UC San Diego

Abstract Background The emergence of organismal complexity has been a difficult subject for researchers because it is not readily amenable to investigation by experimental approaches. Complexity has a myriad of untested definitions and our understanding of its evolution comes primarily from static snapshots gleaned from organisms ranked on an intuitive scale. Fisher's geometric model of adaptation, which defines complexity as the number of phenotypes an organism exposes to natural selection, provides a theoretical framework to study complexity. Yet investigations of this model reveal phenotypic complexity as costly and therefore unlikely to emerge. Results We have developed a computational approach to study the emergence of complexity by subjecting neural networks to adaptive evolution in environments exacting different levels of demands. We monitored complexity by a variety of metrics. Top down metrics derived from Fisher's geometric model correlated better with the environmental demands than bottom up ones such as network size. Phenotypic complexity was found to increase towards an environment-dependent level through the emergence of restricted pleiotropy. Such pleiotropy, which confined the action of mutations to only a subset of traits, better tuned phenotypes in challenging environments. However, restricted pleiotropy also came at a cost in the form of a higher genetic load, as it required the maintenance by natural selection of more independent traits. Consequently, networks of different sizes converged in complexity when facing similar environment. Conclusions Phenotypic complexity evolved as a function of the demands of the selective pressures, rather than the physical properties of the network architecture, such as functional size. Our results show that complexity may be more predictable, and understandable, if analyzed from the perspective of the integrated task the organism performs, rather than the physical architecture used to accomplish such tasks. Thus, top down metrics emphasizing selection may be better for describing biological complexity than bottom up ones representing size and other physical attributes.