Neuromodulation and the toolkit for behavioural evolution: can ecdysis shed light on an old problem?

• Published in: The FEBS journal 2024-03, Vol.291 (6), p.1049-1079
• Main Authors: Sullivan, Luis F., Barker, Matthew S., Felix, Princess C., Vuong, Richard Q., White, Benjamin H.
• Format: Article
• Language: English
• Subjects: Animal behavior; Behavior; Brain; Circuits; Ecdysozoa; Ecological adaptation; Evolution; Evo‐Devo; Genomes; GPCR; Molting; motor programme; Neuromodulation; neuropeptide; Substrates
• ISSN: 1742-464X; 1742-4658
• DOI: 10.1111/febs.16650

The geneticist Thomas Dobzhansky famously declared: ’Nothing in biology makes sense except in the light of evolution’. A key evolutionary adaptation of Metazoa is directed movement, which has been elaborated into a spectacularly varied number of behaviours in animal clades. The mechanisms by which animal behaviours have evolved, however, remain unresolved. This is due, in part, to the indirect control of behaviour by the genome, which provides the components for both building and operating the brain circuits that generate behaviour. These brain circuits are adapted to respond flexibly to environmental contingencies and physiological needs and can change as a function of experience. The resulting plasticity of behavioural expression makes it difficult to characterize homologous elements of behaviour and to track their evolution. Here, we evaluate progress in identifying the genetic substrates of behavioural evolution and suggest that examining adaptive changes in neuromodulatory signalling may be a particularly productive focus for future studies. We propose that the behavioural sequences used by ecdysozoans to moult are an attractive model for studying the role of neuromodulation in behavioural evolution. Altered neuromodulatory signalling via GPCRs frequently underlies evolutionary changes in behaviour. GPCRs and their ligands might thus represent a ‘toolkit’ akin to the Evo‐Devo toolkit responsible for animal development. Just as evolutionary changes in the Evo‐Devo toolkit can alter gene regulatory network function and morphology, changes in neuromodulatory toolkit genes may alter neural circuit function and behaviour. Moulting behaviours used by ecdysozoans may facilitate the study of neuromodulation's role in evolution.