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.