Behavioral Ecology Vol. 10 No. 2: 209-212
© 1999 International Society for Behavioral Ecology
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The overlooked signaling component of nonsignaling behavior
a Department of Zoology, Faculty of Life Sciences, Tel-Aviv University, Tel-Aviv 69978, Israel b Department of Biology, York University, North York, Ontario M3J 1P3, Canada c Konrad Lorenz Institute for Comparative Ethology, 1a Savoyenstrasse, A-1160 Vienna, Austria
Received 24 March 1998; revised 22 July 1998; accepted 13 August 1998.
The handicap principle (Zahavi,
1975
, 1987;
Zahavi and Zahavi, 1997) is
now widely used to explain the evolution of conspicuous signals such as tail
ornaments, courtship displays, and nestling begging
(Godfray, 1991;
Grafen, 1990a,
b;
Johnston, 1997;
Maynard Smith and Harper,
1995). The essence of the model is that signals must be costly to
be honest. Females have evolved preferences for males with longer tails or
brighter plumage, for example, because only males of high quality can survive
and perform with handicapping ornaments. Despite the general acceptance that
the handicap principle explains extravagant morphological and behavioral
signals, the model's mechanism has not been broadly applied to explain a host
of other behaviors. Here we suggest that the selection on animal behavior to
be performed differently when observed by other animals can lead to
significant quantitative changes in behavior. Although such changes in the
level or intensity of a behavior may not justify calling the behavior a
signal, they can evolve as signaling components to behaviors whose primary
function is not signaling (i.e., they can shift the level of the behavior from
its nonsignaling optimum). We call this idea the overlooked signaling
component of behavior. We explore this issue using three examples: (1) prey
fleeing a predator; (2) human behavior in the presence of others; and (3)
parental care behavior. We then apply the overlooked signaling component to
reexamine Zahavi's (1977,
1995) suggestion that altruism
is a signal of social prestige. Whereas Zahavi presents his "prestige
hypothesis" as an alternative to kin selection, we show how both
theories can work together. We suggest that helping behavior among kin, which
increases inclusive fitness, may also eventually evolve into signals of
individual quality, condition or need. We conclude by suggesting ways to test
for signaling components of animal behaviors.
Speed of prey fleeing a predator
An animal fleeing from a predator may use conspicuous pursuit deterrent
signals. Stotting behavior in Thomson's gazelles Gazella thomsomi
(Fitzgibbon and Fanshaw, 1988)
and flight song in skylarks Alauda arvensis
(Cresswell, 1994) are examples
of behaviors used by prey animals to signal predators that they are in
sufficiently good condition to avoid capture (see
Hasson, 1991, for a review).
Although the prey's running behavior itself is not considered a signal
(Maynard Smith and Harper,
1995), running speed can provide information to the predator about
capture probabilities. Speed may thus play a role in predator-prey
communication. Animals fleeing from predators probably adjust their running
speeds according to several factors, such as their ability to sustain speed
for the expected length of pursuit, the predator's speed, and their need to
conserve energy. Because individuals vary in quality, and thus in the cost
they incur by running, the speed at which they run should differ among
individuals. If predators can assess capture probabilities by comparing the
running speeds of different potential prey and use running speed to decide
whether to begin, continue, or cease their pursuit, then the prey's optimal
running speed may be selected to shift upward. Prey animals will benefit by
running faster than is necessary to escape. This extra investment in running
speed is what we call the signaling component of running.
Note that we do not claim that prey running speed is necessarily correlated
with capture probabilities in all predator-prey systems. Nevertheless, in
cases where such correlations do exist, and predators therefore benefit from
selecting slow runners, a signaling component of running is expected to
evolve. Hasson (1994) and
Maynard Smith and Harper
(1995) considered this
predator-prey example and predicted a change in the prey running speed to
result from the predator's attention to the prey speed. They used this example
to illustrate the difficulties in defining biological signals. According to
Hasson's (1994) definition,
the prey's increased speed is a signal because the added cost of running
faster is not balanced by improving running efficiency, but only by altering
the behavior of the predators (see also
Hasson, 1997, for a
mathematical definition). According to Maynard Smith and Harper, on the other
hand, the change in prey running speed cannot be viewed as a signal because it
has no characteristics that have evolved specifically to alter the predator's
behavior. They explain, for example, that although a trait such as body size
could have changed as a result of its role as a source of information, only
structures that emphasize size, such as manes and ruffs, can be viewed as
signals (Maynard Smith and Harper,
1995). Accordingly, stotting behavior in gazelles that emphasize
running ability is a signal, but the extra running speed discussed here is
not. Hence, by making signal definitions more specific, cases like the change
in prey running speed were left out. We suggest that in these cases the
concept of signaling components may be useful.
Many models of signal evolution assume that the first step toward a signal
is a trait or behavior that was not a signal initially
(Krebs and 0Dawkins, 1984;
Michod and Hasson, 1990;
Rodriguez-Gironés,
1996;
Rodriguez-Gironés
et al., 1996; Zahavi,
1987). Our novel point is that although many traits or behaviors
may never evolve into full-blown signals, they may nonetheless be shaped by a
subtle signaling component. In the example of predator-prey pursuits, the
signaling component may simply cause running speed to change, but the act of
running does not change.
Signaling components of human behavior: performing slightly better in the presence of others
Humans commonly modify their performance of everyday activities if observed by others (or merely suspect they are observed). The amount that we alter our performance when being watched defines the signaling component of our behavior. For example, a young man who jogs daily may "optimize" his running speed according to several factors such as his ability to sustain a given speed, the risk of straining a muscle, and his motivation to improve. When he passes a group of young women, however, he might increase his running speed, improve his posture and attempt to conceal his fatigue. Although we would not claim that the man's motivation for running was to signal to the women (i.e., that jogging is a signal), it is apparent that the women can affect the runner's speed and behavior. It is hard to tell whether such behavior still contributes to male fitness in modern society or simply reflects its evolutionary heritage. However, the logic is basically the same as in the predator-prey example: if the speed or mode of running is correlated with certain male qualities that women use for selecting potential mates (such as health or body condition), the women should use running as a source of information. When they do, the man may benefit from changing his jogging speed or behavior, thus advertising his quality and increasing his sexual attractiveness.
Humans may use their well-developed cognitive skills and self-awareness to produce signaling components. The phenomenon, however, is simple, and its evolution does not require cognitive skills. Selection can simply operate on variations in the tendency of animals to perform slightly better when they are observed. We present this human example to illustrate the ease with which one can overlook the signaling component of many common behaviors. The difficulties in detection arise because the signaling component primarily changes the magnitude of the behavior rather than its nature. However, considering the prevalence of the phenomenon in humans and its simple evolutionary mechanism, it is reasonable to expect signaling components to evolve in many aspects of behavior.
Sexually selected signaling components of parental care
The signaling component idea is especially relevant to studies that link
male parental care and sexual selection. In many species, males were
originally selected to perform parental chores such as nest building and
offspring feeding, and a signaling component to these behaviors could have
evolved subsequently. For example, courtship feeding by male birds can
increase the female's clutch size (Nisbet,
1973, 1977),
leading to higher fitness. But if females choose males based on their parental
ability, sexual selection may favor males that can procure food at extravagant
rates. Reyer (1980,
1986) implicitly assumed a
signaling component to parental care when he suggested that male pied
kingfishers (Ceryle rudis) become helpers in order to impress
unrelated females with their parental ability. Evans and Burn
(1996) have shown that in the
wren (Troglodytes troglodytes), the number of nests that males build
in their territories is correlated with the number of females they attract and
suggested that extra investment in nest building advertises the male's quality
(although, as we note below, alternative interpretations exist). In all these
examples, the behavior did not evolve changes in their original function, but
the optimal level of the males' performance apparently shifted as a result of
its signaling effect.
In many monogamous bird species, certain males have low or even no
paternity (Birkhead and Møller,
1992), yet often feed offspring at the same rates as males with
complete paternity. Numerous reasons have been proposed to explain the lack of
male response to lowered paternity, including the idea that a signaling
component exists in male parental performance. Males that reduce their effort
and allow offspring to starve in view of their mates and neighbors may suffer
lower mating success in the future
(Wagner, 1992;
Wagner et al., 1996). This is
an extension of Zahavi's idea (Carlisle and
Zahavi, 1986; Zahavi,
1977, 1995) that
individuals help others in cooperative groups in order to increase their
prestige and thereby their direct fitness. Evidence consistent with the
prestige hypothesis in a monogamous species was found in savannah sparrows
Passerculus sandwichensis, in which males achieved paternity in the
second brood in proportion to the amount they provisioned in the first brood,
suggesting that females preferentially allowed fertilizations from their mates
when they performed better as parents
(Freeman-Gallant, 1997). Thus,
it is possible that a signaling component of chickfeeding behavior has
evolved.
Extra investment in helping: reconciling kin selection and social prestige
Zahavi (1977,
1987,
1995) proposes that seemingly
altruistic acts are actually costly signals of quality (i.e., handicaps) by
which the performer gains social prestige. By advertising its quality to group
members through the performance of costly helping behaviors, a helper might
gain direct benefits (such as mate acquisition). This idea is not widely
accepted as one of the major explanations of apparent altruism
(Emlen, 1991;
Pusey and Packer, 1997). A
difficulty that many behavioral ecologists might have with the social prestige
hypothesis is that Zahavi presents it as an alternative to kin selection, a
theory that he rejects but that most behavioral ecologists accept. We suggest
that kin selection is not inconsistent with Zahavi's prestige hypothesis and
that the two models may often operate in tandem. Moreover, we suggest that the
evolution of signaling components in kin-selected helping behaviors is
actually expected by optimization reasoning.
Let us take for example a group of cooperatively breeding birds that are related to each other and in which helping has evolved via indirect benefits (i.e., kin selection). The level of helping performed by three helpers that are equally related to the breeding pair can be derived from Hamilton's rule; i.e., at any particular moment, helpers help when r(b) > c, where r = the coefficient of relatedness, b = the benefit of helping, and c = the cost of helping. Because r is equal for the three helpers, they are expected to help at the same level (or as frequently) as long as c and b are also equal. However, whereas the benefit of helping is likely to be the same in this case (because all three helpers help the same breeding pair), the cost of helping is likely to vary among the three helpers (because the performance of a certain act of helping should be easier for high-quality helpers). Individual differences in quality, therefore, should enable some helpers to help more than others. Considering this variation in the cost of helping, the optimal level of helping according to Hamilton's rule will actually differ among the three helpers and will be positively correlated with their quality (the term "quality" can be used for both genotypic or phenotypic quality, or even for phenotypic condition at the moment the help is given). Hence, a situation in which the level of help is correlated with helper quality may be common. This does not imply that the level of helping is already affected by a signaling component, but under such circumstances it has the potential to become affected. If other group members begin to use the level of helping to assess the quality of the helper and adjust their behavior toward that helper accordingly, then selection should favor the modification of the level of helping according to its value as a signal.
Why should individuals use the level of helping by other group members as a
source of information? The answer is that group members are not only
cooperative partners, they often are also competitors or potential mates.
Having information about each other's quality would allow them to make better
decisions regarding their competitive and sexual interactions within the
group. Take for example two male group members who cooperatively defend a
territory. By so doing, they can also appraise each other's fighting ability
without engaging in costly fights with one another. Thus, information gathered
in intergroup conflicts may help to settle intragroup conflicts at a lower
cost. Considering that social animals frequently inspect each others'
activities (Pusey and Packer,
1997) and that helping behavior such as feeding nestlings or
defending a territory can easily be observed by other group members (e.g.,
Heinsohn and Packer, 1995;
Reyer, 1986;
Zahavi, 1990), it is
reasonable to expect that a mutant that uses helping behavior to assess an
individual's quality or condition would have a selective advantage. We predict
that when the level of helping provides visible and reliable information about
individual quality, animals will eventually use it, and when they do, the
level of helping will shift into a new equilibrium that is modified by a
signaling component. In other words, it will become adaptive to help at higher
levels than would be predicted by Hamilton's rule because helpers also benefit
directly by advertising their quality to other group members. At equilibrium,
even poor-quality individuals may help slightly more than predicted by
Hamilton's rule in order to advertise that they are still above the lowest
possible quality. In summary, the evolution of a signaling component of
helping behavior can be favored in a system in which helping initially evolved
via kin selection.
A complementary argument is that, whereas all social animals need some
information about the quality of their group members to make decisions about
competitive and sexual interactions, cooperative animals additionally need
this information to optimize their level of cooperation. When helping is
maintained by kin selection, the relative quality of the recipient can
determine how much help should be given because the quality of this recipient
has a direct effect on the benefit parameter "b" in
Hamilton's rule. Consider a group of related individuals cooperating in
territorial defense or in mobbing a predator. An individual will gain greater
indirect benefits by helping a brother of high quality, who is likely to
produce many viable offspring, than by helping a brother of lower quality
(assuming that both brothers benefit equally from receiving help). Hence, when
r and c are equal, donors need information about the quality
of prospective recipients in order to determine b. The same logic has
been applied in the context of parental investment in offspring that vary in
quality (Godfray, 1995;
Haig, 1990;
O'Connor, 1978). Thus, just as
parents choose which offspring to feed, group members must choose which
relative to help. Under these circumstances, group members may benefit from
advertising their quality by performing predominately nonsignaling behaviors
(such as territorial defense or feeding offspring) at exaggerated levels to
prove they are worthy of receiving help.
The evolution of a signaling component of helping behavior can also be
favored when unrelated individuals cooperate for direct benefits (e.g.,
reciprocity, territory inheritance, or parental experience). Regardless of
relatedness, the optimal level of helping should vary among individuals of
different quality because a given level of helping is cheaper for high-quality
individuals. Hence, high-quality individuals can afford to help more. Again,
the level of helping has the potential to be a source of information about an
individual's quality, and if used as such, will eventually be modified by a
signaling component (see also Roberts,
1998, for a related discussion on the evolution of handicap-based
altruism from reciprocity). In short, the evolution of a signaling component
of helping behavior can be favored in systems in which helping initially
evolved for either direct or indirect benefits.
Signaling components may also provide information about need
Throughout this paper we have suggested that signaling components can
provide information about the quality of the individual performing a certain
behavior. This idea can be extended to the signaling of need. Costly signals
of need have been suggested to evolve when parents seek information about the
food requirements of their offspring
(Godfray, 1991), or when
individuals must assess the amount of help their close kin require
(Maynard Smith, 1991). In this
context, some traits or behaviors may not evolve into signals of need (like
nestling begging), yet may evolve signaling components. A model by
Rodriguez-Gironés
(1996) has shown that sibling
aggression can evolve a signaling role and shift from its nonsignaling optimum
into a new higher level. Initially, the aggressive behavior evolved as direct
competition for food, with large chicks often killing their smaller siblings,
resulting in some level of parent-offspring conflict. However, the model
illustrates that the parents' best response to such aggression is to provide
more food to the aggressor to prevent siblicide. As a result, large siblings
were selected to exaggerate aggression, thus blackmailing their parents to
give them more food. Hence, although we do not in general consider sibling
aggression as a signal to the parents, the model suggests that a signaling
component of chick need can greatly affect the larger sibling's level of
aggression. In a similar manner, signaling components of need may also evolve
in helping behavior. If helpers adjust their effort in relation to their need
to participate in helping (i.e., in relation to the expected benefit a helper
gains from helping), variations in the level of help may evolve to signal the
helper's need or motivation to help, rather than to signal its individual
quality. To date, most models treat signaling of quality and signaling of need
separately, even though a combined effect of a signaler's need and quality may
be inevitable in some cases. The possibility that a signal, or a signaling
component, will reflect the product of both is yet to be explored.
Testing for signaling components of animal behavior
Some evidence supports the idea that there is a signaling component of
parental care or helping behavior. However, the evidence is indirect and
subject to alternative interpretations. For example, a correlation between
feeding rates and mating success
(Freeman-Gallant, 1997), might
be explained by confounding variables, such as male age or phenotypic
condition (Freeman-Gallant,
1997; Wright, 1998). Similarly, apparent competition for helping
opportunities, which was suggested as evidence that helpers compete for
signaling benefits (Carlisle and Zahavi,
1986), has been recently interpreted to be a result of a high
density of helpers around the nest
(Wright, 1997). Experimental
manipulation of individual quality (e.g., by providing extra food or by
handicapping physical performance) can test the extent to which a behavior is
correlated with quality, but it cannot determine whether other individuals use
it as a source of information. It will be more convincing if manipulating the
presence or size of an audience will cause animals to alter their level of
behavior. It might be difficult, however, to manipulate the size of the
audience without affecting the need for help or the cost of helping. For
example, mobbing a predator may become less dangerous as the number of group
members increases.
The best and perhaps only way to test for the existence of signaling
components in animal behavior is by experimentally manipulating the behavior
itself. However, because signaling components may affect a trait or a behavior
only in a quantitative way, a rigorous test requires several stages. First,
one has to manipulate the level or intensity of the behavior and to show that
other individuals respond to the change in the behavior (i.e., that they use
the behavior as a source of information). This type of experimental
manipulation has been applied successfully to illustrate that long tail
ornaments of males attract females
(Andersson, 1982;
Møller, 1988). The
second and more difficult stage is showing quantitatively that the observed
level of performance is indeed influenced by a signaling effect (i.e., that it
is influenced by the fact that other individuals use the behavior as a source
of information). This stage be followed by a detailed measurement of the
behavior's costs and benefits to test whether (1) the level or intensity of
the behavior is considerably higher than could be explained by the primary
function of the behavior (i.e., than could be explained without the existence
of a signaling component), and (2) the level of exaggeration in the behavior
is related to quality (or need), as required by a handicap mechanism. This
type of experiment has been used to in some degree to study sexually selected
signals. Other studies that experimentally manipulated tail ornaments were
able to quantify the costs and benefits of a signal in relation to an
individual's quality (Evans and Hatchwell,
1992; Evans and Thomas,
1992; Møller,
1989). The main challenge is to find practical ways to manipulate
behaviors in the way we manipulate morphological traits.
Unfortunately, it is difficult to manipulate behaviors to demonstrate their hypothetical signaling effects. We need to find ways to alter the behavior of some individuals without affecting their other traits. Much originality and effort is required. However, we suspect that the reason such tests have rarely been attempted is not because they are impractical but because few researchers believe that the role of signaling components of predominately nonsignaling behaviors is worth testing. Our main motivation in writing this paper is to convince them that it is.
ACKNOWLEDGEMENTS
We thank Oren Hasson and an anonymous reviewer for constructive comments and suggestions and Noam Leader, Trevor Pitcher, Miguel Rodriguez-Gironés, Michael Taborsky, Noam Werner, David Winkler, Jon Wright, and Amotz Zahavi for their very helpful comments and discussions. This paper was inspired by projects on cooperatively breeding cichlids and on communication between bird nestlings and their parents, supported by the Israel Academy of Science and Humanities, and by the U.S.-Israel Bi-National fund.
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