Perspectives on Animal Behavior

432 Chapter 19 / Group Living, Altruism, and Cooperation

together. Unrelated larvae that happen to share an allele may recall from Chapter 18 that evolutionary game
are just as likely to settle together as are siblings that theory is designed to handle situations such as this, in
share an allele (Grosberg and Quinn 1986). MHC has which the best course of action depends on what others
been reported to play a role in kin recognition in a vari- are doing.
ety of other taxa, including amphibians (Villinger and
Waldman 2008) and mammals, including humans The name of the game comes from an imaginary
(reviewed in Johnston 2003). Most effects of MHC- story in which two suspects are arrested for a crime and
based recognition have been found in the context of kept in separate jail cells to prevent them from commu-
mate choice and incest avoidance. To date there is no evi- nicating. Certain that one of them is guilty, but lacking
dence that MHC genes influence the perception of odor, sufficient evidence for a conviction, the prosecutor offers
which is necessary for MHC to be a “recognition allele” each a deal. Each prisoner is told that there is enough
under our strict definition above (Mateo 2004). incriminating evidence to guarantee a short jail term, but
Nonetheless, the MHC system remains an interesting freedom can be obtained by providing enough evidence
case of a close link between genes and kin recognition. to send the other to jail for a long time. However, if each
informs on the other, they both go to jail for an inter-
RECIPROCAL ALTRUISM mediate length of time. We can construct a payoff matrix
(Table 19.1), just as we did for hawk–dove games of con-
As we have seen, helping relatives is favored by natural flict in Chapter 18. The possible strategies available to
selection when the inclusive fitness of the helper is each player are to cooperate (don’t squeal on your part-
increased. However, in everyday speech, we typically ner) or to defect (squeal). The best that you can do is to
use the word “altruist” not to describe a person help- defect while your partner cooperates (getting a payoff of
ing a relative, but a person helping a nonrelative. Can T, which stands for the temptation to defect). If both you
altruism toward nonrelatives be favored by natural and your partner cooperate, the payoff is R (for reward
selection? for cooperation). If both partners defect, the payoff is P
(for punishment for defection). If you cooperate and
The answer is yes, but only under a narrow set of your partner defects, you get the lowest possible payoff,
circumstances. Altruism between nonrelatives can S (for sucker’s payoff). For a game to be a Prisoner’s
evolve if there is an opportunity for payback in the Dilemma, the payoffs in the four cells illustrated in Table
future. We call this reciprocal altruism, evolution’s 19.1 must be in the order T > R > P > S.
version of “you scratch my back and I’ll scratch yours”
(Trivers 1971). In order to determine the best strategy, examine the
payoff matrix. If you are Player A, what is your best strat-
In order to think about the circumstances that egy if your opponent cooperates? Because T > R, it is bet-
might favor reciprocal altruism, it’s helpful to follow the ter to defect—you will go free. Similarly, if your
lead of many other behaviorists and think about a opponent squeals, compare the payoffs of your two
particular scenario: the Prisoner’s Dilemma. In recip- options. Because P > S, it is again better to defect, rather
rocal altruism, the costs and benefits to the altruist than taking the rap for both of you. Therefore, in a sin-
depend on whether the recipient returns the favor. You gle round of playing the game, it is always better to

TABLE 19.1 Fitness Payoffs for Player A in the Prisoner’s Dilemma. The payoffs are ordered T > R > P > S

Strategy of Player B

Cooperate Defect

Strategy of Player A Cooperate R S
Defect Reward for mutual Sucker’s payoff

cooperation P
Punishment for mutual
T
Temptation to defect defection

The Puzzle of Altruism 433

defect. If both players follow this logic, they will both Vampire bats meet the conditions that Trivers laid
defect and will each do worse than if they cooperated. out that are favorable to the evolution of reciprocal altru-
ism. First, the benefit to the recipient of the blood gift
If we translate jail sentences into fitness payoffs, the is greater than the cost to the donor. Since a bat’s body
solution to the Prisoner’s Dilemma seems to imply that weight decays exponentially after a meal, the recipient
reciprocal altruism cannot evolve. Indeed, this may be may gain 12 hours of life and, therefore, another chance
true if the prisoners will never meet again. In real life, to find food. However, the donor loses fewer than 12 hours
however, individuals often interact repeatedly, and when of time until starvation and usually has about 36 hours,
they do, reciprocal altruism may evolve. another two nights of hunting, before it would starve.

One strategy, called “tit-for-tat,” can be a winner in a
repeated games of Prisoner’s Dilemma. In this strategy,
an individual begins by being cooperative and in all sub- b
sequent interactions matches the other party’s previous
action. This strategy, then, has the characteristics of c
being “nice” (it begins with cooperation), it is retaliatory
(if the partner defects, it defects in return), and forgiv- FIGURE 19.9 A vampire bat that was unsuccessful in
ing (it immediately “forgets” a defection and cooperates obtaining a meal during a night’s hunt begs for food
if the partner later cooperates). If a population of indi- from a roostmate. (a) First it grooms the roostmate by
viduals adopts this strategy, it cannot be overrun by a licking it under the wings, (b) then it licks it on the lips.
selfish mutant that always defects (Axelrod 1984). So, (c) If receptive, a well-fed roostmate will respond by
when the individuals have repeated encounters, recipro- regurgitating blood to the hungry partner. (From
cal altruism can be an evolutionarily stable strategy Wilkinson 1990.)
(ESS), one that cannot be invaded by another strategy
(see Chapter 4).

Given these results from game theory, let’s step back
and think more generally about when reciprocal altru-
ism is likely to evolve. Trivers (1971) outlined several
conditions that favor reciprocal altruism: (1) the benefit
of the act to the recipient is greater than the cost to the
actor, (2) the opportunity for repayment is likely to
occur, and (3) the altruist and the recipient are able to
recognize each other. These factors are most likely to
occur in a highly social species with a good memory, long
life span, and low dispersal rate (Trivers 1971).

One of the best-known examples of reciprocal altru-
ism among nonhuman animals, partly because it is such
a startling species in which to find this trait, is vampire
bats (Desmodus rotundus). Vampire bats fly out at night
to find their favorite prey, large mammals such as cattle
or unsuspecting tropical biologists. The bats land near
the sleeping victim and then skitter silently toward it
along the ground. They then climb aboard and bite the
prey with razor-sharp teeth specialized for slicing
through skin, lapping up the blood. Anticoagulants in
the bats’ saliva keep the blood flowing. Successful bats
can have giant meals—they can consume up to 50% of
their body mass.

At the end of the night, vampire bats return to their
communal roosts. Here is where altruistic acts take place:
an unlucky bat that did not obtain a blood meal begs for
food by licking one of its roostmates under the wings and
on its lips. A receptive donor will then regurgitate blood
(Figure 19.9). The regurgitated food is enough to sus-
tain the hungry bat until the next night, when it may find
its own meal. Donors may give blood to recipients that
are not related to them (DeNault and McFarlane 1995;
Wilkinson 1984, 1990).

434 Chapter 19 / Group Living, Altruism, and Cooperation

Physiological studies of metabolism suggest that vampire and offspring are not genetically identical, their interests
bats are unusually susceptible to the effects of starvation are not always perfectly aligned. Parents have an advan-
(Freitas et al. 2003, 2005). tage in power struggles, as they are generally larger and
more experienced than their offspring. Because offspring
Second, bats are likely to have the opportunity to are related to their parents, their motivation to resist
repay favors and to get favors repaid. Most bats are likely coercion is reduced—if, for example, they forgo their
to be in the position of needing blood from roostmates, own breeding in order to help their parents reproduce,
because on any given night, roughly 33% of the juveniles they at least gain indirect fitness.
that are less than two years old and 7% of older bats fail
to feed. Bats are also likely to encounter the same individ- EXAMPLES OF COOPERATION
uals time and again. Vampire bats roost in somewhat sta- AMONG ANIMALS
ble groups of both related and unrelated members. A
typical group consists of 8 to 12 adult females and their As we consider various forms of cooperation among ani-
pups, a dominant male, and perhaps a few subordinate mals, we will note many similarities among distantly
males. Males leave their mothers when they are about 12 related groups. We will also notice that the selective
to 18 months old, but females usually remain well past forces leading to similar forms of cooperation may be
reproductive maturity. New females occasionally join the quite different.
group. Although the groups may change slightly over time,
there are numerous opportunities to share food. Females ALARM CALLS
may live as long as 18 years, and in one study, two tagged
females shared the same roost for more than 12 years. Some of the classic long-term field studies of coopera-
tion come from studies of alarm calls—warnings that
Trivers’s third condition is that individuals that rec- animals give to alert others of danger. Let’s examine a
ognize each other can thus direct help appropriately. particularly well-studied taxon, ground squirrels and
Generally, only bats that have had a prior association share their relatives.
food. In an experiment, a group of bats was formed in the
laboratory. Aside from a grandmother and granddaugh- Belding’s Ground Squirrels
ters, all the bats were unrelated. The bats were fed nightly
from plastic measuring bottles so that the amount of blood High in the mountains of the Sierra Nevada in California,
consumed by each bat could be determined. Then, every in Tioga Pass in Yosemite National Park, lives a very
night one bat was chosen at random, removed from the well-studied population of Belding’s ground squirrels
cage, and deprived of food. When it was reunited with its (Spermophilus beldingi). During most of the year, the alpine
cagemates the following morning, the hungry bat would meadows are covered in deep snow, but in the short sum-
beg for food. In almost every instance, blood was shared mer season, the meadows are awash in flowers and grasses.
by a bat that came from the starving bat’s population in It is then that the ground squirrels become active, forag-
nature. Furthermore, there seemed to be pairs of unre- ing in the fields during the day and returning to under-
lated bats that regurgitated almost exclusively to each ground burrows to sleep and care for their offspring.
other, suggesting a system of reciprocal exchange.
It’s not only ground squirrels that call these lush
If Trivers’s three characteristics of species likely to meadows home. Squirrels are attacked both from the
show reciprocal altruism bring our own species to mind, ground (badgers, snakes, weasels, coyotes) and the air
it is not surprising. Robert Trivers (1971) points out that (hawks and eagles). When squirrels spot a predator, they
reciprocal altruism is particularly common among humans. give an alarm call—a series of short sounds for a terres-
Not only do humans help the needy through social pro- trial predator, and a high-pitched whistle for an aerial
grams (with the expectation that they, too, might someday predator (Figure 19.10).
benefit from such a program), but they also help one
another in times of danger and they share food, tools, and Paul Sherman (1977; 1980a,b; 1985) studied the
knowledge. Trivers even argues that our feelings of envy, function of these calls: are they directed at the predator
guilt, gratitude, and sympathy have evolved to affect our to let it know it has been detected? Or are they directed
ability to cheat, spot cheaters, or avoid being thought of at kin? The answers seem to differ depending on the
as a cheater ourselves. We’ll see more examples of recip- circumstances.
rocal altruism among our primate kin later in this chapter.
Individual Selection When a hawk is spotted over-
MANIPULATION head or when an alarm whistle is heard, near pandemo-
nium breaks out in the colony. Following the first
In some cases, animals can coerce others to help them. warning, others also whistle an alarm and all scurry to
This is especially likely to occur between parents and off- shelter. When a hawk is successful, the victim is most
spring (Alexander 1974, Trivers 1974; reviewed in
Crespi and Ragsdale 2000). Recall that because parents

Examples of Cooperation Among Animals 435

FIGURE 19.10 A female Belding’s ground squirrel emits seems that the alarm whistles given at the sight of a
an alarm call. predatory bird directly benefit the caller by increasing its
chances of escaping predation in the ensuing chaos
likely to be a noncaller. In one study, only 2% of the (Sherman 1985).
callers but 28% of the noncallers were caught (Table
19.2). The most frequent callers were those that were in Kin Selection In contrast, individual selection does
exposed positions and close to the hawk, regardless of not seem to be behind the evolution of the ground
their sex or relationship to those around them. Thus, it squirrels’ alarm trills, given in response to terrestrial
predators. In this case, the caller is truly assuming a risk;
we know this because significantly more callers than
noncallers are attacked. As can be seen in Table 19.2, 8%
of the ground squirrels that called in response to terres-
trial predators were captured, whereas only 4% of the
noncallers were caught. The predators, even coyotes
whose hunting success often relies on the element of sur-
prise, did not give up when an alarm call was sounded.
Furthermore, the caller was not manipulating its neigh-
bors to its own advantage. Generally, the reaction of
other ground squirrels was to sit up and look in the
direction of the predator or to run to a rock. Their reac-
tion did not create the chaos that might confuse a preda-
tor. Nor did the caller seek safety in the midst of
aggregating conspecifics (Sherman 1977).

The evidence that kin selection is the basis for alarm
trills to terrestrial predators by ground squirrels is
strengthened by information on the structure of their
society. Daughters tend to settle and breed near their
birthplace, so the females within any small area usually
are genetically related to one another. The sons, on the
other hand, set off independently before the first winter
hibernation, never to return to their natal burrow.
Sherman knew the relationships and the identity of the
squirrels (and could identify them from a distance
because he marked them by painting their flanks with
Lady Clairol hair dye).

TABLE 19.2 Alarm Calling and Survival in Belding’s Ground Squirrels at Tioga Pass, California. All Data

Are from Observations Made During Attacks by Hawks (n ‫ ؍‬58) and Predatory Mammals
(n ‫ ؍‬198) That Occurred Naturally During 1974–1982 (Data from Sherman 1985)

Number of Ground Squirrels

Aerial predators Captured Escaped % Captured P value
Callers <0.01
Noncallers 1 41 2% <0.05
Total 11 28 28%
Terrestrial predators 12 69 15%
Callers
Noncallers 12 141 8%
Total 6 143 4%
18 284 6%

436 Chapter 19 / Group Living, Altruism, and Cooperation

Whistles to aerial predators nonoffspring relatives does not significantly affect their
likelihood to call (Blumstein et al. 1997). Other rodent
C––a–t–e–g–o–ry– Expected to call Observed to call species (e.g., mice of the genus Peromyscus) apparently do
Adult females 80 60 40 20 0 20 40 60 80 not call at all. Shelley and Blumstein (2005) carried out
Adult males a comparative analysis (see Chapter 4 for more details on
this research technique) in which they plotted traits onto
1–year females a phylogenetic tree to see which traits were likely to have
1–year males evolved together. Social species were more likely to call
than nonsocial species. However, an even stronger rela-
Juvenile females tionship was that diurnal (day-active) rodent species were
Juvenile males more likely to call than nocturnal (night-active) species
and that the evolution of diurnality precedes the evolu-
(n = 210) tion of alarm calling. Shelley and Blumstein argue that,
G = 4.8, p > 0.50 in general across rodent species, alarm calling serves pri-
marily to communicate with predators and that benefits
Trills to terrestrial predators arising from kin selection are secondary. Belding’s
Expected to call Observed to call ground squirrels may benefit more from kin selection
80 60 40 20 0 20 40 60 80 than some other rodent species because they live in high-
density meadows where many relatives are likely to be
Adult females within earshot (Blumstein 2007).
Adult males
1–year females COOPERATION IN ACQUIRING A MATE
1–year males
Juvenile females Males of some species cooperate in attracting a mate.
Juvenile males Some even relinquish the opportunity to pass their
alleles into the future generation personally, at least tem-
(n = 127) porarily. Indeed, these males concentrate their efforts on
G = 73.5, p > 0.001 making another male more attractive to females. This
seems like a guaranteed route to lower fitness, but in
FIGURE 19.11 Expected and observed frequencies of some cases it can be advantageous. Let’s look at four
alarm calls by Belding’s ground squirrels in response to examples, two from birds and two from mammals. As
aerial and terrestrial predators. Expected frequencies you will see, sometimes the benefits to cooperators can
are those that would be predicted if the animals called arise via individual selection, kin selection, or reciprocal
randomly. The calls in response to aerial predators are altruism, and sometimes a combination.
close to the expected frequencies. However, the calls in
response to terrestrial predators are more likely to be Wild Turkeys
given by females with relatives nearby than would be
predicted if the animals called randomly. (From Strangely, most male wild turkeys (Meleagris gallopavo) in
Sherman 1985.) some Texas populations never mate. Toward the end of a
young male’s first autumn, when he is about six to seven
Sherman’s data (Figure 19.11) suggest that the months old, he and his brothers forsake the others in their
ground squirrels practice nepotism, or favoritism for family and form a sibling group that will be an inseparable
family members. Notice in the figure that when a ter- unit until death. This sibling group and all other juvenile
restrial predator appears, females are more likely than male sibling units in the area flock together for the winter.
males to sound an alarm. This is consistent with kinship
theory because it is females that are more likely to have Only the dominant male in each group mates. During
nearby relatives that would benefit from the warning. In the first winter, each male’s status within this fraternity is
addition, reproductive females are more likely than non- decided by the outcome of two contests. One competition
reproductive females to call. An even finer distinction is for dominance within the sibling group. Brothers battle
can be made: reproductive females with living relatives by wrestling, spurring, striking with their wings, and peck-
call more frequently than reproductive females with no ing at each other’s heads and necks. Endurance is the key
living family members. to success: the turkeys fight until they are exhausted. When
only one is able to do battle, however weakly, he is the win-
Alarm Calls in Other Rodents ner. The second contest is between rival sibling groups.
The groups challenge and fight one another until a dom-
Many rodent species, not only Belding’s ground squir- inance hierarchy is established. The sibling group with the
rels, give alarm calls, providing us with a powerful tool most members is usually victorious. Renegotiation of rank
for comparative analysis. Species vary in whether alarm
calling increases the caller’s own chance of survival, pri-
marily aids the caller’s own offspring, or helps other ani-
mals. For example, yellow-bellied marmots are most
likely to call when their own offspring are nearby, and
(unlike Belding’s ground squirrels) the presence of

Examples of Cooperation Among Animals 437

is rare; the dominance hierarchy within and between sib- every 15 minutes around the clock. Any of the males in
ling groups is stable. the coalition may be the first to find her, mate with her,
and keep others away by his presence. A female may
When the breeding season begins, females inter- change mates during this period but generally not more
ested in mating visit the open meadows, where the males than once a day (Bertram 1975, 1976).
congregate. Two to four siblings form display partner-
ships within larger aggregations of males. The brothers In turkeys, we saw that males helped their brothers
of each unit court the hens by strutting in unison, even gain mates. Could kin selection also underlie the forma-
though only the dominant male in the highest-ranking tion of coalitions in lions? Coalitions of more than three
sibling group will mate. Of 170 tagged males displaying individuals usually consist of close relatives that left their
at four grounds, not more than 6 males accounted for all natal pride as a group (Packer et al. 1991). They remain
59 observed matings. If a subordinate male is presump- together, and after one to three years of traveling
tuous enough to attempt a mating, the dominant male nomadically, they challenge the males of other prides.
chases him away and then mates with the hen. Thus, a male in a coalition with relatives has the chance
to gain reproductive success indirectly (by helping his
Watts and Stokes (1971) were the first to suggest that male relatives mate with the female).
kin selection is the major driving force behind the evo-
lution of this behavior, and this was confirmed recently Kin selection can’t be the entire story behind coop-
by genetic analysis (Krakauer 2005). A subordinate male erative groups of male lions, or even most of it. It is now
gains inclusive fitness by helping his brother to perpetu- known that roughly half of male coalitions contain at
ate his alleles. On the other hand, without his assistance, least one unrelated male, and coalitions of two or three
the brother could not be successful. The cooperative usually consist of unrelated males (Packer 1986; Packer
efforts of siblings are necessary for their unit to become et al. 1991; Packer and Pusey 1982). When presented
dominant, and the synchronous strutting of siblings with a stuffed “intruder” lion accompanied by playback
makes the dominant male more attractive to the hens. of recorded roars, lions attacked it (Figure 19.13),
Thus, the subordinate brother reproduces by proxy.

Lions a
b
Male lions (Panthera leo) also cooperate in acquiring
mates. They form coalitions, or partnerships, that chal-
lenge the males of other prides. Coalitions may take
over a pride by slowly driving out the resident males, or
it may be a hostile takeover, involving serious fighting
(Figure 19.12). In such contests, the larger coalition
usually wins.

The reward for the victors is a harem of lionesses.
When the females come into reproductive condition
(which is sometimes hastened if the new males kill cubs
that were sired by other males), they often do so simul-
taneously. During the two- to four-day period when a
female is in reproductive condition, she mates about

FIGURE 19.12 Two male lions fight for control of a FIGURE 19.13 A male lion attacks a stuffed lion after
pride. hearing the recorded roar of a male intruder.

438 Chapter 19 / Group Living, Altruism, and Cooperation

6Expected reproductive Long-Tailed Manakins
success per male
4 The Costa Rican rainforest is filled with fascinating ani-
mals, but a standout is a small bird called the long-tailed
2 manakin (Chiroxiphia linearis). Walking through the for-
est near Monteverde, one can often hear in the distance
1 2 3 4 5–7 their calls of “To-lay-do! To-lay-do!” A quiet approach
Coalition size yields a remarkable sight: in a small clearing, two or even
three males work together to attract a mate. They begin
FIGURE 19.14 Males in larger coalitions have greater with the call, emitted as many as 19 times a minute and
reproductive success. (Data from Packer and Ruttan 5000 times a day. Once a female arrives, they begin a
1988.) visual display. In one of the most common variations of
the display, called the up-down jump display, the birds
regardless of whether they were related to other perch side by side on a branch. One male jumps into the
members of their coalition (Grinnell et al. 1995). air, emitting a wheezy buzzee call, and hangs there
Lions attacked the model regardless of the behavior of momentarily; just as he lands, the other male jumps up.
other coalition members and did not appear to moni- Alternately jumping up and down, the males are remi-
tor the actions of others, suggesting that reciprocal niscent of children on a see-saw. Even more spectacular
altruism is not playing an important role (Grinnell et is the cartwheel. Here, males again begin by perching
al. 1995). next to each other. Then, one male jumps upward and
backward over the second male. Meanwhile, the second
Why, then, do unrelated males gather into coali- male hops along the branch to take over the first male’s
tions? The answer turns out to be quite simple—the spot. Now this male takes a turn at jumping up and mov-
larger the coalition, the greater a male’s reproductive ing to the rear. The dance looks as if the two birds were
success (Figure 19.14). Larger coalitions have a better balls being juggled. The courtship sequence may be
chance of ousting the current coalition in a pride, main- repeated only once or as many as a hundred times in suc-
taining control of that pride, and perhaps even gaining cession. When the display bout is over, one male leaves
residence in a succession of prides. A solitary male has the display branch and watches while the remaining male
little chance of reproducing and, therefore, much to does a solo performance. If his gymnastics have
gain by joining a coalition. A small coalition may also impressed the female, she mates with him.
benefit by accepting an unrelated male because the
extra member may help it take over prides. Indeed, Although the males take turns jumping during their
coalitions accept unrelated companions only while tandem courtship display, the same male always mates.
coalition members are not yet resident in a pride The benefit of this elaborate dance to the mating male
(Packer and Pusey 1987). is obvious, but what about the other male? It is not indi-
rect fitness because it seems unlikely that the two males
Larger coalitions also remain in control of a pride are related. A typical brood consists of only one or two
longer than smaller ones. A coalition of three to six offspring, and there is no reason to assume that the siblings
males may remain in control as long as two to three are necessarily the same sex. Furthermore, just before
years. A coalition of two might be in possession for over and after each breeding season, the young, particularly the
a year. If a lone male manages to gain control of a pride, subadult males, disperse. It seems unlikely, therefore,
which happens infrequently, his tenure generally lasts that male relatives would stay in proximity for the three
only a few months (Bertram 1975). As a result, the life- to four years it takes them to acquire adult plumage. If
time success of a male lion increases by cooperating the partners are not genetically related, the nonbreeder
with other males in taking over a pride, even if all the is not increasing his indirect fitness. So why does a sub-
males are not related. Packer et al. (1988) estimated ordinate bird stay?
that each additional member of a coalition increases
individual reproductive success by 0.64 surviving cubs A subordinate bird’s chances of mating would not be
per male. increased by deserting his partner. Solitary males cannot
mate. They cannot even perform the courtship display.
If a male cannot dominate his current partner, his
chances of becoming the dominant member of another
pair will be low. However, if the subordinate male out-
lives his partner, it is likely that a younger male, one that
can be dominated, will become his new associate. Then
it will be his turn to mate and raise his direct fitness
(Foster 1977; McDonald and Potts 1994). In addition,
singing—in particular the ability to match a partner’s

Examples of Cooperation Among Animals 439

FIGURE 19.15 An alliance between two male olive FIGURE 19.16 An acorn woodpecker places an acorn in a
baboons. The two males on the right are cooperating to hole drilled in a dead tree. Food stores must last the
challenge the male on the left. At a later time, the male communal group through winter.
that was assisted will have to reciprocate to maintain the
alliance. What leads us to begin this section with acorn wood-
peckers, however, is not their bizarre food-storing habits
song, which impresses the females—improves with age but their extensive social networks. These birds live in
and practice (Trainer and McDonald 1995; Trainer at al. family groups of up to 15 or so, containing one to four
2002). Thus, the most likely reason for cooperative breeding males, one or two breeding females, and from
courtship in this species is that it increases the chances zero to ten nonbreeding helpers. It is these nonbreeding
of obtaining direct fitness benefits in the future. helpers that are of particular interest. They are adult birds,
physiologically capable of breeding themselves, that
Olive Baboons instead stay to help their parents raise additional young.
Acorn woodpeckers thus fit the definition of cooperative
Male olive baboons (Papio anubis, Figure 19.15) also breeding: some individuals (helpers) assist in the care and
cooperate in attracting a mate, but here we see yet rearing of another’s young rather than producing offspring
another evolutionary mechanism at work. A male who of their own. Cooperative breeding was first described in
lacks a female consort sometimes enlists the help of a birds (Skutch 1935) but has since been documented in
friend to win another male’s mate. The following scenario many taxa, including birds, mammals, insects, and spiders,
is typical of what often occurs: Male A is associating although it is quite rare (e.g., it is found in only about 3%
(called consorting) with an estrous female. Male B, who of birds and mammal species; Emlen 1997).
has no female of his own, solicits the help of male C, and
the two form an alliance and challenge male A. While the There are many variations on the theme of coop-
battle is in progress, male B gets away with the female. erative breeding. Instead of limiting ourselves to the
Male C has acted altruistically; he risked injury while woodpecker example, we will organize the remainder of
assisting another to acquire a mate. However, at some this section by the questions that have intrigued
time in the future, he will enlist the help of male B in win- researchers.
ning a consort of his own (Packer 1977). You will recog-
nize this as an example of reciprocal altruism. How Do Helpers Help?

COOPERATIVE BREEDING In many species, helpers pitch in to feed offspring. The
AND HELPING time-intensive task of rearing baby birds is easily shared
because anybody, not just the parents, can collect and
When hiking in the California woodlands, keep alert for
the unmistakable signs of the acorn woodpecker
(Melanerpes formicivorus). If you don’t recognize it by its
harsh “waka-waka-waka” call, or by its black-and-white
plumage topped off by a snazzy red cap, the dead give-
away that you are in its habitat is a dead tree or even a
telephone pole peppered with a multitude of holes, each
with an acorn inserted snugly in it. Acorn woodpeckers
drill these holes to make their granaries, and they store
their acorns for leaner times (Figure 19.16). (One group
of woodpeckers got a bit carried away and stored 485
pounds (220 kg) of acorns in a water tank in Arizona!)

440 Chapter 19 / Group Living, Altruism, and Cooperation

a helpers mainly contribute by protecting offspring; they
can contribute little to the nourishment of the young
b (Dugatkin 1997).

FIGURE 19.17 A jackal helper (a) prepares to regurgitate Provisioning of food and extra protection are the
food to a pup and (b) chases away an intruder. most common services offered by helpers, but other tasks
also lend themselves to sharing. In some bird species,
carry food to the nest and pop it in a nestling’s mouth. helpers may build and clean nests or incubate and brood
Acorn woodpeckers provide nestlings with food, both the nestlings (Skutch 1987). In saddle-backed tamarins
insects and acorn fragments (Koenig and Mumme 1987). (Saguinus fuscicollis), a small primate, male helpers lug
Helpers in the well-studied Florida scrub jay (Aphelocoma around the offspring. At birth a tamarin is almost 20%
coeruslescens) deliver about 30% of the food consumed by of its adult weight, and litters typically consist of twins.
nestlings. The parents’ job is thus reduced, and, as a Thus, carrying these youngsters is burdensome, and if
result, they enjoy better health. In one study, 87% of the the duty were not shared the mother might not be able
breeders with helpers survived to the next year, com- to obtain enough nourishment for herself and to ensure
pared to 80% of breeders without helpers (Stallcup and an adequate milk supply (Terborgh and Goldizen 1985).
Woolfenden 1978).
Is “Helping” Really Helpful?
Although mammalian mothers are uniquely Given all the useful tasks helpers can perform, this may
equipped to provide milk to their offspring, helpers can seem a silly question. However, not every study has
deliver other kinds of food by carrying it in their jaws or found a relationship between the presence or number of
in their stomachs. Blackbacked jackals (Canis mesomelas) helpers and the reproductive success of the breeding
regurgitate food to eager pups (Figure 19.17). Helpers individuals (reviewed in Clutton-Brock 2002), so it is
not only contribute 18 to 32% of all regurgitations to wise not to make assumptions.
pups, but they sometimes also regurgitate to the lactat-
ing mother, allowing her more time to remain with the In many species, researchers have shown that the
pups instead of hunting (Moehlman 1979). number of helpers correlates with the survival of the
young, the survival of the breeders, or both. For exam-
Help can also come in the form of extra protection ple, we have already mentioned the Florida scrub jay
for the young. Florida scrub jays give alarm calls to (Woolfenden 1975; Woolfenden and Fitzpatrick 1990).
predators such as snakes and even help to drive them These birds have been studied for many years in the scrub
away by mobbing them (Woolfenden 1975). Jackal fam- habitat of Florida, currently threatened by development.
ilies with helpers always have an adult on guard to drive The jays have proven to be easily tamed, allowing for
away predators, whereas groups lacking helpers may close observation (Figure 19.18). The jays form territo-
have to leave the pups unattended while hunting. In fish, ries that contain one breeding pair and a varying num-
ber of helpers—from none to as many as six. The
breeding success of pairs with helpers clearly exceeds that
of pairs without helpers (Woolfenden 1975). Figure 19.19

FIGURE 19.18 Florida scrub jays are not difficult to
observe.

Examples of Cooperation Among Animals 441

Eggs Number of Number of Number of lives in year-round territorial groups of 1 to 13 birds in
5 nestlings fledglings independent the open woodland of Queensland, Australia. Parents are
usually assisted by a variable number of their offspring
4 young from previous broods, but in this experiment, nine of the
breeding groups were reduced to a single helper. These
Average number of young 3 groups then raised an average of 0.8 young, less than half
the number of fledglings produced by the 11 control
2 groups, which had more assistance. Therefore, the pos-
itive relationship between breeding success and the num-
1 ber of helpers found in gray-crowned babblers does seem
to be a result of the presence of helpers (Brown et al.
0 1 2 3–5 0 1 2 3–5 0 1 2 3–5 0 1 2 3–5 1982). However, a problem with this experimental
Number of helpers approach is that removal or addition of helpers has other
unintended effects: it can be very disruptive to the social
FIGURE 19.19 The relationship between the number of structure of a group, and it also changes group size,
Florida scrub jay helpers and the breeding success of the which in turn can affect the group’s success (reviewed in
experienced parents. Helpers do not increase the number Wright and Russell 2008).
of eggs laid. They do, however, increase the chances that
the eggs will hatch and that the young will survive to Another experimental approach to measuring the
become independent. (Data from Woolfenden 1975.) benefits of helping is to change the ratio of helpers to
young in a different way, by temporarily removing or
shows the breeding success of experienced pairs with and adding young while the number of helpers remains con-
without helpers during one five-season study. Notice that stant. When Clutton-Brock et al. (2001) performed this
the presence of helpers has no effect on the number of manipulation in meerkats, which are (quite adorable)
eggs laid but does increase the chances that the young will mammals (Figure 19.20), pup weight gain was increased
hatch, leave the nest, and become independent birds. when the number of pups was reduced, and decreased
when the number of pups was increased. Extra food
Similarly, breeding success increases with the pres- helps the pups by reducing the age at which they first
ence of helpers in some mammalian and fish species. For
example, pairs of blackbacked jackals are joined by FIGURE 19.20 A meerkat helper with pups.
between one and three young from previous litters, who
help them rear the next pups. The reproductive success
of a pair of blackbacked jackals increases with the num-
ber of helpers (Moehlman 1979).

But we must be cautious: finding that there is a cor-
relation between breeding success and the presence of
helpers is not by itself sufficient to demonstrate that
helping causes increased breeding success (Brown et al.
1982). It’s quite possible that another factor, such as ter-
ritory quality, causes both an increase in the number of
helpers and increased breeding success, thus creating the
correlation. In addition, helpers are often the offspring
of the breeders they are assisting—perhaps there is a
correlation between breeding success and the number of
helpers simply because the breeding pair is of consis-
tently high quality from year to year. How might we be
sure that it is really the helpers that caused increased
reproductive success of the breeders?

One way to increase our certainty that helping
causes increased reproductive success in breeders is by
removing helpers and measuring the consequences. For
example, helpers were removed from the nests of gray-
crowned babblers (Pomatostomus temporalis), a bird that

442 Chapter 19 / Group Living, Altruism, and Cooperation

reproduce and by increasing the chance that they can Is It Costly to Help?
successfully compete for a high-ranking spot in the social
hierarchy (Russell et al. 2007). Helping behavior becomes a more interesting evolu-
tionary puzzle if it has a cost, and you won’t be sur-
A third way to approach the problem of teasing apart prised to learn that it often does. For example,
correlation from causation, at least in long-term studies mongoose (Suricata suricatta) helpers forgo feeding and
with plenty of data, is with statistical techniques by which stay at the burrow to baby-sit for the young pups and
different variables can be controlled (Cockburn et al. guard them from predators for an entire day while the
2008; Wright and Russell 2008). Cockburn et al. (2008) parents and others forage. During a 24-hour shift, the
used elegant statistics to analyze 19 years of data on the baby-sitter loses 1.3% of its body weight. In contrast,
superb fairy-wren. They found that helpers did not the foraging group members gain roughly 1.9% of their
increase the survival of offspring but instead increased body weight (Heinsohn and Legge 1999). Helping may
the future survival of breeding females. even reduce survival. For example, the helpers among
stripe-backed wrens (Campylorhynchus nuchalis) that
Do breeders always want help? Not always. After bring the most food die more quickly than other birds
all, an extra helper around might mean competition for (Rabenoid 1990).
resources or increase the chance that your mate has an
extra-pair copulation. In the pied kingfisher (Ceryle STOP AND THINK
rudis), helpers are tolerated only when their services are
needed. These birds usually have primary helpers, Imagine you are spending your graduate school years
which are older offspring, but may also have secondary studying helping behavior in a little-known bird species.
helpers, which are unrelated. Heinz-Ulrich Reyer You find that birds that remain behind on their natal ter-
(1980) compared two colonies of pied kingfishers in East ritory to help their parents are far more likely to die than
Africa. Breeding pairs at Lake Naivasha typically have those that go off to breed on their own. In your disserta-
only one primary helper. When males apply for a job as tion defense, you would like to make the argument that
secondary helpers, they are persistently chased away by helping is costly. How confident are you? What experi-
the male territory holder. In contrast, at Lake Victoria, ment(s) would you like to perform in order to increase
secondary helpers are eventually tolerated and permit- your confidence?
ted to stay and feed the young. Why? The answer is that
the services of secondary helpers are needed to raise off- If it is costly to help, why do it? We can break this ques-
spring at Lake Victoria but not at Lake Naivasha. These tion down into two parts: (1) Why would an offspring delay
birds fish for a living, and Lake Victoria is a harder lake dispersal and stay near home? (2) Why would it help? It
to fish. Victoria’s rougher waters increase the time it makes sense to address these as separate questions because
takes to catch a fish, and the fish are smaller. not every offspring that delays dispersal offers assistance,
Furthermore, the fishing grounds are farther from the and sometimes offspring that have dispersed to nearby areas
colony. With the additional fish provided by secondary return to their parents’ area in order to provide care
helpers, the breeding pair can raise more offspring (reviewed in Pruett-Jones 2004; Ekman et al. 2004).
(Table 19.3).

TABLE 19.3 The Effect of Helpers on the Reproductive Success of Pairs of Pied Kingfishers. Shown Are

Mean, Standard Deviation, and Sample Size

Lake Victoria Lake Naivasha

Mean SD n Mean SD n

Clutch size 4.9 0.6 22 5.0 0.6 8

Young hatched 4.6 0.5 14 4.5 0.7 2

Young fledged

No helpers 1.8 0.6 14 3.7 0.9 9

1 helper 3.6 0.5 12 4.3 0.5 4

2 helpers 4.7 1.0 6 ———

Examples of Cooperation Among Animals 443

Why Should an Offspring Delay Dispersal? breeding units had helpers. In short, the frequency of
helping in populations of acorn woodpeckers varies
In Chapter 11, we discussed the costs and benefits of dis- directly with the scarcity of open territories.
persal and philopatry (staying near home). For example,
animals may disperse in order to avoid inbreeding, Not all territories are equal in quality, and it might
reproductive suppression by their relatives, and compe- be better to stay home if the only other choice is a poor-
tition. On the other hand, animals may exhibit philopa- quality territory. The interaction between habitat satu-
try because they are adapted to the local conditions, and ration and territory quality has been nicely demonstrated
familiar with the physical and social settings of home. by Jan Komdeur (Komdeur 1992; Komdeur et al. 1995),
Dispersal may be risky: for example, small individuals of who transplanted Seychelles warblers to unoccupied
a species of cichlid fish (with the evocative name of the islands. At first, these small birds bred independently.
Princess of Burundi) are very likely to be eaten by preda- When territories began to fill up, some birds stayed to
tors when they venture off their territory. Even when help their parents rather than move to low-quality ter-
breeders are experimentally removed from a territory, ritories that had relatively few insects. When breeders on
potential helpers choose to stay at home instead of mov- low-quality territories were removed, the territories were
ing to the unoccupied territory (Taborsky 1985). filled only by helpers from territories that were equiva-
lent or worse in quality.
Animals might also delay dispersal because other
options may be limited. Let’s look at two major ways in Lack of Mates In addition to habitat, mates can also
which this might happen. be a limited resource (Emlen and Vehrencamp 1983).
For example, splendid fairy-wren females (Figure 19.21)
Habitat Saturation Florida scrub jays live only in a suffer much greater annual mortality than do males
special scrub habitat, comprised of dry-adapted shrubs (57% and 29%, respectively; Rowley 1981), and thus
and understory plants in sandy soils, that is already lim- females are frequently in short supply. Helpers tend to
ited in its distribution and growing ever scarcer because be males that are awaiting an available mate. For some
of human development. Habitat availability is so limited individuals, the wait can be as long as five years. As pat-
that virtually every territory is filled. Once a scrub jay is terns of mortality and the resultant sex ratios vary, so
lucky enough to acquire a territory, it generally keeps it does the percentage of groups with helpers: when
for life (Woolfenden 1975). The most common way for females are scarce, male helpers are plentiful (Russell and
a male to acquire a territory is by inheriting a portion of Rowley 1988; Rowley and Russell 1990).
his parents’ property, either by replacing his father after
his death or by subdivision of his father’s territory. If FIGURE 19.21 A male splendid wren carries an insect to
there is more than one son helping, the dominant one feed its young. When adult females are in short supply
is favored in the property settlement (Woolfenden and in the population, this breeding male can count on his
Fitzpatrick 1978). Otherwise, a scrub jay can only claim sons to help rear the next brood.
a territory of its own if it defeats a breeder or success-
fully competes for the territory of a breeder that has
died. Thus, we believe that a major reason that scrub jays
help their parents is that they are making the best of a
bad set of circumstances.

Support for the idea that the availability of territo-
ries is important in determining helping has also been
found in acorn woodpeckers. Study sites in California,
New Mexico, and Arizona vary with respect to wood-
pecker density, territory turnover rate, and territory
fidelity. In California, the habitat is extremely saturated:
not a single territory became vacant during a three-year
study (MacRoberts and MacRoberts 1976). Forty-nine
percent of the juveniles remained at home, and 70% of
the groups had helpers. Young acorn woodpeckers in the
Magalena Mountains of New Mexico face somewhat
better odds in their quest for suitable territories than do
those on the West Coast: 19% of the territories in New
Mexico became vacant over a three-year study (Stacey
1979). Here, 29% of the youngsters stayed at home, and
59% of the groups had helpers. In the Huachuca
Mountains of southeastern Arizona, there is no shortage
of territories (Stacey and Bock 1978). Only 16% of the

444 Chapter 19 / Group Living, Altruism, and Cooperation

Why Should a Helper Help? FIGURE 19.22 On the left is a nest built by a 4-year-old
female Seychelles warbler with no experience. Note that
Even if an animal does not have the opportunity to it is built between a tree branch and a thin leaf stalk. On
breed, that does not automatically mean it will become the right is a nest built by a 4-year-old female that had
a helper. Many animals become “floaters” and wander experience in being a helper. Note its placement in a
around without a territory. Even if an individual remains sturdy tree fork.
on its own territory, it may not help (as we know from
television sitcoms, if not our own experience), so there tion between helping behavior and relatedness. As a
must be other reasons besides lack of other opportuni- result, the literature on cooperative breeding that once
ties that underlie helping behavior. focused largely on studying indirect fitness benefits has
shifted emphasis to a study of direct benefits (Cockburn
As with other forms of cooperative behavior, we can 1998; Clutton-Brock 2002; Dickinson and Hatchwell
categorize fitness benefits as direct benefits, in which a 2004). To see how animals might improve their own
helper’s own lifetime reproductive success is increased by reproductive success by helping, we’ll look at several
its actions, and as indirect benefits, in which a helper case studies.
benefits by increasing the production of relatives. The
relative importance of direct and indirect fitness bene- Our first example comes from the Seychelles war-
fits depends on the species. blers we met earlier. Although these birds normally
remain on their natal territory to help their mothers raise
Helpers May Get Indirect Fitness Benefits As we additional offspring, they are not as related to the off-
have seen, in most species, helpers are older offspring spring they help as you might expect. In this species,
who help their parents raise their younger siblings. Thus, extra-pair copulation is common, so often a helper will
in cases where helpers improved the survival of nestlings, not have the same father as the offspring it helps. In
helpers may gain indirect fitness benefits by increasing addition, sometimes eggs are deposited in a nest by other
the number of their younger siblings. birds. Indirect benefits are thus relatively lower in this
species; instead, helpers gain direct benefits in several
Some long-term studies suggest that kin selection ways. Genetic analyses of offspring show that helpers
can be important. For example, researchers collected may add their own eggs to a nest (Richardson et
five years of data on white-fronted bee-eaters to test al. 2002). Second, subordinates may be able to take over
alternate hypotheses for helping behavior (Emlen 1991; a territory budded off from the main territory (Komdeur
Emlen and Wrege 1989). They found no evidence for and Edelaar 2001). Finally, helpers have a chance to
direct benefits to the helpers (increased survival to the practice their parenting skills. When they finally acquire
next breeding season, increased chance of mating in their own territory, they are superior breeders (Figure
subsequent years, or increased success in rearing young), 19.22; Komdeur 1996).
but concluded that helping led to increased production
of related young, suggesting that indirect fitness bene- When mates are scarce, a helper may increase its
fits are important. own reproductive success by mating with the original
breeder in a later year or if the original mate dies.
Another line of evidence supporting the hypothesis Remember that in pied kingfishers, the secondary
that indirect benefits can be important comes from cases helpers are unrelated to the breeders. More than half of
in which animals have a choice of whom to help. In pied these helpers return to the same area the following year.
kingfishers, there are two kinds of helpers: as we defined Of these, half succeed in mating with the female they had
previously, secondary helpers help unrelated offspring, assisted (Reyer 1980, 1984, 1986).
and primary offspring help related individuals.
Kingfishers become secondary helpers only when both
their parents are dead; otherwise they are primary
helpers (Reyer 1984, 1990). In long-tailed tits, helpers
are failed breeders. When nests failed either naturally or
because of the interference of researchers, the failed
breeders helped at the nests of relatives rather than at
equidistant nests of nonrelatives. In fact, if close relatives
were not available, failed breeders didn’t help at all
(Russell and Hatchwell 2001).

Helpers May Get Direct Fitness Benefits Many
social groups are comprised of relatives, so it is not sur-
prising that indirect fitness benefits have drawn the
attention of many researchers. However, many groups
have unrelated members, and many studies find no rela-

Examples of Cooperation Among Animals 445

STOP AND THINK guards and will quickly sting you, losing their lives in the
process—as they pull away, their stingers rip out of their
Helping behavior in humans has also been studied from an abdomens and remain in your flesh, into which venom
evolutionary perspective. Because human children are very continues to pump. There is a dearth of males in the
dependent for years, and mothers can give birth to a num- hive—all those busy workers are female. Only one indi-
ber of children in rapid succession, most mothers require vidual in the hive lays eggs, a bloated queen.
help from others to successfully raise their children. In a
review of 45 studies done across many cultures, Sear and Bees are an example of a eusocial (literally “truly
Mace (2008) found that the presence of maternal grand- social”) species. Eusocial species are defined by three
mothers (the mother’s mother) and sibling helpers improves characteristics: reproductive division of labor (some indi-
child survival, but surprisingly, fathers improved child sur- viduals have offspring, and others do not), cooperation in
vival in only one-third of studies. What is a hypothesis the care of young, and overlap of at least two generations
based on kin selection that might explain these data? capable of sharing in the colony’s labor (Michener 1969;
Wilson 1971). The astute reader may realize that these
EUSOCIALITY characteristics also apply to some of the cooperative
breeders that we have just discussed. Species range along
If you’ve spent any time watching a glass-walled obser- a eusociality continuum according to how evenly repro-
vation hive of honeybees, you were probably impressed duction is shared among group members (Figure 19.23)
by the sense of purpose in the colony. The packed-in bees (Lacey and Sherman 1997; Sherman et al. 1995). At one
bustle around, busy at their tasks. Watch for longer, and end, all or many of the group members breed. At the
you’ll notice that younger workers stay inside the hive other end, breeding is restricted to one or several group
and feed the queen’s helpless larval offspring, each tucked members. One way that biologists have described the
carefully away in its own cell. Other workers maintain the degree of eusociality is by measuring “reproductive skew,”
hive and carry out the dead. Older workers forage at flow- or the proportion of individuals that give up reproduction.
ers and, upon returning to the hive, communicate the
location of these resources to their hive mates in an elab- Eusociality is rare. For many years, the only species
orate dance (Chapter 16). If you are foolish enough to known to be eusocial were insects from only two taxonomic
threaten the hive, you will discover that some bees are groups: either hymenopterans (ants, bees, and wasps) or
isopterans (termites). More recently, the list of eusocial
invertebrates has been expanded to include species of

The Eusociality Continuum

Index of Reproductive Skew

0 Florida scrub jays Dwarf mongooses 1
Stripe-backed wrens Naked mole-rats
Groove-billed anis Golden jackals African wild dogs Fungus ants
Acorn woodpeckers Stenogastrine wasps Halictid bees e.g., Atta app.)
Black-tailed prairie
(e.g., Parischnogaster (e.g., Augochlorella Yellow-jacket wasps
dogs nigricans striata) (e.g., Vespula spp.)
Spotted hyenas Carpenter bees Paper wasps
(e.g., Xylocopa sulcatipes) (e.g., Polistes fuscatus) Mound-building termites
Social spiders Damp-wood termites (e.g., Macrotermes spp.)
(e.g., Anelosimus eximius) (e.g., Zootermopsis
nevadensis) Pemphigid aphids
(e.g., Pemphigus spp.)

Honey bees
(e.g., Apis spp.)

FIGURE 19.23 The eusociality continuum blurs the distinction between cooperative breeders and eusocial species.
The traditional definition of a eusocial society is one with reproductive division of labor, cooperation in caring for the
young, and an overlap of adult generations. Cooperative breeding species share these characteristics with eusocial
species, and so it has been suggested that they form a continuum of social systems. The primary differences among
the social systems is the degree to which reproduction is shared among group members. When reproduction is
restricted to a single individual, the reproductive skew is 1. A reproductive skew of 0 indicates that the lifetime
reproductive success of all group members is equal. This diagram shows predicted locations of a variety of coopera-
tively breeding species along the eusociality continuum. (From Lacey and Sherman 1997.)

446 Chapter 19 / Group Living, Altruism, and Cooperation

aphids (e.g., Aoki 1972, 1979, 1982), an ambrosia beetle good of another organism, but members of eusocial
(Kent and Simpson 1992), tiny insects called thrips species may relinquish all chances of reproduction. It is
(Crespi 1992), spiders (Vollrath 1986), and snapping no wonder that some researchers describe colonies such
shrimp (Duffy 1996). In each case, the colonies meet the as these as “superorganisms”—much as cells and tissues
criteria described above but with variations across taxa. function together for the survival and reproductive suc-
For example, some ant species are well known for their cess of the body, members of a eusocial colony function
striking morphological castes. Whereas all worker hon- efficiently together to ensure the survival and reproduc-
eybees look more or less the same, in some ant species tive success of the colony.
individuals vary tremendously according to their job, such
as intimidating soldier ants with their giant heads and In the remainder of this section, we’ll examine euso-
strong jaws that deliver a memorable bite. cial species from two perspectives: first, what favors the
evolution of eusociality? Second, how do eusocial
Eusociality is extremely rare in mammals, and in fact colonies function on a day-to-day basis?
the only well-accepted examples are species in a group
called the mole rats. Of mole rats, the most studied is the The Evolutionary Origins of Eusociality
naked mole rat, Heterocephalus glaber (Jarvis 1981). This
bizarre creature, furless and with long buck teeth, con- Haplodiploidy and the Hymenoptera Perhaps the
structs massive burrows where it feeds on giant under- most common feature of eusocial societies is that they
ground tubers. Naked mole rats fit the classical definition are family groups (Strassman and Queller 2007). As we
of eusociality originally applied to social insects. Breeding have seen, relatedness among individuals can favor the
is restricted to a single female, the queen, even in groups evolution of altruism, so the role of relatedness has long
with almost 300 members (Figure 19.24). Other adult been a focus of research.
females are smaller than the queen and neither ovulate
nor breed. Only one to three males breed with the queen, We’ll begin by examining a special case of related-
although most adult males do produce sperm. Mole rat ness that has generated a great deal of ink. As we’ve
colonies contain overlapping generations of offspring, already seen, eusociality is found only in a handful of
which are communally cared for, and there is division of species. What attracted the attention of researchers
labor among individuals within the colony. The duties (especially before the recent expansion of the list of euso-
assumed by the nonbreeding members seem to depend cial species) is that many of these species have an unusual
on their size and age. Smaller members generally gather genetic system called haplodiploidy. The females are
food and transport nest material. As they grow, they begin diploid, with two sets of chromosomes, as are most
to clear the elaborate tunnel system of obstructions and familiar animals. The males, however, are haploid, with
debris. Larger members dig tunnels and defend the a single set of chromosomes. Males grow from an unfer-
colony (Honeycutt 1992; Lacey and Sherman 1991; tilized egg and produce sperm that are genetically iden-
Sherman et al. 1992). tical to themselves. When a male mates with a female,
the female offspring get a sampling of 50% of their
Eusociality presents an obvious puzzle. As we have mother’s DNA but all of the father’s DNA.
seen in our earlier discussions, it is rare that an animal
gives up even a portion of its reproductive success for the Haploidiploidy changes the coefficients of related-
ness among family members. Full sisters (that share both
FIGURE 19.24 A queen naked mole rat, the only repro- a mother and a father) get half of their DNA from their
ductive female of the colony, is resting on the workers mothers. Each sister gets a sample of 50% of mom’s
that feed her and help care for the young. DNA, so on average, full sisters share 50% of their
maternally derived DNA. Full sisters also get half their
DNA from their fathers, but because fathers are haploid
and all of a male’s sperm is identical, this paternally
derived DNA is identical for every sister. When we con-
sider together the paternally and maternally derived
DNA, full sisters share 75% of their DNA with one
another (r = 0.75). Thus, a female of a haplodiploid
species shares more DNA with her full sister than with
her mother or daughter (r = 0.5) (Figure 19.25).

Hamilton (1964), whose work we have already met
earlier in this chapter (recall Hamilton’s Rule), realized
the potential implications of haplodiploidy for the evo-
lution of eusociality. Because sisters are more related to
one another than to their own daughters, they pass on
more genes by rearing reproductively capable siblings
than they would if they produced their own offspring.

Examples of Cooperation Among Animals 447

chromosomes copy copy chromosomes FIGURE 19.25 The genetic contributions of a
male and female of a haplodiploid species to
AB #1 #1 AB their offspring. Males are haploid and have
only one set of chromosomes. They arise from
#2 unfertilized eggs of the female. All their sperm
are identical. Females are diploid, and each of
Queen Drone their haploid eggs contains half their genes.
(Female parent) (Male parent) Females have half of their mother’s genes and
all of their father’s genes. On average, two full
AB AB AB AB sisters share all the genes they got from their
father and half the genes they got from their
mother.

AB AB AB AB

Male offspring Female offspring

Degrees of relatedness in haplodiploid species
Daughter Son Mother Father Sister Brother

Female to her: 0.5 0.5 0.5 0.5 0.75 0.25
Male to his: 1 N/A 1 N/A 0.5 0.5

This insight quickly captured the imagination of animal working diligently as nursemaids and performing other
behaviorists. Could haplodiploidy be key to understand- tasks. Because the nursemaids that care for the brood are
ing eusociality? unrelated to the colony, their fitness is not increased by
altering the 1:1 sex ratio that is optimal for the queen.
Counterintuitively, some of the strongest evidence Although sex ratio data were available for only two slave-
for the importance of relatedness in eusocial groups is not making species, Trivers and Hare (1976) found that the
cooperation but conflict. The flip side to the argument investment in females and males was about 1:1.
that individuals should cooperate most with their closest
relatives is that they should have the most conflict with These results, as well as other evidence of the
those that are least related. Favoritism of close over dis- importance of relatedness in colony function, led
tant relatives is demonstrated in a number of ways in researchers to hypothesize that there might be a tight
eusocial colonies. For an example, let’s look at whether relationship between haplodiploidy and eusociality. But
individuals should favor rearing male or female larvae. As how well has the haplodiploidy hypothesis stood the test
Figure 19.25 illustrates, a queen shares, on average, an of time? Unfortunately, not nearly as well as was initially
equal percentage of alleles with her sons and her daugh- hoped (reviewed in Linksvayer and Wade 2005, Wilson
ters. Thus, from a queen’s perspective, she should invest 2008). First, as noted earlier, we now know of a number
equally in both sexes and should favor a 1:1 sex ratio. In of eusocial species, such as termites, that are not hap-
contrast, as we have seen, worker bees (all females) share lodiploid. Thus, haplodiploidy is not necessary for the
an average of only 25% of their genes with their broth- evolution of eusociality. Second, there are many hap-
ers, but 75% with sisters. Thus, from a worker’s point of lodiploid species that are not eusocial. Thus, hap-
view, the optimal sex ratio is 3:1 in favor of females. lodiploidy alone is not sufficient for the evolution of
eusociality. Finally, even in haplodiploid species that are
So who gets to decide the sex ratio in a colony? eusocial, the picture is complicated by the fact that
Workers care for the brood and thus have an opportu- females very often mate with more than one male (e.g.,
nity to manipulate the sex ratio. The investment in off- Laidlaw and Page 1984; Page and Metcalf 1982; Ross
spring is indeed nearly 3:1 in favor of females, in line with 1986; Strassmann et al. 1989). Multiple mating reduces
the idea that workers are manipulating the sex ratio for the relatedness among sisters and also reduces the ben-
their own benefit (Trivers and Hare 1976). For compar- efit of helping sisters compared to producing offspring.
ison, consider the slave-making ants. Soldiers of slave- However, a recent comparative study shows that mating
making species wage war against colonies of other ant with a single female is ancestral in all eight eusocial lin-
species and drag back the pupae or larvae. When the cap- eages that were examined. The authors suggest that
tives grow into adults, they serve their colony as slaves,

448 Chapter 19 / Group Living, Altruism, and Cooperation

monogamy was critical to the origin of eusociality and FIGURE 19.26 In some species of ants, all individuals
that multiple mating evolves only after workers have lost look very similar, whereas in others there are strikingly
the ability to breed (Hughes et al. 2008). different morphological castes. In this species of
Acanthomyrmex, there are minor workers (top) and
The extent to which haplodiploidy makes the evo- major workers (bottom). The latter have giant heads,
lution of eusociality more likely is still under debate. specialized for milling seeds and colony defense. (From
There may be an indirect route: haplodiploidy may make Hölldobler and Wilson 1990.)
the evolution of maternal care more likely, which in turn
is necessary for the evolution of eusociality (Linksvayer flict is often quite vicious and may even result in death
and Wade 2005). In any case, it is clear that we need to (reviewed in Strassman and Queller 2007).
look beyond haplodiploidy for a complete explanation
of eusociality. Coordination Despite the existence of conflict, what
is most impressive to the casual observer of eusocial
Extended Parental Care and Long-Lasting Sibling groups is the level of cooperation. Although all eusocial
Associations The existence of parental care may well colonies show coordinated behavior, perhaps the most
be a prerequisite for the evolution of eusociality, as has impressive examples are found among the ants. In some
long been noted (reviewed in Linksvayer and Wade species, different functions are carried out by morpho-
2005). Long-lasting associations between parents and logically distinct castes, as illustrated in Figure 19.26.
offspring allow for kin selection and inclusive fitness, as Some castes have giant heads useful in milling grains and
we saw for other social species. In addition, long-lasting in defending the colony against intruders, whereas small
associations allow the opportunity for parents to manip- castes specialize in foraging and nest maintenance.
ulate their offspring by, for example, restricting food to
make the offspring smaller, or by aggressively harassing In other species, the workers are all morphologically
offspring in order to make them cooperate (Crespi and similar but divide up tasks according to the needs of the
Ragsdale 2000). colony. If we saw such organization on a factory floor,
we would assume that there was some sort of central
Sharing a Defendable Resource Most eusocial command with a manager in charge of assigning tasks.
species rely on some sort of defendable resource, such But how can such complex behavior be carried out by
as a nest, burrows, or tunnels bored in wood. For exam- individuals with brains smaller than pinheads? Is there
ple, eusociality has arisen at least seven times in the some sort of a central organizational structure?
50,000–60,000 species of nest-building aculeate wasps,
but never (to our knowledge) in the 70,000 species of The short answer is no. Instead of a central com-
wasps that do not build nests but instead lay their eggs mand, ants make their decisions about which tasks to
on prey (Wilson and Hölldobler 2005). Our one exam- perform based on simple rules. These rules depend on
ple of a eusocial mammal, the mole rat, also vigorously the information they gain from their immediate environ-
defends its system of tunnels. There is strength in num- ment and their interactions with others (reviewed in
bers: for example, Gamboa (1978) found that a paper Bourke and Franks 1995). For example, red harvester
wasp that founded a nest by herself more often lost it ants (Pogonomyrmex barbatus) live in the deserts of the
to a challenger than did wasps that founded nests with southwestern United States and Mexico. They rely on
other females. Thus, defense of a resource can favor patchily distributed seeds that vary over time. After a
group living and cooperation. However, many animals heavy rain, many buried seeds are exposed, so it makes
share communal resources but do not have reproduc- sense for foraging efforts to increase. When food is
tive division of labor, so this alone cannot be the sole depleted, colony members should not bother going out
explanation for eusociality.

Day-to-Day Functioning of Eusocial Groups

Conflict Individuals within eusocial colonies are gen-
erally not genetically identical and thus may have con-
flicting goals. We described above how workers and
queens in haplodiploid species might favor different sex
ratios of the colony’s offspring. Conflict occurs in other
contexts as well: for example, some wasp colonies are ini-
tiated by multiple cofoundresses, often sisters. Given
that the cofoundresses are not genetically identical, we
predict—and generally see—conflict between them over
who gets to produce more offspring. In fact, this con-

Summary 449

to forage. Deborah Gordon and her colleagues (2008) reproductive success they enjoy will also perpetuate the
tested whether ants inside a colony make decisions about alleles that the altruist shares with them by virtue of their
whether to forage based on the success of other foragers. common descent. The altruist’s relatives are more likely
By the simple strategy of capturing and briefly detain- than nonrelatives to carry the alleles that lead to altru-
ing ants carrying seeds back to the nest, the researchers ism. Another way of saying this is that an individual may
were able to slow down the apparent rate of foraging raise its indirect fitness by helping relatives raise more
success. A decrease in the forager return rate of only offspring than they could without help. We make this
three to five minutes led to an almost immediate reduc- more explicit with Hamilton’s Rule. Hamilton’s Rule
tion in the number of new foragers that left the colony. states that an individual should help its relative raise off-
Instead, those ants could then turn their attention to spring if B/C > 1/r, where B is the benefit to the recipi-
other tasks. We see similar phenomena in other social ent in terms of offspring produced because of the
insects: a bee’s decision whether to collect nectar altruistic act, C is the cost to the actor in terms of off-
depends on the amount of nectar already stored, and a spring it does not produce because of the altruistic act,
wasp’s decision whether to collect more wood pulp for and r is the coefficient of relatedness between the recip-
building depends on how long she had to wait since her ient and the actor.
last load was accepted at the nest (reviewed in Gordon
1996). The take-home message is that behaviors that How might an animal identify its relatives? There are
appear to be very complex and highly coordinated can several possibilities. One way might be to use location as
be generated by a handful of simple decision rules. a cue: the individuals that share one’s home are likely to
be kin. Individuals might also be identified as kin because
SUMMARY they are familiar. Animals that have never been encountered
before may be recognized as kin through phenotype
A wide variety of animal species live in groups, from sim- matching. In other words, an individual compares a
ple aggregations to highly coordinated societies. As with stranger’s traits to those of a known family member or
many other behaviors we discussed in this book, it’s valu- even to itself. Finally, recognition may be genetically
able to consider the costs and benefits that group living based. Perhaps there are alleles that in addition to label-
may provide. Benefits can include increased foraging suc- ing relatives with a noticeable characteristic cause the
cess, decreased predation risk, conservation of heat and altruist to assist others that bear the label.
water by huddling together and conservation of energy
by moving together. Costs include increased competition, Reciprocal Altruism Altruism might also evolve in
risk of disease and parasites, and interference with repro- spite of the initial cost to the altruist if the service is
duction. How costs and benefits are balanced vary repaid with interest. In other words, altruism will be
according to the species, the ecological circumstances, favored if the final gain to the altruist exceeds its initial
and even across individuals within a group. cost. However, for reciprocal altruism to work, individ-
uals that fail to make restitution must be discriminated
Altruism is the performance of a service that bene- against. Because of this requirement, three factors make
fits a conspecific at a cost to the one that does the deed, reciprocal altruism more likely: the benefit of the act to
all measured in terms of units of fitness. The occurrence the recipient is greater than the cost to the actor; there
of altruism is puzzling. If aiding a conspecific costs the should be a good chance that an opportunity for future
altruist, the altruist should leave fewer offspring than do repayment will arise; and the individuals involved must
the beneficiaries of its services. As a result, the alleles for be able to recognize one another.
altruism would be expected to decrease in the popula-
tion over generations. Hypotheses for the evolution of Manipulation Sometimes animals can coerce others
altruism can be classified into four overlapping classes. into helping them by threatening even greater harm.

Individual Selection The general thrust of these No single hypothesis applies to every example of
hypotheses is that when the interaction is examined altruistic behavior. In addition, these evolutionary mech-
closely enough, the altruist will be found to be gaining, anisms are not mutually exclusive; more than one may
rather than losing, by its actions. The benefit may not be responsible for a single example of altruism. To com-
be immediate; sometimes the gain is in the individual’s plicate matters even further, similar behaviors may
future reproductive potential. Another way of saying this evolve by different mechanisms in different species.
is that an individual may receive direct benefits over the
course of its life by being altruistic. Members of some social species emit alarm calls to
warn their neighbors of a predator’s approach. Belding’s
Kin Selection When the beneficiaries of the good ground squirrels emit two types of alarm calls—one in
deeds are genetically related to the altruist, the enhanced response to terrestrial predators and one in response to
aerial predators. The calls seem to have been selected in
different ways. Individual selection seems to be the best
explanation for the evolution of alarm calls in response to

450 Chapter 19 / Group Living, Altruism, and Cooperation

aerial predators. However, kin selection seems to be the asking two questions. First, we can ask why an offspring
most likely mechanism for the evolution of ground squir- might delay dispersal. As we saw in Chapter 11, disper-
rels’ alarm calls in response to terrestrial predators. sal may be dangerous or entail other costs. In addition,
Belding’s ground squirrels may be something of an excep- other options, such as empty habitat or available mates,
tion: in a comparative study across all rodents, calls gen- may be unavailable. However, just because an offspring
erally serve to communicate with predators rather than kin. delays dispersal does not mean it will help. In a number
of species, animals gain indirect fitness by helping to
Many species cooperate in acquiring a mate. We raise kin. In other species, help goes to nonrelatives, so
reviewed four different examples. (1) In wild turkeys, direct benefits are important. These may include inher-
males display in a group, but only one mates. Generally iting a territory or a mate.
males display with their siblings, so they receive indirect
benefits from helping. (2) The situation is more compli- Eusocial species present an extreme example of
cated in lions. Male lions form coalitions to challenge cooperative breeding. Eusocial species have reproductive
other prides. When members of a coalition are related, division of labor (some animals have no offspring), coop-
males can benefit from helping their brothers mate. eration in the care of young, and overlap of at least two
Males also benefit directly from being in larger groups, generations that care for the colony. Eusociality was
even if they are composed of unrelated males. (3) Long- originally described in insects, but the list of eusocial
tailed manakins perform a carefully choreographed species now includes representatives from other taxa,
courtship dance in which displaying males fly around including mammals. Early researchers were intrigued by
each other. Only one of the displaying males mates with a correlation between eusociality and haplodiploidy
the females that are attracted to the show. However, the (a genetic system in which males are haploid and females
subordinate male may become a dominant male if it outlives are diploid). This genetic system means that sisters have,
his partner. Males improve their dancing with practice, on average, a higher level of relatedness to one another
so a long apprenticeship may pay off. (4) Olive baboons than to their own mothers or daughters. By Hamilton’s
form alliances to challenge another male in the troop. In Rule, a higher level of relatedness means that kin selec-
return, they may receive help later, in an example of rec- tion is more likely to evolve. However, haplodiploidy is
iprocal altruism. neither necessary nor sufficient for eusociality to evolve.
Other factors that favor the evolution of eusociality are
Another form of altruism is cooperative breeding. A extended parental care, long-lasting sibling associations,
helper is an individual that assists in the rearing of off- and sharing a central resource, such as a wasps’ nest or
spring that are not its own, usually by providing food or the giant tubers fed upon by naked mole rats.
protecting or carrying the young. In most cases, helping
appears to be beneficial, but it is a good idea to confirm Recently, a great deal of work has focused on how
this experimentally. For example, pairs on high-quality eusocial groups function from day to day. It is common
territories may attract additional helpers, and their to see eusocial individuals favor colony-mates that are
increased reproductive output may be due to the help more closely related over those that are more distantly
they have received or to the territory quality. An exper- related. An impressive level of coordinated behavior
iment is needed to tease these hypotheses apart. among hundreds of individuals can arise from simple
rules, and does not require any particular individual to
Helping is generally costly to the helpers. We can have oversight over the colony’s operations.
ask about the conditions under which helping evolves by

Glossary

Acoustic adaptation hypothesis The idea that the acoustic Altricial Describes young that are virtually helpless and inca-
properties, such as pitch, of auditory signals are shaped by pable of feeding on their own or following their parents for
habitat structure. For example, songs in open habitat are the first few weeks after birth or hatching. Compare with
predicted to have higher frequencies than those in heavily precocial.
vegetated habitat.
Altruism One animal’s apparent aid to another animal at its
Action potential A nerve impulse. An electrochemical signal own expense.
conducted along an axon. A wave of depolarization caused
by the inward flow of sodium ions followed by repolariza- Amplexus The reproductive embrace in which a male
tion resulting from the outward flow of potassium ions. amphibian grasps a female with his front legs from a dor-
sal position.
Activational effects Effects of steroid hormones that typi-
cally occur in adulthood and tend to be transient, lasting Antihormones Drugs that can temporarily and reversibly
only as long as the hormone is present at relatively high suppress the actions of specific hormones.
levels. For example, increases in circulating levels of sex
steroids activate mating behavior. Activational effects may Aposematism See warning coloration.
involve subtle changes in previously established connec- Apostatic selection A form of frequency-dependent selec-
tions rather than gross reorganization of neural pathways.
Compare with organizational effects. tion that occurs when one morph in a polymorphic popu-
lation is much more common than another morph.
Adaptation (1) The process of natural selection in which Predators may develop a search image for the more com-
evolutionary modification occurs in response to selection mon, rather than the rare, morph, and take more of the
pressures. (2) The result of natural selection; that is, common form relative to its frequency in the population.
behavioral, morphological, developmental, or physiologi- Predators need not hunt by search image to cause apostat-
cal changes that have been preserved because they have ic selection in prey; some predators may simply have an
had a selective advantage. (3) The immediate physiological aversion to rare or unfamiliar prey.
response of an organism to a change in conditions, such as Artificial selection The process by which humans change
an increase in temperature. In this book, we are generally the frequency of traits within populations by intentional
concerned with one of the first two definitions. selective breeding. Dog breeds provide an example of arti-
ficial selection.
Afferent neuron A sensory neuron. A nerve cell that carries Associated reproductive pattern Pattern shown by some
information from the peripheral receptors toward the cen- vertebrates in which there is a close temporal association
tral nervous system. between gonadal activity and mating. Gonadal growth and
an increase in circulating levels of sex steroids activate mat-
Aggression A behavior apparently intended to inflict noxious ing behavior.
effects or destruction on another organism. Associative learning The formation of some sort of mental
connection between representations of two stimuli.
Aggressive mimicry Phenomenon whereby a predator can Audience effect The impact that passive onlookers have on
get close to its prey because it imitates a signal that is not the behavior and physiology of an individual performing a
avoided by the prey or that even attracts it. task.
Autotomy The ability to break off a body part when attacked.
Agonistic behavior Behavior that encompasses all conflict Axon A long extension from the cell body of a neuron that
between conspecifics, including threats, submissive behav- carries an electrochemical message away from the cell
ior, chasing, and physical combat. It is not used to describe body toward another neuron or effector (muscle or gland).
aggressive acts between species, such as predation. The tips of the axon release a chemical called a neuro-
transmitter that can affect the activity of the receiving cell.
Allee effect Phenomenon whereby having a few neighbors is Typically, there is one long axon on a neuron.
beneficial, especially for gaining access to potential mates Batesian mimicry Phenomenon whereby a palatable species
and defense against predators. According to this idea, indi- adopts the warning characteristics of a noxious or harmful
vidual fitness increases with number of conspecifics at low species. The harmless species is called the mimic and the
to moderate densities, and then declines from moderate to noxious one, the model. By resembling a noxious species,
high densities. With regard to habitat selection, compare the mimic gains protection from predators.
with ideal free distribution. Behavioral ecology A discipline that examines the evolu-
tionary and ecological bases of the behavior of animals. It
Allele Alternative form of a gene. One of two or more slight- grew out of the ethological approach to studying animal
ly different versions of a gene that code for different forms behavior. Behavioral ecologists examine the costs and ben-
of the same trait. efits of behaviors, such as foraging, mating, group living,
and communicating.
Allogrooming Caring for the fur, skin, or feathers of a con-
specific; it is distinguished from autogrooming (self-
grooming). Allogrooming functions in hygiene and also
builds and maintains social bonds.

451

452 Glossary

Breeding dispersal The movement an animal makes background and thereby reduces risk of detection by visu-
between two successive breeding areas or social groups. It ally hunting predators. It is sometimes called cryptic col-
is sometimes called postbreeding dispersal. oration.
Communication The process of transferring information
Camouflage A collective term used to describe several from sender to receiver to the benefit of the sender, on
antipredator devices, such as disruptive coloration, coun- average.
tershading, and transparency, whose general message is “I Comparative method Using the evolutionary relationships
am not here.” among species in order to gain insights into adaptation.
For example, unrelated species that share similar environ-
Candidate gene A gene that is hypothesized to be involved in ments may evolve similar traits, while related species that
a particular behavior based on a search of the literature for live in different environments may evolve different traits.
genes known to be involved in producing a similar behav- Comparative psychology A branch of psychology that stud-
ior in another organism or by comparing the sequence of ies the behavior of animals, with a focus on physiology,
the gene to the sequences of genes in other organisms using learning, and development. The experiments are quantita-
genome-sequencing data. tive and often laboratory-oriented.
Compass orientation The ability to find one’s way without
Carnivory Feeding on other animals. using landmarks. The animal keeps a certain angle toward
Central pattern generator A neuron or network of neurons an external reference system used as a compass. External
reference systems include the sun, the stars, and the earth’s
that is capable of generating a rhythmic pattern of activity in magnetic field.
motor neurons, even when all sensory input has been Conditional strategy In agonistic encounters, a strategy that
removed from the system. is adjusted according to the conditions of a particular fight.
Chain of reactions A behavioral repertoire built from a Conditioned response In the study of classical condition-
sequence of fixed action patterns. Each fixed action pattern ing, the learned behavioral response elicited by the condi-
brings the animal into a situation that triggers the next tioned stimulus.
fixed action pattern in the sequence. Conditioned stimulus In classical conditioning, an innocu-
Challenge hypothesis Hypothesis that levels of hormones ous stimulus, such as a tone or a light, is paired with an
involved in dominance and aggression rise during times of unconditioned stimulus that is rewarding to an animal,
social challenge or instability, such as during the initial such as food. Animals that have learned the pairing
period of territory establishment. respond to the tone or light, which is then called the con-
Chase-away model An explanation for the evolution of ditioned stimulus.
extreme traits in males that exploit a sensory bias of Confusion effect Situation in which predators are less suc-
females. Females receive no benefits from being selective cessful in attacking grouped prey because they are unable
in their choice of mate. The model is based on sexual con- to single out and attack an individual prey.
flict. Conspecific attraction hypothesis Hypothesis proposing
Circadian rhythm Biological rhythms that are about a day in that individuals choose habitat patches based on the pres-
length (circa, about; diem, a day). Used formally, it refers to ence of established residents of their own species.
a solar-day rhythm that persists in constant conditions of Constant reproductive pattern Pattern shown by some
light and temperature with a period length that is slightly vertebrates inhabiting harsh environments where suitable
longer or shorter than 24 hours. Its period length is rela- breeding conditions occur suddenly and unpredictably.
tively independent of temperature, and its phase can be While waiting for suitable circumstances in which to
reset with pulses of light. breed, these species maintain large gonads, mature
Circalunadian rhythm A basic lunar-day rhythm that per- gametes, and high circulating levels of sex steroids for pro-
sists in constant conditions with a period that is slightly longed periods of time. Sometimes called the opportunis-
longer or shorter than 24.8 hours. A circalunadian rhythm tic reproductive pattern.
is usually bimodal. Constraint In mathematical modeling, a limitation that we
Circamonthly rhythm A synodic monthly rhythm that per- place on a behavior. For example, we may create a model
sists in constant conditions with a period length that differs in which the amount of food an animal can eat is con-
slightly from 29.5 days. strained by gut capacity.
Circannual rhythm An annual rhythm that persists in a con- Continuous reinforcement schedule In the study of learn-
stant light-dark cycle with a period length that differs ing, a reinforcement schedule in which each occurrence of
slightly from 365 days. a desired behavior is rewarded. This reinforcement sched-
Circatidal rhythm A rhythm that persists in constant condi- ule is effective when initially training an animal to perform
tions with a period length that differs slightly from 12.4 a behavior.
hours. It is the same as a circalunadian rhythm. Cooperative hunting Coordinated foraging efforts among
Classical conditioning In the study of learning, the pairing predators.
of an innocuous stimulus with a rewarding stimulus, so Copulatory plug A plug made of thick, viscous secretions
that the animal learns to respond to the innocuous stimu- deposited by males in the reproductive tract of females at
lus. This procedure was made famous by Pavlov and his mating. Copulatory plugs occur in many vertebrates,
study of dogs. including snakes, lizards, marsupials, rodents, bats, and
Coefficient of relatedness (r) The probability that a partic- primates. Several functions have been suggested for copu-
ular pair of animals share the same allele through common
descent.
Coloration matching the visual background An antipreda-
tor device in which a prey animal’s coloration resembles its

Glossary 453

latory plugs, among them: (1) “enforcing chastity” in parental care includes behaviors such as nursing (and feed-
which the plug acts as a barrier to subsequent insemina- ing), grooming, transporting, and huddling with young.
tions; (2) ensuring the retention of sperm in the female Displacement activities Irrelevant actions performed in sit-
reproductive tract; (3) aiding the transport of sperm with- uations in which an animal has conflicting motivations.
in the female reproductive tract; (4) providing for the grad- Display A stereotyped sequence of behaviors that has a sig-
ual release of sperm as the plug disintegrates; and (5) pro- naling function.
viding a means by which a male can scent-mark a female’s Disruptive coloration Coloration designed to prevent per-
body and convey information regarding his identity and ception of a prey animal’s form.
dominance status. Dissociated reproductive pattern Pattern shown by some
Core area The area of a home range in which the activities vertebrates in which mating behavior is completely uncou-
of an animal are concentrated. pled from gamete maturation and secretion of sex steroids.
Countershading Pattern of coloration characterized by dark Gonadal activity occurs only after all breeding activity for
backs and light bellies, which may achieve camouflage the current season has ceased, and gametes are thus pro-
through either self-shadow concealment (obscuring the duced and stored for the next breeding season.
ventral shadow) or background matching. Dominance The ability of an animal to assert itself to others
Counting The process of assigning a tag such as “1, 2, 3” to in acquiring access to a resource such as food, a mate, or a
individual numbers. display or nesting site.
Cross-fostering A technique for detecting maternal influ- Dominant allele The allele that is fully expressed in a het-
ences by transferring shortly after birth the offspring from erozygous individual.
one strain (or species) to the mother of another strain (or Dove In game theory, the strategy of immediately fleeing if
species). confronted by an opponent that is playing the hawk strat-
Cryptic female choice Selection by females who have mated egy, and displaying if confronted by an opponent that is
with several males of the sperm that will fertilize their also playing a dove strategy. See also hawk.
eggs. This ability is described as cryptic because it is a hid- Ecological trap A low-quality habitat that animals prefer
den, internal decision made after copulation. over a high-quality habitat.
Cue Information transmitted from one animal to another, Efferent neuron A motor neuron specialized to carry
but not necessarily to the benefit of the sender, such as the information away from the nervous system to an effector
rustling noise made by a mouse and detected by an owl. (muscle or a gland).
Currency In mathematical modeling, the common unit in Emancipation Over evolutionary time, a behavior that has
which costs and benefits of different strategies are measured. lost its original function and now serves only a commu-
Examples are the number of offspring produced or the nicative function.
number of calories gained. Entrainment The process by which an environmental
Dead reckoning See path integration. rhythm, such as a light-dark cycle, regulates the period and
Dendrite A process of a neuron specialized to pick up mes- phase of a biological rhythm.
sages and transmit them toward the cell body. There are Environmental enrichment Efforts made to enrich the lives
typically many short branching dendrites on a neuron. of captive animals. Such efforts usually involve social hous-
Deoxyribonucleic acid (DNA) The molecular basis of ing and the provision of larger cages, a more complex and
genetic inheritance. A category of nucleic acids that usual- variable physical environment with nesting material, for-
ly consists of a double helix of two nucleotide strands. The aging devices, toys, hiding places, and the opportunity for
sequence of nucleotides carries the instructions for assem- voluntary exercise.
bling proteins. Epigenetics A stable change in a gene that does not involve
Depolarization A change in the difference in electrical changes in nucleotide sequence. Genes become active or
charge across a membrane that moves it from a negative are shut down due to unwinding or winding of DNA.
value toward 0 mV. During a nerve impulse (action poten- Ethology The study of animal behavior that focuses largely
tial), depolarization is caused by the inward flow of posi- on the evolution and function of behavior. Many early
tively charged sodium ions. ethological studies were comparative and took place in the
Detouring The ability to identify an alternative route to a field.
reward when the direct route is blocked. Evolution A change in the frequencies of alleles in a popula-
Developmental homeostasis Ability of developmental tion of organisms over generations.
processes to buffer themselves against potentially harmful Evolutionary stable strategy (ESS) A behavioral strategy
influences to produce functional adults. that when adopted by all members of the population can-
Dilution effect Phenomenon whereby individuals living in not be replaced by a different strategy. A pure ESS con-
groups are safer from predators because each has a smaller sists of a single strategy, while a mixed ESS consists of sev-
chance of becoming the next victim. eral strategies in a stable equilibrium.
Direct fitness Fitness gained by an individual through its Excitatory postsynaptic potential (EPSP) A temporary
own reproduction, generally measured as the number of electrical change (depolarization) in the membrane of the
surviving offspring it produces. Compare with indirect postsynaptic neuron that is caused by the binding of an
fitness. excitatory neurotransmitter. An EPSP makes it more like-
Direct parental care Patterns of behavior performed by par- ly that the postsynaptic neuron will generate an action
ents that have an immediate physical impact on offspring potential.
and their survival. In mammals, for example, direct

454 Glossary

Extinction In classical conditioning, presenting a condi- viability have a genetic basis. If a female preference (also
tioned, or learned, stimulus without the reinforcer, leading genetically based) for the male trait should arise, then
to a loss of the learned response over time. these females mate with males carrying genes for the trait
and enhanced viability. In this way, genes for the male
Female defense polygyny Form of polygyny in which a trait, high viability, and the female preference become
male defends a harem of females. This type of polygyny associated.
occurs when females live in groups that a male can easily Habitat selection Process by which animals that disperse
defend. from their natal site or breeding site eventually select a
new location in which to settle. Habitat selection has three
Filial imprinting Process by which a young bird learns, phases: (1) search (animal searches for a new habitat); (2)
through exposure to its mother, her particular characteris- settlement (animal arrives in a new habitat and begins to
tics and then preferentially follows her. Filial imprinting establish a home range or territory); and (3) residency (ani-
may function to allow young birds to recognize close rela- mal lives in the new habitat).
tives and thereby distinguish their parents from other Habituation In learning, the waning of a behavioral response
adults that might attack them. to a stimulus because during repeated presentations of that
stimulus it was shown to be harmless.
Fitness The reproductive success of an allele or an individual Hamilton’s rule A rule designed to determine whether an
compared to other alleles or individuals in the same popu- animal should behave altruistically toward another animal.
lation. See also direct fitness, indirect fitness, and inclusive It includes three variables: the coefficient of relatedness,
fitness. the benefit to the receiver in terms of the number of addi-
tional offspring it produces because of the altruistic act,
Fixed action pattern An innate stereotyped motor response and the cost to the altruist in terms of the number of off-
that is initiated by a stimulus but that can continue to com- spring it does not produce because of the altruistic act.
pletion without ongoing stimulation. Handicap principle An example of a good genes model for
mate choice. According to this principle, females prefer a
Fixed ratio schedule In the study of learning, a reinforce- male with a trait that reduces his chances of survival but
ment schedule in which the animal must respond a set announces his superior genetic quality precisely because he
number of times before a reward is given. This schedule has managed to survive despite his “handicap.” In short,
generally results in very high response rates. male secondary sexual characteristics act as honest signals,
indicating high fitness, and females choose males with the
Foraging Finding, processing, and eating food. greatest handicaps because their superior genes may help
Free-running period The period length of a biological produce viable offspring.
Handling time The time required to process a food item.
clock when it is not being influenced by external time cues. Hawk In game theory, the strategy of immediately attacking
Frequency-dependent selection A type of natural selection an opponent. See also dove.
Herbivory Feeding on plant material.
in which an allele has a greater selective advantage when it Heritability The portion of the variability in a specific trait
is rare in a population and a smaller selective advantage in a population that is due to genetic factors; the ratio of
when it is common. For example, one type of frequency- the phenotypic variance due to genetic factors to total phe-
dependent selection occurs when females prefer to mate notypic variance.
with males of a rare phenotype. Frequency-dependent Heterospecific attraction hypothesis Hypothesis propos-
selection results in the fluctuation of allele frequencies ing that individuals choose habitat patches based on the
over time. presence of established residents of another species.
Full song In songbirds, the final adult song that in many Heterozygous The condition of having two different alleles
species will remain virtually unchanged for the rest of the for a particular gene.
male’s life. Sometimes called crystallized song. Home range The area in which an animal carries out its nor-
Game theory A type of mathematical model in which the mal activities.
optimal strategy of one animal depends on the behavior of Homing See true navigation.
its opponent. Homozygous The condition of having two identical alleles
Gene flow The movement of genes from one population to for a particular gene.
another. Gene flow causes populations to become more Honest signals Signals that accurately convey information
similar to one another. about the sender. Not all signals are honest, and honest
Genetic drift Evolutionary change in a population due to signals are likely to evolve only under particular condi-
chance events. Genetic drift is more likely to be an impor- tions.
tant evolutionary force in small populations than in large Hot spots Areas in which males gather because they are most
populations. likely to encounter receptive females.
Genetic monogamy An exclusive mating relationship Hotshots Males that are extremely successful at attracting
between one male and one female. Compare with social females. Less successful males may increase their chances
monogamy. of mating by staying near these highly successful males.
Genomics The study of all the genes in an organism.
Genotype The genetic makeup of an individual. It refers to
the precise alleles present.
Goal-directed emulation Behavior whereby an observer
seems to learn from observation what goal is to be achieved
but does not precisely copy what the demonstrator does.
Compare with imitation.
Good genes models Models that assume that a particular
trait in males indicates viability and that both the trait and

Glossary 455

Hypothesis A logical, testable explanation for a specific set Interspecific brood parasites In birds, species that lay their
of observations that serves as the basis for experimentation. eggs in the nests of other species. Interspecific brood par-
asites never build nests in which to lay eggs and raise their
Ideal free distribution A method to describe how animals own young, so they are described as obligate brood para-
distribute themselves in space if they know the value of sites.
each habitat and are free to go where they choose.
Intrasexual selection Mechanism of sexual selection where-
Imitation An observer’s exact copying of what a demonstra- by members of one sex (usually males) compete with one
tor does. Compare with goal-directed emulation. another for access to the other sex. Intense fighting and
competition for mates can lead to selection for increased
Inbred lines Domestic animals that have very little genetic size and elaborate weapons.
variability. They are created by mating close family mem-
bers with one another. Intraspecific brood parasites In birds, species that lay their
eggs in the nests of conspecifics. In some cases of intraspe-
Inclusive fitness The sum of both direct fitness (fitness cific brood parasitism, the brood parasite occasionally lays
gained through offspring) and indirect fitness (fitness eggs in the nests of conspecifics, while still laying eggs in
gained by helping relatives raise additional offspring they her own nest. In other instances, the brood parasite lays
would not be able to raise without help). eggs in the nests of conspecifics and does not maintain a
nest of her own.
Indirect fitness Fitness gained by helping relatives raise
additional offspring that they would not have been able to Intrauterine position effects In rodents, effects on mor-
raise on their own. Compare with direct fitness. phology, physiology, and behavior caused by exposure to
hormones secreted by contiguous littermates during gesta-
Indirect parental care Patterns of behavior performed by tion.
parents that may not involve direct physical contact with
offspring, but still affect offspring survival. In mammals, Ion An atom or group of atoms that carries an electric charge
for example, indirect forms of parental care include acquir- resulting from the loss or gain of electrons.
ing and defending critical resources, building and main-
taining nests or dens, defending offspring against preda- Ion channel A protein-lined pore or channel in a plasma
tors or infanticidal conspecifics, and caring for pregnant or membrane through which one type or a few types of ions
lactating females. can pass. Ion channels in nerve cells are important in the
generation and propagation of nerve impulses.
Infanticide The killing of a conspecific infant to acquire cop-
ulations or resources. Can also occur in response to severe Kin selection A type of natural selection in which animals
disturbance of the physical or social environment. help their relatives reproduce, thereby helping pass the
alleles that they share to the next generation. See also coef-
Information center Communal roosts or colonies from which ficient of relatedness and direct, indirect, and inclusive
animals can follow successful conspecifics to food sites. fitness.

Information sharing Improving foraging by paying atten- Landmark An easily recognizable cue along a route that can
tion to the behavior of group members. be quickly stored in memory to guide a later journey.

Infrasound Sounds whose frequencies are below those audible Language A term that has four elements: first, words or signs
to humans, which means frequencies lower than about 20 must be used as true symbols that can stand for, or take the
Hz. Some animals, such as elephants, use infrasound to com- place of, a real object, event, person, action, or relation-
municate over long distances. Other animals may use infra- ship. Second, symbols should permit reference to objects
sound during orientation. or events that are not present. Third, there should be some
elements of grammar, or rules that determine the relation-
Inhibitory postsynaptic potential (IPSP) A temporary ship between words. Fourth, words or signs should be
electrical change (hyperpolarization) in the membrane of combined to form novel phrases or sentences that are
the postsynaptic neuron that is caused by the binding of an understandable to others.
inhibitory neurotransmitter. An IPSP makes it less likely
that the postsynaptic neuron will generate an action poten- Latent learning Learning that occurs without any obvious
tial. immediate reward. For instance, an animal can learn
important characteristics of its environment during unre-
Insight An example of animal cognition in which under- warded explorations and then use this information later.
standing seems to occur suddenly and without practice.
Learning A change in the capacity for behavior as a result of
Intention movements A behavior, such as spreading the experience, excluding the effects of fatigue, sensory adap-
wings for flight, that signals an animal’s behavior to an tation, or maturation of the nervous system.
observer. Intention movements are thought to be a route by
which some signals evolve. Lek polygyny Form of polygyny in which males defend
“symbolic” territories that are often located at traditional
Intermediate-term memory Memory of new information display sites called leks. Males of lek species do not provide
that may last a day or so. Habituation and sensitization are parental care and defend only their small territory on the
examples of intermediate-term memory formation. lek, not groups of females that happen to be living togeth-
er nor resources associated with specific areas. Females
Interneuron An association neuron. Neurons located within visit these display arenas, select a mate, copulate, and leave.
the central nervous system between sensory and motor
neurons that integrate information. Local enhancement A type of social learning in which an
animal is attracted to a particular location because a con-
Intersexual selection Mechanism of sexual selection where- specific is there.
by members of the sex in demand (usually females) choose
mates with certain preferred characteristics. Thus, males
compete to attract females through the elaboration of
structures or behavior patterns.

456 Glossary

Long-term depression (LTD) A lasting decrease in respon- that it has been spotted early in its hunting sequence; (3)
siveness of postsynaptic neurons after sensory neurons alerting others, particularly relatives, of the danger; and
have received a slow train of stimuli. LTD is a mechanism (4) providing an opportunity for others, again particularly
that weakens the effectiveness of a synapse, decreasing the relatives, to learn to recognize and fear the object that is
magnitude of a response by the postsynaptic cell. It may being mobbed.
play a role in memory formation. Model organism A species chosen to study particular bio-
logical principles with the expectation that the information
Long-term memory Memory that lasts weeks, months, or learned from the model organism can be applied to other
years. Changes in synapses underlie long-term memory. species.
Monogamy Mating system in which a male and female have
Long-term potentiation (LTP) A stable and long-lasting only a single mating partner per breeding season. Further
responsiveness to an action potential by the receiving neu- classified as genetic or social monogamy.
ron caused by rapidly repeated strong stimulation. LTP Motor neuron A neuron specialized to carry information
strengthens the connections between the adjacent neurons. away from the nervous system to an effector (muscle or
It is the molecular mechanism that underlies the acquisition gland).
and storage of memories. Müllerian mimicry Antipredator strategy in which two
warningly colored species look alike. Two noxious species
Lordosis The copulatory posture that some female mammals may benefit from a shared pattern because predators con-
assume when ready to mate. The posture typically involves sume fewer of each species in the process of learning to
ventral curvature of the vertebral column. avoid all animals of that general appearance.
Multimodal communication Communication that contains
Macroevolution Large-scale evolutionary changes in lin- signals from two or more sensory modalities (e.g., vision,
eages, generally observed over geological time. Compare audition, and touch). Signaling in different channels can
with microevolution. occur either simultaneously or sequentially and the mes-
sages can be redundant or nonredundant.
Major histocompatibility complex (MHC) A large chro- Mutation A change in the DNA sequence of an organism,
mosomal region that varies tremendously among individu- such as an addition or a deletion of nucleotides.
als and is important in the immune responses that protect Myelin sheath An insulating layer around axons of nerve cells
against disease-causing organisms. Some animals may that carry action potentials (nerve impulses) over relatively
identify kin and choose mates based on MHC genes. long distances. It is composed of multiple wrappings of the
plasma membrane of certain glial cells. The myelin sheath
Marginal value theorem A model that predicts when a for- greatly increases the speed at which impulses travel. The cells
aging animal should leave a patch of food. It is generally that form the myelin sheath are separated from one another
depicted in a graph. by short regions of exposed axon. The nerve impulse “jumps”
from one exposed region of axon to the next.
Mate guarding Strategies employed by males to increase the Natal dispersal The movement an animal makes from its
probability that their sperm, and not the sperm of a com- natal area or social group to the area or social group where
petitor, will fertilize the eggs of a particular female. Mate it first breeds.
guarding can occur before or after copulation or both. Natal habitat preference induction (NHPI) Phenomenon
whereby an animal’s experience in its natal habitat induces a
Meta-analysis A statistical approach in which one collects all preference for a postdispersal habitat with similar qualities.
the studies that test a particular hypothesis and then com- Natal philopatry Occurs when offspring remain at their
bine the results in order to look for significance in the natal area and share the home range or territory with their
overall pattern. parents.
Natural selection Process by which organisms with favor-
Microarray analysis An analysis that reveals which of hun- able characteristics are more likely to survive and repro-
dreds or thousands of genes are active at any moment. duce than those with unfavorable characteristics.
Thousands of genes are stamped on a solid surface, and Negative-assortative mating A mating pattern in which
molecular tags are used to identify the messenger RNA animals preferentially mate with those with phenotypes
(mRNA) produced by each gene. The more active a gene, different from their own.
the more mRNA is produced. Genes that are active only Neurite A small-diameter process extending from a neuron’s
during a particular behavior may play a role in producing cell body. A neurite can be either an axon or a dendrite.
that behavior. Neurogenesis The creation of new neurons.
Neuromodulators Chemicals that cause voltage changes
Microevolution Minor evolutionary changes within a that occur over seconds, minutes, hours, and perhaps even
species. Compare with macroevolution. days. Neuromodulators alter neuronal activity slowly, by
biochemical means. Different neuromodulators can act on
Migration Movement away from the home range that does the same neural elements to produce different behaviors.
not stop upon encountering the first suitable location. Neurons Nerve cells involved in intercellular communi-
Migrating animals continue to move until they eventually cation.
become responsive to the presence of resources, such as
nest sites and food, and then they stop. Within a particular
species, migratory movements occur over greater distances
than dispersal movements.

Mobbing An antipredator strategy whereby prey approach,
gather around, and harass their predators. Mobbing is
usually initiated by a single individual, and then con-
specifics, or members of another species, join. The possi-
ble functions of mobbing include, but are not limited to,
(1) confusing the predator; (2) discouraging the predator
either through harassment or through the announcement

Glossary 457

Neurosteroids Steroid hormones produced by the nervous Peptide hormones Water-soluble hormones that cannot
system that act in the nervous system on either nearby cells pass through the plasma membrane of target cells on their
or the same cell that produced the hormone. This mode of own, so they influence cells indirectly through second
action contrasts with peripheral steroids produced by the messenger systems. These hormones activate existing
gonads or adrenal glands that travel in the bloodstream enzymes. Examples of peptide hormones are luteinizing
and act on target cells some distance from their gland of hormone (LH) and follicle-stimulating hormone (FSH)
origin. produced by the anterior pituitary gland.

Neurotransmitter A chemical released from the axon tip of Period The time interval of one complete cycle of a biologi-
a neuron that affects the activity of another cell (usually a cal rhythm.
nerve, muscle, or gland cell) by altering the electrical
potential difference across the membrane of the receiving Peripheral-control hypothesis Hypothesis proposing that
cell. rhythmic behavior occurs because the first movement
stimulates sensory receptors, which in turn trigger the next
Nuptial gifts Food or other valuable substances offered by movement in the sequence. The second movement stimu-
males to females during courtship or mating. lates other sensory receptors that trigger the first compo-
nent. Thus, sensory feedback is necessary for this hypoth-
Observational conditioning A type of classical conditioning esis.
that takes place when an animal observes another animal
rather than going through a conditioning experience Phenotype The observable physical and physiological traits
directly. of an individual. Phenotype results from the inherited alle-
les and their interactions with the environment.
Omnivory Feeding on both plants and animals.
Operant conditioning A form of associative learning in which Phenotype matching A type of kin recognition accomplished
by assessing the degree of similarity between one’s pheno-
the outcome (positive or negative) depends on the animal’s type and that of another individual, or by learning the phe-
behavior, such as an animal that learns to run a maze in order notypes of relatives.
to receive a reward. Also called trial-and-error learning and
instrumental conditioning. Pheromones Chemicals that convey information to other
Operational sex ratio The ratio of potentially mating males members of the same species. Some pheromones, called
to fertilizable females. releaser pheromones, have an immediate effect on the
Optimality modeling The use of mathematical procedures recipient’s behavior. Other pheromones, known as primer
to weigh the costs and benefits of different strategies and pheromones, exert their effect more slowly, by altering the
determine which strategy provides the maximum award physiology and subsequent behavior of the recipient.
under a specified set of assumptions.
Organizational effects Effects of steroid hormones that Piloting The ability to find one’s way using landmarks.
occur early in life, usually just before or after birth or Play Behavior that borrows pieces of other behavior patterns,
hatching, and tend to be permanent. This permanence
implies structural changes in the brain or nonneural sys- usually incomplete sequences and often in an exaggerated
tems. For example, steroid hormones around hatching form. It consists of elements drawn from other, functional-
organize the brain of a male songbird to make him capable ly different behavior patterns juxtaposed in new sequences.
of singing in adulthood. Compare with activational effects. Play includes social play, locomotor play, and object play.
Own-species bias In studies of bird song, the preference of Players Individuals whose strategies are modeled in game
young male songbirds to learn their songs from members of theory.
their own species. Polyandry Mating system in which a female has more than
Parental investment Any investment by parents in an off- one mate during a breeding season.
spring that increases the survival of that offspring while Polygyny Mating system in which one male mates with more
decreasing the ability of the parent to invest in other off- than one female during a breeding season.
spring. Polygyny threshold hypothesis Hypothesis proposing that
Path integration Process by which an animal integrates polygynous matings will be advantageous to females when
information on the sequence of direction and distance the benefits achieved by mating with a high-quality male
traveled during each leg of the outward journey. Then, and gaining access to his resources more than compensate
knowing its location relative to home, the animal can head for costs. Thus, a female may reproduce more successfully
directly there, using its compass(es). A compass may also as a secondary mate on a high-quality territory than as a
be used to determine the direction traveled on each leg of monogamous mate on a low-quality territory. The term
the outward journey, or the direction may be estimated polygyny threshold describes the difference in a territory’s
from the twists and turns taken, sounds, smells, or even the quality needed to make secondary status a better repro-
earth’s magnetic field. Information from the outward jour- ductive option for females than primary status.
ney is used to calculate the homeward direction (vector). Polymorphism Phenomenon whereby a species occurs in
Also called dead reckoning. several different shapes and/or color forms. This may pre-
Payoff matrix In game theory, a table used to organize the vent predators from forming search images.
values of each strategy when it is played against each of the Potential reproductive rate The maximum number of
other strategies. independent offspring that each parent can produce per
unit of time.
Precocial Describes young that are capable of moving about
and feeding on their own just a short time after birth or
hatching. Compare with altricial.

458 Glossary

Quantitative trait A trait that is influenced by several genes Ritualization Phenomenon whereby over evolutionary
acting together, rather than by any one gene acting alone. time, incipient signals become more stereotyped and
unambiguous.
Receiver-bias mechanism Hypotheses about the evolution
of communication that focus on the characteristics of the Round dance A circling dance performed by honeybees that
receiver of signals rather than those of the sender. indicates a food source is nearby.

Recessive allele The allele whose effects are usually masked Rule of thumb A term indicating that instead of following
in the heterozygous condition. precisely the behavioral strategy that would be optimal, an
animal may follow a rule of thumb that yields adequate
Reciprocal altruism One animal helps another, which in results under most circumstances.
turn helps the first animal at a later time.
Runaway selection A form of sexual selection in which a
Recognition allele An allele or group of alleles that enable positive feedback loop is created when genes for mate
an animal to recognize others with the same genotype. choice in the female become genetically linked to genes
for the preferred traits in males. In this way, runaway
Recombination The production of a new combination of selection can produce increasingly exaggerated male traits
genes in offspring that differ from either of the parental and a stronger female preference for them.
genotypes, generally through the process of crossing over
during meiosis. Satellite male A male that remains silent and associates
closely with a signaling male, ready to intercept females
Regulatory gene A gene that influences the activity of other that are attracted to the other male’s signals or resources.
genes. Regulatory genes often produce transcription factors.
Scent-marking The act of strategically placing a chemical
Reinforcement schedule In the study of learning, the fre- mark in the environment.
quency and timing with which an experimenter rewards a
particular behavior. Schreckstoff An alarm chemical produced by some species
of fish when physically attacked.
Reinforcer A stimulus that changes the probability that an
animal will repeat its behavior. Reinforcers can be positive Scientific method A procedure underlying most scientific
or negative. investigations that involves observation, formulating a
hypothesis, making predictions, experimenting to test the
Relative plasticity hypothesis The hypothesis relating predictions, and drawing conclusions. Experimentation usu-
alternative phenotypes to the different effects of steroid ally includes a control group and an experimental group that
hormones. It states that developmentally fixed alternative differ in one or very few factors (variables). New hypotheses
phenotypes (i.e., individuals are one phenotype or the may be generated from the results of experimentation.
other and remain so for life) rely on organizational effects
of steroid hormones, whereas developmentally plastic Search image The heightened ability to detect a particular
alternative phenotypes (i.e., individuals switch between target with experience.
phenotypes in response to environmental conditions) rely
on activational effects of steroid hormones. Search time The time it takes a forager to find food.
Seismic signals Signals that are encoded in the pattern of
Releaser A sign stimulus that is emitted by a member of the
same species. vibrations of the environmental substrate. These signals
can be produced through percussion on the environmental
Repolarization The return of the membrane potential to substrate, such as when rodents drum their feet on the
approximately its resting value. Repolarization of the nerve ground or insects tap the surface of water to create ripples.
cell membrane during an action potential occurs because Seismic signals can also be generated when an airborne
of the outflow of potassium ions. vocalization couples with the ground, such as when ele-
phants produce infrasonic calls.
Resource defense polygyny Form of polygyny in which Selfish herd An antipredator mechanism that considers the
males defend resources essential to female reproduction spatial arrangement of individuals within a group. In most
(e.g., nest sites or food) rather than defending females groups, centrally located animals are safer than those at the
themselves. edges. By obtaining a central position, animals can
decrease their chances of being attacked and increase the
Resource-holding potential The ability of an animal to probability that one of their more peripheral colleagues
defend a resource from competitors. will be eaten instead. This mechanism emphasizes that
although a given group appears to consist of members that
Resting potential The separation of charge across the plas- coordinate their escape efforts, it is actually composed of
ma membrane of a neuron when the neuron is not trans- selfish individuals, each trying to position as many others
mitting an action potential. It is primarily caused by the as possible between itself and the predator.
unequal distribution of sodium ions, potassium ions, and Self-shadow concealment The mechanism by which coun-
large negatively charged proteins on either side of the plas- tershading can achieve camouflage by obscuring the ven-
ma membrane. The resting potential of a neuron is about tral shadow. An alternative mechanism is background
–70 mV. matching.
Sensitive period A time during development when certain
Ribonucleic acid (RNA) A single-stranded nucleic acid that experiences have a greater influence on the characteristics
plays several roles in protein synthesis. of an individual than at other stages.
Sensitization A simple type of learning that involves an
Risk sensitivity When an animal’s decisions depend on the enhanced response to repeated stimuli.
variance, or riskiness, of an option, it is said to be risk sen-
sitive. An example of a risky option is a foraging patch that
has a fluctuating amount of food. A risk-prone animal
chooses a risky option because there is a chance it will pro-
duce a high payoff. A risk-averse animal chooses a safe
option that has a low variance.

Glossary 459

Sensorimotor stage In songbirds, phase when singing Short-term memory Memory of new information that lasts
learned song actually begins. Birds retrieve a learned song for a few seconds or minutes.
from memory and rehearse it, constantly matching their
sounds to those they memorized months earlier during the Siblicide The killing of a sibling. Siblicide is most common
sensory phase. in those species in which parents face limited resources and
deposit eggs or young in a “nursery” with limited space;
Sensory bias model A model for mate choice which states the nursery could be a uterus, a brood pouch, a parent’s
that female preferences for certain traits in males could back, a nest, or a den. Siblicide can be advantageous to par-
evolve because male traits stimulate an existing bias in the ents when more young are produced than can be raised
female’s sensory system. The original bias might relate to successfully.
feeding or avoiding predators. For example, females might
have a sensory bias to help them find food of a particular Sign stimulus A stimulus that triggers a fixed action
color; males can then exploit this bias by using the same pattern.
color to attract females during courtship.
Social learning Learning in which animals acquire informa-
Sensory drive In the study of communication, the hypothe- tion from other animals.
sis suggesting that receiver characteristics are shaped by
the environment and will thus affect signal evolution. Social monogamy An exclusive living arrangement between
one male and one female that makes no assumptions about
Sensory exploitation In communication, when a receiver mating exclusivity or biparental care. Compare with genet-
has a preexisting bias for a particular stimulus and a ic monogamy.
sender’s signal evolves to exploit that bias.
Societies Structured animal groups.
Sensory neuron A nerve cell that carries information from Sociobiology A discipline that applies the principles of
the peripheral receptors toward the central nervous system.
evolution to social behavior.
Sensory phase In songbirds, phase during which songs are Sodium-potassium pump A molecular mechanism in a
learned and stored in memory for months without
rehearsal. plasma membrane that uses cellular energy in the form of
adenosine triphosphate (ATP) to pump ions against their
Sex allocation The manner in which parents distribute concentration gradients. Typically, each pump ejects
resources between the production of sons and daughters. three sodium ions from the cell while bringing in two
Parents can bias their allocation of resources in two main potassium ions.
ways: they can either produce more offspring of one sex or Sperm competition Competition that results when two or
they can provide more (or better) resources to offspring of more males have deposited sperm in the reproductive tract
one sex. of one female.
Sperm heteromorphism The simultaneous production by a
Sex-role reversal Pattern shown by some species in which single male of at least two types of sperm in the same ejac-
parental investment by males exceeds that of females. In ulate.
these species, females often compete for access to males Spermatophore A packet used by many species to transfer
and males are selective in their choice of mates. sperm from the male to the female.
Star compass orientation The ability to use the star con-
Sexual conflict A conflict between the evolutionary interests stellations in the northern part of the sky to determine
of males and females. It takes several forms, but the two compass directions.
main ones concern mating/fertilization and parental Steroid hormones A group of closely related hormones
investment. chemically derived from cholesterol and secreted by the
gonads and adrenal glands in vertebrates. The four major
Sexual dimorphism A difference, for example in behavior or classes of steroids include progestogens, androgens, estro-
appearance, between the sexes. gens, and corticosteroids. Steroid hormones are fat-soluble,
so they move easily through the plasma membranes of tar-
Sexual imprinting Learning process through which experi- get cells into the cell interior, where they affect gene expres-
ence with parents and siblings early in life influences sexu- sion and protein synthesis. See neurosteroids for steroid
al preferences in adulthood. hormones produced by the nervous system.
Stimulus enhancement A type of social learning in which an
Sexual interference Any behavior that reduces a rival’s fit- animal is attracted to a particular object because a conspe-
ness by decreasing his mating success. cific is near it or is interacting with it.
Stotting A stiff-legged bounding display performed by many
Sexual selection A form of natural selection that occurs species of deer and antelope which appears to have several
through male competition for access to mates and female functions, including announcing to a predator that it has
choice of mates. been detected.
Strategy A behavioral option available to an animal, often
Sexy son hypothesis Hypothesis proposing that access to used in the context of mathematical models.
good genes for offspring compensates a female for the Submissive individual An animal that predictably yields to a
costs of polygyny. A female may benefit from mating with dominant animal.
an already mated male if her sons inherit the genes that
made that male attractive. Her sexy sons will presumably
provide her with many grandchildren, so the female’s life-
time reproductive success may be enhanced by choosing to
mate with a male that is attractive to many females.

Shaping In learning, changing the behavior of an animal by
rewarding increasingly closer approximations of the
desired behavior. This procedure often is used in animal
training.

460 Glossary

Subsong Vocalizations produced by young songbirds during cetaceans, bats, and rodents, produce and detect ultra-
the sensory phase that do not involve retrieval or rehearsal sounds as part of echolocation or communication systems.
of previously learned material. Ultrasound is not restricted to mammals.
Unconditioned stimulus In classical conditioning, a
Sun compass orientation The ability to use the sun as a rewarding stimulus (such as food) that is paired with an
visual cue to determine compass directions. Because the innocuous stimulus (such as a tone or light).
sun appears to move across the sky throughout the day, an Variable ratio schedule In learning, a reinforcement sched-
animal must constantly change the angle it maintains with ule in which the number of responses required to receive a
the sun to remain headed in the same compass direction. reward varies randomly. Because of the variability, the ani-
Thus, sun compass orientation is usually time compensat- mal cannot easily detect when reinforcement has stopped,
ed. so the response tends to persist. This is the reinforcement
schedule used in slot machines.
Suspension feeding Removing small food particles suspend- Vector navigation An inherited program that tells an animal
ed in the water by means of several techniques. the compass direction to head in and for how long. Certain
species of migratory birds use this type of navigation on
Synapse The site of communication between a neuron and their first migration.
another cell, such as another neuron or a muscle cell. Vomeronasal organ An accessory olfactory sense organ
found in some species of amphibians, reptiles, and mam-
Synaptic remodeling A refinement of synaptic connections mals. Located in the roof of the mouth or between the
caused by the development of new synapses and the loss of nasal cavity and the mouth, the vomeronasal organ is
others that often occurs during development. anatomically separate from other chemosensory structures,
and its neural wiring goes to brain regions other than those
Syntax In communication, a change in the order of symbols associated with the main olfactory system. Sometimes
that alters the meaning of the message. called Jacobson’s organ, the vomeronasal organ can be
stimulated by either pheromones or general odorants.
Territory As used here, a defended space. Many other defin- Waggle dance A figure-eight dance performed by honeybees
itions exist. that indicates the direction and distance of food resources.
Warning coloration The phenomenon by which conspicuous
Tool use Use of an object in order to obtain a goal. coloration advertises dangerous or unpleasant attributes.
Traditions Learned behaviors that are stable in a group over

time.
True navigation The ability to maintain or establish refer-

ence to a goal, regardless of its location, without the use of
landmarks. Sometimes called homing.
Ultrasound Sounds whose frequencies are above those audi-
ble to humans, which means frequencies greater than
about 20 kHz. Several groups of mammals, including

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