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 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.
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 primates species. In 2004, Martin N. Muller and Richard W. Wragham 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 Wragham 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. 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 of the challenge hypothesis
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). 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.
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.
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.
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.
- Buss, D. M. (2002). Human mate guarding. Neuroendocronology Letters Special Issue, 23, 23-29.
- Wingfield, J. C., Hegner, R. E., Dufty, A. M., & Ball, G. F. (1990). The 'challenge hypothesis': Theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. American Naturalist, 136, 829-846.
- Wingfield, J.C., Jacobs, J.D., Tramontin, A.D., Perfito, N., Meddle, S., Maney, D.L., Soma, K. (2000). Toward an ecological basis of hormone-behavior interactions in reproduction of birds. In: Wallen, K., Schneider, J. (Eds.), Reproduction in Context. MIT Press, Cambridge, MA, pp. 85–128.
- Goymann, W., Landys, M. M., Wingfield, J. C. (2007). Distinguishing seasonal androgen responses from male-male androgen responsiveness—Revisiting the challenge hypothesis. Hormones and Behavior, 51, 463-476.
- Chastel, Olivier; Barbraud, Christophe, Weimerskirch, Henri, Lormée, Hervé, Lacroix, André, Tostain, Olivier. "High levels of LH and testosterone in a tropical seabird with an elaborate courtship display". General and Comparative Endocrinology 140 (1): 33–40. doi:10.1016/j.ygcen.2004.10.012. PMID 15596069.
- Wingfield, John C., Ball, Gregory F., Dufty Jr, Alfred M., Hegner, Robert E., Ramenofsky, Marilyn (1987). "Testosterone and Aggression in Birds". American Scientist 5 (6): 602–608.
- Herting, Brian., Belthoff, James R. (1997). "Testosterone, Aggression, and Territoriality in Male Westerm Screech Owls (Otus kennicottue): Results from Preliminary Experiments". United States Department of Agriculture Forest Service General Technical Report NC (190): 213–217.
- Herting, Brian., Belthoff, James R. (1997). "Testosterone, Aggression, and Territoriality in Male Westerm Screech-owls (Otus kennicottue): Results from Preliminary Experiments". United States Department of Agriculture Forest Service General Technical Report NC (190): 213–217.
- Soma, K. K.; Tramontin, A. D.; Wingfield, J. C. (7 June 2000). "Oestrogen regulates male aggression in the non-breeding season". Proceedings of the Royal Society B: Biological Sciences 267 (1448): 1089–1096. doi:10.1098/rspb.2000.1113.
- Soma, K. K (1 July 2006). "Testosterone and Aggression: Berthold, Birds and Beyond". Journal of Neuroendocrinology 18 (7): 543–551. doi:10.1111/j.1365-2826.2006.01440.x. PMC 2954190. PMID 16774503.
- Archer, John. "Testosterone and human aggression: an evaluation of the challenge hypothesis". Neuroscience & Biobehavioral Reviews 30 (3): 319–345. doi:10.1016/j.neubiorev.2004.12.007.
- Wingfield, John; Robert E. Hegner, Alfred M. Dufty, Gregory F. Ball (December 1990). "The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies". The American Naturalist. 6 136 (6): 829–846. doi:10.1086/285134. JSTOR 2462170.
- Klukowski, Matthew; Nelson, Craig E. "The Challenge Hypothesis and Seasonal Changes in Aggression and Steroids in Male Northern Fence Lizards (Sceloporus undulatus hyacinthinus)". Hormones and Behavior 33 (3): 197–204. doi:10.1006/hbeh.1998.1449. PMID 9698502.
- Hirschenhauser, K.; Taborsky, M.; Oliveira, T.; Canàrio, A.V.M.; Oliveira, R.F. (1 October 2004). "A test of the 'challenge hypothesis' in cichlid fish: simulated partner and territory intruder experiments". Animal Behaviour 68 (4): 741–750. doi:10.1016/j.anbehav.2003.12.015.
- Muller, Martin N; Wrangham, Richard W. "Dominance, aggression and testosterone in wild chimpanzees: a test of the 'challenge hypothesis'". Animal Behaviour 67 (1): 113–123. doi:10.1016/j.anbehav.2003.03.013.
- Gray, P. B. & Campbell, B. C. (2009). Human male testosterone, pair-bonding, and fatherhood. In P. T. Ellison & P. B. Gray (Ed.), Endocrinology in social relationships (pp. 270-293). Cambridge, MA: Harvard University Press.
- Creel, S., Creel, N. M., Mills, M. G. L., & Monfort, S. L. (1997). Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behavioral Ecology, 8, 298–306.
- Wynne-Edwards, K. E. (2001). Hormonal changes in mammalian fathers. Hormones and Behavior, 40, 139–145.
- Ketterson, E. D., & Nolan Jr., V. (1999). Adaptation, exaptation, constraint: a hormonal perspective. American Naturalist, 154S, S4–S25.
- Klukowski, M. & Nelson, C. E. (1998). The challenge hypothesis and seasonal changes in aggression and steroids in male northern fence lizards (Sceloporus undulatus hyacinthinus). Hormones and Behavior, 33, 197-204.
- Wingfield, J. C. (1984). Androgens and mating systems: Testosterone-induced polygyny in normally monogamous birds. Auk, 101, 655-671.
- Turner, A. K. (1994). Genetic and hormonal influences on male violence. In: J. Archer (Ed.), Male violence ( pp. 233–252). New York: Routledge.
- Harding, C. H. (1981). Social modulation of circulating hormone levels in the male. Am. Zool., 21, 223-232.
- Dittami, J. P. & Reyer, H. U. (1984). A factor analysis of seasonal behavioral hormonal and body weight changes in adult male bar-headed geese, Anser indicus. Behaivour, 90, 114-124.
- Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour, 66, 551-560.
- Muller, M. N. & Wrangham, R. W. (2003). Dominance, aggression, and testosterone in wild chimpanzees: A test of the 'challenge hypothesis'. Animal Behaviour, 67, 113-123.
- Benshoof, L. & Thornhill, R. (1979). The evolution of monogamy and concealed ovulation in humans. J. Social. Biol. Struct., 2, 95-106.
- Alexander, R.D., and Noonan K.M. (1979). Concealment of ovulation, parental care, and human social evolution. In N.A. Chagnon and W. Irons (Ed.), Evolutionary biology and human social behavior (pp. 436-453). North Scitute, MA: Duxbury Press.
- Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319-345.
- Berg, S. J. & Wynne-Edwards K. E. (2001). Changes in testosterone, cortisol, and estradiol levels in men becoming fathers. Mayo Clin. Proc., 76, 582-592.
- Haselton, M. G. & Gildersleeve, K. (2011). Can men detect ovulation? Current Directions in Psychological Science, 20, 87-92.