5

Evolutionary and Behavioural Aspects

of Altruism in Animal Communities:
Is There Room for Intelligence?
Zhanna Reznikova

1. The Paradox of Altruism

An individual animal can play different roles in communities in dependence of
its sex, age, relatedness, rank, and last but not least, intelligence. An indivi-
dual's path to the top of a hierarchically organised community may be paved by
highly developed individual cognitive skills. A classic example came from
Goodall's (1971) book In the shadow of man: Mike, the young chimpanzee,
gained top rank at once by making a terrible noise with empty metal jerricans
stolen from the researchers' camp.
At the same time, the upper limit of the individual's self-expression may be
specified by the specific structure of communities. There are several variants of
division of social roles, from division of labour in kin groups to the thin balance
between altruism and ‘parasitism’ within groups of genetically unrelated indi-
viduals. Task allocation in animal communities can impose restrictions on
the display of members' intelligence. For instance, rodents, termites and ants
condemned to digging or baby-sitting or suicide defending can not forage,
scout, or transfer pieces of information even if they are intelligent enough to do
this. Furthermore, subordinate members of cooperatively breeding societies
sacrifice their energy to dominating individuals serving as helpers or even as
sterile workers.
Lev Tolstoy in his novel Anna Karenina focused attention on several dra-
matic dilemmas in women's life and among them the dilemma: to give birth to chil-
dren or to stay in a family as a perpetual helper. In many novels of the 19th century
lives of members of a facultative ‘sterile cast’, governess, were described: intelli-
gent but poor members of the society often devoted their whole lives to caring for
offspring of rich ones (recall, for example, Charlotte Brontë's Jane Eyre). Indeed,
baby-sitting is one of the most costly and essential tasks in animal communities
including human ones. Some members of communities serve as helpers that are
physically able to breed, but most never will.

Evolution: Cosmic, Biological, and Social 2011 122–161

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 Zhanna Reznikova 123

To be serious, analysing the problem of division of roles in animal societies,

we face the paradox of altruism – that is, the situation in which some individu-
als subordinate their own interests and those of their immediate offspring in
order to serve the interests of a larger group beyond their offspring. That altru-
istic behaviour is possible did not always seem natural for biologists. Darwin's
followers, and among them Thomas Henry Huxley, the most enthusiastic popu-
lariser of natural selection as a factor of evolution, concentrated mainly on in-
ter- and intraspecific competition, arguing that the ‘animal world is on about
the same level as the gladiator's show’ (Huxley 1893), and thus nature is
an arena for pitiless struggle between self-interested creatures. This concerns
also human beings, although Darwin himself discussed the idea of how altruism
can evolve in human societies in The Descent of Man (1871). Kropotkin (1902)
was one of the first thinkers who countered these arguments and considered
mutual aid as a factor of evolution, in particular of human evolution. He viewed
cooperation as an ancient animal and human legacy.
In contemporary evolutionary biology, an organism is said to behave altru-
istically when its behaviour benefits other organisms, at a cost to itself.
The costs and benefits are measured in terms of reproductive fitness, or ex-
pected number of offspring. So by behaving altruistically, an organism reduces
the number of offspring it is likely to produce itself, but increases the number
that other organisms are likely to produce.
Eusociality can be considered an extreme form of altruism in animal com-
munities because sterile members of a group sacrifice the opportunity to pro-
duce their own offspring in order to help the alpha individuals to raise their
young. Evolution favours individuals whose inherited predisposition enabled
them to behave in ways that maximise their reproductive success. What induces
individuals to be engaged in behaviour that decreases their individual fitness?
Here is one of many interesting examples of biological altruism. The trade-
off between individual sacrifice and colony welfare in social insects can be
easily estimated in the cases of colony defence. Thus, in the green tree ant of
Australia (Oecophylla smaragdina) ageing workers emigrate to special ‘barrack
nests’ located at the territorial boundary of the colony. When workers from
neighbouring nests or other invaders cross the line, guards are the first to attack
and to be attacked (Fig. 1). Hölldobler and Wilson (1990) joke that a principal
difference between human beings and ants is that whereas we send our young
men to war, they send their old ladies.
124 Evolutionary and Behavioural Aspects of Altruism

Fig. 1. A major worker Oecophylla smaragdina in the aggressive

posture. Transferred from en.wikipedia; Author Tuan Cao
(en:User:Tuancao1)
Charles Darwin saw that the paradox of altruistic behaviour of animals, in par-
ticular, social insects, was dangerous to his theory of evolution by natural selec-
tion. In his Origin of Species (1859) Darwin thought that sterile workers in
a bee colony, being unable to transmit their genes, represent a special challenge
to his theory of natural selection. This is because natural selection depends on
the transmission of traits that convey selective advantages to the individuals,
and these traits have to be determined genetically (so they are heritable). If
workers are sterile, how can they transmit the ‘helping traits’ to the next gen-
eration? Even more simple cases of cooperation in animal communities which
are not based on differentiation between sterile and fertile castes can be diffi-
cult for evolutionary explanation in terms of individual fitness.
Analysis of these problems became possible on the basis of ideas of gene
dominance and fitness outlined by Ronald Fisher (1925, 1930). Haldane (1932,
1955) suggested that an individual's genes can be multiplied in a population
even if that individual never reproduces, providing its actions favour the differ-
ential survival and reproduction of collateral relatives, such as siblings, nieces
and cousins, to a sufficient degree. This hypothesis later came to be known as
kin selection, the phrase coined by Maynard Smith (1974). These ideas can be
illustrated by the following construction. Suppose an organism produces off-
spring some of which are reproducing, while others are non-reproducing but
help greatly in caring for the reproducing ones. Compare this strategy with pro-
ducing only offspring that reproduce. For an individual offspring it is advanta-
geous to reproduce itself, but since it has the genes of its parent, it will follow
the same strategy, that is, produce only reproducing offspring. Since we sup-
posed that a non-reproducing child helps greatly in caring for the others, we can
see that the average number of grandchildren will be greater if some of the off-
spring are non-reproducing. Note that here we assume that all offspring (repro-
ducing and non-reproducing) have the same genes, and have shown that it can
 Zhanna Reznikova 125

be advantageous for the population that an individual with some probability (or
better to say, under some circumstances) becomes non-reproducing. In this
construction altruism is directed at the certain groups or nearest relatives (par-
ents, siblings, etc.). However, sometimes models of less direct altruism are also
considered. A popular (although somewhat speculative) example concerns be-
haviour in populations of wild rabbits. It is assumed that some rabbits drum
with their hind legs when they see a predator instead of running immediately to
the nearest hole. Being warned by this alarm signal, other rabbits have time to
flee. Of course, this does not mean that the drumming rabbit makes a decision
to sacrifice its own life to the community (Fig. 2). It simply acts in accordance
with its inherited behavioural program. Some members of a group of rabbits
give alarm drums when they see predators (because they have a hypothetical
‘drumming gene’) but others (that lack such a gene) do not. By selfishly refus-
ing to give an alarm signal, a rabbit can reduce the chance that it will itself be
attacked, while at the same time benefiting from the alarm signals of others.
However, it is possible to show that, under certain conditions, if there are suffi-
ciently many relatives among the recipients of the altruistic behaviour, then
altruistic behaviour is promoted within the population. For details and discus-
sion of this model and accompanied ideas see Grafen (1984, 2007), Axelrod
et al. (2004), and Rice (2004).

Fig. 2. A bunny preparing to sacrifice himself. Cartoon by P. Ryabko

2. The Main Evolutionary Concepts of Altruism

in Animals
In the 1960s and 1970s two theories emerged which tried to explain evolution
of altruistic behaviour: ‘kin selection’ (or ‘inclusive fitness’) theory, due to
Hamilton (1964), and the theory of reciprocal altruism, due primarily to Triv-
ers (1971) and Maynard Smith (1974).
126 Evolutionary and Behavioural Aspects of Altruism

The main mechanism of kin selection is nepotism, that is, preferential treat-
ment for kin. Many social species including humans form nepotistic alliances to
keep the flag of family interests flying. There is much evidence that animals
behave nepotistically when facing vital problems in their life. For example, pig-
tailed macaques, when helping group members who were attacked, do so most
readily for close relatives, less readily for more distant relatives, and least read-
ily for non-relatives (Massey 1977). To do so, animals must recognise their
relatives, but there is no a strong correlation between nepotism and recognition
ability. For example, Mateo's (2004) data on closely related species of ground
squirrels support a hypothesis that kin favouritism and recognition capacities
can evolve independently, depending on variation in the costs and benefits of
nepotism for a given species. A highly nepotistic species, Spermophilus beld-
ingi, produces odours from two different glands that correlate with relatedness
(‘kin labels’). Using these odours ground squirrels make accurate discrimina-
tions among never before encountered unfamiliar kin. A closely related species
S. lateralis similarly produces kin labels and discriminates among kin, although
it shows no evidence of nepotistic behaviour.
For kin selection to occur it is not strongly necessary for individuals to rec-
ognise their kin. Returning to the example with rabbits that alarm its neighbours
by drumming, it is not that these animals must have the ability to discriminate
relatives from non-relatives, less still to calculate coefficients of relationship.
Many animals can in fact recognize their kin, often by smell, but kin selection
can operate in the absence of such an ability. If an animal behaves altruistically
towards those in its immediate vicinity, then the recipients of the altruism are
likely to be relatives, given that relatives tend to live near each other.
The ability to discriminate between kin and non-kin displays in many spe-
cies, and is due either to the innate recognition of character traits associated
with relatedness, or to the recognition of specific individuals with whom they
have grown up. Nepotism is not always clearly altruistic and does not necessar-
ily requiring genuine cognitive skills. For instance, most young plains spade-
foot toads are detritivorous and congregate with kin. Some of the tadpoles be-
come carnivorous, and such individuals live more solitarily and at least when
satiated prefer to eat non-kin than kin, reducing the damage they might other-
wise do to the survivorship of their relatives. Cannibalistic tiger salamander
larvae Ambystoma tigrinum also discriminate kin and preferentially consume
less-related individuals (Pfenning et al. 1999). Genetic analyses of numerous
fish species have shown that shoals formed by larvae often consist of closely
related kin (Krause et al. 2000). Recent experiments have shown that juvenile
zebrafish can recognise and prefer their siblings to unrelated conspecifics based
on olfactory cues (Mann et al. 2003).
Chimpanzees possibly solve much more complex problem of kin recogni-
tion. Mechanisms underlying male cooperation in chimpanzee communities are
still enigmatic (van Hooff and van Schaik 1994). Chimpanzees live in unit
 Zhanna Reznikova 127

groups, whose members form temporary parties that vary in size and composi-
tion. Females usually leave their natal groups after reaching sexual maturity
whereas males do not disperse (Ghiglieri 1984). Male chimpanzees develop
strong bonds with others in their communities being engaged in a variety of
social behaviour. Field observations together with DNA analysis showed that
such affiliations join together males of close rank and age rather than males
belonging to the same matrilines (Mitani and Watts 2005). It is worth noting
that females give birth to a single offspring only once every 5–6 years, so
brothers obviously should have an essential disparity in years. Do chimpanzees
bias their behaviour to non-kin? Although current evidence indicates that Old
World monkeys are unable to discriminate paternal relatives (Erhart et al.
1997), a recent study suggests that chimpanzees may be able to identify kin
relationships between others on the basis of facial features alone, overmatching
humans in sorting photographs by features of family relatedness (Parr and de
Waal 1999). This raises the intriguing possibility that male chimpanzees might
be able to recognise their paternal relatives (Mitani et al. 2002).
The importance of kinship for the evolution of altruism is widely accepted
today, on both theoretical and empirical grounds. However, as it has been noted
before, altruism is not always kin-directed, and there are many examples of
animals behaving altruistically towards non-relatives.
The theory of reciprocal altruism is an attempt to explain the evolution of
altruism among non-kin. Reciprocity involves the non-simultaneous exchange
of resources between unrelated individuals. The basic idea is straightforward: it
may benefit an animal to behave altruistically towards another, if there is
an expectation of the favour being returned in the future: ‘If you scratch my
back, I'll scratch yours’. In his now classic paper ‘The evolution of reciprocal
altruism’, Trivers (1971) argued that genes for cooperative and altruistic acts
might be selected if individuals differentially distribute such behaviours to
others that have already been cooperative and altruistic towards the donor.
The cost to the animal of behaving altruistically is offset by the likelihood of
this return benefit, permitting the behaviour to evolve by natural selection. This
evolutionary mechanism is termed reciprocal altruism.
A study of blood-sharing among vampire bats suggests that reciprocation
does indeed play a role in the evolution of this behaviour in addition to kinship
(Wilkinson 1984). Vampire bats Desmodus rotundus typically live in groups
composed largely of females, with a low coefficient of relatedness. It is quite
common for a vampire bat to fail to feed on a given night. This is potentially
fatal, for bats die if they stay without food for more than a couple of days. On
any given night, bats donate blood (by regurgitation) to other members of their
group who have failed to feed, thus saving them from starvation. Since vampire
bats live in small groups within large colonies and associate with each other
over long periods of time, the preconditions for reciprocal altruism – multiple
encounters and individual recognition – are likely to be met. Wilkinson's study
128 Evolutionary and Behavioural Aspects of Altruism

showed that bats tend to share food with their close associates, and are more
likely to share with those who had recently shared with them. These findings
provide a confirmation of reciprocal altruism theory.
Maynard Smith (1974, 1989) suggested that cooperative behaviour can be
an evolutionary stable strategy, that is, a strategy for which no mutant strategy
has higher fitness. His concept is based on game theory which, in turn, attempts
to model how organisms make optimal decisions when these are contingent on
what others do.
Cognitive aspects of reciprocal altruism are the source of much debate. In-
deed, cooperation based on reciprocal altruism requires certain basic cognitive
prerequisites, among which are repeated interactions, memory, and the ability
to recognise individuals. Experimental evidence that reciprocal altruism relies
on cognitive abilities, making current behaviour contingent upon a history of in-
teraction, comes from primate studies. For example, de Waal and Berger (2000)
made a pair of brown capuchins work for food by pulling bars to obtain trains
with rewards. They found that monkeys share rewards obtained by joint effort
more readily than rewards obtained individually. De Waal (1982) also demon-
strated a strong tendency to ‘pay’ for grooming by sharing food in captive
chimpanzees who based their ‘service economy’ on remembering reciprocal
exchanges.
In many examples of cooperation among nonrelated animals such as groom-
ing and food sharing behaviour in primates, or cooperative hunting in lions,
wolves, hyenas and chimpanzees, it is still under discussion whether they can
be interpreted in terms of reciprocal altruism. Several alternative concepts exist
which explain evolution of altruistic and cooperative behaviour (Clutton-Brock
and Parker 1995; Sober and Wilson 1998).
It is worth of noting that both kin- and non-kin-altruism in animal societies
are based on great individual variability which includes behavioural, cognitive
and social specialisation. Let us consider these aspects in more details.

3. A Harsh Environment for Pluralism in Animal

Societies: Behavioural and Cognitive Specialisation
Two extreme approaches to consider species-specific behaviour exist in eco-
logical and ethological studies: those that distinguish unique individualities of
members of species and those that consider a population as a whole treating
conspecific individuals as ecologically equivalent. Applying the ideas of evolu-
tionary ecology helps to find a middle course and to reveal relatively stable
fractions of populations that differ by sets of behavioural characteristics, a dif-
ferentiation that covers routine differences of individuals by sex and age.
There are at least two levels of behavioural specialisation within popula-
tions. In some species members of a population comprise distinct groups that
behave differently according to their evolutionary stable strategies. In some
cases members of these groups can be easily distinguished by certain morpho-
 Zhanna Reznikova 129

logical markers. Besides, more flexible individual specialisation can be ex-

pressed in differences in diets, techniques of getting food, forming searching
images, escaping predators, nestling and so on. Relatively stable groups can
exist in populations that differ by complexes of behavioural characteristics.
3.1. Evolutionary Stable Strategies: A Battle of Behavioural
Phenotypes
The theory of evolutionary stable strategy (or ESS) introduced by Maynard
Smith and Price in 1973 is based on the concept of a population of organisms
divided into several groups which use different strategies. A group is in a stable
state if it is disadvantageous for any individual to change its strategy. In other
terms the proportion of individuals using each strategy is optimal; natural selec-
tion suppresses any deviation from the current proportion.
Maynard Smith's best known work incorporated game theory into the study
of how natural selection acts on different kinds of behaviour. He developed
the idea of an evolutionary stable strategy as a behavioural phenotype that can-
not be invaded by a mutant strategy. A classic example is a balance between
hawks-like (aggressive) and doves-like (non-aggressive) individuals in natural
populations. Maynard Smith and Price (1973) demonstrated that both carriers
of aggressive and non-aggressive behavioural strategies can coexist comfort-
able and stable in populations for a long time, and neither aggressors nor non-
aggressors can invade the population.
Males of many species are characterised by alternative mating strategies and
thus compose a representative set of examples concerning distinct behavioural
strategies of carriers of different ESS. These strategies are based on complex
behaviour sequences and thus may give to observers the impression of deliber-
ate choice of variants.
For instance, Sinervo and Lively (1996) revealed impressive mating strategies
within populations of the side-blotched lizard (Uta stansburiana) native to Cali-
fornia. These lizards have three mating strategies: distinct types of behaviour
that constantly compete with one another in a perpetual cycle of dominance.
Carriers of different behavioural strategies are marked by morphological signs.
The researchers described the cycle of dominance in lizards in terms of ESS as
the ‘rock-paper-scissors’ game.
In the side-blotched lizards males have one of three throat colours, each one
declaring a particular strategy. Dominant, orange-throated males establish large
territories within which live several females. Orange males are ultra-dominant
and very aggressive owing to high levels of testosterone, and attack intruding
blue-throated males that typically have more modest levels of testosterone.
Blue males defend territories large enough to hold just one female. These males
spend a lot of time challenging and displaying, presumably allowing males
to assess one another. Territories of both orange and blue males are vulnerable to
infiltration by males with yellow-striped throats – known as sneakers. Sneakers
130 Evolutionary and Behavioural Aspects of Altruism

have no territory of their own to defend, and they mimic the throat colour of
receptive females. It is interesting that yellows also mimic female behaviour.
When a yellow male meets a dominant male, he pretends he is a female –
a female that is not interested in the act. In many cases, females will nip at the
male and drive him off. By co-opting the female rejection display, yellow
males use a dishonest signal to fool some territory holding males. The ruse of
yellows works only on orange males. Blues are not fooled by yellows. Blue
males root out yellow males that enter their territories. Blue males are a little
more circumspect when they engage another blue male during territory con-
tests. Attack may or may not follow as blue males very often back down against
other blue males. Indeed, neighbouring males use a series of bobs to communi-
cate their identity, and the neighbours usually part without battle.
Thus, each strategy has strengths and weaknesses and there are strong
asymmetries in contests between morphs. Trespassing yellows, with their fe-
male mimicry, can fool oranges. However, trespassing yellows are hunted
down by blue males and attacked. While oranges can easily defeat blues, they
are susceptible to the charms of yellows. In contrast, contests between like
morphs (e.g., blue vs. blue, orange vs. orange or yellow vs. yellow) are usually
more symmetric. Field data showed that the populations of each of these three
types, or morphs, of male lizard oscillate over a six-year period. When a morph
population hits a low, this particular type of lizard produces the most offspring
in the following year, helping to perpetuate the cycle. This arrangement some-
how succeeds in maintaining substantial genetic diversity while keeping
the overall population reasonably stable. This is a good example of genetically-
based control over morphotype and behavioural type development (Sinervo and
Colbert 2003).
3.2. Individual Behavioural and Cognitive Specialisation
An impressive example of behavioural specialisation came from the study on
how insects of different sizes and level of intelligence catch jumping spring-
tails, small inoffensive creatures that nevertheless are equipped with a jumping
fork appendage (furcula) attached at the end of the abdomen. The furcula is
a jumping apparatus enabling the animal to catapult itself (hence the common
name springtail), thereby changing sharply the direction of movement and to
escape attacks of predators. Reznikova and Panteleeva (2001, 2008) revealed
springtail hunters in beetles of the family Staphylinidae as well as in several
species of ants. Although beetles are taxonomically far from ants, there are
three similar groups both in the beetles and ants: (1) good hunters that catch
a jumping victim from the first spurt; (2) poor hunters that perform several
wrong spurts until they catch a springtail; and (3) no-hunters that even do not
display any interest to the victims (Fig. 3). Behavioural stereotypes were simi-
lar in ants and beetles, with one great difference: ants were able to bring their
hunting technique up to standard of the next level whereas beetles were not.
 Zhanna Reznikova 131

It turned out later that hunting behaviour in ants incorporated several variants
of development, one of them is based on maturation rather than learning, while
others include elements of social learning and different levels of flexibility.
There are three distinct types of behaviours relative to jumping victims in popu-
lations, and this is one of examples of individual behavioural specialisation.

Fig. 3a

Fig. 3b
132 Evolutionary and Behavioural Aspects of Altruism

Fig. 3c

Fig. 3d
 Zhanna Reznikova 133

Fig. 3е
Fig. 3. Springtail hunters in beetles of the family Staphylinidae
(3-a) a good hunter that catches a jumping victim from
the first spurt; (3-b) a poor hunter that performs several
wrong spurts until they catch a springtail; and (3-c)
the no-hunter that even do not display any interest to the
victim; springtail hunters in Myrmica ants: a good hunter
(3-d) and the no-hunter (3-e). Photo by S. Panteleeva
Bolnick et al. (2003) present a huge collection of examples of individual behav-
ioural and ecological specialisation for 93 species distributed across
a broad range of taxonomic groups. In many species some specimens in popula-
tions are more risk-averse than others, possibly reflecting different optimisation
rules. Besides, individuals vary in their prey-specific efficiency because of
search image formation. Individuals also vary in social status, mating strategy,
microhabitat preferences and so on. In some species individuals constitute
groups on the basis of relatively stable features. Bluegill sunfish serves as
a good example of differentiation of individuals relatively to their foraging
strategy. When a population of bluegills was experimentally introduced to
a pond, individuals quickly divided into benthic and limnetic specialists.
The remanding generalists constituted 10–30 % of the population and appeared
to have a lower intake rate of food.
There is an example of more complex individual specialisation in the oyster-
catcher Haematopus ostralegus. In this species individual birds specialise both on
prey species and on particular prey-capture techniques such as probing mud for
worms or hammering bivalves. Individuals that use bivalves tend to specialise
on different hammering or stabbing techniques that reflect intraspecific varia-
tion in prey shell morphology (Fig. 4). Individuals are limited to learning
a small repertoire of handling behaviours, while additional trade-offs are intro-
duced by functional variation in bill morphology. Subdominant and juvenile
birds are often restricted to sub-optimal diets rather than those they would
134 Evolutionary and Behavioural Aspects of Altruism

choose in the absence of interference competition (Goss-Custard et al. 1984). It

is interesting to note that a dabbling duck endemic to New Zealand was ob-
served opening bivalves in a manner similar to oystercatchers'. Despite having
the bill morphology of a typical dabbling duck, these birds were adept at this
feeding method (Moore and Battley 2003). This enables us to suggest that be-
havioural specialisation could be based on highly stereotypic behaviours re-
tained within the whole Class of animals and implemented even on the sub-
strate of somewhat irrelevant morphology.

Fig. 4a

Fig. 4b
Fig. 4. Oystercatchers Haematopus ostralegus specialise on different
hammering (4a) and stabbing (4b) techniques
 Zhanna Reznikova 135

Fig. 4c. This bird seems to find similarity between a bivalve's shell
and a sheep's ear (Copyright: Omar Bronnstrom)

Fig. 4d. Oystercatchers possess enough flexibility to catch fishes as

well (Copyright: Dirk Vorbusch)
In all cases described above behavioural specialisation within populations is
based on intricate composition of innate predisposition and individual experi-
ence of animals to choose a way of prey handling, to avert risk or not, to domi-
nate over conspecifics or to avoid conflicts, and so on. Some specimens can
possess complex behavioural patterns that allow them to learn readily within a
specific domain. This ability can be called cognitive individual specialisation
(for details see Reznikova 2007). More exactly, cognitive specialisation in ani-
mal communities is based on the inherited ability of some individuals to form
certain associations easier than others. For example, in Myrnica ants some
members of a colony learn to catch difficult-to-handle prey much easier and
earlier in the course of the ontogenetic development than others do (Reznikova
and Panteleeva 2008), and in red wood ants some members of a colony display
similar abilities concerning battles with enemies and competitors such as
136 Evolutionary and Behavioural Aspects of Altruism

ground beetles (Reznikova and Iakovlev 2008). These individuals can serve as
‘etalons’ for those members of communities that possess poorer skills and can
learn from others by means of simple forms of social learning.

4. Social Specialisation in Animal Communities

There are many gradations of social specialisation, from rigid caste division to
constitutional and (or) behavioural bias towards certain roles in groups accom-
plishing certain tasks.
4.1. Caste Division and Polyethism in Eusocial Communities
The system of caste division was firstly described for social insects. Wheeler
(1928) was the first who proposed a detailed description of caste system in so-
cial insects based on anatomy with no fewer than 30 categories. Hölldobler and
Wilson (1990) define a caste as a group that specialises to some extent on one
or more roles. Role means a set of closely linked behavioural acts (for example,
queen care). Broadly characterised, a caste is any set of a particular morpho-
logical type, age group, or physiological state (such as inseminated versus bar-
ren) that performs specialised labour in the colony. A physical caste is distin-
guished not only by behaviour but also by distinctive anatomical traits. A tem-
poral caste, in contrast, is distinguished by age. The term task is used to denote
a particular sequence of acts which serves to accomplish a specific purpose,
such as foraging or nest repair. Finally, the division of labour by the allocation
of tasks among various castes is often referred to as polyethism, a term appar-
ently first employed by Weir (1958).
A good example of division of labour in eusocial communities based on cast
differentiation is existence of soldiers, that is, a specialised cast of workers that
defend the colony against intruders (for a review see Judd 2000). Termites,
social aphids, social thrips, and some ants produce special casts of soldiers.
Some species of ants as well as eusocial shrimps and naked mole-rats show
a distinct polymorphism among workers with larger individuals specialised as
guards. In some species of bees and wasps guards differ from other colony
members only by their aggressive behaviour but not morphologically.
Let us consider several examples of animal social systems based on caste
determination and polyethism.
Eusocial insects. Eusociality is displayed in three main insect orders: Hy-
menoptera (ants, bees and wasps), Isoptera (termites) and Homoptera (aphids).
We consider here only a rough schema. There is a great diversity of species:
only ants include about 12 000 species and termites about 2 300 species. Dif-
ferent taxa have different numbers of castes, and different degrees of caste
specification.
 Zhanna Reznikova 137

Ants, bees and wasps belong to the haplodiploid group Hymenoptera

(it should be noted that Hymenoptera is a large group and the majority of Hy-
menoptera are not social). The termites, in contrast to the Hymenoptera, exhibit
diploidy. The strategy of eusociality arose once in an ancestral termite, whilst it
arose several times in the Hymenoptera. Recently, some species of aphids have
been found to be eusocial, with many separate origins of the state. This is ex-
plicable due to their partially asexual mode of reproduction. Most aphids that
are related within a colony are members of the same clone. When social aphids
form a gall (a special structure of a plant) and concentrate there, some soldiers
will not reproduce. This form of eusociality tends to be restricted to a few sol-
diers, because the sterile forms only defend and do not care for the young.
Therefore, there is less potential for the development of advanced societies.
In general, in social insects most members of a community sacrifice their
own reproductive potential to provide food and protection for the few reproduc-
tive members and their offspring. The so-called primer pheromone causes long-
term physiological changes in nestmates within a colony by controlling their
endocrine and/or reproductive systems. The primer pheromone is usually dis-
persed by only one or a few individuals (‘queens’) and may regulate sexuality
and caste expression. In contrast, chemical signals that cause immediate behav-
ioural changes in conspecifics are defined as releaser pheromones and are pro-
duced by numerous nestmates (Wilson 1971). The social organisation in colo-
nies depends on the control of the proportion of different castes, and on effi-
cient recognition and communication system.
Apis mellifera, the honey bee, has the best studied system of caste differen-
tiation. Differences in caste-specific behaviour are understood for many years
(Michener 1974), but recent molecular studies have shed new light on
the mechanisms by which it occurs. In honey bees, the primary determination is
between worker bees and gynes (future queens). Gynes are given a special diet
that activates queen specific development. Workers assume different roles in
the nest as they age, a pattern known as temporal polyethism. Young workers
stay in the nest, and as they age they replace foragers, and are replaced by
younger workers within the nest. The timing of the progression through
the tasks is not fixed. The progression can be delayed, or even reversed, if
young workers die. Over the winter, the progression is also delayed, so that
there are workers to staff the hive early in the spring.
Some ants also have age-correlated division of labour. In ants with multiple
worker castes, different morphological types assume different tasks (usually
soldiers versus workers), but within each morphological type, work is divided
in a temporal fashion.
In termites, in contrast to hymenopterans, the only adults present in colonies
are the king and the queen. This one adult caste is initially winged (alate). Ter-
mite queens typically become physogastric, due to an enormous growth of
138 Evolutionary and Behavioural Aspects of Altruism

the fat bodies and ovaries while the males remain relatively small. Indeed,
the termite queen looks awfully fat and large in comparison to workers. For
example, in the African termite, Macrotermes subhyalinus, the queen's body
becomes so swollen with eggs that she is incapable of movement. When fully
engorged, she may be 14 cm long (more than 10 times as long as a worker ter-
mite), and capable of producing up to 30 000 eggs per day.
The second true caste in termites comprises the soldiers. They are always
non-reproductive and are more sclerotised and more heavily pigmented than
workers. They also have highly sclerotised and powerful mundibles, which
make them suitable for colony defence. Soldiers cannot feed themselves and
have to be fed by workers. In some species members of the sub-cast ‘minor
soldiers’ serve as scouts and leaders for workers being more sensible than
workers to trial pheromones. Soldier termites can regulate their own numbers
by inhibiting the larval development of other soldiers. Worker termites may be
more or less differentiated, depending on the evolutionary status of the species.
In primitive species, social tasks are accomplished by unspecialised larvae or
nymphs. In the more highly developed Termitidae, and some other termites
groups, workers constitute a true caste, specialised in morphology and behaviour
and permanently excluded from the nymphal development pathway. In theory,
each nymph can be developed to an alate and leave the natal colony. In some
species the workers are dimorphic having large and small forms; in the Macro-
termitinae the larger workers are the males and the smaller workers the females.
Workers accomplish different tasks and subtasks in the colony. For example, in
the termite Hodotermes mossambicus, one set of workers climbs up grass stems,
cuts off pieces of grass, and drops them to the ground below (subtask 1) while
the second set of workers transports the material back to the nest (subtask 2). Ter-
mites' lifetime is amazingly long for insects. Sterile workers live for 2–4 years
while the primary sexuals live for at least 20 and perhaps 50 years (for details
see Eggleton 2000)
Social aphids introduce a whole new direction in the evolution of eusocial-
ity. Like termites, they are diploid, but in contrast to termites, aphids reproduce
both sexually and parthenogenetically, so they have the ability to produce ge-
netically identical individuals. In these clonal stages large colonies are formed
comprising of genetically identical individuals. Aphids are the only colonial
species that exhibit eusocial behaviour (Alexander et al. 1991). Aoki (1977)
was the first who found that the aphid, Colophina clematis, produced instars
that defend the colony from intruders. Since then many species of social aphids
have been described in the two families Pemphigidae and Hormaphididae
(Stern and Foster 1996). Social aphids produce galls, which are tough pockets
artificially induce in a plant by the aphids. All of the alates and reproductive
destined instars are normally found inside the galls. The individuals on the out-
side are the soldiers which defend the gall from any predator that would destroy
 Zhanna Reznikova 139

this nest and its contents. Stern and Foster (1996) describe several types of sol-
diers based on physical characteristic and behaviour.
Eusocial rodents. In the same way as calling termites ‘white ants’ one can
call naked mole-rats (Heterocephalus glaber) ‘mammalian termites’. These
unique eusocial mammals share many features with termites. They spend virtu-
ally their entire lives in the total darkness of underground burrows, they are
very small (7 to 8 cm long, and weigh between 25 and 40 g), and, what is
the most important, they are eusocial. Besides, like in termites, in mole-rats
high-cellulose diet is also rather hard to digest, and their stomachs and intestines
are inhabited by bacteria, fungi, and protozoa that help break down the vegetable
matter. Similarity with insects intensifised with the fact that the naked mole-rat is
virtually cold-blooded; it cannot regulate its body temperature at all and re-
quires an environment with a specific constant temperature in order to survive.
These eusocial rodents cooperate to thermoregulate. By huddling together in
large masses, they slow their rate of heat loss. They also behaviorally thermo-
regulate by basking as needed in their shallow surface tunnels, which are
warmed by the sun.
These amazing creatures are neither moles nor rats. Like rats, they are ro-
dents, but they are more closely related to porcupines and chinchillas. Hetero-
cephalus glaber is known since 1842, but only in 1981 Jarvis discovered their
eusocial organization system that is believed to be unique among mammals.
Since that, this species has been intensively studied (see Jarvis 1981; Sherman
et al. 1991; Bennett and Faulkes 2005). There are essential ecological reasons
for which naked mole-rats have broken many mammalian rules and evolved
an oddly insect-like social system. These animals are ensconced in the arid soils
of central and eastern Ethiopia, central Somalia, and Kenya, where they must
continually dig tunnels with their enlarged front teeth, in search for sporadic
food supplies and evade the deadly jaws of snakes.
Naked mole-rats live in well-organized colonies, with up to 300 members in
a group (20 to 30 is usual). A dominant female (the queen), who outweighs
the others by up to 20 g, leads a colony. The queen is the only female that
breeds, and she breeds with one to three males. When a female becomes
a queen she actually grows longer, even though she is already an adult, by in-
creasing the distance between the vertebrae in her spine. These animals are ex-
tremely long living; in captivity some mole-rats have lived to 25 years old. One
naked mole-rat queen, as the breeding females are called, produced more than
900 pups in her 12-year lifetime at a laboratory colony. The young are born
blind and weigh only about 2 g. The queen nurses them for the first month, and
then the other members of the colony feed them by faeces (again like termites)
until they are old enough to eat solid food (Fig. 5).
140 Evolutionary and Behavioural Aspects of Altruism

Fig. 5. Naked mole-rat (Heterocephalus glaber). Images from Bioi-

mages home. Copyright: 2003 Steve Baskauf http://www.cas.
vanderbilt.edu/bioimages/animals/mammalia/naked-mole-
rat.htm
The breeding female (the queen) suppresses the breeding of all the other fe-
males in the colony. She sometimes leaves her nest chamber to check on her
workers and to keep them unfertilized by pheromone control as well as by
swoops and bites thus demonstrating that they should not ‘think’ about any-
thing but digging tunnels and defending a colony from snakes and newcomers.
The worker males are also suppressed, although they do produce some sperm.
When the queen dies, several of the larger females fight, sometimes to death, to
become a queen. They can regain their fertility quickly.
The majority of workers (both males and females) spend their entire lives
working for the colony. Workers cooperate in burrowing, gathering food, and
bringing nest material to the queen and non-workers. They use their teeth to
chisel earth and to create piles of soil. There is a great deal of branching and
interconnection of tunnels, with the result that a colony's total tunnel length can
add up to 4 km. Tunnels connect nest chambers, toilet areas, and food sources.
Burrowing is the only way these animals find food, since they do not travel
above ground. Some colony members ‘farm’ succulent tubers that are formed
by many of the plant species that grow in arid areas. They generally bore
through the tuber, eating mainly the interior flesh while leaving the thin epi-
dermis intact. This behaviour may allow the plant to remain healthy for some
time, indeed even to continue growing, thereby providing a long-term food re-
source for the colony. Judd and Sherman (1996) studied captive colonies in
order to determine whether successful foragers recruit colony mates, like many
eusocial insects do. It has been revealed that individuals that found a new food
source typically give a special vocalisation on their way back to the nest, wave
the food around once they got there, and lay odour track for other nestmates to
follow.
 Zhanna Reznikova 141

Whilst most offspring become workers, some continue to grow and become
colony defenders. Their main duty is to defend the colony against predators. In
particular, rufous-beaked snakes (Rhamphiophis oxyrhynchus rostratus) are
attracted to the smell of freshly dug soil and will slither into burrows through
mole hills in search of a rodent meal. Soldier mole-rats fight back with their
teeth and attempt to block the entrance with dirt. If everything fails, a soldier
will directly attack the snake, sometimes sacrificing its own life while others
escape.
Should a breeder die, just one of defenders will become reproductive to re-
place it. They can occasionally disperse to found a new colony with an unre-
lated member of the opposite sex.
In general, caste differentiation in mole-rats bears a strong resemblance (of
course, merely superficial) with termite's one. The sterility in the working fe-
males is only temporary, and not genetic. Like in termites, there are castes of
fertilised queens and kings and unfertilised workers and soldiers, and workers
descend from ‘nymphs’, that is, under-grown members of the colony. The life
span of mole-rats is unprecedented among small rodents just like the life span
of termites is unprecedented among insects. It is possible that these long living
animals will surprise experimenters with their cognitive abilities.
Eusocial shrimps. Tiny marine coral-reef Crustacea offer a new data about
the ecology and evolution of eusociality. Colonies of the social snapping
shrimp Synalpheus regalis share several features with those of eusocial insects
and cooperatively breeding vertebrates (Duffy 1996). Synalpheus regalis inhab-
its internal canals of tropical sponges, living in colonies of up to a several hun-
dreds of individuals. Colonies consist of close kin groups containing adults of
at least two generations which cooperatively defend the host sponge using their
large and distinctive snapping claws, and in which invariably only a single fe-
male breeds. Irreversible caste differentiation is governed by the queen that
typically sheds her large snapping claw and re-grows a second minor-form
chela, rendering her morphologically unique among the members of the colony.
It is still not completely known how the queen accomplishes social control over
sexual maturation of other colony members. Both genetic data and colony
structure confirm that many offspring remain in the natal sponge through adult-
hood. Colonies consist largely of full-sib offspring of a single breeding pair
which ‘reigns’ for most or all of the colony's life. In captive colonies research-
ers have regularly observed a large male in association with the queen behaving
aggressively with other large males approach her. The inference of monogamy
from genetic data suggests that the queen associates with a single male for
a prolonged period. There is a strong competition for suitable nest site and
a shrimp attempting to disperse and breed on their own would have low suc-
cess. Colony members discriminate between nestmates and others in their ag-
gressive behaviour. Laboratory experiments revealed behavioural division of
142 Evolutionary and Behavioural Aspects of Altruism

labour within colonies. Large males shoulder the burden of defence, leaving
small juveniles free to feed and grow, and the queen free to feed and reproduce
(Fig. 6). Such size- and age-related polyethism in shrimps has many similarities
with poyethism in social insects (Duffy et al. 2002).

Fig. 6. Defending snapping shrimp. Photograph by A. Bray. Courtesy

of A. Bray
Considering intellectual potential of social shrimps, Duffy (2003) refers to
Darwin's (1871) note that ‘the mental powers of the Crustacea are probably
higher than might be expected’. Social shrimps demonstrate coordinated behav-
iour. For example, they pick up dead colony members and push out of their
sponge dwelling. Recent experiments suggested coordinated snapping, during
which a sentinel shrimp reacts to danger by recruiting other colony members to
snap intruders. The phenomenon of ‘mass snapping’ begins by rhythmic snap-
ping of one individual, following by rapid recruitment of many others. The ini-
tial one-to-one confrontation elicited a snap response from the defender. Col-
ony members joined in with a cacophony of snapping thus providing an un-
equivocal signal that the sponge is already colonized. This distinctive behaviour
is the first evidence for coordinated communication in the social shrimp and
represents yet another remarkable convergence between social shrimps, insects
and vertebrates (Tóth and Duffy 2005).
Summarising the data on caste division of labour within communities of
eusocial organisms we have to admit that the correlation between cognitive and
morphological specialisation in these animals is not yet completely described.
Even in ants and bees which have been intensively studied for more than hun-
dred years, it remains unclear what effect does the caste determination has on
their intelligence. Further we will consider a more gentle system of division of
labour in animal societies that perhaps leave more room for intelligence.
 Zhanna Reznikova 143

4.2. Division of Labour in Cooperative Breeders

Eusociality can be considered an extreme of cooperative breeding systems be-
ing based on irreversible caste determination. However, many vertebrate spe-
cies possess more flexible social systems which are based on facultative divi-
sion of labour and temporal limits on breeding for some members of communi-
ties. In cooperative breeding vertebrates, a dominant pair usually produces
the majority of the offspring, whereas the cost of caring for offspring is shared
by non-breeding subordinates. In certain cooperative breeding animals one or
a few dominant females are the only capable of breeding; the subordinates do
not have the proper hormone levels to be fertile although they are physiologi-
cally equipped for the task.
There is still a great controversy in literature about to what extent coopera-
tive breeding can be explained in terms of kin selection theory. Results so far
are mixed: while some studies have produced evidence supporting the associa-
tion between kinship and contributions for cooperative activities, others have
found no consistent association between contributions to helping behaviour and
variation in relatedness (for reviews see Clutton-Brock et al. 2002).
Cognitive aspects of cooperative breeding are intriguing and have not been
studied enough. Serving as helpers for the ‘royal family’ young animals gain
experience that can be useful for them in future when they establish their own
families. Nevertheless, in many cases helpers have no chance to have their
own offspring. Somehow or other, cooperative breeding system enables helpers
to sacrifice their intelligence for other members of the community. It is possible
that helping individuals accomplish a wider variety of tasks and under more
risky circumstances than those who have the opportunity to raise their young
being given every support by helpers. Several examples will give us an impres-
sion of how division of labour occurs within communities which are based on
communal breeding.
In birds about 3 percent (approximately 300 species) of species are known
as cooperative breeders. Helpers (also called auxiliaries) at the nest were first
described by Skutch in 1935. It was not until the mid-1960s, however, with
the advent of modern behavioural ecology, that widespread attention began to
focus on cooperatively breeding species (Emlen 1995).
Cooperative systems often appear to arise when environmental constraints
force birds into breeding groups because the opportunities for younger birds to
breed independently are severely limited. Limitations may include a shortage of
territory openings, a shortage of sexual partners, and unpredictable availability
of resources. That cooperative breeding is a common strategy in arid and semi-
arid portions of Africa and Australia lends strong support to this line of reason-
ing. For some species the role of ecology is not completely clear (Arnold and
Owens 1999).
Cooperative breeding may be viewed primarily as a means by which young
adults put off the start of their own breeding in order to maximize their lifetime
144 Evolutionary and Behavioural Aspects of Altruism

reproductive output, and in the process occasionally promote genes identical

with their own via kin selection. There are two types of cooperative arrange-
ments: those in which mature nonbreeders help protect and rear the young, but
are not parents of any of them, and those where there is some degree of shared
parentage of offspring. Cooperative breeders may exhibit shared maternity,
shared paternity, or both.
The best-studied North American cooperative breeders, the Scrub-Jay,
Gray-breasted (Mexican) Jay, Groove-billed Ani, and Acorn Woodpecker pro-
vide good examples of communal breeding (see Ehrlich et al. 1988). Scrub-
Jays in Florida reside in permanent, group-defended territories. Woolfenden
and Fitzpatrick (1984) have found that groups consist of a permanently bonded
monogamous pair and one to six helpers, generally the pair's offspring of previ-
ous seasons. About half the territories are occupied by pairs without helpers,
and most other pairs have only one or two helpers. Although pairing and breed-
ing can occur after one year spent as a helper, birds often spend several years as
non-breeding auxiliaries. Males may remain in this subsidiary role for up to six
years; females generally disperse and pair after one or two years of helping.
Helpers participate in all non-sexual activities except nest construction, egg
lying, and incubation. Pairs with helpers are more successful – they fledge one
and a half times younger than pairs without helpers. Like the Florida Scrub-
Jays, the closely related Gray-breasted Jays live in permanent group-defended
territories, and breeding adults are monogamous. Brown (1974) has shown that
the cooperative system of this species is more complex than that of its south-
eastern relative in several ways. Gray-breasted Jay groups are much larger,
ranging from 8 to 18 individuals; thus, they usually include offspring from
more than just the preceding year. Within each group, two and sometimes three
breeding pairs nest separately but simultaneously each season, and some inter-
ference among them often occurs. Interference usually involves theft of nest-
lining materials, but can include tossing of eggs from nests by females of rival
nests. Although the laying female does all the incubating, she is fed on the nest
both by her mate and by auxiliaries. Nestlings receive more than half of their
feeding from auxiliaries.
Acorn Woodpecker group of communal breeders is composed from up to
15 members whose territories are based on the defence and maintenance of grana-
ries in which they store acorns (Koenig and Dickinson 2004). Groups consist
largely of siblings, their cousins, and their parents. Some of the sexually mature
birds are non-breeding helpers. Within each group, up to four males may mate
with one (or occasionally two) females, and all eggs are laid in a single nest. Thus
paternity and sometimes maternity of the communal clutch is shared.
In mammals more than 100 species have been described as cooperative
breeders, and among them are cooperative carnivorous, mongooses (meerkats,
dwarf mongooses), primates (marmosets and tamarins), as well as several spe-
 Zhanna Reznikova 145

cies of rodents and shrews. As it was noted before, some rodent species possess
facultative communality in dependence of their habitat and many ecological
factors.
The painted hunting dog (African wild dog) Lycaon pictus provides a good
example of obligate cooperative breeding. These dogs live in packs of up to
20 adults, in which most of the time only the alpha pair breeds. The remaining
adults are reproductively suppressed and help to raise the pups; they must wait
to breed until their circumstances improve, either through the death of a higher-
ranking female or by finding a mate with an unoccupied territory (Fuller et al.
1992). Baby sitting is a costly task and this includes: watching pups to prevent
loss, alerting them to danger (lions, hyenas), protecting them from smaller
predators or alien dogs, and moving them under cover in heavy rain. Other
members of the pack are also involved in caring for common babies: they feed
pups with regurgitated meat when return from successful hunting. Baby sitting
is not an obligatory load for pack members, as they can choose between hunt-
ing and guarding young. Researchers observed situations where a dog returned
to a den to baby-sit after encountering a predator close by (Malcolm and Mar-
ten 1982). At the same time, Lycaon hunt cooperatively and baby sitting draws
a member of a pack away from hunting where both efficiency and the risk to
lose prey for kleptoparasites depend on the size of the party (Gorman et al.
1998). It is worth to note that in contrast to queens in eusocial communities that
are specialised baby-machines, the breeding female in wild dogs, as in other
cooperative carnivorous, is often an experienced hunter, and her presence in
the hunting pack may increase efficiency of enterprise. Besides, there is
a threshold for the group size to survive. Smaller packs need to hunt more often
to feed their pups, especially when using a pup guard (Courchamp et al. 2002).
Another impressing example of obligatory communal breeding in mammals
comes from small arboreal monkeys, marmosets and tamarins of the family
Callitrichidae endemic to the Northern half of South America. Within the fam-
ily, cooperative breeding strategies are widespread and virtually all species are
characterised by small territorial groups of approximately 4–15 individuals,
where reproduction is monopolised by one or a small number of dominant indi-
viduals. Typically one dominant female breeds, normally producing dyzigotic
twins. An important role of helpers in the group is to assist in the care of
the dominant female's offspring. This is principally by sharing the burden of
carrying the relatively bulky twin infants around their arboreal habitat. Each
group member helps rear the young, which involves food sharing, caring and
defence against predators (Snowdon and Soini 1988).
Life history of Callitrichidae can serve as an example of cooperative breed-
ing in groups consisting both of related and unrelated individuals. Helping be-
haviour in these primates is thus possibly governed by mechanisms of recipro-
cal rather than kin altruism. This raises a question to what extend cognitive
146 Evolutionary and Behavioural Aspects of Altruism

abilities allow these small primates to calculate reciprocity in their groups.

Hauser et al. (2003) have conducted experiments on food sharing within groups
of cotton-top tamarins (Saguinus oedipus) concentrating on psychological
mechanisms of reciprocity. The design of experiments was based on animals'
tool-using abilities. The apparatus consisted of a tray with an inverted L-shaped
tool. When food was on the actor's side, pulling the tool's stem brought the food
within rich. Similarly with experimental paradigm used in many experiments
on social learning (for details see Reznikova 2007) where researchers trained
several animals to be the demonstrators of new skills, here again stooge ‘altru-
ists’ and ‘defectors’ were specially trained to pull pieces of food to their part-
ners or to themselves. Results clearly showed that tamarins discriminate be-
tween altruistic and selfish actions, identify and recall conscpecifics by their
cooperativeness and give more food to those who give food back. Special series
of experiments also demonstrated that tamarins give food to genetically unre-
lated conspecifics even though they obtain no immediate benefit from doing so.
Tamarins therefore have the psychological capacity for reciprocally mediated
altruism.
The ability to estimate partner's cooperativeness and remember the history
of inter-individual relationships is particularly important for those communal
breeders that incorporate both kin and non-kin into their communities, and
whose altruistic acts are costly. This is well illustrated by experiments of Clut-
ton Brock et al. (2000) on individual contributions to babysitting in a coopera-
tive mongoose, Suricata suricatta.
Meerkats (suricates) are desert-adapted animals living in groups of 3–25
animals that typically include a dominant female that is responsible for more
than 75 % of all breeding attempts, a dominant male that fathers most of
the offspring born in the group and a number of helpers of both sexes. A domi-
nate female controls the presence of subordinate adult females in the group. Dur-
ing the first month of pup's life babysitters usually remain at the burrow with
young for a full day while the rest of the group is foraging and feed little or not at
all during their period of babysitting. Clutton-Brock et al. (2000) have shown
how costly babysitting is: helpers suffer substantial weight losses. It is important
that large differences in contribution exist between helpers. These differences are
correlated with such characteristics of group members as age, sex, and weight,
but, surprisingly, not with their kinship to the young raising. In field experi-
ments researchers regularly provided some group members with food (boiled
eggs) matching them with controls of the same sex and age. It turned out that
feeding essentially increased contribution of helpers to babysitting. So a regular
salary may increase and equalise individual contributions of co-operators.
However, in natural situations meerkats cannot rely on donations from above,
they rather depend on their ability to distinguish between more and less consci-
entious cooperators (Fig. 7).
 Zhanna Reznikova 147

Fig. 7. A daily procedure of feeding and weighing meerkats.

Photograph by L. Hollén. Courtesy of L. Hollén
4.3. Teams in Animal Societies
In group living animals division of labour is sometimes based on coordinated
activities of group members. In relatively rare cases individuals form groups in
which the members stay together for extended periods to accomplish a certain
task. Such groups are called teams or cliques (Hölldobler and Wilson 1990;
Anderson and Franks 2001).
For example, when working together to dig tunnels, naked mole-rats line up
nose-to-tail and operate like a conveyor belt. A digger mole-rat at the front uses its
teeth to break through new soil. Behind the digger, sweepers use their feet and
the fine hairs between their toes to whisk the dirt backwards. At the back of the line
a trailing member of the group kicks the dirt up onto the surface of the ground, cre-
ating a distinctive volcano-shaped mole hill. One of folk names of naked mole-
rats is ‘sand puppies’. There are several other creatures that join efforts of group
members to survive in the running sand. Desert ants Cataglyphis pallida dem-
onstrate the same manner of coordinated working digging tunnels like a con-
veyor belt.
There are several examples of hunting teams in vertebrates. Usually indi-
viduals coordinate efforts so that one or more individuals chase the prey, or
flush it from hiding, while others head off its escape. For instance, in chimpan-
zees (Pan troglodytes), some group members chase and surround the prey (usu-
ally juvenile baboons) forcing it to climb a tree while at the same time other
chimpanzees climb adjacent trees ready to capture the prey when it attempts to
leap across to escape. In African wild dogs (Lycaon pictus) some individuals
chase the prey, and can change leaders during the chase (van Lawick-Goodall,
Hugo and Jane 1970).
148 Evolutionary and Behavioural Aspects of Altruism

The most organised teams in animal societies are based on discrete division
of labour that may be called ‘professional specialisation’. Stander (1992) has
shown that lion teams can be particularly organized in that an individual will
tend to stick to a particular position (subtask) during the hunting on successive
hunts. That is, some lions can be classed as ‘wingers’, individuals who always
tend to go around the prey and approach it from the front or from the side,
while others are better classified as ‘centres’, individuals who remain chasing
directly behind the prey. Perhaps the most organized hunting teams in verte-
brates occur in Galapagos and Harris' Hawks (Faaborg et al. 1995). Hawks hunt
cooperatively with several birds simultaneously swooping on their prey on such
animals as wood rats, jackrabbits and other birds. However, if the prey item
finds cover, some birds land and surround it, while one or two hawks will walk
or fly into the vegetation to kill the prey. Once the prey is killed, all the birds
feed together on the prey.
Until recently, the existence of teams within insect colonies, possibly based
on individual identification, has not been known. According to Hölldobler and
Wilson (1990), ants do not appear to recognise each other as individuals. In-
deed, their classificatory ability is limited to recognition of nestmates, different
castes such as majors and minors, the various growth stages among immature
nestmates, and possibly also kin groups within the colony. There are, however,
several examples showing elements of team task distribution. In swarm-raiding
army ants, large prey items are transported by the structured teams which in-
clude members of different castes (Franks 1986). In the desert ant Pheidole
pallidula Ruzsky, minor workers pin down intruding ants and later major
workers arrive to decapitate the intruders (Detrain and Deneubourg 1997).
Robson and Traniello (2002) found complex relations between discovering and
foraging individuals in group retrieving ant species; removal of the discovering
ant during the process of recruitment led to dissolution of the retrieval group.
The question of constant membership and individual recognition within
group of workers in ant colonies has been so far obscure. Reznikova and Ry-
abko's (1994, 2003) findings on teams in ants are connected with the discovery
of the existence of complex communicative system in group retrieving ant spe-
cies by means of the special maze called ‘binary tree’ (for details see Ryabko
and Reznikova 2009). Such communication system is based on scouts-foragers
informative contacts where each scout transfers messages to a small (5 animals
in average) constant group of foragers and does not pass the information to
other groups. The ants thus work as co-ordinated groups which may be called
teams. Does this necessarily mean that they recognise each other as individu-
als? Indeed, it is possible that the animals presume on recognition of specialists'
roles rather than their personal traits.
 Zhanna Reznikova 149

Donald Michie (personal communication) has referred to his experience as

a Rugby player. Being a scrum half, he was always confident on his ability to
spot his opposite number (that is, another scrum half) when meeting an oppos-
ing team socially before the game. To be adapted to the scrum half's specialist
role, one must typically be small, resilient, agile, not necessarily a fast runner.
The only other typically agile team member is the fly half, but he has also to be
a fast accelerator and need not be resilient. A year later he might still recognise
one of that same team's forwards, for example, but not remember the face of
the scrum half.
One can find it hard to say that ants are able to recognise each other person-
ally. That a scout can distinguish members of its own team from members of
another team is not the same thing as individual recognition. Continuing the use
of the metaphor from football, one can imagine a team manager who might be
able to distinguish players of his own team from those of a different team (for
example by the patterns of their shirts), and this is yet not to distinguish same-
team players one from another.
We have not yet distinguished reliable behavioural signs in ants indicating
personal recognition like the well-knowing ‘eyebrow flash’ in humans (see
Eibl-Eibesfeldt 1989); neither are we able to train ants for distinguishing be-
tween pictures of different individuals like in Kendrick et al.'s (2001) experi-
ments with sheep (for details see Reznikova 2007). Nevertheless, we can be
confident on at least circumstantial evidences that group-retrieving ant species
possess personalised teams as functional structures within their colonies.
The first evidence comes from ontogenetic studies. Reznikova and Nov-
gorodova (1998) observed the ontogenetic trajectories of 80 newly hatched
F. sanguinea ants in one of laboratory colonies and watched the processes of
shaping of teams. There were 16 working teams in that colony which mastered
the ‘binary tree’ maze. From 80 individually marked naive ants, 17 entered
7 different working teams, 1 to 4 individuals in each. Only 3 became scouts,
2 of them starting as foragers joining 2 different teams and 1 starting as a scout
at once. The 3 new groups were composed of workers of different ages, mainly
from reserve ones. The age at which the ants were capable to take part in
the working groups as foragers ranged from 18 to 30 days, and the ants could
become scouts at the age of 28 to 36 days. Constancy of membership was ex-
amined in two colonies of F. sanguinea and F. polyctena. In a separate experi-
ment researchers isolated all team members from 9 scouts. 3 scouts appeared to
mobilize their previous acquaintances and attract new foragers, 4 scouts were
working solely, and 2 ceased to appear on the arenas. In another experiment we
removed scouts from 5 F. polyctena teams. It was possible to see foragers from
those groups on the arenas without their scouts. 15 times different foragers
150 Evolutionary and Behavioural Aspects of Altruism

were placed on the trough with the food, but after their return to home they
contacted other ants only rarely and occasionally. These results suggest that
formation of teams in group retrieving ants is a complex process which is based
on extensible relations and possibly include individual identification.
Another evidence of existence of teams in ants is based on division of la-
bour within groups of aphid tenders discovered in red wood ants. It is well
known that ants look after symbiotic aphids, protect them from adverse condi-
tions, and in return, ants ‘milk’ the aphids, whose sweet excretions are one of
the main sources of carbohydrate for adult ants. In an ant family, there is
a group of ants dealing with aphids (aphid-milkers), which has a constant com-
position. Reznikova and Novgorodova (1998) were the first to describe a sys-
tem of intricate division of labour (professional specialisation) in aphid milkers:
‘shepherds’ only look after aphids and milk them, ‘guards’ only guard the aphid
colony and protect them from external factors, ‘transit’ ants transfer the food to
the nest, and ‘scouts’ search for the new colonies (see Fig. 8). This professional
specialisation increases the efficiency of ant-aphid mutualistic relations. When
ants were experimentally forced to change their roles, much food was lost.
The ants belonging to the same aphid tending group, distinguish at least 2–3 shep-
herds from 2–3 guards within this group. Such professional specialisation was
only found in the same species that exhibited the complex communication sys-
tem in experiments of Reznikova and Ryabko (1994, 2003).

Fig. 8a. ‘Shepherd’ milking aphids and a ‘guard’ (with open mandi-
bles) protecting an aphid colony
 Zhanna Reznikova 151

Fig. 8b. ‘Transit’ ant is receiving the food from a shepherd in order
to transport it to the nest; a ‘guard’ is also present here.
Photographs by T. Novgorodova

5. Social Intelligence in Animals

Since the second part of the twentieth century a growing body of field data
about wild social life have led researchers to the idea that social animals should
display advanced cognitive abilities within specific domains related to social
living and that intelligence is not a monolithic functional entity but includes
a number of specialised mental abilities to cope with life in complex and
changeable social environment. Thus, to the primary components of intelli-
gence, such as the ability for flexible problem solving and the ability to cope
with novel situations, we can add the ability for solving social problems.
According to the social intelligence hypothesis, which was first articulated
by Jolly (1966) and Humphrey (1976), complex social interactions (including
cooperation, competition, manipulation, and deception) can occur when ani-
mals live in large and stable social groups. After spending three months with
Dian Fossey and her gorillas in Rwanda (see Fossey 1983), Humphrey wrote
a review essay in 1976 titled ‘The Social Function of Intellect’ on the evolution
of cognitive skills. He argued that primate and human intelligence is an adapta-
tion to social problem-solving, well suited to forward planning in social interac-
tion but less suited to non-social domains. These subforms of intelligence as-
sumed the name ‘Machiavellian intelligence’ after the 16th century Italian poli-
tician and author, Niccolò Machiavelli. It provides individuals or groups with
a means of social manipulation in order to attain particular goals. In 1532 Ma-
chiavelli published his book The Prince. Giving somewhat cynical recommen-
dations to an aspiring prince, he was prescient in his realisation that an indivi-
152 Evolutionary and Behavioural Aspects of Altruism

dual's success is often most effectively promoted by seemingly altruistic, hon-

est, and prosocial behaviour. According to Machiavelli's real politic, a popular
leader had to give the impression of being sincere, trustworthy, and merciful.
To retain his power, however, a prince can set himself above all moral rules
and use cunning, lies, and force. Skill in deception and maintaining alliances
are two of the prince's most important properties. ‘Machiavellian intelligence’
seemed an appropriate metaphor that inspired primatologists to explicit com-
parison between the animal social strategies and some of the advice offered five
centuries earlier.
De Waal, in his book Chimpanzee Politics (1982), describes how clever
high-ranking chimpanzees are at manipulating others. Byrne and Whiten (1988)
propose that the ability to use other individuals as tools, manipulating the social
environment in order to meet preconceived goals, is an important factor in
the evolution of primate intelligence. In order to compete successfully within
groups, apes and monkeys have to recognise who outranks whom, who is
closely bonded to whom, and who is likely to be allied to whom.
Skilfulness in navigating social landscape is based on the advanced ability
that seems to be unique to primates, that is the ability to keep track of how
other animals relate to each other and thus to recognise the close relationships
that exist among individuals (Cheney and Seyfarth 2003; Kitchen et al. 2005).
Experimental evidence for animals' ability for tracking social and kin rela-
tions came from the laboratory study performed by Dasser (1988) on captive
longtail macaques Macaca fascicularis. The monkeys were shown a pair of
slides of members of the group, and their task was to identify another pair
of photographs which ‘matched’ the first one. The first pair could be, for exam-
ple, a mother and a daughter, two sisters, or two unrelated individuals. The ma-
caques quickly learned to identify the right kinship patterns. The experiment
indicates that they do not just recognise their own offspring and siblings, but
that they also keep track of other individuals' kinship relations. For example, in
one test, Dasser trained a female to choose between slides of one mother –
offspring pair and slides of two unrelated individuals. Having been trained to
respond to one mother – offspring pair, the monkey was then tested with
14 novel slides of different mothers and offspring paired with an equal number
of novel pairs of unrelated animals. In all tests, she correctly selected
the mother – offspring pairs. Dasser suggests that the monkeys can use the ab-
stract category to classify pairs of individuals that was analogous to our concept
of ‘mother – child affiliation’.
The experiments of Parr and de Waal (1999) demonstrated chimpanzees as
being able to judge about mother – offspring relationships by comparing pairs
of photographs of mothers and sons and mothers and daughters. Surprisingly,
 Zhanna Reznikova 153

within mother – offspring category, the chimpanzees could find similarities

between mothers and sons much better than between mothers and daughters.
The authors suggest that facial similarities are more noticeable to chimpanzees
in males in view of their male philopatric society and the tendency towards
‘political’ alliances in which males incur great risk on behalf of other males
(de Waal 1982). Phenotypic matching might assist the recognition of subsets of
related males who tend to support each other.
A number of naturalistic studies have suggested that monkeys recognise
the close associates of other group members. For example, play-back experi-
ments using the contact calls of rhesus macaques have demonstrated that fe-
males not only distinguish the identities of different signallers but also catego-
rise signallers according to matrilineal kinship (Rendall et al. 1996). In play-
back experiments with vervet monkeys Cheney and Seyfarth (1990) found that
when females were played the scream of an unrelated juvenile, they were more
likely to look towards that juvenile's mother than towards other females. Also
Cheney and Seyfarth (1990, 2003) argue that vervets can perform vendettas:
they prefer to attack relatives of the individuals who have attacked their own
relatives.
Knowledge of the relationship between other group members, the so-called
third-party relationships, play a particular important role in formation of coali-
tions, helping individuals to predict who will support or intervene against them
when they are fighting with particular opponents, and to assess which potential
allies will be effective in coalitions against their opponents (Tomasello and Call
1997). There is much evidence that monkeys and apes cultivate relationships
with powerful supporters. Silk (1999) has demonstrated that male bonnet ma-
caques put their knowledge of their own relationships with other males and
their knowledge of relationships among other males to good use when they
recruit coalitions. By selectively soliciting males that most frequently supported
them and animals that outranked them and their opponents, males focused their
recruitment efforts on the candidates that were most likely to intervene on their
behalf and those whose support was most likely to be effective in defeating
their opponents. They avoided soliciting top-ranking males that were more
loyal to their opponents than to themselves. For this they have to have some
knowledge of the pattering of support amongst other individuals, another kind
of third-party knowledge.
Although not so well studied as monkeys and apes, several non primate
species also show the ability to acquire information about many different indi-
vidual social relationships. Male dolphins form dyadic and triadic alliances
when competing over access to females, and allies with the greatest degrees of
partner fidelity are most successful (Connor et al. 1992). Analysis of patterns
154 Evolutionary and Behavioural Aspects of Altruism

of alliance formation in hyenas suggests that they do monitor other individuals'

interactions and extrapolate information about other animals' relative ranks
from their observations. During competitive interactions over meat, hyenas
often solicit support from other, uninvolved individuals. When choosing to join
ongoing skirmishes, hyenas that are dominant to both of the contestants almost
always support the more dominant of the two individuals. When the ally is in-
termediate in rank between the two opponents, it inevitably supports the domi-
nant individual. These data enable researchers to suggest that hyenas are able to
infer transitive rank relations among other group members. However, unlike
monkeys, they showed no evidence for recognising third-party relationships
(Engh et al. 2005).

Conclusion
Altruistic behaviour of animals is still enigmatic for evolutionary biologists in
many aspects, although a great deal of data have been analysed and rational
concepts have been developed such as the theory of inclusive fitness and
the theory of reciprocal altruism. Altruistic behaviour in animal societies is based,
to a greater or lesser extent, on the division of roles between individuals in de-
pendence of their behavioural, cognitive and social specialisation. There are
many gradations of social specialisation, from rigid caste division to constitu-
tional and (or) behavioural bias towards certain roles in groups accomplishing
certain tasks. In some situations behavioural, cognitive and social specialisation
can be congruent; maybe this is the formula for happiness in animal societies.
To navigate social landscape, animals need a surplus of intelligence that
overcomes the immediate survival needs, such as eating, avoiding predators,
feeding offspring, etc., and this surplus intelligence might have been advanta-
geous for social manipulation. There is much work to be done to evaluate
the role of intelligence in maintaining cooperative behaviour. We can assume
that cooperation that is based on reciprocal altruism requires more advanced
cognitive skills than altruism towards kin because reciprocity demands remem-
bering and discounting levels of cooperativeness among individuals. Specific
cognitive adaptations can be expected in some species such as specific concen-
tration of attention and calculation of mutual aids.
However, we should not expect to find a linear correlation between social
complexity and levels of intelligence in non-human species. Although experi-
ments based on pair comparison of intellectual abilities in group-living and
solitary species have brought some positive results, we should take into consid-
eration that animals that live in solitary in complex and risky environment relay
on their own memory and learning skills and may enjoy freedom of restrictions
 Zhanna Reznikova 155

and obligations imposed upon them by their possibly narrow roles within
a community.

Acknowledgements
The work is supported by the Russian Fund for Basic Research (08-04-00489).

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 Zhanna Reznikova 161

Abstract
Altruistic behaviour of animals is still enigmatic for evolutionary biologists in many
aspects, although a great deal of data have been analysed and rational concepts have
been developed such as the theory of inclusive fitness and the theory of reciprocal altru-
ism. Altruistic behaviour in animal societies is based, to a greater or lesser extent, on
the division of roles between individuals in dependence of their behavioural, cognitive
and social specialisation. It is a challenging problem to find room for intelligence within
the framework of social specialisation in animal communities. In this review characteris-
tics of different levels of sociality are considered, and the role of flexibility of individual
behaviour in functional structure of animal communities is analysed. In some situations
behavioural, cognitive and social specialisation can be congruent; maybe this is the for-
mula for happiness in animal societies.