Abstract

A fundamental task of evolutionary biology is to explain the pervasive impression of organismal design in nature, including traits benefiting kin. Inclusive fitness is considered by many to be a crucial piece in this puzzle, despite ongoing discussion about its scope and limitations. Here, we use individual-based simulations to study what quantity (if any) individual organisms become adapted to maximize when genetic architectures are more or less suitable for the presumed main driver of biological adaptation, namely cumulative multi-locus evolution. As an expository device, we focus on a hypothetical situation called Charlesworth's paradox, in which altruism is seemingly predicted to evolve, yet altruists immediately perish along with their altruistic genes. Our results support a recently proposed re-definition of inclusive fitness, which is concerned with the adaptive design of whole organisms as shaped by multi-locus evolution, rather than with selection for any focal gene. They also illustrate how our conceptual understanding of adaptation at the phenotypic level should inform our choice of genetic assumptions in abstract simplified models.

Highlights

  • A central idea in evolutionary theory is that natural selection shapes organisms through a process of cumulative improvement (Darwin, 1859; Dawkins, 1986)

  • Fromhage and Jennions (2019) have argued that their version of inclusive fitness theory applies to multi-­locus evolution involving genes of various effect sizes, requiring no general assumption of ‘weak selection’

  • We mostly found close agreement between our simulations and predictions of IFfolk theory (Figures 1–­3)

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Summary

Introduction

A central idea in evolutionary theory is that natural selection shapes organisms through a process of cumulative improvement (Darwin, 1859; Dawkins, 1986). By contrast, Fromhage and Jennions (2019) have argued that their version of inclusive fitness theory applies to multi-­locus evolution involving genes of various effect sizes, requiring no general assumption of ‘weak selection’.

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