The evolutionary dynamics of male-killers and their hosts

Abstract

Male-killing bacteria are cytoplasmic sex-ratio distorters that are transmitted vertically through females of their insect hosts. The killing of male hosts by their bacteria is thought to be an adaptive bacterial trait because it augments the fitness of female hosts carrying clonal relatives of those bacteria. Here we attempt to explain observations of multiple male-killers in natural host populations. First we show that such male-killer polymorphism cannot be explained by a classical model of male-killing. We then show that more complicated models incorporating the evolution of resistance in hosts can explain male-killer polymorphism. However, this is only likely if resistance genes are very costly. We also consider the long-term evolutionary dynamics of male-killers, and show that evolution towards progressively more 'efficient' male-killers can be thwarted by the appearance of host resistance. The presence of a resistance gene can allow a less efficient male-killer to outcompete its rival and hence reverse the trend towards more efficient transmission and reduced metabolic load on the host.

An Ancient Mitochondrial Polymorphism in Adalia bipunctata Linked to a Sex-Ratio-Distorting Bacterium

“…The first hypothesis is that the fitness of male killers is frequency dependent. Theory predicts that frequency dependence can result if there are costly host genes that confer resistance to specific male killers (Randerson et al 2000). Models of host genes that confer resistance against specific parasite (Barrett 1988) or sex-ratio-distorter (Frank 1989) genotypes also predict the geographical variation that we observed.…”

“…One important factor that may influence the dynamics of sexratio distorters is antagonistic coevolution with nuclear genes. For example, theoretical models have shown that if there are specific gene-for-gene-type interactions between sex-ratio distorters and their hosts, then both the cytoplasmic and nuclear genes may be highly polymorphic (Frank 1989;Randerson et al 2000). Furthermore, instead of reaching a stable equilibrium the two sets of genes may cycle in frequency through time (Charlesworth 1981;Gouyon et al 1991).…”

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

“…In two‐distorter simulations with low suppressor costs, the first distorting cytotype was lost after the spread of its suppressor, immediately followed by the invasion of the second distorting cytotype, mirroring the pattern predicted by Randerson et al. (2000). Subsequent alternating cycles of the two distorting cytotypes prevented the spread of the wild cytotype, allowing a consistent female bias to be maintained over time (Figure 1b).…”

Variable fitness effects of Wolbachia infection in Drosophila melanogaster

“…Symbioses between Wolbachia and their hosts may be further complicated by evidence for considerable involvement of host nuclear genes in the expression of Wolbachia phenotypes (eg, Poinsot et al, 1998;Bordenstein and Werren, 2000;McGraw et al, 2001;Olsen et al, 2001;this report). Although the competing interests of Wolbachia and such host resistance genes have been modeled previously (eg, Randerson et al, 2000), more empirical work is needed to determine which host genes might be involved.…”