Early diet programs feeding circuits and food solicitation behavior

From birth, offspring must balance internal energy state with the costs of signaling need to caregivers to secure nutrition for growth and healthy development. Although appetite-regulating networks are organized early in life, whether variation in diet programs their development and subsequent behavioral outputs is understudied. Here, we use poison frog tadpoles as a vertebrate model in which offspring develop outside of a womb, can be reared independently under precisely controlled dietary conditions and display diverse behaviors at young age. By independently manipulating dietary quantity and quality, we link early nutrition to growth, brain development, and social behavior during ontogeny. We found that diet quantity increased body size, whereas diet quality accelerated development. Diet quality, but not quantity, shaped behavior, where tadpoles fed a natural diet showed increased affiliation during food solicitation and reduced feeding, while aggression and risk avoidance remained unchanged. Diet affected body and brain development differently, where artificial diets produced larger tadpoles with reduced brain volume in some regions, including areas associated with begging behavior. Anorexigenic urocortin-1 neurons were active during begging behavior and decreased in their abundance, together with another anorexigenic midbrain population, under an artificial diet. Functionally, urocortin-1 reduced feeding without directly increasing begging, indicating that it might gate socio-positive behavior by suppressing a competing drive. Together, this work suggests the quality of diet during development programs brain circuits that permit begging behavior, while growth is determined by food quantity. Significance: How early-life nutrition shapes the developing brain and behavior is a central question in biology and is increasingly relevant to understanding the developmental origins of metabolic disorders such as obesity. Yet most studies examine growth, neural development, or behavior in isolation and often long after critical developmental windows have closed. Using poison frog tadpoles, we experimentally disentangle the effects of dietary quantity and quality during development and show that these nutritional dimensions regulate distinct biological processes. While food quantity primarily determines somatic growth, dietary quality programs region-specific brain development and selectively modifies social food-solicitation behavior. We further demonstrate that dietary quality shapes the development of conserved anorexigenic neuron populations, including urocortin-1 and CART-expressing neurons, and that urocortin-1 functionally suppresses feeding during social engagement. By linking diet, neural circuit organization, and juvenile social behavior within a single system, this work demonstrates that nutritional quality, not just caloric intake, shapes the development of appetite-regulating circuits that influence early-life behavior.