The incidences and evolution of cytoplasmic male killers

Abstract

Two types of male-killing cytoplasmic gene are distinguished by their time of action. Early male killers strike embryos, whereas late killers, so far only observed in mosquitoes, kill fourth instar larvae. Maternal inheritance of cytoplasmic factors underlies the sex bias in mortality in both instances. However, the evolutionary logic of early and late killing is, it is argued, otherwise different. Early male killing is interpreted in terms of kin selection. The death of male embryos early on allows resources (food or space) to be redistributed to the surviving females. A simple model relying on the redirection of resources after male death indicates that so long as a more than critical proportion o f 'freed' resources goes to females containing clonal relatives of the male-killing cytoplasmic gene, then that gene can invade and go to an equilibrium. This equilibrium is significant in that it allows a population to avoid extinction prior to the evolution of a nuclear repressor gene. The distribution of male killing is discussed in the light of these findings. The late male-killing microsporidians of mosquitoes differ from early male killing factors in possessing horizontal, as well as vertical, transmission between generations. It is argued that to maximize the efficiency of horizontal transmission it is in the interests of the microsporidians to maximize their number by waiting for the host to grow before killing it. Not all microsporidians kill only the male mosquito, some also kill the female. The variety of mosquito-microsporidian pathologies is interpreted by considering a trade-off between the efficiency of vertical against horizontal transmission. A review of possible incidences of cytoplasmic male killing is presented.

Evolution of early male-killing in horizontally transmitted parasites

“…R. Soc. B 282: 20152068 efficacy and a benefit provided to the surviving host offspring by killing the infected male embryos [10], and may also depend on their spatial distribution [11]. We showed that a purely vertically transmitted non-MK bacterium, otherwise able to invade the host as a highly efficient male-killer (electronic supplementary material, appendix S3), cannot persist and evolve MK gradually unless at least a bit of HT is present.…”

“…Purely vertically transmitted bacteria (strains with l ¼ 0) which kill infected male offspring with 100% efficacy can successfully establish in the host population if the VT efficacy j and fitness compensation parameter g (equation (2.2)) are high enough [10]. However, highly efficient male-killers might have evolved gradually from less-efficient male-killers, and from bacteria that did not possess any MK ability [17].…”

“…While we present them here only briefly, all are discussed at large in the electronic supplementary material, appendix S2. Given the VT efficacy j, the fitness benefit r conferred to the surviving offspring is expressed as [10,11] …”

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

“…When I ¼ 0, there is no Spiroplasma infection in the host population. Hurst (1991) modeled the invasion of a male killer under the resource release hypothesis; thus, this equilibrium will not be discussed further here. The other equilibrium is reached when I ¼ I 0 ,…”

Taking Stock: Relating Theory to Experiment

“…The latter occurs only when male death allows the symbiont to be transmitted horizontally (e.g., via consumption of the lethargic male). Thus, virulence is sex specific: symbiont-induced mortality is much higher in the horizontally transmitting sex than in the vertically transmitting sex (Hurst 1991;Ebert and Herre 1996).…”