Nutrient status shapes selfish mitochondrial genome dynamics across different levels of selection.

Bryan L Gitschlag,Ann T Tate,Maulik R Patel

doi:10.7554/elife.56686

Abstract

Cooperation and cheating are widespread evolutionary strategies. While cheating confers an advantage to individual entities within a group, competition between groups favors cooperation. Selfish or cheater mitochondrial DNA (mtDNA) proliferates within hosts while being selected against at the level of host fitness. How does environment shape cheater dynamics across different selection levels? Focusing on food availability, we address this question using heteroplasmic Caenorhabditis elegans. We find that the proliferation of selfish mtDNA within hosts depends on nutrient status stimulating mtDNA biogenesis in the developing germline. Interestingly, mtDNA biogenesis is not sufficient for this proliferation, which also requires the stress-response transcription factor FoxO/DAF-16. At the level of host fitness, FoxO/DAF-16 also prevents food scarcity from accelerating the selection against selfish mtDNA. This suggests that the ability to cope with nutrient stress can promote host tolerance of cheaters. Our study delineates environmental effects on selfish mtDNA dynamics at different levels of selection.

Highlights

Life is generally organized into a hierarchy of cooperative collectives: multiple genes make up a genome, different genomes combine to form the eukaryotic cell, individual cells give rise to communities and multicellular organisms, and multicellular organisms are often organized into larger groups
How does resource availability shape the multilevel selection forces acting on selfish mitochondrial DNA (mtDNA)? We address this using the model species Caenorhabditis elegans harboring the well-characterized heteroplasmic mutant genome uaDf5 (Figure 1A,B), hereinafter referred to as DmtDNA (Ahier et al, 2018; Gitschlag et al, 2016; Liau et al, 2007; Lin et al, 2016; Tsang and Lemire, 2002)
The vast majority of mitochondrial content in the adult hermaphroditic nematode Caenorhabditis elegans is confined to the germline (Bratic et al, 2009), which exists as a contiguous syncytium of cytoplasm until the final stages of oocyte maturation (Pazdernik and Schedl, 2013)

Summary

Introduction

Life is generally organized into a hierarchy of cooperative collectives: multiple genes make up a genome, different genomes combine to form the eukaryotic cell, individual cells give rise to communities and multicellular organisms, and multicellular organisms are often organized into larger groups. By benefiting from the contributions of cooperators without reciprocating, cheaters gain a fitness advantage (Aktipis et al, 2015; Dobata et al, 2009; Ghoul et al, 2014; Strassmann et al, 2000) This advantage can break down at higher levels of biological organization, which rely on cooperation at lower levels (Aktipis et al, 2015; de Vargas Roditi et al, 2013; Fiegna and Velicer, 2003; Moreno-Fenoll et al, 2017; Rainey and Rainey, 2003; Wenseleers and Ratnieks, 2004). We conclude that food availability and resilience to food scarcity govern the relative fitness of the cooperators and cheaters both within and between collectives

Results

D Wildtype daf-2 ts

Discussion

20 Restricted diet Control diet

Materials and methods

Funding Funder