Bridging non-replicating and replicating living systems in a unitary evolutionary framework

Wong et al. (PNAS, 2023, https://doi.org/10.1073/pnas.2310223120 [1]) recently introduced a revolutionary perspective by proposing “selection for function” as a universal mechanism of evolution, extending beyond self-replicating entities to encompass non-living systems such as minerals and stars. While they suggested that biological evolution could be understood within this broader framework, they did not fully explore how it aligns with or challenges classical Darwinian selection. Our article directly addresses this gap. In this work, best described as a Critical Review rather than a classical survey, we propose a conceptual integration between Darwinian selection and “selection for function,” demonstrating how these complementary processes jointly shape evolutionary trajectories. By doing so, we provide a unified framework that links self-reproducing and non-reproducing entities, thereby advancing evolutionary theory beyond its traditional boundaries. This novel synthesis has important implications for longstanding debates on the origin of life, the evolution of sex, and group or species selection, and also opens new avenues for applied fields such as cancer biology and microbial resistance. We believe we are particularly well suited to write this Critical Review. Our consortium brings together internationally recognized experts in evolutionary biology, theoretical ecology, and philosophy of biology, all with strong publication records across these domains (e.g., Thomas et al. [2],[3],[4]; Hamant [5]; Selosse [6]). This diversity of expertise ensures a rigorous and balanced synthesis of both theoretical and empirical aspects. This diversity of expertise ensures a rigorous and balanced synthesis of both theoretical and empirical aspects. Importantly, our Review differs from recent contributions in the field. For example, Lynch [7] has raised doubts about the generality of “selection for function,” while Jaeger [8] critiqued Assembly Theory for overextending evolutionary principles. Unlike these external commentaries, our work offers a constructive, framework-building effort that situates “selection for function” squarely within mainstream evolutionary biology. Furthermore, whereas Doolittle & Inkpen [9] or Bouchard [10] emphasized non-replicative dynamics at ecosystem or Gaia scales, our Review provides concrete biological case studies (e.g., tumors, dormancy, microbial biofilms, mutualisms) that demonstrate how “selection for function” interacts with Darwinian selection across multiple levels of organization. We are convinced that this Critical Review moves the field forward by offering an integrative and testable framework, expanding the conceptual reach of evolutionary theory while remaining firmly grounded in empirical biology. References 1. Wong, M. L., Cleland, C. E., Arend, D., Jr, Bartlett, S., Cleaves, H. J., 2nd, Demarest, H., Prabhu, A., Lunine, J. I., & Hazen RM. On the roles of function and selection in evolving systems. Proceedings of the National Academy of Sciences of the United States of America, 120(43), e2310223120 https://doi.org/101073/pnas2310223120. 2023. 2. Thomas, F. DeGregori, J. Marusyk, A. Dujon, A.M., Ujvari, B., Capp JPGBNAM. A New Perspective on Tumor Progression: Evolution via Selection for Function,. Evolution, Medicine, and Public Health. 2024;eoae021, h. 3. Thomas, F., Capp, J.-P., Dujon, A. M., Marusyk, A., Asselin, K., Campone, M., Pujol, P., Alix-Panabières, C., Roche, B., Ujvari, B., Gatenby, R., & Nedelcu AM. Leveraging selection for function in tumor evolution: System-level cancer therapies. Evolution, Medicine and Public Health. 2025;Accepted. 4. Dujon AM, Asselin K, Lemaître JF, Capp JP, Pujol P, Ujvari B, DeGregori J, Nedelcu AM TF. The Role of Selection for Function in Aging and Chronic Diseases: A Novel Evolutionary. Aging Cell. 2025;in press. 5. Hamant O (2024). Is incoherence required for sustainability? The Anthropocene Review. 2024;https://do. 6. Selosse MA, Rousset F. The plant-fungal marketplace. Science. 2011. doi:10.1126/science.1210722 7. Lynch M (2025). Complexity myths and the misappropriation of evolutionary theory. Proceedings of the National Academy of Sciences of the United States of America. 2025;122(23), h. 8. Jaeger J. Assembly Theory: What It Does and What It Does Not Do. Journal of Molecular Evolution. 2024. doi:10.1007/s00239-024-10163-2 9. Ford Doolittle W, Andrew Inkpen S. Processes and patterns of interaction as units of selection: An introduction to ITSNTS thinking. Proceedings of the National Academy of Sciences of the United States of America. 2018. doi:10.1073/pnas.1722232115 10. Bouchard F. Ecosystem Evolution is About Variation and Persistence, not Populations and Reproduction. Biological Theory. 2014;9. doi:10.1007/s13752-014-0171-1