Coordinating morphology with behavior during development: An integrative approach from a fly perspective

Abstract

Animals in the wild live in highly variable and unpredictable environments. This variation in their habitat induces animals, at all stages of their development, to make decisions about what to eat, where to live, and with whom to associate. Additionally, animals like insects show dramatic restructuring of their morphology across life stages, which is accompanied by alterations in their behavior to match stage-specific functions. Finally, in a process called developmental plasticity, environmental conditions feed back onto developmental mechanisms producing animals with stage-specific variation in both morphological and behavioral traits. In this review, we use examples from insects to explore the idea that animals are integrated units where stage-specific morphological and neurological traits develop together to increase individual fitness within their natural environments. We hypothesize that the same mechanisms act to alter both morphological and behavioral traits in response to the environment in which an organism develops. For example, in insects the steroid hormone ecdysone orchestrates the restructuring of the body from larva to adult form during metamorphosis at the same time as it rebuilds the central nervous system. The remodeling of both body form and nervous system structure results in behavioral alterations that match the morphological functions of the emerging adult. We review relevant findings from the fruit fly Drosophila melanogaster, combining insights from different fields like developmental biology, neurobiology and developmental plasticity. Finally, we highlight how insights drawn from D. melanogaster can be used as a model in future efforts to understand how developmental processes modify behavioral responses to environmental change in a stage-specific manner in other animals.