A phenotypic view of evolution Evolution in Structured Populations

Defining Evolution

One of the unusual things about books about evolution is how frequently they fail to actually define evolution.  Typically such books will have several pages describing evolution, so that by the time you have finished reading the section you have a pretty good idea of what they are talking about.  But generally speaking if after reading one of these sections you were asked to complete the sentence “Evolution is defined as . . .” you would be unable to do it.  The hesitance to define evolution is quite understandable.  Indeed, the word “evolution” does not appear in Darwin’s Origin of Species.  Instead, he uses the term “descent with modification”, a phrase that remains as a good definition of evolution.  Darwin’s idea of descent with modification emphasizes both the important aspect of change (modification), but also the idea of transmission between generations.  That is, change within an individual is not enough, rather it is change among individuals, and more specifically change that persists across generations.

Darwin’s definition raises the important point that any definition of evolution has implicit in it the concept of change, but the context in which that change is described is an essential element of the definition.  I am told that this is the reason that Darwin avoided the term evolution.  At the time he was writing his book evolution typically was used to describe the change in an human as they matured, or otherwise went through intellectual or spiritual changes.  If indeed, in Darwin’s time “evolution” referred to a theory that an embryo was a growing or unfolding from a preexisting form with rudimentary parts of the future organism.  At the time evolution would have also been used to refer to the orderly unfolding of events, such as the intellectual or physical developmental changes within an individual over time.   Because of this, he was absolutely correct to avoid using that term.

In common language we are quite comfortable with the thought that a persons opinions can evolve, however, this is not compatible with the generally held concepts of organic evolution.   In organic evolution it is generally held that it is a set of objects that evolves or changes, and that the set changes through the addition, subtraction, or replacement of the objects that make up the set.  In typical thinking about evolution the set is a population and the objects are organisms, however, this need not be the case.  There is no reason why the objects cannot be cells, and the set an individual organism.  Conversely, the objects could be populations and the set could be a group of populations, or as it is typically called, a metapopulation.  Indeed, evolutionary change can be described for any entity that can be described as an object, and is contained within any group of those objects that can be described as a set.  The important point is that in common thinking change in the objects is not considered to be evolution.  This is not to deny that objects change.  An organism is a typical object within a group that is a population.  Organisms are born, grow, mature, and eventually senesce and die.  However, these changes are not considered evolution, rather we give them a different name.  For organisms we would call these changes “development”.  If the object were a population within a metapopulation then we might consider the changes that take place within the population to be development, ecological changes or demographic changes.  However, again, we would not consider the changes within the object to be evolution.  This is a subject I will discuss in a later post.

Darwin deals with the distinction between change within objects (development, ecology, demography) versus the change between objects (evolution) by emphasizing the concept of descent.  Descent with modification alludes to the fact that organic evolution involves objects that reproduce in some form, and generally have a finite life span.  Thus, new objects enter the group through some form of reproduction, and old objects leave the group through some form of mortality.  Evolution occurs because the new objects entering the group are in some way different from the old objects that are leaving the group.

Over the years many definitions of evolution have been presented.  One of the more famous suggested definitions is that evolution may be defined to be a change in gene frequency.  I cannot find the original source for this, but it clearly dates from the 1930s and 40s, that is the time of the “new synthesis”.  The new synthesis was a theoretical consilience of the (at that time new) field of genetics with the changes in appearance, behavior, and physiology of organisms that scientists had been studying for years.  One of the main fields to come out of this synthesis was the field of population genetics, which is the study of gene frequencies in populations.  Seen in this light it is quite clear that by this definition that genes are considered to be the determinants of phenotype, thus the “modification” in descent with modification are changes in the frequencies of the underlying genes.  The implication being that phenotypic changes could ultimately be traced to genetic changes, thus it is reasonable to define evolution strictly in these terms.

There are, however, two issues with this gene-centric definition that make it inadequate.  The first is the obvious issue that this definition eliminates any changes that do not have a genetic basis.  The most obvious of these is “cultural evolution” that is changes that are learned from other members of the population.  Such changes need not, and in many cases don’t, have a genetic basis, and yet they lead to changes in a population that can persist for many generations.  Another interesting example is changes in a population due to the prions.  Prions are alternate conformation of otherwise normal proteins.  In their normal conformation these proteins perform a normal cell function, in their alternate conformation they are the causes of diseases, the most important example of which is spongiform encephalopathy, or so called mad cow disease.  A protein takes on this alternate disease conformation only in the presence of other proteins that are also in that disease conformation.  Without going into detail about these diseases, the point is that prions do cause changes in populations, and these changes are based on conformational changes of proteins rather than changes in the frequency of alleles.

The second issue is subtler.  In standard genetics text books there are generally three domains that are identified.  These are the phenotype, the genotype and the genes.  The phenotype is the appearance of an organism broadly defined.  That is the phenotype is all aspects of the morphology, behavior and physiology of an organism.  The genotype is the genetic makeup of an individual, and finally the genes are the genes that are present in the population.  For the present discussion the important aspect of the phenotype is all aspects of the morphology behavior and physiology of an organism. Thus the genes that make up an organism belong to the phenotype to the extent that they are part of the “morphology” of that organism, however they are part of the genotype to the extent that they cause other aspects of the phenotype. Thus, the sequence of nucleotides in the DNA is part of the phenotype, however the effect of a gene on other aspects of the phenotype (say hoof shape) is not part of the phenotype.  The important aspect of the genotype is that it is the specific assemblage of genes in an individual that interact with the environment to produce the phenotype.  Thus, we need to recognize that it is the genotype in its interaction with the environment and things like culture that determines the phenotype.  Finally, the genes are important because it is these that are passed from parent to offspring.  Thus, the resemblance between parents and offspring is to a major extent due to the transmission of genes.  The genes, as such, to not determine what a trait will be.  It is only after they are assembled into a genotype that a gene affects the phenotype.  Ignoring cultural transmission, offspring resemble their parents only to the extent that the genes transmitted by the parent influence the genotype to affect the phenotype in a predictable manner.  Thus, the genes themselves have no influence on the phenotype, rather they are assembled into the genotype, and it is the genotype that influences the phenotype.  The point is that the gene domain is important in the transmission of traits between generations, not about the expression of the phenotype.

When Darwin spoke of descent with modification he was referring to changes in phenotype, and we should not lose sight of the idea that evolution is about changes in phenotype.   Defining evolution as change in gene frequency misses the fundamental point that evolution should be defined in terms of phenotype, the domain that is changing, rather than in terms of genes, the domain that is mediating that change.

A second definition I will consider is one provided by Futuyma in his book Evolutionary Biology.  In this book he defines evolution as “lasting change in the mean phenotype of a population that transcends the life of an individual”.  This definition is actually quite similar to Darwin’s in that it focuses on changes in phenotype, and specifically excludes changes within an object.  The first clause of this definition, lasting change in the mean phenotype of a population, emphasizes that indeed evolution is about changes in phenotype, but further demands that those changes be of a more or less permanent nature.  That is, this definition specifically excludes temporary changes due to short-term environmental effects.  As an absurd example, the fact that leaves change from dry to wet during a rainstorm is not an example of evolution.  The second clause, that change must transcend the life of an individual, specifically excludes developmental change.  In North America many insects over-winter as eggs.  In the spring the eggs will hatch, the insects will emerge, develop and mature into adults.  Over the course of a season the population will change from a population of eggs to a population of mature flying adults.  The second clause tells us that this is not evolution since it is a result of developmental changes taking place within an individual.  Thus, whereas Darwin’s definition emphasizes that evolution is change among units by emphasizing the reproduction and replacement aspect of living systems, Futuyma’s definition emphasizes that evolution is among objects by specifically excluding change within objects.

It is also interesting to note that Futuyma specifically identifies the objects to be individuals and the groups to be populations of individuals.  By individual it seems that he is referring to organisms.  However, as I suggested above, there is no reason that the objects cannot be cells and the groups organisms, nor is there any reason that the objects cannot be populations and the groups metapopulations.  There are two ways that this problem can be handled.  One is to change Futuyma’s definition to use a more generic term than individual.  The other is to decide that individual does not necessarily refer to organism.  The question becomes whether and under what circumstances it is reasonable to refer to a cell within an organism to be an “individual”, and conversely when a population within a metapopulation can be considered an “individual”.  I will address this in a later post.

Finally, a third definition of evolution that is frequently used is heritable change in the mean phenotype of a population.  This definition is similar to Futuyma’s definition in that it does emphasize the change in the mean phenotype of the population, and the term “heritable” is intended to separate within object developmental change from changes taking due to changing the objects in the set.  However, this definition falls short in the question of what does heritable mean.  Heritable in its most basic form means that the offspring resemble the parents.  The choice of this term over the gene-centric concept of change in gene frequency is good, in that the specific mechanism causing the resemblance is not specified.  However, this definition emphasizes that only changes that can be passed from parent to offspring count as evolution.  The problem comes when a trait is not completely heritable.  Consider the situation when the resemblance between parent and offspring is only 50%.  In that case we would certainly believe that change in the trait is evolution.  On the other hand if the resemblance between parent and offspring is 0, then the trait is not heritable, and we would not consider change in that trait to be evolution.  The question now becomes how low does the resemblance between parent and offspring have to become before we don’t consider it evolution?  That is, if the resemblance between parent and offspring is only 0.01% (which in any reasonable experiment would not be detectable) is that evolution?  Unfortunately, this definition of evolution puts an arbitrary break point in what is actually a continuous range of possibilities from traits not being heritable to traits being highly heritable.

This leads us to what is an appropriate definition for evolution.  I would argue that both Darwin’s definition of descent with modification, Futuyma’s definition of lasting change in the mean phenotype of a population that transcends the life of an individual, and heritable change in the mean phenotype of a population are adequate.  However, we need to recognize that evolution need not change just the mean of a population.  One of the forces of evolution is selection, and one form of selection is stabilizing selection.  Stabilizing selection does not change the mean of a population, rather it reduces the variance in a population.  This occurs because extreme individuals do not survive and reproduce as well as individuals near the optimum, which is usually very close to the population mean.  Thus, we should probably consider any changes in the distribution of a population, not just changes in the mean, to be evolution.  I would go on to argue that neither definition explicitly states that evolution takes place by replacements.   Thus, I would first argue that Futuyma’s concept of change in the mean phenotype needs to be expanded to include any changes in the distribution of phenotypes, including both changes in the mean and changes in variance.  Second, we need to explicitly recognize the idea that our concept of evolution is change due to the turnover of objects, not due to the change in those objects themselves.  Thus, I suggest that a first pass of a definition of evolution is change in the distribution of phenotypes in a set due to the addition, loss or replacement of objects.  If we decide that “sets” always refers to some form of population, and that objects can always be called “individuals” then we get a less clumsy definition that uses a language that is consistent with other definitions.  Replacing set with population and object with individual we can define evolution as change in the distribution of phenotypes in a population due to the gain, loss, or replacement of individuals.  This definition conveys nearly the same information as Darwin’s and Futuyma’s, however it makes explicit that evolution is due to a change in the makeup of a population through the gain and loss of individuals.


Thus, we can finish the sentence posed at the beginning of this post:

Evolution is defined as the change in the distribution of phenotypes in a population due to the gain, loss, or replacement of individuals.

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