Evolutionary construction by staying together and coming together

• Published in: Journal of theoretical biology 2013-03, Vol.320, p.10-22
• Main Authors: Tarnita, Corina E., Taubes, Clifford H., Nowak, Martin A.
• Format: Article
• Language: English
• Subjects: Animals; Biological Evolution; Complexity; equations; Eukaryotic Cells - physiology; Evolutionary game theory; games; labor; Models, Biological; Multicellularity; mutation; natural selection; Origin of Life; reproduction
• ISSN: 0022-5193; 1095-8541
• DOI: 10.1016/j.jtbi.2012.11.022

The evolutionary trajectory of life on earth is one of increasing size and complexity. Yet the standard equations of evolutionary dynamics describe mutation and selection among similar organisms that compete on the same level of organization. Here we begin to outline a mathematical theory that might help to explore how evolution can be constructive, how natural selection can lead from lower to higher levels of organization. We distinguish two fundamental operations, which we call ‘staying together’ and ‘coming together’. Staying together means that individuals form larger units by not separating after reproduction, while coming together means that independent individuals form aggregates. Staying together can lead to specialization and division of labor, but the developmental program must evolve in the basic unit. Coming together can be creative by combining units with different properties. Both operations have been identified in the context of multicellularity, but they have been treated very similarly. Here we point out that staying together and coming together can be found at every level of biological construction and moreover that they face different evolutionary problems. The distinction is particularly clear in the context of cooperation and defection. For staying together the stability of cooperation takes the form of a developmental error threshold, while coming together leads to evolutionary games and requires a mechanism for the evolution of cooperation. We use our models to discuss simple aspects of the evolution of protocells, eukarya, multi-cellularity and animal societies. ► Mathematical theory that explores how evolution can be constructive. ► Two fundamental operations: ‘staying together’ (ST) and ‘coming together’ (CT). ► ST-individuals form larger units by not separating after reproduction. ► CT-independent individuals form aggregates. ► ST and CT are very different mechanisms.