The potential role of the X chromosome in the emergence of male-killing from mutualistic endosymbionts

Endosymbionts infect most arthropods and cause a wide variety of phenotypes in their hosts, ranging from obligate mutualists to reproductive parasites. One of the most dramatic forms of reproductive parasitism is male-killing which involves the endosymbiont killing all of the sons of infected females. A phenotype with such a dramatic effect on host fitness is expected to provide strong selection for suppressors of male-killing, yet in many well-studied male-killer/arthropod systems, no suppressors have been found. Plausible explanations for a lack of resistance exist and include cryptic cytoplasmic incompatibility (males that survive male-killing are therefore infected and matings with uninfected females are incompatible) and deleterious pleiotropic effects of altering early embryonic development—the precise time when male-killing often occurs. Here I describe another possible scenario that sidesteps the problem: male killing may arise through an epistatic interaction between an endosymbiont and a paternally acting locus on the X chromosome. Since paternal X chromosomes never find themselves in sons, they never suffer from male-killing and instead enjoy any benefits (decreased sibling competition, inbreeding avoidance) caused by killing males. This scenario allows for the possibility that male-killing arose recently, even if there is no evidence for evolution in the endosymbiont genotype.

► A paternally acting X locus may act with an endosymbiont to cause male-killing. ► The Killer X increases endosymbiont frequency and sex-ratio (proportion female). ► Models with female cost were examined through simulation. ► This provides an explanation for the apparent stability of male-killer systems.