Challenge hypothesis

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.^[1] 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.^[2] The challenge hypothesis has come to explain patterns of testosterone production as predictive of aggression across more than 60 species.^[3]

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 leads to this rise in testosterone above breeding baseline, which serves to increase the frequency and intensity of aggression in males, particularly for competing with other males or interacting with sexually receptive females.^[4]

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.^[5]

Research on nonhuman species has found that testosterone levels are positively associated with mating effort^[6] and negatively related to parenting effort.^[7] Moreover, experimental manipulations have revealed a causal role of testosterone, such that elevations in testosterone are associated with increased mating effort and decreased parenting effort.^[8]

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,^{[2] [9]} 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.^[4] 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.^[10]

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 testosteron increases aggression,^[11] aggression and testosterone are not always directly related.^[12] 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.^[2]

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.^[2]

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.^[13]

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.^[14][15] While the challenge hypothesis has not been examined in humans, some have proposed that the predictions of the challenge hypothesis may apply.^[16]

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,^[17] and preliminary evidence suggests that men may be able to discern cues of fertility in women.^[18] 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.

References

1. ^ Buss, D. M. (2002). Human mate guarding. Neuroendocronology Letters Special Issue, 23, 23-29.
2. ^ ^{a b c d} 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.
3. ^ 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.
4. ^ ^{a b} 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.
5. ^ 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.
6. ^ 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.
7. ^ Wynne-Edwards, K. E. (2001). Hormonal changes in mammalian fathers. Hormones and Behavior, 40, 139–145.
8. ^ Ketterson, E. D., & Nolan Jr., V. (1999). Adaptation, exaptation, constraint: a hormonal perspective. American Naturalist, 154S, S4–S25.
9. ^ 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.
10. ^ Wingfield, J. C. (1984). Androgens and mating systems: Testosterone-induced polygyny in normally monogamous birds. Auk, 101, 655-671.
11. ^ Harding, C. H. (1981). Social modulation of circulating hormone levels in the male. Am. Zool., 21, 223-232.
12. ^ 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.
13. ^ 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.
14. ^ Benshoof, L. & Thornhill, R. (1979). The evolution of monogamy and concealed ovulation in humans. J. Social. Biol. Struct., 2, 95-106.
15. ^ 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.
16. ^ Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319-345.
17. ^ 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.
18. ^ Haselton, M. G. & Gildersleeve, K. (2011). Can men detect ovulation? Current Directions in Psychological Science, 20, 87-92.