Accumulation of Deleterious Mutations in Endosymbionts: Muller's Ratchet with Two Levels of Selection

Abstract

Many eukaryotes host mutualistic, maternally transmitted prokaryotic symbionts. Two kinds of evolution within symbiont genomes threaten to erode the benefits of these associations. First, because symbionts reproduce asexually, are sequestered within hosts, and undergo bottlenecks at infection, they are subject to the long-term accumulation of deleterious mutations through Muller's ratchet. Second, "selfish" mutations, benefiting symbionts at host expense, could cause the ultimate decline of both host and symbionts. We performed simulations to assess how the fate of each mutation type is affected by host population size, numbers of symbionts transmitted to progeny, selection within and between hosts, and mutation rate. Fixation rate always increases with decreasing host population size. However, fixation rates for uniformly deleterious and selfish mutations are oppositely affected by varying transmission numbers, with increased numbers slowing accumulation of strictly deleterious mutations, especially for effects concentrated within hosts, but speeding fixation of "selfish" mutations. In aphid symbionts, most genes underlie basic cellular processes and are probably selected at both levels, but a substantial minority of genes contribute only to host fitness. No inoculum size is optimal for minimizing deleterious evolution for both categories of gene.

Mutation, Multilevel Selection, and the Evolution of Propagule Size during the Origin of Multicellularity

“…Stochastic population genetics models covering the case of two levels of selection are needed to investigate these questions. Simulation studies of such hostendosymbionts systems have already been performed (Rispe and Moran 2000).…”

Inheritance and recombination of mitochondrial genomes in plants, fungi and animals

“…This might be particularly likely given that the low rate of recombination required to counter mutation accumulation (Charlesworth et al ., 1993) may fall well below the current threshold of detection of methodologies for identifying mitochondrial recombination (M. Neiman and D. R. Taylor, unpublished). Moreover, there are additional mechanisms apart from mtDNA recombination that may provide an effective means of mutational clearance (Bergstrom & Pritchard, 1998; Martin & Herrmann, 1998; Rispe & Moran, 2000; Willett & Burton, 2003). Even if mutations are accumulating in mitochondrial genomes, the rate of accumulation is slow enough that severe fitness losses will occur on a time scale of tens of millions of years (Lynch & Blanchard, 1998).…”

Nematode-bacteria mutualism: Selection within the mutualism supersedes selection outside of the mutualism

“…). As a beneficial interaction becomes a major determinant of fitness for symbionts, selection to maintain a successful mutualism can be quite strong (Axelrod and Hamilton ; Bull and Rice ; Douglas ; Rispe and Moran ; Tamas et al. ; Regus et al.…”