might be constrained from doing so. For example, Hamilton and Zuk (1982)
suggested that plumage brightness and song complexity in birds indicate
parasite load; parasites will directly influence plumage color and, it is
assumed, the energetic potential to make complex songs. If there is a genetic
basis to parasite resistance, then these signals are honest indicators of some
genetic quality. An alternative means for enforcing signal honesty is the
handicap principle (Zahavi and Zahavi 1997). This hypothesis suggests that
males evolve signals that are costly in terms of survivorship; thus, only truly
healthy males can afford the handicapping signal.
Early population-genetic models of the handicap principle did not
support its internal logic (reviewed in Zahavi and Zahavi 1997). Later
models, however, showed that the handicap principle could work through
linkage disequilibrium. In this case, however, the preference genes become
correlated with the “good genes” for survivorship that are being signaled.
For example, let us assume faster call rate, which will be energetically more
expensive than slower call rate, indicates healthier males because they are
better foragers. Once some females begin to prefer faster call rate, the alleles
determining that preference will become associated with the alleles for
better foraging. Natural selection will cause an increase in better foragers,
and the preference for faster call rate evolves as a correlated response.
All good-genes models, and especially the handicap principle, have been
controversial and difficult to support empirically. Only recently have there
been data to show that female preference for male signals influences the
survivorship of their offspring. Most of these studies involve visual signals
(reviewed in Ryan 1997), but data involving long-distance acoustic signals
have recently become available. For example, molecular paternity analysis
has shown that when female great reed warblers seek extra-pair copulations, they do so from males having larger song repertoires. Hasselquist et
al. (1996) speculate that the female pairs with a male with superior territories, thus ensuring the resources necessary for immediate reproductive
success, but seeks extra-pair copulations from males that have “good
genes”; song repertoire size is correlated with survivorship.
One of the best studies comes from anuran communication and is similar
to the hypothetical example given above. Gray tree frogs, Hyla versicolor,
produce a pulse call that can vary among males in pulse rate and pulse duration. Males can increase the energy content of the call by increasing either
call rate or duration; the former is an energetically more expensive option
for the males. Klump and Gerhardt (1987) showed that when given a choice
between a pair of calls varying in rate and duration but similar in overall
energy content, females preferred longer calls. They speculated that this
energy-independent preference might be indicative of selection for good
genes.This hypothesis was supported recently by Welch et al. (1998). Female
gray tree frogs were mated to two males, one that produced short calls and
one that produced long calls; these crosses resulted in sets of maternal
half-sibs. Tadpoles were raised through metamorphosis, and a number of
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M.J. Ryan and N.M. Kime
suggested that plumage brightness and song complexity in birds indicate
parasite load; parasites will directly influence plumage color and, it is
assumed, the energetic potential to make complex songs. If there is a genetic
basis to parasite resistance, then these signals are honest indicators of some
genetic quality. An alternative means for enforcing signal honesty is the
handicap principle (Zahavi and Zahavi 1997). This hypothesis suggests that
males evolve signals that are costly in terms of survivorship; thus, only truly
healthy males can afford the handicapping signal.
Early population-genetic models of the handicap principle did not
support its internal logic (reviewed in Zahavi and Zahavi 1997). Later
models, however, showed that the handicap principle could work through
linkage disequilibrium. In this case, however, the preference genes become
correlated with the “good genes” for survivorship that are being signaled.
For example, let us assume faster call rate, which will be energetically more
expensive than slower call rate, indicates healthier males because they are
better foragers. Once some females begin to prefer faster call rate, the alleles
determining that preference will become associated with the alleles for
better foraging. Natural selection will cause an increase in better foragers,
and the preference for faster call rate evolves as a correlated response.
All good-genes models, and especially the handicap principle, have been
controversial and difficult to support empirically. Only recently have there
been data to show that female preference for male signals influences the
survivorship of their offspring. Most of these studies involve visual signals
(reviewed in Ryan 1997), but data involving long-distance acoustic signals
have recently become available. For example, molecular paternity analysis
has shown that when female great reed warblers seek extra-pair copulations, they do so from males having larger song repertoires. Hasselquist et
al. (1996) speculate that the female pairs with a male with superior territories, thus ensuring the resources necessary for immediate reproductive
success, but seeks extra-pair copulations from males that have “good
genes”; song repertoire size is correlated with survivorship.
One of the best studies comes from anuran communication and is similar
to the hypothetical example given above. Gray tree frogs, Hyla versicolor,
produce a pulse call that can vary among males in pulse rate and pulse duration. Males can increase the energy content of the call by increasing either
call rate or duration; the former is an energetically more expensive option
for the males. Klump and Gerhardt (1987) showed that when given a choice
between a pair of calls varying in rate and duration but similar in overall
energy content, females preferred longer calls. They speculated that this
energy-independent preference might be indicative of selection for good
genes.This hypothesis was supported recently by Welch et al. (1998). Female
gray tree frogs were mated to two males, one that produced short calls and
one that produced long calls; these crosses resulted in sets of maternal
half-sibs. Tadpoles were raised through metamorphosis, and a number of
254
M.J. Ryan and N.M. Kime