Evolution__3rd_Edition

..
The unit of selection, in a second
sense, is the gene ...
. . . because only genes last long
enough for natural selection to
adjust their frequencies
CHAPTER 11 / The Units of Selection 307
success of the lions as a whole increases, the frequency of lions in the ecosystem will
increase too, and lions might, over geological time, come to replace other competing
predators on the plains. The question in this section is whether natural selection
directly adjusts the frequency of any of these units a nucleotides, genes, neurons, individual
lions, lion prides, lion species?
The answer was most clearly given by Williams in Adaptation and Natural Selection
(1966) and Dawkins in The Selfish Gene (1989a). It is at least implicit in all theoretical
population genetics and, indeed, in the previous section of this chapter. For natural
selection to adjust the frequency of something over the generations, the entity must
have a sufficient degree of permanence. You cannot adjust the frequency of an entity
between times t 1 and t 2 if between the two times it has ceased to exist. A character that is
to increase in frequency under natural selection therefore has to be inherited.
We can work through the argument in terms of the example of an improvement in
lion hunting skill. (We shall express it in terms of selection on a mutation: the same
arguments apply when gene frequencies are being adjusted at a polymorphic locus.)
When the improvement first appeared, it was a single genetic mutation. At a physiological
level, the mutation would produce its effect by making some minor change in the
lion’s developmental program. After the mutation has appeared, there is a “pool” of
two types a the new mutation, and all the rest (i.e., all alleles of the mutation, and the
behavior patterns they produce). There will, of course, be genetic variation at loci other
than the one where the mutation arose, but that variation can be ignored because it will
be randomly distributed among the mutant and non-mutant types. The lions with the
mutation will survive better and produce more offspring. Natural selection is starting
to work. Now we can ask what natural selection is adjusting the frequency of. Is it lions?
Lion genomes? Or the mutation?
Williams and Dawkins’ answer is the gene a the particular mutation that produces
improved hunting. Natural selection cannot work on whole lions because lions die:
they are not permanent. Nor can it work on the genome. The mutant lion’s offspring
inherit only genetic fragments, not a copy of a whole genome, from their parents.
Meiotic recombination breaks the genome. In Williams’ expression, “meiosis and
recombination destroy genotypes [i.e. genomes] as surely as death.” What matters, in
the process of natural selection, is that some of the lion’s offspring inherit the mutation.
These offspring in turn produce more offspring, and the gene increases in frequency.
The gene can increase in frequency because it is not (like the genome) fragmented by
meiosis or (like the phenotype) returned to dust by death. The gene, in the form of
copies of itself, is potentially immortal, and is at least permanent enough for it to be
possible to alter its frequency in successive generations.
It may be objected that recombination breaks genes as well as genomes. Recombination
strikes at almost random intervals in the DNA and therefore could strike within
the mutation we are concerned with. A little reflection, however, shows that is irrelevant.
The information of the gene, not its physical continuity, is what matters. Consider
the length of chromosome containing the gene and its mutant form; there will usually
be a number of polymorphic loci around the mutant locus (Figure 11.3a). Now consider
what happens when recombination strikes either in a neighboring gene or in the
gene itself. Nearby recombination breaks the information in the chromosome a which
is just to repeat the point already made, that recombination destroys the genome