Behavioral insensitivity to testosterone: why and how does testosterone alter paternal and aggressive behavior in some avian species but not others?

Considerable research has been conducted on the interrelationships of the steroid hormone testosterone and reproductive behavior in seasonally breeding birds. In species in which males provide paternal care, males experience a peak in testosterone secretion that coincides with territory establishment and pair bonding, and then drops to a breeding baseline as nests are initiated. A large body of evidence suggests that a male's seasonal profile of testosterone reflects a trade-off between expression of sexual and territorial behavior and expression of paternal behavior. For example, studies utilizing testosterone implants to extend the early season peak in plasma testosterone have demonstrated that testosterone tends to increase sexual behavior as well as intensity and persistence of male-male aggression, but also decreases paternal care of offspring. However, recent studies demonstrate that in some species, males do not respond to experimentally elevated testosterone with alterations in aggression and/or paternal care. This phenomenon of "behavioral insensitivity" to testosterone may relate to a variety of environmental factors, particularly those that necessitate high levels of paternal investment. This review explores both ultimate and proximate explanations for behavioral insensitivity to testosterone, and explores hypotheses to explain how this phenomenon may relate to androgen responses to social interactions during breeding. Further research into behavioral insensitivity to testosterone in a variety of vertebrates may provide additional insights into the complex patterns of sex steroid secretion and its behavioral consequences.