Indicators: Their Utility in Male Trait Evolution
Byron Kho
Evolution of male traits is thought to have occurred in one of two ways: by malemale competition or by intersexual selection – female choice, through the use of
ornaments. However, unlike the easily realized function of weapon-related traits in male
competition, the function of courtship-related traits has been historically harder to
decipher. These traits tend to be deleterious for male fitness and theories attempting to
explain this puzzling limitation generally fall under the runaway hypothesis or the “good
genes” hypothesis. The runaway hypothesis supports a co-evolution of female preference
and male traits (Fisher 1930, Arnold 1983), while the “good genes” or indicator
hypothesis supports the position of the heritable male trait as a reliable indicator of
genetic quality, thus tilting the direction of selection in its direction (Madsen et al. 1992,
Krebs and Davies 1993).
The indicator model tends to be more easily accepted as an explanation for
ornamentation, especially if mate choice is costly – if that is true, the runaway model is
usually inadequate (Pomiankowski 1988, Iwasa et al. 1991). To hold, the indicator
model must meet at least four conditions: that the trait is believed to be an honest
indicator of robustness and vitality in the male; that it contains genetic variability and the
possibility of additive genetic variance in the future; that it provides direct benefits to
females or indirect benefits through heritability to offspring; and that it be correlated with
female preference and mate choice.
The preliminary indicator model was outlined by Amotz Zahavi, who suggested
that exaggerated male traits might be preferred by females because they were handicaps
(Zahavi 1975, 1977). Though his primary example was the long tail of the peacock,
many other examples in nature – the “stotting” behavior of gazelles, the bugle-like
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mating calls of bull elks, breeding coloration in guppies – illustrate behavior that is
attention-creating to predators as well as potential mates, and are thus extremely costly
(Houde 1987, Petrie 1994). The male’s ability to survive even with the handicap should
then be a reliable indicator of robustness: “an individual with a well developed sexually
selected character is an individual which has survived a test… females which selected
males with the most developed characters can be sure that they have selected from among
the best genotypes of the male population” (Zahavi 1975). The elaborateness of the
character was thought to indicate a high heritability and viability, culminating in the label
“good genes.” The costly nature of the character would serve as a reasonable
justification of the genetic quality of the creature.
One problem did exist with his formulation, as Zahavi did not make it clear why
this “test” should be so eminently believable. To correct this oversight, Grafen instead
viewed the process as a communications game with many possible equilibrium strategies
(Grafen 1990). The handicap was not merely a costly signal with vague limitations, but
one in which signalers could vary the size of the handicap, taking into account the risks
and benefits associated with receiver responses. This was known as the “strategic
choice” handicap. Other specifically described handicaps include the survival handicap,
described above (Grafen 1990, Michod and Hasson 1990, Iwasa et al. 1991); the
amplifier handicap, in which signalers expend effort in easing the ability of signalreceivers to judge their quality; and condition-dependent handicaps, in which the
exaggerated trait is one that only a few signalers are capable of producing, as the
physiological requirements or time constraints don’t allow everyone to develop the
signal. The usage of such strategies allows for the possibility of falsification of
indicators, as it is assumed that males are aware at some level of female requirements.
However, faking can become impractical when the female tests the veracity of individual
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claims around a large group of males; if a challenge turns up a false positive, selection
can proceed by direct male-male competition (Iwasa et al. 1991). The equilibrium
strategy view also covers condition-dependent mechanisms which are evident when
smaller males resort to sneaking to obtain reproductive success – where otherwise female
choice would work against them (Sargent 1998).
The heritability of such a trait is important in sexual selection. Without passage
into following generations, the evolutionary process cannot work in favor of the trait and
thus it is extremely necessary. Zahavi argued that traits, acting as handicaps, would
reduce viability or all males would already have developed the trait (Zahavi 1975).
Though indicators need not necessarily be handicaps, the variation created by differing
levels of viability creates a constantly changing regime of selection pressures that will
prevent equilibrium. By doing so, the heritability in fitness will never be zero, as
predicted by Fisher’s fundamental theorem (Fisher 1930). Hamilton and Zuk proposed
an alternate version of the “good genes” hypothesis that described the situation as an
evolutionary arms race between hosts and parasites (Hamilton and Zuk 1982). Though
this model only fits a few species including guppies, swallows and pheasants (Andersson
1994), the interplay between the host and parasites creates a logical situation that both
prevents equilibrium and maintain additive genetic variance in fitness. With increased
parasite load, host fitness will decrease as will ornament condition. Selection favors less
parasitized males, who are more ornamented. By extension, heritable variation will be
passed in the form of resistance to parasites (Foldstad and Karter 1992). Still, the
mechanism for variation in heritability is not well understood in general circumstances.
In order to be swayed by selective pressures, traits must be beneficial to potential
mates during nesting as well as to potential offspring. Most valuable to a future family is
the ability to be a superior provider, a factor easily rated by the male’s ability to provide
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for himself. As most of the ornamentative traits are physiologically related, females need
only observe the quality level of the male’s condition-dependent ornamentation to rate his
ability (Houston and McNamara 1988, Mangel and Clark 1988). The direct link to
female survivorship and fecundity ensures a strong reason to accept or reject a mate,
depending on his performance. However, some species only require males to provide
sperm within the context of a relationship; they do not take up the “provider” role and
this reasoning is not entirely applicable. In this case, the ability to survive is only rated as
an indirect benefit that will affect the offspring but not necessarily the parent. While the
heritability factor usually ensures good results in the next generation, the exaggerated
male traits can sometimes lower the fitness of male offspring rather than increasing it.
The mothers of sons who have high fitness can gain: by the sexy son hypothesis, they do
gain indirectly in terms of reproductive success (Arnold 1985).
Finally, the presence of indicators must be associated with female preference. As
the display of the trait is supposed to reflect the honest condition of host genes, its
evolution can be directly correlated with the evolution of female preference. In fact,
there is much more evidence that female preference evolves when indicator mechanisms
provide a direct benefit to the female rather than an indirect benefit. Using strategies
within the so-called “communications game” (Grafen 1990), males provide females with
distinct displays that can only be interpreted as honest because they are either 1) direct
assessments of quality, 2) too costly to produce and reliable for that reason, and 3) can be
used in other contexts which cannot be faked (Fisher 1915, 1930, Williams 1966, Zahavi
1975). The evolutionary preference for more exaggerated traits shows a general selection
trend for increasing fitness; female preference then evolves to follow this trend.
Following this circular logic, reproduction success can only be had if males can show
more exaggerated traits – at significant risk to itself (Hasson 1989, 1997, Folstad and
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Karter 1992, Price et al. 1993, Wolf et al. 1997). Darwin also recognized this fact in his
original formulation of the theory of sexual selection (Darwin 1874).
Though the general development of extensive ornamentation can be explained
using the indicator model, there are still weaknesses in all theories under its umbrella,
especially concerning mechanisms that promote genetic variation. The theory promotes
costly traits that honestly promote gene quality at the same time they add risk to a
creature’s survival; evolution only supports its development because the trait enhances
reproductive success. At this rate, it would seem that traits would develop to capacity
and all representatives of the species would show some level of the traits, but that is not
the case. Instead, physiological and time constraints like resource-handling limit the
possible development of the trait. As well, the various evolutionary strategies practiced
by species individuals allow user-defined displays depending on condition. These
constraints, along with the parallel evolution of parasite and predators, somehow
encourage additive genetic variance in fitness such that heritability never reaches zero. It
must also be noted that while the theory usually applies to male ornamentation, females
also practice costly signaling to advertise their own genetic quality. While certainly not
an all-encompassing theorem, the indicator model of inter-sexual selection provides a
sufficiently plausible explanation for the development of ornamentation in nature.
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