Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae

Abstract

The somatic accumulation of defective mitochondria causes human degenerative syndromes, senescence in fungi, and male sterility in plants. These diverse phenomena may result from conflicts between natural selection at different levels of organization. Such conflicts are fundamental to the evolution of cooperating groups, from cells to populations. We present a model in which defective mitochondrial genomes accumulate because of a within-cell replication advantage when among-cell selection for efficient respiration is relaxed. We tested the model by using experimental populations of the yeast Saccharomyces cerevisiae. We constructed yeast strains that were heteroplasmic for mitochondrial mutations that destroy the ability to respire (the petite phenotype) and followed the accumulation of mitochondrial defects in cultures with different effective population sizes. As predicted by the model, the inability to respire evolved only in small populations of S. cerevisiae, where among-cell selection favoring cells that can respire was reduced relative to within-cell selection favoring parasitic mitochondria. In a control experiment, mitochondrial point mutations that confer resistance to chloramphenicol showed no tendency to change in frequency under any culture conditions. The accumulation of some mitochondrial defects is therefore an evolutionary process, involving multiple levels of selection. The relative intensities of within-and among-cell selection may also explain the tissue specificity of human mitochondrial defects.

Bcl‐2 family proteins: The sentinels of the mitochondrial apoptosis pathway

“…Implicit in the term ''symbiont'' is the mutual beneficial association between the two interacting partners. However, to a great extent, the functional mitochondrial genomes are altruistic; they contribute to the respiration machinery of the cell at the expense of their own rate of replication (1). Further, mitochondrial genomes have, to some extent, undergone a streamlining process or ''reductive evolution'' (2), leading to a marked loss of coding capacity compared with that of their closest eubacterial relatives.…”

Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects inNeurospora

“…Although there is substantial circumstantial evidence for the significance of high relatedness among the mtDNA within an individual, direct evidence supporting this hypothesis is scarce [4,18]. In this paper, we experimentally study the significance of high relatedness among the mtDNAs within an individual for selection among individuals against dysfunctional selfish mtDNA variants.…”

“…by a replication benefit) can increase in frequency even if these decrease individual-level fitness [3]. Such selfish mitochondrial mutants are well known from yeast [4]. With a frequency of about 1%, yeast cells mutate to form mini colonies containing far fewer cells than the wild-type.…”

“…Selection within cells and among individuals (or cells) can thus act in opposite directions, creating a genetic conflict [4,5]. Selection between individuals favours functional mtDNA genomes, whereas selection within cells may favour selfish, less functional, variants.…”

Genetic analysis of metapopulation processes in Silene latifolia

“…Theoretical and empirical studies have indicated that multilevel selection in structured populations may be important in explaining diverse biological phenomena, including the evolution of social behavior (FRANK 1998;HAMILTON 1996;HAMILTON 1964;WILSON 1997), intragenomic conflict (HURST et al 1996INGVARSSON and TAYLOR 2002;TAYLOR et al 2002), reduced pathogen virulence (KERR et al 2006;, sex ratio evolution (MCCAULEY and TAYLOR 1997;OLSON et al 2005), and the origins of multi-cellularity (MICHOD 1997;MICHOD 1999;SZATHMARY and SMITH 1995) . Recent conceptions of multilevel selection theory have broadened its applicability by recognizing that the effects of group membership on individual fitness, so-called contextual effects (HEISLER and DAMUTH 1987), is a group-level effect that can be distinguished from a group's potential to give rise to other groups (HEISLER and DAMUTH 1987;OKASHA 2004; so-called multilevel selection 1 (MS1) and MS2, respectively) .…”