The gene’s eye view that forged a neo-Darwinian synthesis

Abstract The gene’s eye view of adaptive evolution was conceptualized in the 1960s by W.D. Hamilton and G.C. Williams, inspired primarily by R.A. Fisher’s theoretical genetics and David Lack’s and Niko Tinbergen’s empirical research. In the decades that followed, the new inclusive fitness view of individuals as optimizing agents facing trade-offs, opportunity costs, and reproductive conflicts was further developed and disseminated mainly by Robert Trivers, Richard Dawkins, John Maynard Smith, and Helena Cronin. Because neo-Darwinism originally arose in the UK and the modern synthesis was forged in the US, differences in emphasis on adaptive versus non-adaptive evolution persisted across the Atlantic throughout the 20th century. The gene’s eye theory of adaptation offered groundbreaking and often counterintuitive understanding of the evolution of somatic senescence, parent–offspring conflict, clutch-size optimization, and the costs and benefits of animal aggression—shedding general light on how cooperation and conflict are shaped by natural selection. In this chapter I explain the fundamental logic of Hamilton’s rule as it emerged from inclusive fitness theory, using the most general notation possible, and I briefly review the principle of co-replication as a key concept for understanding how potentially conflicting social and life-history traits are maintained by natural selection. I also highlight the two major assumptions behind the gene’s eye view of adaptation: optimality principles as drivers of naturally selected adaptive design and the simplification of genetics to breeding values for complex phenotypic traits. I then summarize theoretical advances and empirical research efforts that were instrumental for completing a neo-Darwinian synthesis of organismal biology towards the end of the 20th century.