The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies

A number of investigations in recent years have shown that seasonal profiles of testosterone (T) levels in the blood of male birds breeding under natural condi- tions are highly variable. As a result of the application of field endocrinology techniques (see Wingfield and Farner 1976), the temporal patterns of T secretion in free-living males are now known for over 20 species (from 6 orders and 14 families), representing three mating systems (monogamy, polygyny, and polyan- dry) and several breeding strategies. Results of these studies provide the impetus for an assessment of the potential relationships between T and breeding systems. The concepts emerging from their analysis can serve both as a framework for further investigation of the hormonal mechanisms underlying social behavior of vertebrates in general and as a guide for manipulating social systems to gain new insights into the ultimate cause of different mating strategies. The extent of these differences varies considerably among species (Wingfield 1984a; Wingfield et al. 1987) and raises a number of questions. Why is there so much variation in the temporal patterns of circulating T levels between captive and free-living populations and among species? Are there relationships between temporal patterns of T secretion and mating systems or the breeding strategies of individuals? What are the environmental and genetic determinants of these patterns and their functions? In this article we consider some theoretical approaches to the interrelationships of T, mating system, and breeding strategy in male birds using data from captive and free-living populations. To make our assumptions explicit, we begin with a summary of the actions of T in male birds. We then address the questions above by considering the temporal patterns of T secretion and their correlations with mating systems and breeding strategies. We have restricted this discussion and analysis mostly to the class Aves simply because there is a large data base from a wide range of mating systems and breeding strategies. It should be noted, however, that the conclusions made here may also be equally applicable to all the vertebrate classes.