Communication theory and multicellular biology

In this Perspective, we propose that communication theory--a field of mathematics concerned with the problems of signal transmission, reception and processing--provides a new quantitative lens for investigating multicellular biology, ancient and modern. What underpins the cohesive organisation and collective behaviour of multicellular ecosystems such as microbial colonies and communities (microbiomes) and multicellular organisms such as plants and animals, whether built of simple tissue layers (sponges) or of complex differentiated cells arranged in tissues and organs (members of the 35 or so phyla of the subkingdom Metazoa)? How do mammalian tissues and organs develop, maintain their architecture, become subverted in disease, and decline with age? How did single-celled organisms coalesce to produce many-celled forms that evolved and diversified into the varied multicellular organisms in existence today? Some answers can be found in the blueprints or recipes encoded in (epi)genomes, yet others lie in the generic physical properties of biological matter such as the ability of cell aggregates to attain a certain complexity in size, shape, and pattern. We suggest that Lasswell's maxim "Who says what to whom in what channel with what effect" provides a foundation for understanding not only the emergence and evolution of multicellularity, but also the assembly and sculpting of multicellular ecosystems and many-celled structures, whether of natural or human-engineered origin. We explore how the abstraction of communication theory as an organising principle for multicellular biology could be realised. We highlight the inherent ability of communication theory to be blind to molecular and/or genetic mechanisms. We describe selected applications that analyse the physics of communication and use energy efficiency as a central tenet. Whilst communication theory has and could contribute to understanding a myriad of problems in biology, investigations of multicellular biology could, in turn, lead to advances in communication theory, especially in the still immature field of network information theory.