A "double tale" of module creation in evolving networks

Abstract

In biology, structure is driven by accretion and change. Accretion brings together disparate parts to form bigger wholes, while change provides opportunities for growth and innovation. Here we review patterns and processes that are responsible for a "double tale" of evolutionary accretion and change at various levels of complexity. We focus on proteins and nucleic acids. In our "linkage" model, parts are at first weakly linked and associate variously. As they diversify, they compete with each other and are selected for performance. The emerging interactions constrain their structure and associations. This causes parts to self-organize into modules with tight linkage. In a second phase, variants of the modules evolve and become new parts for a new generative cycle of higher-level organization. As a way forward, we formalized the concept of linkage with a network in which nodes represent parts and links describe node interactions, predicting that the "double tale" induces both hierarchy and modularity in evolving networks. Remarkably, evolutionary genomics and network biology support the linkage hypothesis and validate an evolutionary "principle of granularity" that drives the gain and loss of modules. © 2021 Elsevier B.V., All rights reserved.