The Impact of Male-Killing Bacteria on Host Evolutionary Processes

Abstract

Male-killing bacteria are maternally inherited endosymbionts that selectively kill male offspring of their arthropod hosts. Using both analytical techniques and computer simulations, we studied the impact of these bacteria on the population genetics of their hosts. In particular, we derived and corroborated formulas for the fixation probability of mutant alleles, mean times to fixation and fixation or extinction, and heterozygosity for varying male-killer prevalence. Our results demonstrate that infections with male-killing bacteria impede the spread of beneficial alleles, facilitate the spread of deleterious alleles, and reduce genetic variation. The reason for this lies in the strongly reduced fitness of infected females combined with no or very limited gene flow from infected females to uninfected individuals. These two properties of malekiller-infected populations reduce the population size relevant for the initial emergence and spread of mutations. In contrast, use of Wright's equation relating sex ratio to effective population size produces misleading predictions. We discuss the relationship to the similar effect of background selection, the impact of other sex-ratio-distorting endosymbionts, and how our results affect the interpretation of empirical data on genetic variation in male-killer-infected populations. . To our knowledge, there is only one study on the impact of male-killing bacteria on the population genetics of nuclear genes (Telschow et al. 2006). In this theoretical investigation, the process of host adaptation was analyzed in a two-island model, and it was demonstrated that adaptation can be impeded when one population is infected with male-killing bacteria and the other is not infected.Here, we investigate the interplay between selection and drift acting on nuclear alleles in populations infected with male-killing bacteria. We present both analytic approximations and simulation results on the probability of fixation of mutant alleles, the rate of evolution, and expected times until fixation or extinction of alleles. We demonstrate that with respect to these quantities, a male-killer-infected population behaves approximately as it would if it consisted of uninfected individuals only. This means, for example, that the probability of fixation of deleterious alleles is increased in infected compared to uninfected populations, while beneficial alleles have a lower chance of fixation in infected populations. This effect is not due to the distorted population sex ratio, but stems from the peculiar inheritance pattern of nuclear alleles in male-killerinfected populations, in which gene flow from infected to uninfected individuals is constrained. The effects are observed even when the male-killer is inefficiently transmitted.

The Effective Size of Populations Infected With Cytoplasmic Sex-Ratio Distorters

“…This result has been anticipated through verbal arguments (Sullivan and Jaenike 2006;Engelstädter and Hurst 2007) and was also confirmed in computer simulations (Engelstädter and Hurst 2007).…”

“…[With fast fluctuations in population size, N e is given by the harmonic mean of the actual sizes of the population, which is smaller than the arithmetic mean (Kimura and Crow 1963;Sjö din et al 2005)]. For the case of male-killing bacteria, this reasoning is in accord with simulation results by Engelstädter and Hurst (2007).…”

“…In some special cases, this formula can be reduced considerably. In particular, the nuclear effective size of a male-killer infected population is often given to a good approximation by twice the number of uninfected individuals, a simple result obtained previously through verbal arguments and computer simulations (Sullivan and Jaenike 2006;Engelstädter and Hurst 2007). In situations where feminizing microbes have become fixed in the population, N e is given by Wright's wellknown formula for sex-biased populations (Wright 1931).…”

“…In other words, the equilibrium N e equals approximately the number of infected females in this case. Conversely, for nuclear host genes, Engelstädter and Hurst (2007) showed through computer simulations that to a good approximation, a male-killer infected population behaves as if only uninfected individuals were present.…”

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“…The consequences of a highly distorted sex ratio are likely to be large (for discussions of 256 evolutionary consequences see (Charlat, Hurst & Mercot, 2003;Engelstädter & Hurst, 2007)). 257 As perhaps can be expected, one direct effect is that a large number of females remain unmated.…”