The Strategic Reference Gene: an organismal theory of inclusive fitness

TL;DR

This paper proposes a broader and more justified definition of inclusive fitness that applies to organisms, emphasizing the importance of maximizing offspring and relatives' offspring, based on the genome's 'majority interest' in gene propagation.

Contribution

It introduces a new organismal theory of inclusive fitness that extends its applicability beyond previous limitations, emphasizing genome-level interests.

Findings

Inclusive fitness can be applied under broader conditions than previously thought.

Organisms are predicted to maximize their total reproductive output and relatives' offspring, weighted by relatedness.

Most phenotypes appear designed to maximize gene propagation in individuals and relatives.

Abstract

How to define and use the concept of inclusive fitness is a contentious topic in evolutionary theory. Inclusive fitness can be used to calculate selection on a focal gene, but it is also applied to whole organisms. Individuals are then predicted to appear designed as if to maximise their inclusive fitness, provided that certain conditions are met (formally when interactions between individuals are 'additive'). Here we argue that applying the concept of inclusive fitness to organisms is justified under far broader conditions than previously shown, but only if it is appropriately defined. Specifically, we propose that organisms should maximise the sum of their offspring (including any accrued due to the behaviour/phenotype of relatives), plus any effects on their relatives' offspring production, weighted by relatedness. In contrast, most theoreticians have argued that a focal individual's inclusive fitness should exclude any offspring accrued due to the behaviour of relatives. Our approach is based on the notion that long-term evolution follows the genome's 'majority interest' of building coherent bodies that are efficient 'vehicles' for gene propagation. A gene favoured by selection that reduces the propagation of unlinked genes at other loci (e.g. meiotic segregation distorters that lower sperm production) is eventually neutralised by counter-selection throughout the rest of the genome. Most phenotypes will therefore appear as if designed to maximise the propagation of any given gene in a focal individual and its relatives.