Human reproductive behavior, life history, and the Challenge Hypothesis: A 30-year review, retrospective and future directions

Abstract

The Challenge Hypothesis (Wingfield et al., 1990) originally focused on adult male avian testosterone elevated in response to same-sex competition in reproductive contexts. The purpose of the present paper is to demonstrate how the Challenge Hypothesis has shaped ideas about human life histories. We conduct a citation analysis, drawing upon 400 Google Scholar citations in the human literature to identify patterns in this body of scholarship. We cover key factors, such as context and personality traits, that help explain variable testosterone responses such as winning/losing to adult competitive behavior. Findings from studies on courtship and sexual behavior indicate some variation in testosterone responses depending on factors such as motivation. A large body of research indicates that male testosterone levels are often lower in contexts of long-term committed partnerships and nurturant fathering and aligned with variation in male mating and parenting effort. As the Challenge Hypothesis is extended across the life course, DHEA and androstenedione (rather than testosterone) appear more responsive to juvenile male competitive behavior, and during reproductive senescence, baseline male testosterone levels decrease just as male life history allocations show decreased mating effort. We discuss how research on testosterone administration, particularly in older men, provides causal insight into effects of testosterone in humans, and how this “natural experiment” can be viewed in light of the Challenge Hypothesis. We synthesize central concepts and findings, such as an expanded array of costs of testosterone that inform life history tradeoffs between maintenance and reproductive effort, and we conclude with directions for future research.