darwinian' means.

The usual argument is that there is a back-and-forth feedback between natural selection and niche construction.  But whether this is a chicken-and-egg debate about which came first, and how and when and to what extent natural selection was important, niche construction is clearly an example of evolution by means beyond the usual view. Again, as with our other examples, niche construction doesn't 'overthrow' Darwinian processes, but it does show that the classical view needs to be nuanced. And, again, nothing mystical or even mysterious or strange is involved!

Friday, July 18, 2014

On the mythology of natural selection: Part IV. Functional selection

Not all evolutionary change has to be based on overpopulation and resulting vicious competition for scarce resources in a cruel and bloody Nature.  Yesterday, we suggested that organismal selection, a kind of inverted natural selection, is another means by which adaptive complex traits could arise.  But there are others.

Functional selection
Multicellular organisms develop from single cells. A cell is a very complex structure with all sorts of components.  Genomes code for hundreds to thousands and more different forms of functional RNA and protein.  These must interact for the organism to produce the structures it has evolved to need.  These ideas apply to single-cell species and to 'higher' organisms.

Cellular organelles.  From Weiss and Buchanan, 2009, The Mermaid's Tale

In multicellular organisms, each individual arises from a single initial cell (say, a fertilized egg) that then divides into specialized cells, forming different tissues and organ systems.  These largely are formed by processes of embryogenesis, before the organism is 'presented' to the environment as a free-standing individual--a new baby, say.  This is true of plants and animals.

The cells in an embryo are not in any serious sense competing for scarce resources and they don't overpopulate, say, relative to their their resource supply in the Darwinian concept of evolution.  But if their molecules fail to interact in ways needed for their particular species, the embryo will fail to develop into a viable adult.  Or, some favorable variants might lead to a greater chance of successful hatching.  These phenomena can be called functional selection.

While one can cite some rather post hoc ways to force this to seem like Darwinian selection (for example, in utero competition among pups in a litter), functional selection within given conceptuses can remove harmful variants in a way that doesn't really involve any sort of competition among individuals. The result will appear in DNA sequence comparisons as greatly reduced variation in important regions of the genome--such as is routinely found in protein-coding genes, and referred to as purifying selection.

Frog development.  From Weiss and Buchanan, The Mermaid's Tale, 2009

The usual explanation for sequence conservation is Darwinian competition or, rather, a kind of inverted Darwinism.  Darwin was trying to explain the positive evolution of new complex traits over time, leading to the world's diversity of differently adapted plants and animals.  The faster fox got the rabbit, the slower ones died.  Genetic variants that led to faster feet rose in frequency, and are what we see today in fox genomes.  Darwin's idea was that the environmental mix is always changing, always and relentlessly forcing this sort of adaptation due to competition for limited resources.

But what we mainly see in sequence comparisons is conservation, with known functional regions of the genome varying less than areas with less, unknown, or no function.  This is so widely observed that it has, perhaps somewhat incorrectly been taken as one of, if not the criterion for asserting function to some area of the genome.

So even here, even to the extent that Darwinian ideas of relentless competition are right, the effect is an inversion of the relentless race to be different.  Instead, it's a relentless guardian of the status quo!  And this raises a serious problem.  Conservation is so widespread in genomes, that one wonders how competitive purifying selection could actually work, because so many individuals would have inherited mutations, mostly harmful, that hardly any could survive the conservative screening of selection.  Too much genetic load, as it's called.

Functional selection perhaps provides a way out of this problem.  Organisms typically produce scads more gametes (pollen, sperm, eggs) than they need or will ever actually use.  Genetic variants expressed in the development of these cells will be purged easily and with low cost because the organism will sill produce enough viable gametes.  Similarly, most species produce vastly more zygotes (e.g., fertilized eggs) than ever need hatch as developed embryos.  Most genes are used during gamete or embryo formation, so that very low- or no-cost screening by functional selection can generate the observed kinds of patterns of sequence conservation, without the need for very expensive and extensive natural selection by competition among adults for limited food or mates.

Genetic variants that lead to, say, healthier embryonic development or gamete formation may tend to have a better chance at appearing as an adult and hence being transferred to later generations.  These would be relevant to some sorts of adaptive change (though not to those that do, in fact, require inter-individual competition). So functional selection could also contribute to positive adaptive evolution and new traits.  Again, this would have to be very gradual, just as Darwin said and everybody basically agrees is the case with complex traits.

This is not just an off-the-wall idea.  Decades ago, based on comparative phenotype data, CH Waddington made somewhat similar observations about the apparent high conservation of developmental pathways and how that constrained (he called in 'canalization') development.  He was a quirky nonconformist and was rather derided for it, and his idea was based on standard natural selection; but with modern DNA data and developmental genetic technologies, we see high conservation in developmental mechanisms (many examples are now  well known, perhaps exemplified by the Hox genes and body segment development in animals).  If such genes are not properly expressed in properly combinations and so on during development, the embryo may not form in a viable way even to be born (or, if in the germline, a gamete not to be formed).

And as with organismal selection, while functional selection is not Darwinian natural selection, it isn't mystical or strange, and doesn't provide any sort of challenge to the idea that complex traits and their genomic basis do evolve by normal, natural historical processes.  It's just that evolution is more nuanced, and less about ruthless competition, than is so widely and, we think, uncritically assumed.

Thursday, July 17, 2014

On the mythology of natural selection: Part III. Organismal selection

The entrenched idea of natural selection that is clear from the way that most people have discussed the subject, from Darwin to the present, is that selection is inevitable in nature because all species can reproduce rapidly enough that they will inevitably press up against the ability of their environment to support their needs--they'll overeat their food supply, run out of territories for raising young, and so on.

Ultimately, the idea goes, this will (will, not just might!) lead to competition, in which organisms compete for the now-limited resources.  Since the idea is that there will always be relevant genetic variation, this competition will (will, not just might) inevitably lead to improved genomes for the competitively intense circumstances.  This change is called adaptation.

As we said yesterday, this logic seems fine if the assumptions are correct.  It invokes a rather vague sense in which the environment, broadly conceived, screens --selects-- organisms for their traits, only letting the better ones through to form a next generation.  This is of course a view of the world as coldly, remorselessly, impersonally, and relentlessly cruel.  However, that doesn't make the idea false, and Darwin was indeed inspired to see his ideas because of the cruelty he observed.

There are other inevitable issues, such as the element of chance (known as genetic drift), the stability of the environment relative to the rate of genetic change, and others that should force us to question more seriously the idea in its specific details and even its asserted ubiquity.  But in principle there is no problem with Darwinism of this sort as a possible reason for adaptive change.

An historically clear side effect of this reasoning, we believe, is that this idea has become a dogma or ideology.  Even that would only be somewhat bad, depending on how inaccurate it was for evolutionary change over eons of history in finite populations.  We will comment about our personal views on that subject at the end of this series.  But the more serious problem with unexceptioned, unquestioned Darwinism is that it has routinely been applied to humans, including leading to justification for discrimination of the worst kind in recorded history by some against others.  It's only one rationale that has been used to excuse societal rapine, of course, but if it is not as universally true as the dogma has it, then there is no reason to cling to it.  For those in positions of control who wish to discriminate against others, there will always be alternative reasons.

However, the point is that Darwinism was offered as a deeply insightful and highly plausible theory for explaining the origin of complex organisms without needing to invoke any immaterial creation phenomena, such as spontaneous generation or creation events due to God.

On the other hand, there are ways in which complex traits can evolve that are not based on competition, or the cold cruelty of Nature.

Organismal selection
Organisms, especially animals, explore their environments in many ways.  They have means to sense conditions and respond to them.  This is obvious.  But it follows that they can in this sense 'select' their environment, rather than their environment selecting them (as in Darwin's natural selection).

Individuals can identify environments for which they are suited.  Suitability is just a general term for what one might call 'adapted', that is, environments in which they can find food and survive and so on. Among the variants in a population (and, of course, the responsible genotypes), those that 'like' a particular place will go there.  There, they will encounter others similarly predisposed.  They will mate and the offspring will stay around.  Meanwhile, members of the same population who do not like this particular environment will congregate elsewhere, meeting like fellows, and so on.

We refer to this as organismal selection, because it is the organisms rather than the environment that is doing the selecting.  When this happens, genotypes that confer the reason for the preference will proliferate in the preferred respective areas.  Eventually, genomic changes can occur in the different environments so that speciation (reproductive isolation) has occurred.  Over time, if one examines variation, adaptive variants will be found, and can appear just as if they had been raised to high frequency by competitive natural selection.  But the process need not be based on differential reproduction nor on competition for scarce resources, and in that sense is adaptive evolution that is not 'Darwinian'.

Organismal selection can't immediately produce complex traits any more than classical Darwinian selection can.  It would be expected to work at a similarly slow pace, and require assortative reproduction among existing variation.  It need not, indeed would hardly be expected to, evolve in a straight line from state A to state B.  In that sense, it's not 'anti' to many key aspects of Darwin's ideas.

Plants are more restricted in their ability to choose, so it's not clear how much of these ideas can apply to them.  But they certainly apply to single-celled and other relatively simply organized organisms.  Genetic variants that lead them to move to or inhabit particular environments essentially assorting their genomic variation by location.  This is not a strange suggestion, nor would it challenge to our idea about the relationships between genomes and traits or behavior.

There can, of course, also be competitive evolution going on for other traits, or eventual for the traits in question.  But this need not be so and in any case the point is that complex traits can arise by organismal selection.  If the environmental niches are all in the same place (say, finding food high in trees compared to on the ground), and if the behavior eventually leads to forming new species, it is known as 'sympatric speciation'.  Whether sympatric speciation occurs has long been debated, but in recent decades examples have been found that are convincing.

Speciation in Midas cichlids in different crater lakes in Nicaragua. Geiger et al., 2010

A skeptic wedded to the Darwinian party line might understandably ask how often the appropriate conditions occur.  The answer is that we don't know because nobody's looking (except for some instances of sympatric speciation), because they are mainly looking for classical selection or just assuming it and making up plausibility stories.  There is no reason that every situation should be expected to have the same explanation.  One feature about evolution that seems clear is that each case is different; that is close to being a fundamental attribute of evolution.

There may well be examples of adaptations that could serve to test the idea (one example might be human organismal selection for living at hypoxic high altitude, as in the Andes or Himalayas: how much did people die because of hypoxia when they somehow were forced to live there, as opposed to people settling there because they could do well).   Simplistic answers aren't likely to be found here any more than in the usual Darwinian cases. And the same skeptical question could rightly be asked of these latter, often simplistic tales: how often is the classical process the correct explanation--and how can we know?

This process in no way vitiates the possibility of adaptive evolution in a classical Darwinian competitive way, and nothing mystical or immaterial is involved.  It doesn't mean there is not also a war of all against all in Nature, it doesn't imply 'soft' (Lamarckian) selection.  It is as genetically based as classical Darwinism.  It does not 'overturn' Darwin or anything like that.  However, organismal selection is a means by which complex traits can arise without his idea of evolution driven by competitive natural selection.  Unless, of course, you just want to define any evolutionary change is due to natural selection.

Wednesday, July 16, 2014

On the mythology of natural selection. Part II: Classical Darwinism

Darwin didn't invent the idea of natural selection as a way of adaptive advance for traits in organisms that better suited their environmental conditions. But he basically coined the term and institutionalized the view that persists to this day, often invoked in a largely unchanged way despite 150 years of biological and evolutionary research. It was a strikingly perceptive idea, that others had had in previous decades (or, in some ways, even in the classical Islamic world; see our post on Ibn Khaldun), but only in rudimentary expression and not pursued, perhaps it seemed so obvious but also because there wasn't the kind of data, such as fossils and broad biogeographic knowledge, that led the insightful Darwin to generalize it into a basic worldview.

Darwin wanted to explain a purely material, historical process by which life could have evolved its remarkable complexity from rudimentary beginnings, no divine creationism involved (except possibly at the very beginning). The idea of a 'blind' screening force has penetrating appeal to anyone wanting a purely material understanding of our world. But to accept it you also had to accept the brutal heartlessness of that world. That of course went against religious promises of better things to come, of the truth of basic moral precepts, and so on.

To Darwin, and he was completely clear and explicit about this both in his writing (primarily, On the Origin of Species) as well as his private notes and letters, natural selection was a law of Nature, a universal force. That view is no surprise, because Darwin was a product of the post-Enlightenment world of science, ushered in by the likes of Galileo and Newton, in which science used examples and data to formulate precise laws that applied to everywhere beyond those examples. That also meant that in essential ways, it was a deterministic law of cause and effect. Caveats that might modify or soften that universal law were generally uttered in passing, but not really absorbed as an important part of the 'law'.

That dogmatic universalism still characterizes much that is in print in the public media but even in the professional journals, perhaps especially in the peripherally evolutionary fields like social science including our own Anthropology, but also in very technical fields like medicine, information sciences--and even a routinely invoked metaphor for almost anything.

The reason for this is that selection is a potentially all-powerful explanation that does not require foresight or immaterial factors and that to most people there is no alternative material way to explain the origin of complex organisms. But there are such ways, and there is much--very much I think--that we simply do not yet understand even about natural selection itself.

We'll discuss these alternatives, but first it's important to explain just what classical Darwinian selection is.

The conditions for natural selection
Natural selection is about cause and effect (that's what a law of Nature is). Here is a commonly accepted, widely used, textbook way to express that law:
Natural selection means the systematic differential reproductive success of competing organisms. The idea is simple: Since a species over-reproduces so that not all individuals in the next generation can go on to successfully reproduce, and since there is variation in form among that species, and since some forms of an organism do better in a particular environment than other forms, and since the reason for this is included in their heritable genome, and since the environment remains stable long enough over time for this form to be favored persistently, and since the favorable forms are also lucky enough to produce offspring who go on to reproduce, and since they produce more offspring than their competition, then those forms can become ever more common over time at the expense of their competition. Since all these contingencies do occur, indeed co-occur, then the more prolific life form will become more suited—better adapted—to the environment in question. Since the forms are sequestered from each other by some mating barrier, then they would diverge over time, and this was the explanation Darwin and Wallace proposed for the origin as well as specialization of species.
To many this may sound entirely correct and completely obvious. But in fact, surprisingly to many perhaps, it has zero scientific content. Since the assumption is that traits that are here are here for these reasons, whatever you see in the world must be fitted, and all you can do is try to find the details of any given case. It may or may not be a true description of how things are, but it is take-it or leave-it. 

Now compare that to this version:
Natural selection means the systematic differential reproductive success of competing organisms. The idea is simple: if a species over-reproduces so that not all individuals in the next generation can go on to successfully reproduce, and if there is variation in form among that species, and if some forms of an organism do better in a particular environment than other forms, and if the reason for this is included in their heritable genome, and if the environment remains stable long enough over time for this form to be favored persistently, and if the favorable forms are also lucky enough to produce offspring who go on to reproduce, and if they produce more offspring than their competition, then those forms can become ever more common over time at the expense of their competition. If all these contingencies do occur, indeed co-occur, then the more prolific life form will become more suited—better adapted—to the environment in question. If the forms are sequestered from each other by some mating barrier, then they would diverge over time, and this was the explanation Darwin and Wallace proposed for the origin as well as specialization of species.
This version asserts cause and effect in a scientific and testable way: If a cause is present, then the effect will follow. It is an assertion about the world that is so logical that if the conditions are correct, the conclusion must follow. In a sense it defines the conditions for adaptive change. But it doesn’t assert that those conditions actually exist: determining that is where the assertions become science.

Because of this, natural selection is always possible, and sometimes clearly occurring. But that doesn't mean it is occurring in any given case. But it is typically hard if not impossible to actually prove that the 'ifs' apply to a given situation. Indeed, weirdly and ironically, to say that selection is not occurring is almost a mystical and unprovable claim. How can you ever show that there is exactly zero difference in survival or reproductive output of one version of a trait or its underlying genotype compared to another? Since each individual and its circumstances (and its genotype) is different, what kind of evidence could you possibly collect?

In an experimental setting, you can approximate this with large samples, using clones (more or less genetically identical comparison strains) and so on. Even samples from the natural world can sometimes show sufficiently clear differences in fitness between traits or genotypes. Of course, even here the comparison is judged by some sort of inherently subjective statistical criterion, such as a 'significance' test--a topic we've written about before. But in some instances, nobody really argues, when it comes to clear-cut contemporary cases.

It's much more difficult when it comes to trying to give a classical Darwinian natural selection explanation for a trait that is here today, in terms of why it got here. Here we are often in the realm of almost pure story-telling (often, and often properly, derided as Just-So story-telling). We cannot directly observe the requisite ecological, population, competitive, and other aspects of the past, even at any one time, much less over the eons of time over which most complex adaptations seem to have taken place (the idea of Darwinian gradualism).

In fact, Darwin was trying to explain how organisms change to adapt to their changing environments, but by far most selection is about how organisms don’t change! Purifying selection, that is, selection against changes in the established traits (or their underlying genotypes) is far more pervasive and easier to detect (and more convincing) than ‘positive’ adaptive selection. That’s because we clearly find that known functional parts of the genome (that is, areas like regular gene protein codes) vary within and between species by far less than areas with less clear function. Finding DNA evidence for adaptive change is much more difficult—unless, of course, you view the genes being maintained by purifying selection as having got there by adaptive selection. But that view is often if not usually an assumption.

In fact, there are ways in which traits may sometimes, often, or even mainly be determined at any given time, and over evolutionary time, that would undermine even the invocation of conservation as one of, if not the criterion for biologically relevant function. We’ve written about that, but it is beyond our topic today.

When testable becomes ideological
Many biologists are enraptured by Darwinian selection, for various reasons. One is that it provides a satisfying dogma you can invoke without restraint and by assumption rather than any serious standard of proof. Making the assumption is often justified by stating some sort of physics-based general theory of the cosmos, such as that everything biological involves energy, and if something uses more energy than its competitor its fitness will necessarily be less--if you have to eat more than your competitor to maintain your body or genotype, your competitor will have an easier path to success. But an assumption cannot be offered as an explanation of any particular case, and cannot by its very nature be questioned (that's what an assumption is).  Even invoking the laws of thermodynamics or other physics theory were correct doesn't mean the consequence is detectable or meaningful in any given case--such as how much DNA a species' genome can tolerate that has no function, or trying to give an adaptive explanation for how many hairs there are on a rabbit's body.

Even the testable version of natural selection (the ‘if’ rather than ‘since’ version) is close to a tautology because when the ‘ifs’ are true then they are essentially the same as the ‘sinces’: it’s just another way of saying what is reproductively better reproduces better. This problem is widely known to philosophers of biology, and to some biologists, but the behavior and statements of many if not most biologists (including the human geneticists whose work is hyped daily by the media) suggests they’ve rather poorly understood this.

Of course, adaptive scenarios asserting competitive natural selection may be true, and indeed many are. And selection may be the explanation of a large fraction of traits that are here today. But that is not automatically so. First, we should be checking the strength of evidence for each of the ‘ifs’ that are at least implicitly invoked in any such story.

If the story is just offered invoking Darwin’s name or natural selection, without checking that evidence seriously, then what is being stated is an ideology, not science.

Even without being in any way incompatible with the general idea of adaptive evolution, there are a number of ways in which complex traits can arise and evolve in organisms that do not involve competitive Darwinian selection—nor creationism nor implausibly blind luck. We’ll turn to those next….