Early diet programs feeding circuits and food solicitation behavior

Abstract

From birth, offspring must balance internal energy state with the costs of signaling need to caregivers to secure nutrition for growth and healthy development. How diet during this period shapes the developing brain and behavior is a central question in biology, with growing relevance for understanding the developmental origins of metabolic disorders such as obesity. Yet the effects of early nutrition on growth, neural development, and behavior are rarely examined together within a single system. Here, we use poison frog tadpoles as a vertebrate model in which offspring develop outside a womb, can be reared independently under precisely controlled dietary conditions, and display diverse behaviors at a young age. By independently manipulating dietary quantity and quality, we link early nutrition to growth, brain development, and social behavior during ontogeny. Diet quantity increased body size, whereas diet quality accelerated development. Diet quality, but not quantity, shaped behavior: tadpoles fed a natural diet showed increased affiliation during food solicitation and reduced feeding, while aggression and risk avoidance remained unchanged. Diet also affected body and brain development differently, with artificial diets producing larger tadpoles but reduced volume in some brain regions, including areas associated with begging behavior. Anorexigenic urocortin-1 neurons were active during begging behavior and, together with another anorexigenic midbrain population, decreased in abundance under an artificial diet. Functionally, urocortin-1 reduced feeding without directly increasing begging, suggesting it gates socio-positive behavior by suppressing a competing drive rather than initiating it. Together, this work shows that dietary quantity and quality act on distinct developmental processes, with diet quality programming the brain circuits that permit begging behavior while growth is determined by food quantity.