The challenge hypothesis outlines the dynamic relationship between testosterone and aggression in mating contexts. It proposes that testosterone promotes aggression when it would be beneficial for reproduction, such as mate guarding, or strategies designed to prevent the encroachment of intrasexual rivals. The positive correlation between reproductive aggression and testosterone levels is seen to be strongest during times of social instability. The challenge hypothesis predicts that seasonal patterns in testosterone levels are a function of mating system (monogamy versus polygyny), paternal care, and male-male aggression in seasonal breeders.
The pattern between testosterone and aggression was first
observed in seasonally breeding birds, where testosterone levels rise
modestly with the onset of the breeding season to support basic
reproductive functions. However, during periods of heightened male
aggression, testosterone levels increase further to a maximum
physiological level. This additional boost in testosterone appears to
facilitate male-male aggression, particularly during territory formation
and mate guarding, and is also characterized by a lack of paternal
care.
The challenge hypothesis has come to explain patterns of testosterone
production as predictive of aggression across more than 60 species.
Patterns of testosterone
The
challenge hypothesis presents a three-level model at which testosterone
may be present in circulation. The first level (Level A) represents the
baseline level of testosterone during the non-breeding season. Level A
is presumed to maintain feedback regulation of both GnRH
and gonadotropin release, which are key factors in testosterone
production. The next level (Level B) is a regulated, seasonal breeding
baseline. This level is sufficient for the expression of reproductive
behaviors in seasonal breeders and the development of some secondary sex characteristics.
Level B is induced by environmental cues, such as length of day. The
highest level (Level C) represents the physiological testosterone
maximum and is reached through social stimulation, such as male-male
aggression. The challenge hypothesis proposes that social stimulation
which leads to this rise in testosterone above breeding baseline serves
to increase the frequency and intensity of aggression in males,
particularly for competing with other males or interacting with sexually
receptive females.
In birds
It
is thought that testosterone plays an integral part of the territorial
behavior within bird species, in particular the fluctuation of
testosterone mitigated by luteinizing hormone (LH) during different seasons.
Generally, mating behavior is demonstrated in the spring and
accordingly, male birds show a sharp increase in LH as well as
testosterone during this time. This acute rise in LH and testosterone
can be attributed to the increased need for aggressive behaviors. The
first need for aggressive behavior comes from the drive to establish
territory. This typically occurs within the first few weeks of mating season. The second need for aggression occurs after the first clutch of eggs have been laid.
The male not only needs to guard the eggs, but also to guard his
sexually receptive mate from other potential suitors. Thus, the male
adopts an “alpha male status” when acquiring territory as well as during
the egg laying period. This alpha male status, as mentioned before,
comes from the significant increase of testosterone that occurs during
the mating season. Further evidence of LH and testosterone mitigating aggression in bird species comes from studies on bird species such as the song sparrow and the European blackbird who build highly accessible refuges, known as open cup nests.
Because open cup nests can essentially be built anywhere, there is little competition when it comes to nest building sites.
Accordingly, both the song sparrow and the European blackbird do not
show an increase in luteinizing hormone or testosterone during territory
acquisition .
However, not all species of birds show increased levels of testosterone
and LH during aggressive behavior. In a landmark study, it was found
that male western screech owls,
when exposed to another male during the non-mating season showed
aggressive behavior without the increase in LH and testosterone.
However, when the owls were put in a situation that warranted aggressive
behavior during the mating season, there was a large spike in LH and
testosterone during the aggressive act.
This suggests that the mechanisms of aggressive behavior during the
mating and non-mating seasons are independent of each other or perhaps
the increase in testosterone somehow increases the aggressive response
during the mating season.
Estradiol (E2), a type of non gonadal estrogen,
seems to play a key role in regulating aggressive behavior during the
non-mating season in several species of birds. As previously noted, many
bird species during the non-mating season have low testosterone levels
yet still manage to display aggression. As a primary example, when the
Washington State song sparrow, a bird which shows fairly high levels of
aggression during non-mating season despite low testosterone, is exposed
to fadrozole, an aromatase
inhibitor, the levels of aggression are greatly decreased. When the E2
was replaced, the aggressive behaviors reestablished themselves thus
confirming that E2 governs aggressive behavior during the non-mating
season. It is unknown however if this is just specific to birds, or if this extends to other animal species.
These examples all culminate in a challenge hypothesis model
which focuses on the role of testosterone on aggression in the breeding
season. The challenge hypothesis most likely cannot be applied to the
non-breeding season since, as mentioned above, there is most likely a
mechanism independent of testosterone governing aggression in the
non-mating season. A sigmoidal
relationship between testosterone plasma levels and male-male
aggression is observed under the challenge hypothesis when the birds’
testosterone levels were above seasonal breeding testosterone baseline
levels. If birds remained at the seasonal breeding baseline levels
during the breeding season, then there is not a significant difference
observed in male-male aggression. In addition, there is a negative,
sigmoidal relationship between testosterone levels in the birds and the
amount of parental care provided when parents are above the seasonal
breeding testosterone baseline levels. As such, the relationship between testosterone plasma levels and male-male aggression is context-specific to the species.
Figure 2 and 3 describe the relationships observed of many single- or
double-brooded bird species, from male western gulls to male turkeys.
In other animals
The
challenge hypothesis has been used to describe the testosterone levels
in other species to certain social stimuli. The challenge hypothesis
predicts the testosterone influence on aggressive male-male interactions
between male northern fence lizards.
This reinforces the challenge hypothesis by showing rapid changes in
aggressive behaviors of the lizards do not correlate with testosterone
concentrations. Yet, over the mating season, the intensity of the
behavior and the levels of testosterone levels yielded a positive
correlation.
Research has also shown the challenge hypothesis applies to specific
monogamous fish species, with a greater correlation in species with
stronger pair bonding.
In addition, the challenge hypothesis has been adapted to primate
species. In 2004, Martin N. Muller and Richard W. Wrangham applied a
modified challenge hypothesis to chimpanzees. Similar to the original
hypothesis, they predicted that there would be increased male-male
aggressive interaction when a receptive and fertile female chimpanzee
was present. Muller and Wrangham also correctly predicted the
testosterone levels of more dominant chimpanzees to be higher as
compared to lower status chimpanzees.
Therefore, chimpanzees significantly increased both testosterone levels
and aggressive male-male interactions when receptive and fertile
females presented sexual swellings.
This study also highlighted how male testosterone and aggression levels
rise only when males are in the presence of parous females. This is
because nulliparous females are less attractive to males, and they are
not guarded, meaning there is little competition.
This evidence suggests that the increase in testosterone is related to
only aggression – not sexual activity – as male chimpanzees mate equally
with both parous and nulliparous females.
Currently, no research has specified a relationship between the
modified challenge hypothesis and human behavior, yet, many
testosterone/human behavior studies support the modified hypothesis
applying to human primates.
Cornerstones
Mating effort versus parenting effort
A fundamental feature of male life history
is the tradeoff between the energy devoted to male-male competition and
mate attraction (mating effort) versus that allocated to raising
offspring (parenting effort). There is a trade off because decreased
paternal effort caused by increased testosterone dramatically decreases
reproductive success, due to decreased parental care and protection for
the offspring.
Therefore, to maximise reproductive success, the optimal balance
between the two must be found. The challenge hypothesis proposes
testosterone as the key physiological mechanism underlying this
tradeoff. When the opportunity to reproduce arises—namely, the species
enters the breeding season or females enter estrus—males
should exhibit a rise in testosterone levels to facilitate sexual
behavior. This will be characterized by increased mating effort and
decreased parenting effort, as investment in the former may be
incompatible with parental care due to insufficient time and energy to
engage in all of these facets of reproductive effort.
Research on nonhuman species has found that testosterone levels are positively associated with mating effort and negatively related to parenting effort.
Moreover, experimental manipulations have revealed a causal role of
testosterone, such that elevations in testosterone result in increased
mating effort and decreased parenting effort.
Paternal care
The challenge hypothesis makes different predictions regarding testosterone secretion for species in which males exhibit paternal care versus those in which males do not. When aggressive interactions among males arise in species that exhibit paternal care, testosterone levels are expected to be elevated. Males are predicted to exhibit an increase in testosterone to Level C (physiological maximum), but only during periods of territory establishment, male-male challenges, or when females are fertile so that paternal care is not compromised. When aggression is minimal, specifically during parenting, testosterone levels should decrease to Level B (breeding baseline). Level B represents the minimal levels of testosterone required for the expression of reproductive behaviors, and is not expected to drastically interfere with parenting behavior.
In species where males exhibit minimal to no paternal care,
testosterone levels are hypothesized to be at Level C throughout the
breeding season because of intense and continued interactions between
males and the availability of receptive females.
In polygynous species, where a single male tends to breed with more
than one female, males generally do not exhibit a heightened endocrine
response to challenges, because their testosterone levels are already
close to physiological maximum throughout the breeding season.
Experimental support for the relationship between heightened
testosterone and polygyny was found, such that if testosterone was
implanted into normally monogamous male birds (i.e., testosterone levels
were manipulated to reach Level C) then these males became polygynous.
Mating Effort versus Maintenance
There is a broader trade-off to consider when it comes to the challenge hypothesis: maintenance vs reproductive effort. Reproductive effort includes both mating and parental effort. In order to gain the benefits of reproductive effort, individuals have to suffer the costs of testosterone, which can hinder their physiological maintenance. This is a form of life history tradeoff, due to the fact that natural selection favors reproductive success rather than maintenance. Therefore, the ability to find the correct balance between reproductive effort and maintenance would have been positively selected for by natural selection, leading to the physiological and social behaviour we now know as the challenge hypothesis.
One such cost is that increased aggressive activity due to high
levels of testosterone is hypothesised to expose males to increased
predation, which not only endangers them, but also their offspring. A study on the lizard Sceloporus jarrovi,
supported this prediction, as those with induced high levels of
testosterone for extended periods of time had a higher mortality rate
than those with lower levels of testosterone.
Prolonged high levels of testosterone have also been seen to suppress
the immune system, with evidence ranging from human natural experiments
to male-ring-tailed lemurs. Maintaining high levels of testosterone is energetically expensive,
which can hinder reproductive success when a male frequently finds
himself in aggressive and physically demanding situations.
Due to increased aggression as a result of high testosterone levels,
individuals expose themselves to higher injury risk than usual.
Therefore, the costs of maintaining a high testosterone level may outweigh increased reproductive success. A study on male ring-tailed lemurs (Lemur catta)
supports the idea of a compromise between costs and benefits of
increased testosterone levels, as increased levels were tightly timed
around days of female estrus. This shows that there is an optimum length
of time to have high testosterone levels when considering the costs and
benefits.
Male-male aggression
It has long been known that testosterone increases aggressive behavior.
While castration tends to decrease the frequency of aggression in birds
and replacement therapy with testosterone increases aggression, aggression and testosterone are not always directly related.
The challenge hypothesis proposes that testosterone is most immediately
related to aggression when associated with reproduction, such as
mate-guarding. An increase in male-male aggression in the reproductive
context as related to testosterone is strongest in situations of social
instability, or challenges from another male for a territory or access
to mates.
The relationship between aggression and testosterone can be
understood in light of the three-level model of testosterone as proposed
by the challenge hypothesis. As testosterone reaches Level B, or
breeding baseline, there is minimal increase in aggression. As
testosterone increases above Level B and approaches Level C, male-male
aggression rapidly increases.
Continuous breeders
The
challenge hypothesis was established based upon data examining seasonal
breeders. There are many species, however, who are continuous
breeders—namely, species that breed year-round and whose mating periods
are distributed throughout the year (e.g., humans). In continuous
breeders, females are sexually receptive during estrus, at which time ovarian follicles are maturing and ovulation
can occur. Evidence of ovulation, the phase during which conception is
most probable, is advertised to males among many non-human primates via
swelling and redness of the genitalia.
Support for the challenge hypothesis has been found in continuous
breeders. For example, research on chimpanzees demonstrated that males
became more aggressive during periods when females displayed signs of
ovulation. Moreover, male chimpanzees engaged in chases and attacks
almost 2.5 times more frequently when in groups containing sexually
receptive females.
Implications for humans
The
predictions of the challenge hypothesis as applied to continuous
breeders partially rests upon males' ability to detect when females are
sexually receptive. In contrast to females of many animal species who
advertise when they are sexually receptive, human females do not exhibit
cues but are said to conceal ovulation.
While the challenge hypothesis has not been examined in humans, some
have proposed that the predictions of the challenge hypothesis may
apply.
Several lines of converging evidence in the human literature suggest that this proposition is plausible. For example, testosterone is lower in fathers as compared to non-fathers, and preliminary evidence suggests that men may be able to discern cues of fertility in women. The support for the challenge hypothesis in non-human animals provides a foundation for which to explore the relationship between testosterone and aggression in humans.
The Dual Hormone Hypothesis as an Extension of the Challenge Hypothesis
The challenge hypothesis claims that there is an association between testosterone and aggression in mating contexts, and more broadly status-seeking behaviours. However, findings linking testosterone to status-seeking behaviours, especially in humans, are often inconsistent and leave room for critique. In some cases, testosterone has been seen to positively correlate with status-seeking behaviours such as aggression and competitiveness, however, testosterone has also been found to have weak or even null correlations with the same behaviours. Some scholars blame these inconsistencies on limitations in study methods, but the dual-hormone hypothesis has emerged as a theoretical explanation to some of these inconsistencies.
Dual-Hormone Hypothesis
Stress
plays a fundamental role in competition and mating, and therefore, the
hormones released in response to stress should be considered as well as
testosterone when looking at the challenge hypothesis. Cortisol is
produced in the hypothalamic-pituitary-adrenal gland and is released
when one is under physical or psychological stress; this is relevant to
the challenge hypothesis as testosterone-linked status-seeking
interactions are often stressful situations.
According to the dual-hormone hypothesis, the correlation between
testosterone levels and aggression/status-seeking behaviour is reliant
on corresponding cortisol levels; there is a strong correlation between
the two when cortisol levels are low, and a weaker or sometimes reversed
correlation when cortisol levels are high.
There is supporting evidence for this relationship from a study done on
humans, which looked at social status, leadership, and aggression.
Cortisol is seen as a moderator of the relationship between
testosterone and status-seeking/reproductive aggression in this
hypothesis.
However, the dual-hormone hypothesis also has its own flaws, and current evidence appears to only partially support the hypothesis, according to a meta-analytical evaluation in 2019 by Dekkers et al. A proposed reasoning for the occasional weak evidence is that cortisol and testosterone, further interact with social context and individual psychology to regulate status-seeking behaviours. One such context is ‘victory-defeat’, where testosterone and cortisol will interact to increase desire to compete again more after losing than winning, as a method of regaining social status. Individual personality also has an effect on the interaction between cortisol and testosterone, and studies have shown that the cortisol x testosterone interaction was statistically significant for only those with high disagreeableness and high emotional instability.
