Intergenomic Arms Races: Detection of a Nuclear Rescue Gene of Male-Killing in a Ladybird

Abstract

Many species of arthropod are infected by deleterious inherited micro-organisms. Typically these micro-organisms are inherited maternally. Consequently, some, particularly bacteria of the genus Wolbachia, employ a variety of strategies that favour female over male hosts. These strategies include feminisation, induction of parthenogenesis and male-killing. These strategies result in female biased sex ratios in host populations, which lead to selection for host factors that promote male production. In addition, the intra-genomic conflict produced by the difference in transmission of these cytoplasmic endosymbionts and nuclear factors will impose a pressure favouring nuclear factors that suppress the effects of the symbiont. During investigations of the diversity of male-killing bacteria in ladybirds (Coccinellidae), unexpected patterns of vertical transmission of a newly discovered male-killing taxon were observed in the ladybird Cheilomenes sexmaculata. Initial analysis suggested that the expression of the bacterial male-killing trait varies according to the male(s) a female has mated with. By swapping males between females, a male influence on the expression of the male-killing trait was confirmed. Experiments were then performed to determine the nature of the interaction. These studies showed that a single dominant allele, which rescues male progeny of infected females from the pathological effect of the male-killer, exists in this species. The gene shows typical Mendelian autosomal inheritance and is expressed irrespective of the parent from which it is inherited. Presence of the rescue gene in either parent does not significantly affect the inheritance of the symbiont. We conclude that C. sexmaculata is host to a male-killing γ-proteobacterium. Further, this beetle is polymorphic for a nuclear gene, the dominant allele of which rescues infected males from the pathogenic effects of the male-killing agent. These findings represent the first reported case of a nuclear suppressor of male-killing in a ladybird. They are considered in regard to sex ratio and intra-genomic conflict theories, and models of the evolutionary dynamics and distribution of inherited symbionts.

Author Summary

Normally, in sexually reproducing organisms, the sex ratio (ratio of males to females) is 1∶1. However, examples are known where this is not the case and there are more females than males in a population. Extreme bias in sex ratio can lead to females failing to find a mate. We studied Cheilomenes sexmaculata, a ladybird species that has females that produce more female than male offspring. In aphid-eating ladybirds, this phenomenon has been widely reported and is known to be due to the presence of bacteria that live inside the mother and are passed via her eggs to her offspring. In eggs destined to become male, the bacteria kill the embryo by some unknown mechanism. This is known as male-killing. Female offspring develop normally. Evolutionary theory predicts that in such systems, the genome of the host can fight back if a variant arises that stops the bacteria killing male offspring. In C. sexmaculata we found females that carried the male-killer but the sex ratio of their offspring depended on the male that they mated with. We carried out breeding tests to show that some ladybirds had a version of a gene that rescued the male offspring from the pathological effects of the male-killer.