A neuroendocrine perspective on the origin and evolution of cooperative breeding

Abstract

ABSTRACT Cooperative breeding behavior in birds ranges from inducible to obligate strategies and has evolved across diverse taxa, in species that display a wide range of social and reproductive behavior. It is often thought to evolve when independent breeding is constrained, and cooperation increases fitness. Yet many systems show variable, even maladaptive, fitness effects. This observation, together with the wide range in the form and frequency of cooperative breeding, raises the question of how the recurrent appearance of cooperative breeding and its extensive variation across species—from inducible to obligate—can be explained. Here, we take a proximate perspective on the evolution of cooperative breeding to argue that cooperative strategies are delineated by the history of prior adaptations and emerge through the rearrangement of preexisting neuroendocrine mechanisms underlying social, dispersal, and parental behaviors. Natural selection sorts among the resultant variants to alter regulation of cooperation, producing stabilization through either greater developmental entrenchment or greater reliance on environmental cues. Thus, species showing inducible cooperative behavior may be at a transitory stage in this process. To assess this possibility, we first evaluate evidence that the components of cooperative breeding are common across taxa. Then, we review the neuroendocrine mechanisms that regulate the pathways underlying cooperative strategies. Finally, we assess the evidence for neuroendocrine linkages during development that may channel coexpression of some components of cooperative breeding and facilitate its evolution. We conclude that understanding the mechanistic bases of the behaviors comprising cooperative breeding strategies may provide novel insight into the recurrent emergence of this strategy across disparate environments and avian taxa. LAY SUMMARY Cooperative breeding behavior involves 3 or more birds working together to raise young. It has evolved across a diversity of avian taxa and there is a wide range in how often it is expressed within species. How can the recurrent appearance of cooperative breeding and its extensive variation across species be explained? Here, we take a proximate perspective to argue that cooperative strategies appear because the behaviors comprising cooperative breeding are common, and the neuroendocrine mechanisms underlying these behaviors can be easily linked. Recent discoveries in neuroscience show that connections in the brain between neurons that regulate social behavior, parental care and dispersal are ancestral to birds and so this pre-existing network may facilitate the appearance of cooperative breeding across taxa. Understanding the mechanistic bases of cooperative breeding provides new insight into its evolution and provides a framework to explain the breadth and diversity of cooperative strategies.