The challenge hypothesis: Where it began and relevance to humans

A contribution to a special issue on Hormones and Human Competition. Over 40years ago assay methods that allowed the accurate measurement of circulating levels of hormones were developed for the first time enabling us to sample free-living as well as captive animals. This led to a new concept called "field endocrinology". It quickly became apparent that endocrine profiles of animals under natural conditions were very different from congeners in captivity. Furthermore, hormone data could be organized by functional units (e.g. reproductive states) spaced in time according to natural duration of those states rather than simply by date alone. This approach changed how we interpret data and revealed species-specific patterns of hormone secretion. The "challenge hypothesis", stating that the temporal patterns of testosterone in blood were determined by a trade-off between the degree of male-male competition that increased testosterone, and the expression of paternal care that required a decrease in testosterone, grew out of a combination of field endocrine investigations that then informed laboratory experimentation. A strong argument can now be made that the challenge hypothesis is highly relevant for understanding social interactions in humans and non-human primates. Investigations on human subjects provide some of the best models for the challenge hypothesis. However, the central mechanisms by which aggressive and other social interactions regulate the hypothalamo-pituitary-gonad axis will depend upon work on not only primates, but also other vertebrates in very different ecological contexts. Research on the challenge hypothesis in humans will play a critical role as new insight on the interrelationships of testosterone and male-male competition comes from new technologies.