Spiroplasma infection in Drosophila melanogaster: What is the advantage of killing males?

Abstract

Male-killing bacteria are maternally inherited agents that cause death of sons of infected females. Their transmission rate is commonly high but imperfect and also sensitive to different environmental factors. Therefore, the proportion of infected females should be reduced in each generation. In order to explain male-killers spread and persistence in host population, a mechanism resulting in the relative increase of infected females must outweigh the losses caused by the imperfect transmission. The resource release hypothesis states that the males' death results in increased resources available to sibling females which would otherwise be used by their male siblings. Infected females are then expected: to be larger than uninfected females in natural populations; or to have higher viability; or to have shorter development times; or any combination of these outcomes. Here, we tested the resource release hypothesis by measuring body size of infected and uninfected wild-caught Drosophila melanogaster females and carried out other fitness related measures in the laboratory. Wild-caught infected females produced more daughters than uninfected females in their first days in the laboratory. However, although no significant difference in viability was found in a controlled experiment with infected and uninfected flies from a standard laboratory strain, there was a decrease in development time probably mediated by reduced competition. Fitness effects conditioned by the host genetic background are pointed out as a possible explanation for this difference between wild and laboratory flies. Our findings are discussed in the context of the resource advantage hypothesis.

Insect endosymbiont proliferation is limited by lipid availability

“…On nutrient rich media, we found that despite increasing early egg production Spiroplasma infection status did not affect the total number of eggs laid over a 14-day period. The Spiroplasma -induced early increase in egg production has been described previously for other Spiroplasma strains (Ebbert, 1991; Martins et al, 2010). While the mechanistic basis of this increase is unknown, it offers a possible explanation for the greater number of eggs laid by Spiroplasma -infected flies on nutrient poor media, where the majority of eggs laid by all flies are in the first 2 days post-eclosion.…”

“…Experimental studies are generally in line with this prediction, for example Wolbachia and Spiroplasma have relatively minor effects on host fitness (Martins et al, 2010; Unckless and Jaenike, 2012), however, fitness costs usually become apparent as hosts age (Ebbert, 1991; Min and Benzer, 1997; Fry et al, 2004). For endosymbionts that colonize the germline from the adult soma, it has been demonstrated that endosymbiont titers are positively correlated with transmission fidelity (Dyer et al, 2005; Unckless et al, 2009).…”

Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps

“…Therefore, it appears that the selective advantage conferred by defense alone does not guarantee Spiroplasma persistence. Nevertheless, it is possible that a combination of defense and other net fitness benefits conferred by this male-killing strain (i.e., higher fecundity of wild-caught flies and faster development; Martins et al, 2010) ensure its persistence. Furthermore, our experiment was limited to a few host backgrounds (seven isofemale lines not known to harbor Spiroplasma naturally), and two highly virulent wasp strains.…”

“…It is unclear whether direct or indirect fitness effects of male-killing are sufficient to maintain such infection frequencies, particularly those at the higher end. Martins et al (2010) found that MSRO-infected wild females have a higher fecundity (at least over four consecutive days), and their progeny develop faster. In contrast, Montenegro et al (2006) reported no effect of MSRO on larval competitive ability or adult fecundity of D. melanogaster Canton-S strain.…”

Spiroplasma as a model insect endosymbiont

“…However, it seems doubtful that these factors play a significant role in the Spiroplasma-Drosophila male-killing endosymbiosis (Hurst and Majerus, 1993;Martins et al, 2010). It also increases the opportunity of horizontal transfer of the symbiont following male death.…”