NATuRAl SElECTioN ANd AdAPTATioN 63
An example of a selfish genetic element that exhibits segregation distortion is
the t locus of the house mouse (Mus musculus). In a male heterozygous for a t allele
and for the normal allele T, the t allele kills sperm that carry the normal allele. As a
result, more than 90 percent of the male’s sperm carry t. Embryos that are tt homo-
zygotes, however, die or are sterile. Despite these disadvantages to the individual,
segregation distortion is so great that the disadvantageous t allele reaches a high
frequency in many populations of mice.
Selfish genetic elements forcefully illustrate the nature of natural selection: it is
nothing more than differential reproductive success (of genes in this case), which
need not result in adaptation or improvement in any sense. Selection among indi-
viduals is at a “higher level” than selection among genes [37]. Selection at the gene
level may act in opposition to individual selection: it may be harmful to individual
organisms, and might even cause the extinction of populations or species.Selfish genes and unselfish behaviors
Evolutionary geneticists have long recognized that natural selection will cause an
allele to increase in frequency if it consistently leaves more copies of itself to sub-
sequent generations, no matter how it causes its greater success. For example,
plants that produce more pollen are likely to fertilize more ovules, so any allele that
increases pollen production is likely to spread. J. B. S. Haldane wrote in 1932 [24] that
“No sufferer from hay fever will doubt that more pollen is produced than is needed
to assure that almost every ovule should be fertilised.” In the same book, he wrote
that “in a beehive the workers [which do not reproduce] and young queens are sam-
ples of the same set of genotypes, so any form of behaviour in the former (however
suicidal it may be) which is of advantage to the hive will promote the survival of the
latter, and thus tend to spread through the species.”
The key issue is that it is often useful think of selection among genes, based
on the effects that change their frequencies—whether these effects are on the
number of pollen grains, behavior that enhances the survival of relatives that
share the same gene, or many other biological features. In a sense, then, any
gene that has successfully increased in frequency is a selfish gene, as biologist
Richard Dawkins has famously written [9]. The evolution of many puzzling fea-
tures of organisms can be understood by considering the rates at which differ-
ent variants of a gene that affects the trait would change in frequency over the
course of generations.
An important example of this approach is the topic that Haldane addresses
in accounting for the behavior of worker bees: what he called “socially valuable
but individually disadvantageous characters.” Many such altruistic traits are best
explained by the principle Haldane described, which has come to be called kin
selection. An allele for altruistic behavior can increase in frequency in a population
if the beneficiaries of the behavior are usually related to the individual who per-
forms it. Since the altruist’s relatives are more likely to carry copies of the altruistic
allele than are members of the population at large, when the altruist enhances the
fitness of its relatives, even at some cost to its own fitness, it can increase the fre-
quency of the allele. We may therefore define kin selection as a form of selection in
which alleles differ in fitness by influencing the effect of their bearers on the repro-
ductive success of individuals (kin) who carry the same allele by common descent.
The simplest example of a trait that has evolved by kin selection is parental care:
alleles that enhance a parent’s care-giving behavior have increased in frequency
because they promote the survival of identical copies of those same alleles that the
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