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

Abstract

The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within‐organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi‐level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness‐maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.

Conflict and conflict resolution in the major transitions

“…This is timely because evolutionary conflict of all kinds is increasingly recognized as exerting a profound influence on evolution (e.g. [5,25,26]; current special feature). In addition, there has been renewed interest in how conflict affects the major transitions [5,[16][17][18]27].…”

Open questions in the social lives of viruses

“…There is an analogy here with the on-going effort to define an organism within evolutionary biology, as well as with the related field that studies major transitions in individuality (Bourke, 2011;Díaz-Muñoz et al, 2016;Maynard Smith & Szathmary, 1995;Okasha, 2009;Patten et al, 2023;Queller & Strassmann, 2009;West et al, 2015).…”

“…At the other end of the scale, does the presence of selfish genetic elements, such as homing endonucleases in T4 phages, generate sufficient conflict to undermine individual viral genomes themselves as cohesive evolutionary units (Edgell et al, 2010;Gardner & Úbeda, 2017;Patten et al, 2023)? Finally, how do concepts of evolutionary individuality apply when viral genomes are themselves split into different segments (segmented viruses), and especially when those segments can transmit independently (multipartite viruses) (Holmes, 2009;Leeks et al, 2023;Lucía-Sanz & Manrubia, 2017;Michalakis & Blanc, 2020)?…”

Quantifying internal conflicts and their threats to organismal form and fitness

“…Recently, we have outlined how selfish sub-organismal elements use two main strategies to achieve this: distorting their numerical representation (transmission distorters) or distorting organismal traits in order to maximize their own fitness rather than that of their organism (trait distorters) (Patten et al, 2023). A quintessential example of a transmission distorter is a homing endonuclease gene.…”