Dominance Behaviour: Evolution and Endocrinology

Contents Page
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Page
1. Introduction

3-4

2. Dominance Hierarchy
2.1 Invertebrates

4-5

2.2 Vertebrates

5-7

2.3 Evolution

7-9

3. Endocrinology of dominance behaviour

3.1 Testosterone

3.2 Glucocorticoids

9-10

3.3 Juvenile hormone

10

References

11-12

1. Introduction

Dominance can be defined as an attribute emerging from repeated fighting

interactions between two individuals where one of the individuals regularly wins the
contests, being therefore characterized as dominant, and the other one
demonstrates a yielding response, instead of retaliation, being characterized as
subordinate (Drews, 1993).
Dominance status and dominance rank are different aspects of dominance: The first
implies in a relationship between two individuals, where their attributes are being
compared one to the other, while the second refers to the position of an individual
within a group hierarchy, thus having a connection to group composition (Drews,
1993). These terms, however, may be viewed simply as a descriptive tool used by
scientists to measure and classify behaviour, not necessarily portraying the real
complexity of the phenomenon (Drews, 1993), it can also be regarded as a useful
approximation of an animals ability to mould the behaviour of others for personal
benefits (Smuts, 1981).

Likewise, dominance can be viewed as an inevitable

outcome of costs and benefits dynamics inherent to competitive interactions (Drews,

1993), or a propriety of the communication system, since subordinate individuals
avoid fights that could bring them injures or even death when signalizing their
submission (Drews, 1993).
Although most of the times dominance relationships are determined based on oneto-one fighting interactions between two individuals, in some taxon, for example in
some primates, the dominance relationships might be determined by interactions
between more than two animals (Walters, 1980). This way, basic rank is the term
used to define dominance relationships determined only by the interactions between
two individuals, and dependent rank the one for dominance relationships influenced
by action of other individuals (Dewsbury, 1982). Hierarchies can be linear, where you
have a well stablished rank order, A>B>C, or non-linear, where you have a circular
and irregular rank order, A>B>C>A (Chierati et al, 2009). The dominance rank can be
affected by age, weight, sex or territory of the individuals involved (Chiarati et al,
2009).
There are several procedures to determine an individuals dominance rank and the
hierarchy structure of a group, but the two most used are: group observations and
staged paired encounters (Dewsbury, 1982). In the first the groups structure remains
unchanged, and encounters are scored, sometimes resources may be limited, while
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the second is characterized by a pair of individuals putted together, generally with

limited resources, where their fighting interactions and outcomes, which and how
many times one wins or loses, are recorded (Dewsbury, 1982).
Understanding the reproduction benefits brought by dominance can shed some light
in the evolution of social behaviour (Dewsbury, 1982).

2. Dominance Hierarchy

2.1 Invertebrates
Dominance hierarchy was once believed to be a complex behaviour restricted to
highly social vertebrates (Pardi, 1996). However, dominance behaviour has already
been observed in a range of insects, including, among others, social wasps (Jandt et
al, 2014). Polistes is a gender of social wasps that generally builds small nests and
has a linear dominance hierarchy (Jandt et al, 2014). The colony cycle starts with the
founding phase, where its already possible to observe dominance behaviour among
females that are founding a nest together, known as foundresses, although they
have the option of actually building a nest alone as well (Jandt et al, 2014).
Foundresses can also challenge already stabilized dominance hierarchies and try to
usurp a previously existing nest (Nonacs and Reeve, 1995). The first generation of
the females offspring generally turns out to be workers, initiating the worker phase,
with the foundresses exerting dominance in relation to the workers, which even have
limited reproductive capacity (Jandt et al, 2014). Among workers, as noted, there is a
linear hierarchy, with the most dominant individual having a higher chance of
becoming a queen after the resident queen is dead or removed from the nest (Jandt
et al, 2014).
Dominance among Polistes is generally established through intense and quickly
fighting interactions, with one female eventually winning most of the contests (Jandt
et al, 2014). The establishment of a hierarchy leads to physiological changes among
participants, marked by reproductive suppression of subordinates and greater
ovarian development of the dominant female, which results in the dominant being the
only reproductive individual within the group (Reeve, 1991). After establishing her
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dominance rank, the queen may reduce her aggressive behaviour, substituting it for
ritualized, less harmful behaviours (Jandt et al, 2014). Also, wasps of the gender
Polistes may carry visual signals, facial patterns for example, that reduce dominance
conflicts (Jandt et al, 2014).
Another example of dominance in invertebrates occurs in crayfish, Orconectes
rusticus. These crustaceans establish a linear dominance hierarchy through an
intensive phase of fighting interactions, where individuals exhibit ritualized
aggression (Fero et al, 2007). A higher position on hierarchy rank has been observed
to increase access to shelter, but not to food and mate resources (Fero et al, 2007).
Shelter can provide protection from conspecifics competitors and predators, and
therefore is an important ecological resource (Fero et al, 2007). Dominant individuals
are more capable of excluding other crayfish from their shelter, and subordinate
individuals might also evade those shelters to avoid aggression (Fero and More,
2008). However, mating opportunity, which is directly linked to reproductive success,
does not seems to correlate with dominance rank in crayfish (Fero et al, 2007).

2. 2 Vertebrates
Species of vertebrates whose individuals live in groups generally show a dominance
hierarchy among its adults members, and sometimes, even among broods and litters
(Drummond, 2006). There are several mechanisms influencing the generation of
dominance relationships in vertebrates, including asymmetrical fighting ability,
capacity of learning and assessment, which is an animal evaluation of the fighting
ability of its rivals (Drummond, 2006). Instead of having conflicts every single time,
individuals that are weaker may learn to avoid conflict displaying a submissive
posture; also, some vertebrates can assess others fight ability simply by observing
their conflict encounters and outcomes (Drummond, 2006). In relation to dominance
status, there are also a variety of factors influencing it in vertebrates, for example:
age, political machinations, body size and parental ranking, where rank of young
individuals are correlated with those held by their mothers or/and fathers (Engh et al,
2000).
Astatotilapia burtoni, known as African cichid fish, demonstrate dominance
relationships (Renn et al, 2008). In this species, dominant males have bright
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coloration and slow growth, while submissive males have cryptic colours and faster
growth (Renn et al, 2008). Subordinate males have regressed gonads, and therefore
are reproductively inhibited (Burmeister et al, 2005). Male reproductive capacity,
however, is regulated by the social environment: as the individual wins contests
against other males, his phenotype change from submissive characteristics to
dominant ones; in sum, as a male rises in dominance rank, he becomes
reproductively mature and his growth rate slows as he devotes more of his energy to
reproduction (Burmeister et al, 2005).
White-throated Sparrow, Zonotrichia albicollis, are birds that have an almost linear
dominance hierarchy structure within foraging flocks formed during non-breeding
season (Schneider, 1984). Wood pigeons, Columba palumbus, and chickadees,
Parus atricapillus, also have shown dominance behaviour (Schneider, 1984). In all
those bird species, there are evidence that dominant and subordinate individuals
forage in different places within the foraging flocks, with the subordinate birds
feeding next to the front, therefore being more exposed to predators; however, lowranking birds can also benefit from it, since food density is probably higher farther
from the centre (Schneider, 1984).
Spotted hyaenas, Crocuta crocuta, are mammals that live in permanent social
groups whose territory is cooperatively defended by its members (Engh et al, 2000).
Female and male adults, as well as cubs, are ranked in a linear dominance
hierarchy, with female dominance relationships been highly stable; dominance rank
of cubs conform to their mothers position within the hierarchy (Engh et al, 2000). At
first, cubs are equally aggressive towards highborn and low-born youngsters,
however, they rapidly change their behaviour to direct their aggressiveness only
towards individuals of a lower rank than their mothers (Engh et al, 2000).
Conspecifics will support cubs that engage in aggressive interactions against lowerborn individuals, but will not do so if the interactions are against higher-born ones,
what may reinforce high-born cubs aggressiveness, as well as the yielding behaviour
of low-born ones; high-born youngsters have more powerful allies, and the threat of
being attacked by them may ensure that the dominance hierarchy stays the same
(Engh et al, 2000).
Humans, Homo sapiens, also have dominance hierarchies, however, these
hierarchies are not linear nor one-dimensional: humans generally belong to more
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than one hierarchy, valuing mostly the ones where their rank is the highest
(Sapolsky, 2005). There are evidence of a correlation between humans dominance
rank and their health, with lower ranked individuals showing increase risks of
cardiovascular diseases, among others (Sapolsky, 2005).

2.3 Evolution
Living in group, although may bring advantages to group members, for example
better defence against predators, have also disadvantages, as intraspecific
competition; dominance hierarchy in this context, is an efficient mechanism to
prevent direct conflicts between group members, and could have evolved as so (Van
Doorn et al, 2003). Rather than fighting every single time, both dominant and
subordinate individuals make use of this ritualised form of conflict resolution, which
substitute the need of engaging in costly fights. However, individuals still have to
solve another problem: which of them will become the dominant ones or the
subordinate ones? A higher dominance rank is generally correlated with better
accesses to resources, such as food and sexual partners, which are both, in turn,
correlated with reproductive success (Muller and Wrangham, 2004).
One possible resolution for the formation of dominance rank could be based on
some asymmetry between competitors; an asymmetry that underlies their potential
to hold resources, for example, body size (Van Doorn et al, 2003). Nonetheless,
theoretical considerations show that the formation of linear dominance hierarchies,
abundantly observed in nature, could not rely only on these asymmetries, as they
would need to be unrealistically large (Van Doorn et al, 2003). Another possibility is
that individuals submit to a convention, for example, larger animals are always
dominant in relation to smaller ones, and both small and large individuals within a
group accept it and behave accordingly (Van Doorn et al, 2003). However,
experiments with cockroaches and cichlid fish demonstrated that if a previously
established group is repeatedly subjected to reconstruction, the dominance hierarchy
formed does not remain the same, it may result in randomly new dominance
hierarchies (Van Doorn et al, 2003). These experiments, therefore, indicates that
asymmetries between group members are not the only factor directing the formation
of dominance hierarchies.
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Dominance could be based on random historical asymmetries emerging from fights

between individuals, for example, if an organism wins a conflict, whose victory may
happen by chance, this can lead him to behave more aggressively, while losers may
behave more submissively (Van Doorn et al, 2003). This seems to be true for cichlid
fish, where winning conflicts increase individuals aggressiveness, as well as other
dominant traits as coloration (Burmeister et al, 2005).

Rank, therefore, would

emerge from a positive feedback of winning, which leads to a higher probability of

winning in the future. Some theoretical models support that these winner and loser
effects can promote rank differentiation between two individuals, and also a stable
linear dominance hierarchy as an emergent propriety, even without individuals
asymmetries (Van Doorn et al, 2003).
Nevertheless, if dominance rank is at least in part determined by random historical
asymmetries, it give rise to the puzzle of why subordinate individuals would accept
their low position within the dominance hierarchy, when they could fight and have
real chances of winning and becoming dominant (Van Doorn et al, 2003). Breaking
the randomly, at least at some extent, established dominance hierarchy, however,
may be just too costly for low ranking individuals; they would have to fight too many
fights, as dominant individuals would still behave aggressively (Van Doorn et al,
2003). In the case of the spotted hyenas, for example, if a subordinate individual try
to attack a higher ranking hyena, he will probably not receive help from others, while
the opposite can occur (Engh et al, 2000). Also, dominant individuals have more
powerful allies than low ranking individuals, since hyenas prefer to ally with dominant
hyenas (Engh et al, 2000).
Spotted hyenas are also an example of female dominance over males (Engh et al,
2000). Generally, male mammals have to fight other conspecifics males for access to
females, which creates a selective pressure for a larger body size, as well as
aggressive behaviour (Darwin 1871), this way, males are better armed than females
to win aggressive conflicts that may promote dominance rank (Watt et al, 2009). In
spotted hyenas, however, females are more aggressive than males and more
dominant in almost all social contexts (Watt et al, 2009), breaking this male
dominance pattern observed among mammals. How could this female dominance
have evolved in spotted hyenas?

A possible explanation is that maternal support is extremely necessary for offspring

survival, since cubs cannot feed by themselves because of a specialized feeding
apparatus that handicaps them at the first few months of their existence (Watt et al,
2009).

Besides from that, in spotted hyenas, there is an intensive feeding

competition, with offspring relying on their mothers aggressiveness to be proper fed

(Watt et al, 2009). This way, maternal aggression increases offspring survival and
therefore, can be positively selected (Watt et al, 2009).

3. Endocrinology of Dominance behaviour

3.1 Testosterone
There is strong evidence that elevated levels of testosterone, a steroid hormone,
promotes aggressiveness, and consequently, can also promote dominant behaviours
in a diversity of animals species, including humans (Mehta and Josephs, 2010). All
vertebrates share a similar aggressiveness neurophysiological mechanism, and
therefore is not a surprise that aggression seems to be positively influenced by
testosterone in a variety of vertebrate as primates, rodents and carnivores
(Poisbleau et al, 2005). Aggression does not necessarily implies in dominant
behaviour, however, dominance is often correlated with aggressiveness (Poisbleau
et al, 2005).
During periods of hierarchy formation, as well as territory establishment, testosterone
levels increase in a range of different species, with levels decreasing after
dominance rank or territory boundaries are established (Poisbleau et al, 2005).

3.2 Glucocorticoids
Glucocorticoids are a class of steroid hormones directly involved with stress
response in vertebrates (Muller and Wrangham, 2004). In primates the primary
glucocorticoid observed is cortisol, while in many birds and some rodents, it is
corticosterone (Muller and Wrangham, 2004). Prolonged experience of high levels of
glucocorticoids is associated with health problems as cardiovascular diseases

(Sapolsky, 2005), and therefore, glucocorticoids can be interpreted as a cost to

stressful behaviours as dominance interactions (Muller and Wrangham, 2004).
Studies have provided evidence that loss of control and the inability to predict an
environmental stimulus are associated with higher stress levels, which could
therefore implies that subordinate individuals experience a higher level of
glucocorticoids than dominant ones (Muller and Wrangham, 2004). However, in
some species, there is no correlation between dominance and glucocorticoid levels
(Muller and Wrangham, 2004). It can also be argued that in stable dominance
hierarchies dominant individuals can enjoy of a predictable environment and, thus
have indeed less glucocorticoids levels; but, in unstable hierarchies, dominant
individuals have to continuously ensure their position, consequently suffering from
stress and therefore demonstrating higher levels of glucocorticoids than subordinate
animals (Sapolsky, 1992).
A study with humans demonstrated that testosterone and cortisol alone were not
predictors nor related to dominance (Mehta and Josephs, 2010). The only
dominance correlation observed was with the interaction between testosterone and
cortisol (Mehta and Josephs, 2010). They observed that when cortisol was low,
higher levels of testosterone increased dominance, but when cortisol levels were
high, higher levels of testosterone did not seem to influence dominance behaviour.
One possible explanation provided is that cortisol seems to inhibit the action of
testosterone. If stress is low, testosterone is not inhibited and can properly influence
dominance behaviour, but if the human is stressed, cortisol limit testosterone effects
(Mehta and Josephs, 2010). A broader explanation is that since cortisol is associated
with social avoidance, higher levels of cortisol impair a social approach necessary for
the expression of dominance in humans, even with the presence of higher
testosterone levels, while low levels of cortisol facilitates social approach, allowing
dominance interactions to take place (Mehta and Josephs, 2010).

3.3 Juvenile hormone

In poliste wasps juvenile hormone is correlated with dominance rank, as well as
foundress fertility (Jandt et al, 2014). Juveline hormone seems to vary depending on
individual condition: wasps that demonstrate a good physical condition, for example
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the queen and higher rank individuals, respond to juvenile hormone by increasing
their dominance behaviour and fertility, while wasps that have a poor physical
condition, as workers, respond to juvenile hormone by foraging behaviour (Jandt et
al, 2014).

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