Realistic genetic architecture enables organismal adaptation as predicted under the folk definition of inclusive fitness

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.

Adaptation in the face of internal conflict: the paradox of the organism revisited

“…Higher levels of trait distortion inevitably induce selection for suppression, maintaining the status quo of organismal optimality. Other models have argued similarly that cooperative genes ought to be more prevalent than exploitative genes (Fromhage & Jennions, 2019; Garcia‐Costoya & Fromhage, 2021). Consistent with theoretical predictions, genes suppressing selfish genetic elements have been described in numerous species (Hurst, Atlan & Bengtsson, 1996; Ågren & Clark, 2018).…”

Biological adaptation in light of the Lewontin–Williams (a)symmetry

“…Since such trends probably involve contributions from numerous genes, they should come to reflect the majority interest of the “parliament of genes” (Leigh 1971), which is to build organisms that achieve high fitness, or, more generally, inclusive fitness (Hamilton 1964; Fromhage and Jennions 2019). While the true genetic complexity of long‐term trends in adaptive evolution may be beyond mathematical description, simulations suggest that the parliament of genes’ majority interest will tend to prevail under realistic genetic assumptions (Scott and West 2019; Garcia‐Costoya and Fromhage 2021).…”