Fatherhood in the animal kingdom and its intricate relationship with aggression

On Father’s Day, hundreds of thousands of people across the United States will show appreciation for the love, encouragement, and support that their fathers have provided them throughout their lifetimes. Interestingly, numerous animals provide parental care to their offspring, from fish and birds to non-human primates and humans. Yet, there is substantial evidence that many species must juggle parental care with another social behavior that is essential for reproductive success and survival: aggression.

Over twenty-five years ago, field endocrinologist John Wingfield and colleagues proposed the Challenge Hypothesis based on data acquired from seasonally-breeding male birds. The Challenge Hypothesis posits that seasonal changes in the secretion of testosterone (T) — a steroid hormone produced by the gonads that facilitates reproduction and its associated social behaviors — are the result of a trade-off between the extent of parental care that an individual provides and the amount of competition that individual faces in their environment.

Testosterone production plays a crucial role in reproductive behaviors, including mating and aggression, and facilitates territory establishment and defense. Thus, levels of circulating T are predicted to be higher during situations of social instability, when events such as territory formation, dominance disputes, and challenges by males for available territories are more likely to occur. In contrast, circulating T is thought to decline during socially-stable periods, once territories have been established and there is little competition among males.

Collectively, these shifts in T secretion over time are thought to optimize the costs and benefits of high T levels. High T is beneficial during the early parts of the breeding season, when animals mate and acquire territories. However, during the latter part of the breeding season, when situations of social instability are less likely to occur, lowering circulating T is thought to minimize the potential costs of T secretion, such as decreased immune function and increased risk of predation.

Since the birth of the Challenge Hypothesis, the relationship between T and aggression has been established in several bird species native to temperate habitats. In fact, previous work has shown that tenets of the Challenge Hypothesis are relevant to species within all vertebrate taxa, including fish and primates. Furthermore, there is emerging evidence of a positive correlation between aggression and juvenile hormone, a lipid-like hormone that mediates a trade-off between fertility and lifespan, in insects.

However, perhaps some of the most interesting findings are those that represent exceptions to the predictions put forth in the Challenge Hypothesis. For example, many tropical songbirds consistently maintain low circulating T levels throughout the breeding season, an adaptation that has been attributed to their extended breeding seasons and the low seasonality exhibited by tropical habitats. For these species, maintaining low breeding levels of T may prevent the extended costs of elevating T secretion, such as trade-offs with parental care and immune function. Recent work has also demonstrated that certain tissues, such as the brain and the gonads, are capable of locally producing T, and these studies have shown that tissue levels of T can differ significantly from those in circulation. These data strongly suggest that novel mechanisms not initially put forth in the Challenge Hypothesis, such as tissue-specific steroid synthesis, may also be important in mediating seasonal shifts in social behavior.

While research over the past few decades has mostly provided support for a trade-off between parental care and aggression across vertebrates, an important question still remains: does the Challenge Hypothesis apply to humans? In a meta-analysis, data from multiple studies of T in humans showed some evidence for a T-mediated trade-off between mating and parental care. Specifically, fathers and men in committed, long-term relationships tend to maintain lower levels of T than unpaired or married men pursuing additional mates. However, the studies reviewed in this meta-analysis provide only mixed support for a relationship between T and male-male competition. It is important to note that most of the human studies used in this meta-analysis were not specifically designed to test the predictions of the Challenge Hypothesis. Yet, these findings are compelling and suggest that a few more “parents” should be thanked on Father’s Day in addition to Dad: our vertebrate ancestors and, most importantly, the evolutionary forces that drove the conservation of parental care behavior in humans.

Edited by Guillaume J. Dury and Lana Ruck