How Can Sex Ratio Distorters Reach Extreme Prevalences? Male-Killing Wolbachia Are Not Suppressed and Have Near-Perfect Vertical Transmission Efficiency in Acraea Encedon

Jiggins, Francis M.; Randerson, James P; Hurst, Gregory D. D.; Majerus, Michael E. N.

doi:10.1111/j.0014-3820.2002.tb00152.x

Cited by 56 publications

(49 citation statements)

References 23 publications

(31 reference statements)

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“…Further, it should also be noted that although our study is unique in its combination of extreme bias and historical data, other studies have also failed to find resistance to selfish genetic elements in natural populations Fertility is given as percentage of eggs laid showing some sign of development, with interquartile range in parentheses. (19)(20)(21)(22). Most pertinently, there is the case of sex-ratio meiotic drive in Drosophila pseudoobscura.…”

Section: Discussionmentioning

confidence: 99%

Persistence of an extreme sex-ratio bias in a natural population

Dyson

Hurst

2004

Proc. Natl. Acad. Sci. U.S.A.

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185

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The sex ratio is a key parameter in the evolution and ecology of a species. Selfish genetic elements that bias the sex ratio of affected individuals are well known and characterized, but their effect on populations has been considered limited, because either the element does not achieve high prevalence or the host rapidly evolves resistance to the distorting element, reducing its prevalence. We tested whether the host necessarily prevails by using a butterfly system where records from the early part of the 20th century reported extreme sex-ratio bias in nature. We reexamined this population and found the bias was present today, 400 generations after the original record, with a population sex ratio of 100 females per male. The sex-ratio bias was associated with the presence of a heritable male-killing Wolbachia infection in 99% of adult females, against which the host butterfly has failed to evolve resistance. The resultant dearth of males causes an average 57% reduction in the reproductive output of adult females. Persistence of the population despite the very high frequency of the sex-ratio distorter appears to be associated with the ability of males to mate >50 times in their life combined with a high intrinsic rate of increase of the species.

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Section: Discussionmentioning

confidence: 99%

Persistence of an extreme sex-ratio bias in a natural population

Dyson

Hurst

2004

Proc. Natl. Acad. Sci. U.S.A.

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185

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“…This is because first, linkage of all newly arisen alleles in infected females to the male-killing element is complete or at least very high. Linkage here corresponds to the vertical transmission rate of the male-killing bacteria, for which quantity values in the range of 0.8-1 have been reported in natural and laboratory populations of various insect species (Hurst and Majerus 1993 and references therein;Jiggins et al 2002;Dyer and Jaenike 2004). Second, despite their being strongly deleterious to nuclear alleles, male-killing bacteria carry a drive and can be stably maintained in populations at high frequencies (Dyer and Jaenike 2004;Dyson and Hurst 2004).…”

Section: Imperfect Transmissionmentioning

confidence: 97%

“…populations infected with male-killing bacteria (e.g., Jiggins et al 2002;Dyson and Hurst 2004). Moreover, we assume that the prevalence of the male-killing bacteria and the population sex ratio remain constant over the time frame under consideration.…”

Section: The Modelmentioning

confidence: 99%

“…However, in many cases, infected females also produce some uninfected offspring. Transmission rates ranging from 80 to 100% have been reported, although they are usually in the range of 95-100% (Hurst and Majerus 1993;Jiggins et al 2002;Dyer and Jaenike 2004). Thus, let us now assume that only a proportion a ð0:67 , a , 1Þ of the offspring of infected females inherit the infection, and (1 À a) of the offspring are uninfected (a .…”

Section: Imperfect Transmissionmentioning

confidence: 99%

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The Impact of Male-Killing Bacteria on Host Evolutionary Processes

Engelstädter

Hurst

2007

Genetics

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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.

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“…This "best" malekiller does not seem to occur among those that infect coccinellids. In none is the vertical transmission efficiency perfect (Table 1), in A. decempunctata and Cheilomenes sexmaculatus, infected males sometimes survive to adulthood Majerus, 2003a), and in all coccinellid cases studied (but not in one butterfly species (Jiggins et al, 2002)), male-killers have been shown to have direct costs on infected females (Matsuka et al, 1975;Hurst et al, 1994;Majerus, 2003a). Why is this the case?…”

Section: Selection On Host Nuclear Genomes: Vertical Transmission Sumentioning

confidence: 99%

The impact of male-killing bacteria on the evolution of aphidophagous coccinellids

Majerus¹

2006

Eur. J. Entomol.

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Abstract. Many aphidophagous coccinellids harbour male-killing bacteria. These maternally inherited bacteria kill males early in embryogenesis, female offspring of infected mothers gaining a large resource advantage from the consumption of their dead brothers. In this paper, the diversity of male-killing bacteria and their coccinellid hosts will be briefly reviewed. Thereafter, the impact that invasion by male-killers has on coccinellid hosts will be addressed in two ways. First, the selective effects due to the loss of male progeny, and the intra-genomic conflict resulting from the cytoplasmic inheritance of the bacteria will be considered. Reductions in mitochondrial diversity, effects on clutch sizes and the evolution of male-killer suppresser systems will be discussed. Second, the impact of female biased population sex ratios on the evolution of reproductive strategies and the primary sex ratio will be investigated. Preliminary results suggesting changes in male investment per copulation, reductions in female testing behaviour of males, and male biases in the progenic sex ratios of some uninfected male lines will be presented. Avenues for future work will be outlined.

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How Can Sex Ratio Distorters Reach Extreme Prevalences? Male-Killing Wolbachia Are Not Suppressed and Have Near-Perfect Vertical Transmission Efficiency in Acraea Encedon

Cited by 56 publications

References 23 publications

Persistence of an extreme sex-ratio bias in a natural population

Persistence of an extreme sex-ratio bias in a natural population

The Impact of Male-Killing Bacteria on Host Evolutionary Processes

The impact of male-killing bacteria on the evolution of aphidophagous coccinellids

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