Fitness compensation and the evolution of selfish cytoplasmic elements

Abstract

Cytoplasmic incompatibility (CI) and male-killing (MK) are both examples of the action of selfish cytoplasmic elements. Both are found in a wide variety of host arthropod species and sometimes coexist within the same species. Although classical models suggest that fitness compensation is potentially important in explaining the invasion of the MK cytotype, no mode! of CI evolution incorporates this effect. We construct a discrete-time mathematical model which describes a host population containing both CI and MK, permitting fitness compensation for survivors of broods which suffer partial mortality as a result of the behaviour of either element. In the absence of fitness compensation, classical models of CI predict the existence of a threshold frequency at which infected individuals must be introduced in order to spread in a wild-type population. We examine whether fitness compensation will affect the ease of spread of CI (reduce the lower threshold) and its equilibrium frequency. Fitness compensation is found to affect the dynamics of CI in a complex manner. This is so, regardless of whether one considers the introduction of individuals infected with the CI element alone, or the introduction of individuals infected with both CI and MK elements into a wild-type population.The model predicts that fitness compensation has only a small effect on the dynamics of Cl/wild-type population. In contrast, when individuals infected with both CI and MK agents are introduced into a wild-type population, the presence of plausible levels of fitness compensation may greatly facilitate the spread of CI. We note that this apparent synergism may be expected from the coexistence of CI with other sex-ratio distorters.

Space and the persistence of male–killing endosymbionts in insect populations

“…In previous models (Hurst 1991;Hurst et al 1997;Freeland & McCabe 1997;Randerson et al 2000) region III has not been observed, because, in contrast to our model, the number of males was never limiting and the total population size was always xed, i.e. all fractions always added up to 1.…”

“…Previously, a number of mathematical models have been developed to describe a host population with malekilling bacteria in terms of vertical transmission ef ciency, and positive and negative effects of infection (Hurst 1991;Hurst et al 1997;Freeland & McCabe 1997;Randerson et al 2000). Using a discrete generation model, Hurst (1991) showed that invasion of a male killer is only possible when both the vertical transmission is imperfect (described by a , 1) and there is a positive effect on the tness of the female host of carrying the infection.…”

On the Evolution of Cytoplasmic Incompatibility in Haplodiploid Species

“…To date, only one of the published models on CI incorporates such a mechanism. Freeland and McCabe (1997) have shown that a CI element can invade an uninfected population by hitchhiking with a male-killing (MK) element. In essence, the fitness cost of the CI element is compensated with a fitness benefit of the MK element.…”

Discovery and identification of a male-killing agent in the Japanese ladybird Propylea japonica (Coleoptera: Coccinellidae)

“…In addition, the vertical transmission efficiency of different male-killing bacteria varies from almost perfect (> 99% for Spiroplasmas in A. bipunctata and H. axyridis and one strain of Wolbachia in A. bipunctata ) to less than 72% for Rickettsia in some samples of A. bipunctata [ 16 - 18 ]. The vertical transmission efficiency is a critical parameter in the dynamics of male-killer invasion and spread [ 19 ]. Assessments of the vertical transmission efficiencies of newly discovered male-killers are thus valuable to allow assessment of whether levels of vertical transmission are consistent within bacterial clades, or vary case by case as a result of interactions between each symbiont and its host.…”