Modification of feeding circuits in the evolution of social behavior

Abstract

Adaptive trade-offs between foraging and social behavior intuitively explain many aspects of individual decision-making. Given the intimate connection between social behavior and feeding/foraging at the behavioral level, we propose that social behaviors are linked to foraging on a mechanistic level, and that modifications of feeding circuits are crucial in the evolution of complex social behaviors. In this Review, we first highlight the overlap between mechanisms underlying foraging and parental care and then expand this argument to consider the manipulation of feeding-related pathways in the evolution of other complex social behaviors. We include examples from diverse taxa to highlight that the independent evolution of complex social behaviors is a variation on the theme of feeding circuit modification.

Ethological principles predict the neuropeptides co-opted to influence parenting

“…At a minimum, the evolutionary transition from asociality (social interactions limited to mating) to subsociality (extensive social interactions between parents and offspring involving parental care) is predicted to require modification of several contributing behaviours including tendencies for dispersal, feeding, mating, aggression and tolerance of social interactions [1][2][3] . Caring parents no longer disperse from a mating site, they provision food rather than feed themselves, they pause reproduction and mating, they show aggression to protect offspring and shared resources rather than their own resources, and they tolerate the presence of others and increased social interactions [1][2][3][4]6 . The early ethological literature therefore predicts that parental care evolves only when there are suitable behavioural and ecological precursors present within the evolutionary ancestor, such as nest building, defensive postures and aggression, and potentially shared resources 2,3 .…”

Hormonal and neural correlates of care in active versus observing poison frog parents

“…One notable example is the increase in neuropeptide Y expression during tadpole transport in both caring males and observing female frogs. Neuropeptide Y (NPY) is most commonly associated with feeding behavior but several recent reviews have highlighted the adaptive trade-offs between feeding and social behavior and suggesting the circuitry mediating these behaviors is interconnected (Fischer and O'Connell, 2017;Gammie and Nelson, 1999;O'Rourke and Renn, 2015). Indeed, additional peptides and receptors commonly implicated in feeding behavior were also differentially expressed, including bombesin and cholecystokinin in males, and galanin and insulin-like growth factor receptors in females.…”

Evolutionary diversity as a catalyst for biological discovery

“…It has been proposed that evolutionary plasticity within common neurobehavioral substrates—including reward/reinforcement, feeding/foraging, sexual, aggression, and maternal behavior circuits; conserved neuromodulatory systems, including steroid hormone, oxytocin (OT), vasopressin (AVP), and dopamine systems; and conserved transcriptional “toolkits”—has repeatedly contributed to the evolution of convergent social behavioral phenotypes (Ament et al, 2010; Fischer & O’Connell, 2017; Johnson & Young, 2017; Newman, 1999; Numan & Young, 2016; Rittschof & Robinson, 2016; Toth et al, 2007). In vertebrates, these systems are thought to function and interact within a broader “social decision-making” neural network with a predominantly conserved core neuroanatomical architecture (O’Connell & Hofmann, 2011).…”

“…However, the degree to which shared mechanistic pathways contribute to convergent social behavioral evolution remains unclear. It has been proposed that evolutionary plasticity within common neural and genetic networks (including: reward/reinforcement, feeding/foraging, sexual, aggression and maternal behavior neural circuits; conserved neuromodulatory systems, encompassing steroid hormone, oxytocin [OT], vasopressin [AVP] and dopamine systems; and conserved transcriptional "toolkits") has contributed to the convergent evolution of multiple rare social behavioral phenotypes (Newman 1999;Toth et al 2007;Ament et al 2010;Numan & Young 2016;Rittschof & Robinson 2016;Fischer & O'Connell 2017;. In vertebrates, many of these neural systems are thought to function and interact within a broader "social decision-making" network with a predominantly conserved core neuroanatomical architecture (O'Connell & Hofmann 2011).…”