All AbouT SEx 259
fitness. These kinds of displays are called “indicator traits”
because they indicate to females a male’s genetic quality. For
example, males with alleles that make them good at foraging and
resisting parasites may have more energy to grow a long tail. A
female that chooses a long-tailed male is therefore mating with
a male that also carries good genes for foraging and immunity.
The offspring inherit their mothers’ preference for long tails and
their fathers’ good genes. (That is, the preference loci and the
good genes loci are in linkage disequilibrium; see Chapter 5.) A s
natural selection causes the good genes to spread, it also causes
preferences for long tails to spread as well.
Evidence for the good genes mechanism comes from experi-
ments with three-spined stickleback fish (Gasterosteus aculeatus).
Barber and colleagues studied a character preferred by females:
intense red coloration of the male’s belly [5]. They found that
young fish with bright red fathers were more resistant to infec-
tion by tapeworms than were their half-siblings that had dull red
fathers (FIGURE 10.16). The red coloration is based on carotenoid
pigments, which are obtained from food and appear to enhance
development of an effective immune system. The implication of
this result is that female preferences for red males will become
correlated with alleles that strengthen the immune system, and
stronger preferences will evolve as a side effect of natural selection on immunity.
A final mechanism for the evolution of mating preferences is called Fisher’s
runaway, after the pioneering population geneticist R. A. Fisher (see Chapter 1).
Females with preferences for long tails tend to mate with males that have a long tail,
and so their offspring tend to have the genes both for a long tail and the preference
for a long tail. (That is, the genes for the male trait and the female preference are in
linkage disequilibrium.) If the combined forces of natural and sexual selection favor
longer tails, then longer tails and stronger preferences for longer tails will evolve.
The stronger preferences in turn will favor even greater exaggeration of the tails,
causing both the long tails and preferences for them to experience an explosive evo-
lutionary runaway. Unlike the other mechanisms we have discussed for the evolu-
tion of mating preferences, the runaway process has never been directly observed.
The good genes and runaway mechanisms differ in an important way from direct
benefits and pleiotropic effects [27]. With direct benefits and pleiotropic effects,
alleles that affect female mating preferences also influence survival and reproduc-
tion, so they themselves are targets of natural selection. That is, they evolve by
direct selection acting on alleles that affect a mating preference. In contrast, with
the good genes and Fisher’s runaway mechanisms, the preferences evolve by indi-
rect selection. Here preference alleles evolve because they are correlated with (in
linkage disequilibrium with) alleles at other loci that are the targets of selection.
Natural selection acts directly on the “good genes,” but not on the preference genes
themselves. Theoretical analysis suggests that direct selection on preference genes
may often be stronger than indirect selection [26]. While there are many well-docu-
mented examples of direct selection acting on preferences, the evidence for the role
of indirect selection is less strong. Experiments such as that on three-spined stickle-
backs described earlier support the good genes mechanism, but others do not [40].
Female choice and male-male competition are often considered alternative
modes of sexual selection, but in fact they can operate together. A male’s horns (or
other armaments) are frequently tested in combat. Winners of those contests may
be more likely to carry good genes, which would favor female preferences for the
armaments. If this hypothesis is correct, female preferences and male combat can
reinforce each other [9].Futuyma Kirkpatrick Evolution, 4e
Sinauer Associates
Troutt Visual Services
Evolution4e_10.16.ai Date 12-20-2016Offspring infected by tapeworm (%)0.1 0.15 0.2 0.25 0.3 0.35
“Redness” of father2505075100
Pond 1
Pond 2
The offspring of more
brightly colored males
displayed higher
resistance to infection.FIGURE 10.16 Evidence for the good genes mechanism
for the evolution of female choice. The percentage of
young three-spined sticklebacks (Gasterosteus aculeatus)
that became infected when exposed to tapeworm larvae
declined with the intensity of their fathers’ red coloration.
Red males, which are attractive to females, have alleles that
make them resistant to tapeworms and that are passed to
their offspring. (After [5].)10_EVOL4E_CH10.indd 259 3/22/17 2:25 PM