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Levels of Selection

Barry Sinervo©1997


Levels of Selection

Introduction to Levels of Selection

Genic Selection

What is the unit of Selection (individuals or genes)?

t-allele in mice (Lewontin)

Individual selection and the "Whole-organism Approach"

Kin Selection and Hamiltons Rule

Social Hymenoptera (Hamilton)

Cannabalism in Tiger Salamander Larvae (Pfennig)

Group Selection

Reproduction and Density (Wynne-Edwards)

Back to the t-allele in mice (Lewinton)

Artificial Group Selection in Flour Beetles (Wade)

Species Selection

Levels of Selection

The genetic makeup of a population is altered by an interaction with the ecology of the organism. This interaction is the process of natural and sexual selection. We have covered the basics underlying genetics and selection and now we will treat arguments concerning levels of selection. The fundamental premise of Darwinian selection is that natural selection acts on the individual or more properly differences among individuals within a population. In recent years a number of authors have argued that selection might act at a number of different levels and the levels are loosely structured according to heirarchies of biological organization:

genes -> individuals -> kin -> groups -> species

Dawkins has been the most vocal advocate that selection acts not on individuals per se, but on genes. The theory of genic selection is often referred to as the selfish gene theory. Individual selection is next in the hierarchy, followed by kin selection. Kin are defined as closely related individuals and it is thought that it might be beneficial for an organism to aid kin in order to promote inclusive fitness as related individuals are likely to share many genes in common. Group selection is a more difficult concept to grasp and it also is the subject of an ongoing debate in evolutionary biology. Suffice it to say that selection at the level of groups occurs when a group of individuals produces more groups than other groups. Rather than acting on individuals, group selection is a process entirely analogous to individual selection, but acting at the level of groups. Again the traits underlying group selection must be heritable if the species is to evolve by group selection. Finally, species selection acts at yet a higher level. Those members of a clade (e.g., a group of closely related species) that produce more species, or perhaps have greater longevity in the earth's history (lower extinction probability) are going to become overly represented on the planet in much the same way that one allele at a particular genetic locus spreads through a population of individuals and increases in frequency at the expense of alternative alleles.

We will first consider classical Darwinian ideas of natural and sexual selection in great detail, and then we will move onto the ideas of levels of selection. We will end this chapter with a consideration of the process of speciation and the role of animal behavior in the various modes of speciation. Do not confuse models of Speciation Mechanisms with the concept of species selection that is discussed above. Most models of Speciation Mechanisms operate by the process of individual selection or classic Darwinian natural and sexual selection.


Genic Selection

The concept of genic selection is closely allied to answers to the following two questions:

What is the unit of selection?

Is the unit of selection the individual organism? This would be the fundamental tenet of individual selection. Let's explore the concept of individual selection as a review for previous readings. While we measure selection on individual traits and we tend to atomize the phenotype, this is really only a simplification that is necessary from the point of view of statistical power. The individual trait is not the unit of selection. A researcher indentifies a particularly trait that is under selection and tests to see whether the power of selection is statistically significant. In principle, we should analyze each and every trait in an organism and study the correlations between traits to completely describe the evolution of a species. Brodie's study on garter snake morphology (striped vs spotty) and behavior (straight slither vs reversals) would be a classic example of correlated selection. In the study of behavioral traits we must consider selection on morphological, and physiological traits that might be functionally (e.g., selectively) correlated with the behaviors or mechanistically correlated (e.g., by proximate mechanisms) with the behavior. This approach to studying individual selection focusses on the whole organism and is fleshed out in more detail in the next sub-section Individual selection and the whole-organism approach.

Is the unit of selection the gene? In contrast, Dawkins and other adherents to the theory of the selfish gene or genic selection would argue that because selection changes combinations of alleles at a genetic locus, the gene or genetic locus must be the fundamental unit of selection. This is the ultimate in the atomization of concepts of selection. What better way to explore this concept then to read an essay that Dawkins has written on Genic selection (on reserve and on electronic reserve in the library this paper will be the first tutorial paper in Section -- read it for next week). At first glance, this argument seems immenently reasonable. For if natural selection acts to change allele frequencies at a genetic locus, then a purely "reductionist approach" would be to reduce the problem to the lowest common denominator in all evolutionary theories -- the gene. The gene is after all the fundamental unit of inheritance. I suppose a purist reductionist might go further and say that a nucleic acid base pair was even closer to the true unit of inheritance, but that might be going to far. We also want a theory that links selection, inheritance, with at least some aspect of the phenotype, and a gene codes for a protein and the protein would be considered the smallest unit of the phenotype that we could find.

Bottom line on terms: Genic Selection, Selfish Gene, or Replicator Selection. Despite the name, the theory of genic selection considers the allele as the fundamental unit of selection. The allele is the fundamental "replicator" as it gets copied during meiosis and mitosis. Accordingly, the term replicator selection has been synonymized with genic selection. The term selfish gene has also been applied to the theory, with reference to the notion that in the extreme case, the selfish gene is only concerned with propagating itself even at the expense of the individual (see t allele in mice below). Thus when we think of the concept of genic selection, or the selfish gene, or replicator selection think in terms of the allele. Unfortunately, such terminology adds uneeded confusion to what are already difficult concepts.

Bottom line: realize that genic selection, selfish gene, and replicator selection refer to an allelic copy -- the fundamental replicator.

A simple example, should clarify these issues...


t-alleles in Mice: a selfish gene

Some populations of mice possess an interesting mutation that distorts the normal meiotic products of male mice and it is located at the t-locus (Lewontin). Let us denote the wild type allele at the t-locus +. Thus, a homozygous wild type would be +/+. Let us denote the mutant allele at the t-locus: t. Thus, an individual heterozygous at the t-locus is t/+ and a homozygote is t/t. The effect of the t-allele on the phenotype is as follows:

+/+ produce the normal wild type sperm.
t/+ produce normal sperm, however the ratio of sperm of the t-allele vs +-allele is distorted from 50:50 that one would expect by normal meiotic processes. These t/+ heterozygotes produce 85-95% t-allele sperm and only 5-15% +-allele sperm.
t/t homozygotes are sterile.

1. The origin and spread of the t-allele

Because t/+ heterozygotes produce an overabundance of t-alleles, the t-allele is refered to as a selfish gene relative to the +-allele. When such a mutation arises in a population, it should spread rapidly as a male that carries one copy will produce 85-90% sons that also carry the t-allele. This is the classic notion of a selfish gene. Understanding the conditions that lead to its spread after it originates is a key step in describing the evolutionary dynamic. See the lecture notes on History and Method: Probability of a mendelian allele making it through segregation where I describe the likelihood that mutation will spread in a population by the laws of mendelian inheritance. The t-allele greatly enhances the chances that the mutation will spread after the mutant arises.

2. What limits the spread of the t-allele

The case of the t-allele is also useful from the point of view of illustrating a selfish gene. The t-allele spreads and increases in frequency up to the point where a significant number of males in the population are in fact sterile. Thus, without concern for the fitness of the individual (e.g., sterility in some cases), the t-allele marches to very high frequencies, and it leads to a considerable depression in the mean fitness of males in the population. Even the females that happen to mate with such t-allele infested homozygotes will produce no offspring. Hold onto this last fact as it will become important in subsequent consideration of the t-allele when I discuss group selection.

3. Equilibrium for the t-allele

The t-allele cannot spread beyond a certain frequency or the whole population will become sterile. The t-allele needs a few +-alleles around in order to propagate.


Individual Selection and the Whole-organism Approach

The dichotomy between the whole-organism approach and other approaches in biology has its roots in the 'How?' versus 'Why?' questions in evolutionary biology that were first discussed by Ernst Mayr. Recall from the first essay on History and Method in Animal Behavior: Ultimate versus Proximate Mechanisms that I made a distinction between proximate mechanisms and ultimate mechanism. The concept of the gene as a unit of selection indentifies the gene as the source for all proximate mechanistic processes that lead up to the phenotype, and it also identifies the gene as the key element in the selective processes that lead to evolution of the phenotype. In constrast, the whole-organism approach would hold that it is impossible to atomize phenotypic traits and the proximate mechanistic causes of phenotypic traits to such a low level of analysis and students of the organismal approach would maintain that the behavioral phenotypes of organisms are caused by genes, development, physiology, learning and the interaction of all these factors with the environment.

Lets start with the proximate effect of genes. From the discussion on Genes and Selection: Introduction to Genetic Terms and Mendelian Traits, we can see that even an allele at a locus does not produce its effect in isolation, the dominance state and the existence of an allele on the other chromosome could modify the expression of the allele at the first locus. If the first gene was recessive, and the second gene was dominant, then the first gene would have no effect on the phenotype of the organism. This is an example of a higher order interaction between alternative alleles that is difficult to reconcile if we were to consider the allele the unit of selection (what adherents of genic selection believe). Even the fitness of the t-allele is dependent on the allele on the other chromosome.

Let us move up the causal cascade and think about the genetic locus as the unit of selection -- or rather the two alleles that comprise a genetic locus. Several problems arise as we move up to this level of selection. First, the expression of the phenotype as a function of this locus may be contingent on the interaction of this locus with other genetic loci in the organisms -- epistasis may influence the outcome. Moreover, the expression of the gene and its effect on phenoytpe is also shaped by an interaction with the environment. Finally, a gene does not just affect one trait, but can affect many organismal traits through pleiotropy, or the complete expression of a polygenic trait may require the additive effect of many genes.

Proximate mechanisms as the source of correlations between traits

All of these genetic effects serve to link the various organismal traits together in a complicated web of genetic and mechanistic interactions. The end result of such interactions are seen as the correlations between traits. For example, the level of testosterone in an organism is correlated with the aggression as well as with muscle mass (just look at a bull and compare it to a steer of similar age). The essence of the whole organism approach is to try to understand the source of such correlations between organismal traits, and how such correlations govern the evolution of the species. For now, realize that the correlations between traits arise from the proximate mechanisms of genetics and the proximate mechanisms of development, physiology and learning. Such proximate mechanisms govern the forces of selection and they might constrain the direction that evolution can take. [For example, is it possible to get an aggressive, testosterone-landen, care-giving male bird? Is aggression incompatible with parental care?]

Natural and sexual selection as the source for the correlations between traits

Another source for the correlation between traits is the process of natural selection. Natural selection might favor specifc alleles at a gene that controls a behavioral trait and specific alleles at a gene that controls a morphological traits. Such loci are not linked by the mechanisms of genes, development or physiology, but they are linked by the process of selection. The case of stripped versus spotted snakes (Brodie) may be an example where selection bundles up unlinked genes (e.g., genes that control behavior and genes that control morphology). Sexual selection bundles up the alleles for female choice and the allele for the male trait by a similar process. Thus, a correlation between the traits making up the organism also occurs by the process of individual selection.

Neither the interactions of alleles, genes, traits, or the effect of selection can be predicted from the structure of an allele.

It is the existence of higher level properties of genes and proximate mechanisms that presents difficulties for the theory of genic selection. We refer to such higher-level properties of genes as emergent properties. The effect of genes cannot necessarily be reduced to a description of a single allele or even alleles at a locus, because of the emergent properties of the genes that arise at higher levels or organismal integration. These philosphical issues require a bit of thought beyond just lecture and reading, and we will explore them as a group in the tutorial discussion section by reading the Dawkins paper.


Kin selection

J. B. S. Haldane clarified the issues underlying the study of kin selection with his clever and illuminating statements regarding its operation (paraphrased):

He would gladly give up his life for two sibs, 8 first cousins, etc.

Embodied in this statement is the notion of the genetic equivalence of an individual's genome, and shared alleles with related individuals. If 1/2 of the genes are shared with sibs, then it would take 2 sibs to make up for the total genetic material in an individual. Certainly, some genes would be lacking, because of the probabilistic relationship of relatedness that sibs share, but this would be made up for by duplicate copies of other genes.

W. D. Hamilton captured the essence of kin selection in a simple equation that describes the concept of inclusive fitness. From the point of view of individual selection, what is important is not only the individuals genes, but also the success of closely related individuals. A behavior that is deemed altruistic is one that helps another, but in some way costs the altruist. If the benefits of the the altruistic act outweigh the costs, then the behavior will be favored by selection:

Fitness of a behavior =

effect of behavior on the fitness on the individual

+ Sumation for each kin affected (indirect effect on kin's fitness * coefficient of relatedness)


Lets work through Haldane's impeccable logic for a "sib-sacrificial" behavioral act using Hamilton's equation. This argument assumes that the kin were goners unless he intervened.

If he sacrifices his own life, the effect of the behavior on fitness is W = -1.

He has saves two sibs, which yields W = +1 for each sib.

Each sib has a coefficient of relatedness = 0.5.

Thus, the indirect effect of the the behavior on his kin = 2 * 0.5 = 1.0,

and the net fitness of the behavior of saving two sibs at the cost of his own life is

W = -1 + 2 * 0.5 = 0.

He just breaks even. If you were to throw in a first cousin (r = 0.125), he comes up positive in the fitness tally. Lets look at the verbal equation that is stated above in symbols where:

  1. W = fitness of a given behavior
  2. d = direct effect of the behavior on the individual
  3. i = indirect effect of the behavior on the kin of the individual
  4. r = coefficient of relatedness.


W = d + sum(i * r).

if d, the direct effect is deleterious to the invidual, then it is a fitness cost and i should be a fitness benefit to kin for the system to evolve the behavior. The break even point would be W = 0, in the above equation or and the net fitness d+sum(i*r) should be greater than zero:

0 < d + sum(i * r),

or upon rearranging

d < sum(i * r),

and verbally we have a simple statement, as long as

costs to indvidual < benefits to kin,

the behavior is favored by kin selection.


Social Hymenoptera as a Case Study

Hamilton's statements regarding kin selection have a distinct genic selection flavor to them. A behavior can increase in frequency because it favors the fitness of genes per se. Regardless of whether the genes are in the individual or in a closely related kin is irrelevant from the viewpoint of genes. The most striking example of kin selection in the animal kingdom includes those social insects that develop into a sterile worker and allow their sister (the queen) to carry on all reproduction. Such is the case for social hymenoptera: ants, wasps and bees. E. O. Wilson has suggested that such sociality has evolved on at least 11 separate occaissions with this one order of insects. [And rarely in other insects].

A most unusual aspect of hymenopteran reproductive biology is undoubtedly related to the propensity with which this group of insects evolves such self-sacrificing behavior. Sex determination in the hymenoptera is governed by ploidy (n or 2n):

  1. eggs that are fertilized develops into a female (2n),
  2. eggs that are unfertilized develops into a male (n),

This form of sex determination, haplodiploidy, leads to some unusual coefficients of relatedness for females and males. For example, a male receives 100% of his genetic material from his mother. Males also produce genetically identical sperm.

Thus if a foundress (a founding queen) for a hive is fertilized by a single male, the daughters from such a union share 0.75 of their genes on average which is considerably higher than the typical 0.50 shared by sibs. Hamilton has argued that such a high coefficient of relatedness predisposes the hymenoptera to the evolution of kin based altruism.


Cannabilism in Tiger Salamander Larvae

Cannabalisms is a widespread trait in the animal kingdom. Where you find large monotypic stands of an organisms and food becomes limiting, the best item on the menu might just be a conspecific. David Pfennig performed an interesting experiment. He reared the larvae of the cannabalistic Tiger Salamander in various kin groups.

  1. As a control, he reared unrelated individuals in the same tub
  2. He reared half-sibs in the same tub (0.25 relatedness)
  3. He also reared full sibs in the same tub (0.50 relatedness)

He then scored the probability of cannabalism and compared this among his experimental treatments. If the salamanders had sibs in their tubs the probability of cannabilism was less than that for half sibs and the probability of cannabilism for half sibs was dramaatically lower than tubs with unrelated individuals.

These results suggest that:

  1. the larvae have kin recognition
  2. kin recognition alters the behavior of cannabalism
  3. presumably a tadpole that does not eat kin will be favored by kin selection

Pfennig goes on to suggest that recognition of self may arise from the distinct food that an aggregation of tadpoles might ingest. The tadpoles tend to aggregate after hatching and thus a group of related tadpoles might stick around long enough to pick up odors in common with one another during their group feeding.

Tiger salamander photo from


Group Selection

Group Selection and Self-limiting Behaviors

"Classic" group selection stems from arguments that Wynne-Edwards made in the 1960's. Wynne-Edwards was arguing for the evolution of a form of population regulation by the mechanism of group selection in which behaviors evolve because they benefit the groups existence. In this case Wynne-Edwards argued that animals might evolve mechanisms that limit reproductive effort for good of species and the arguments are outlined as follows:

  1. avoid stripping resource base and being exterminated by evolving some kind of self-limiting behavior
  2. difference in groups fitness, not individual fitness are what lead to the evolution of such self-limiting behaviors
  3. group benefit takes precedence over individual benefit
  4. the driving force underlying such group selection pressure is variation in rate of increase or extinction among groups
  5. this behavior has a genetic basis (e.g., in the individuals)
  6. in the case of self-limiting behaviors, those groups that evolve individual behaviors that are self-limiting from the groups perspective are the groups that will have a lower probability of extinction.

As soon as these arguments were made, G. C. Williams and others ralied against them and came up with the following arguments.

problem # 1 - the group can always be invaded by an individual "cheater" strategy.

<see Alcock FAR SIDE - prone to cheating, incr. own success>

The group selection advocated by Wynne-Edwards is a form of altruistic behavior in which individuals limit their own reproductive success to benefit the group. The key distinction in this case is that the members of the group are not kin, or the argument might work as kin selection rather than group selection. The group selection argument requires a special kind of altruism towards non-kin to evolve -- true altruism not kin altruism.

Thus, true altruism not an evolutionary stable strategy - it can be invaded by a selfish morph.

What is an evolutionary stable strategy or ESS? An ESS is a strategy that is so good that it is uninvadable by any (and all) mutant strategies that arise in the population. Thus it is stable over the long haul. The idea of an ESS was originated by Maynard Smith and Price, and we will use the concept over and over again during the semester. It is particularly useful in understanding the evolution of behavioral strategies that involve an interaction between two players -- an evolutionary game.

In the case of group selection, those individuals that are playing the group strategy (be self-limiting) will always do worse than the selfish individual that does not play by the rules. These cheater individuals will produce more progeny at the expense of the other members in the group that are self-limiting. Once the mutant arises, it spreads through the group rapidly.

problem # 2 - relative "lifespan"

Another problem with group selection is the rapidity with individuals reproduce compared to the turnover time involved in group selection. It takes far longer for groups to go extinct or for one group to overwhelm the selective advantage of individuals.

Bottom line: Evolutionary biologists and behavioral ecologists do not say that group selection is impossible, but rather that the conditions required for group selection would be rarely met in natural populations. Groups would have to be very small, and the selective advantage among groups enormous to overwhelm the ever present force of individual selection.

The t-allele in mice illustrates how group selection would work. It is important to realize that group selection is working against genic selection in the following example.


The t-allele Revisited

Lewontin calculated that the t-allele should have a phenomenal advantage over the +-allele (wild type) but it would not completely eliminate it. The equilibrium or expected frequency is:

frequency of t-allele in the population, t = 0.70

However, the observed frequency in populations was

t = 0.36.

Why was there such a large discrepancy?

The spread of the t-allele is in fact limited by the group structure of mice. Mice live in small demes with usually 2 males, and a few females. Recall that the t-allele should increase in frequency to well beyond 50%. With only two males in each group there is a really good possibility that some groups will have no fertile males and other groups will have fertile males. Lets draw out all possible male groups (ignore the females):

1. these groups breed true for +/+:

+/+ and +/+

t/t and +/+ (the t/t is sterile)

2. these groups have a t-allele advantage:

+/t and +/+

+/t and +/t

+/t and t/t

3. this group is sterile and goes extinct

t/t and t/t

The groups that breed true for +/+ spawn off more groups that breed true and are more resistant to extinction.

The groups that have a t-allele advantage have an increasing frequency of individuals with the t-allele. Genetic drift, the random sampling of alleles might actually push some of the spawn of these groups over the top and they go to the "t/t and t/t" state which is sterile. Any sterile group goes extinct. Thus, t=alleles are being continually removed by a group extinction process. Groups that breed true for the wild type +-allele, have a strong group advantage, even over the groups in which the t-allele has an advantage. Eventually the t-allele will increase in frequency in such t-allele infested groups to the point where the spawn of such groups fall into the sterile category.

In the case of the t-allele, group selection balances out the effects of genic selection and it leads to a lower frequency of the t-allele than one would expect if genic selection was the only force acting on the population.


Artificial Selection for "Group Traits"

A final example will serve to illustrate how strong selection must be for group selection to overwhelm the force of individual selection. Michael Wade carried out an experiment in the spirit of Wynne-Edwards. He raised Tribolium, flour beetles, under conditions of high density and under conditions of low density. He raised lots of groups and selected those groups that maintained high output under each of the conditions. He also had some controls in which individual selection was the only force acting on the groups. In the long haul he was selecting for groups that maintained high output under conditions of density and were therefore self-limiting.

This differs from a classic artificial selection experiment in that one would choose those individuals in each group that performed the best in artificial selection. Mike picked entire groups to found the next generation and he replicated his groups to collect lots of data necessary to test group selection.

Over the long haul, he was successful in altering the "self-limiting capabilities" of the beetles and his lab experiments proved that group selection could alter the evolution of the species. But he was also careful to point out that there are very stringent conditions on the strength and efficacy of group selection. It helps to have small groups, rapid group generation time, and very strong group selection to overwhelm the force of natural selection. Wade also described how such group selection is related to kin selection and cannabilism < see lecture for details>.


Species Selection

The principle of species selection has all the same arguments and caveats as group selection. Species selection involves the differential extinction or reproduction of species. The strength of species selection must be strong enough to overwhelm the force of individual selection which is quite powerful, and also fast acting. It is possible that mass extinction events has led to very strong selection for behavioral traits, but without a fossil record for behaviors, how will we ever know for sure?


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