Expression and Modulation of Embryonic Male-Killing in Drosophila Innubila: Opportunities for Multilevel Selection

Abstract

Abstract. Organisms and the symbionts they harbor may experience opposing forces of selection. In particular, the contrasting inheritance patterns of maternally transmitted symbionts and their host's nuclear genes can engender conflict among organizational levels over the optimal host offspring sex ratio. This study uses a male-killing Wolbachia endosymbiont and its host Drosophila innubila to experimentally address the potential for multilevel selection in a host-symbiont system. We show that bacterial density can vary among infected females, and that females with a higher density have a more female-biased offspring sex ratio. Furthermore, bacterial density is an epigenetic and heritable trait: females with a low bacterial load have daughters with a lower-than-average bacterial density, whose offspring then experience less severe male-killing. For infected sons, the probability of embryonic mortality increases with the bacterial density in their mothers. The frequency distribution of Wolbachia density among individual D. innubila females, and therefore the dynamics of infection within populations of these flies, results both from processes affecting the growth and regulation of bacterial populations within cytoplasmic lineages and from selection among cytoplasmic lineages that vary in bacterial density. Estimates of effective population size of Wolbachia within cytoplasmic lineages and of D. innubila at the host population level suggest that selection among cytoplasmic lineages is likely to overwhelm the results of selection within lineages.

Wolbachia-Mediated Male Killing Is Associated with Defective Chromatin Remodeling

“…Consistently, mothers with a higher density of bacteria have more female-biased offspring sex-ratio [34]. Moreover, a Spiroplasma strain that normally causes early male killing also induces late male mortality in larvae and pupae in the offspring of young females [35], suggesting a correlation with maternal host age.…”

A new male-killing parasitism:Spiroplasmabacteria infect the ladybird beetleAnisosticta novemdecimpunctata(Coleoptera: Coccinellidae)

“…Survival of infected male offspring following treatment suggests tetracycline either reduced bacterial density below the threshold required for embryo death, or disrupted male-killing directly. Dyer, Minhas and Jaenike (2005) found maternal bacterial density was inversely correlated with male (Stevens, 1989 ;Hoffmann, Turelli and Harshman, 1990). Rapid recovery of full male-killing in A. novemdecimpunctata following treatment suggests that unless these influences are persistent, such effects on malekiller performance might be short-lived.…”

“…Not all male offspring were killed; those surviving carried the Spiroplasma. Male-killing requires an interaction between the bacterium and host sex determination pathways (Veneti et al 2005), as well as appropriate bacterial density in maternal tissues (Dyer et al 2005) ; either factor may have been altered following transfer. It is notable that A. bipunctata and the native host are not closely related.…”

Wolbachia Infections in Aedes aegypti Differ Markedly in Their Response to Cyclical Heat Stress

“…In insects other than Ae . aegypti , a decline in Wolbachia density can reduce the degree of male-killing [37], feminization [38], parthenogenesis [39], cytoplasmic incompatibility [40, 41] and maternal transmission of Wolbachia [40, 42]. Incomplete cytoplasmic incompatibility occurs when some sperm cysts in the testes are not infected with Wolbachia [43, 44].…”