Population Dynamics of Male-Killing and Non-Male-Killing Spiroplasmas in Drosophila melanogaster

Abstract

The endosymbiotic bacteria Spiroplasma spp. are vertically transmitted through female hosts and are known to cause selective death of male offspring in insects. One strain of spiroplasma, NSRO, causes male killing in Drosophila species, and a non-male-killing variant of NSRO, designated NSRO-A, has been isolated. It is not known why NSRO-A does not kill males. In an attempt to understand the mechanism of male killing, we investigated the population dynamics of NSRO and NSRO-A throughout the developmental course of the laboratory host Drosophila melanogaster by using a quantitative PCR technique. In the early development of the host insect, the titers of NSRO were significantly higher than those of NSRO-A at the first-and second-instar stages, whereas at the egg, third-instar, and pupal stages, the titers of the two spiroplasmas were almost the same. Upon adult emergence, the titers of the two spiroplasmas were similar, around 2 ؋ 10 8 dnaA copy equivalents. However, throughout host aging, the two spiroplasmas showed strikingly different population growth patterns. The titers of NSRO increased exponentially for 3 weeks, attained a peak value of around 4 ؋ 10 9 dnaA copy equivalents per insect, and then decreased. In contrast, the titers of NSRO-A were almost constant throughout the adult portion of the life cycle. In adult females, consequently, the titer of NSRO was significantly higher than the titer of NSRO-A except for a short period just after emergence. Although infection of adult females with NSRO resulted in almost 100% male killing, production of some male offspring was observed within 4 days after emergence when the titers of NSRO were as low as those of NSRO-A. Based on these results, we proposed a threshold density hypothesis for the expression of male killing caused by the spiroplasma. The extents of the bottleneck in the vertical transmission through host generations were estimated to be 5 ؋ 10 ؊5 for NSRO and 3 ؋ 10 ؊4 for NSRO-A.Occasionally, female-biased sex ratios have been found in the progeny of wild-caught female insects. This trait has been referred to as the sex ratio (SR) trait. The mated daughters of such females were found to produce daughters and few or no sons. In many cases, the female-biased sex ratios are expressed through selective death of male offspring. Such SR traits have been reported for a wide variety of insect taxa (reviewed in references 22, 26, and 28). In some of these cases, it has been demonstrated that the SR traits are caused by maternally inherited endosymbiotic bacteria. These microorganisms are called male-killing bacteria and have been found in diverse bacterial taxa, such as the genus Spiroplasma of the class Mollicutes (24, 60), the genera Rickettsia and Wolbachia of the ␣ subdivision of the division Proteobacteria (25, 57), the genus Arsenophonus of the ␥ subdivision of the Proteobacteria (15), an unidentified bacterium belonging to the FlavobacteriumBacteroides group (23) (44). In the D. willistoni group of the genus Drosophila, the causative agents of the S...

Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont

“…However, the issue of reporting bias might suggest that our figure is an overestimate (many isofemale lines of D. melanogaster have previously been collected from tropical Africa without reports of Spiroplasma infection). The amplification success of Spiroplasma loci appears to depend on the age of the fly, which might be expected if Spiroplasma titer is increasing over the lifetime of the host, as demonstrated by Anbutsu and Fukatsu (2003).…”

Endosymbiotic Bacteria in Insects: Their Diversity and Culturability

“…Although most of the biological functions of facultative symbionts remain unclear, several facultative symbionts belonging to the Gammnaproteobacteria inpart on their aphid hosts capabilities such as high-temperature tolerance (77), host plant specificity (71,111), and increased resistance to hemipteran parasitoids (89,90) and fungal pathogens (102), which provide the insect hosts with a great advantage given the heterogeneity in environments. Some other facultative symbionts, like Wolbachia, Spiroplasma and Cardinium (Table 1), are famous as reproductive parasites in insects, which manipulate host reproduction by inducing male-killing, feminization, parthenogensis or cytoplasmic incompatibility (CI) (8,56,86,118,119). Because of their maternal inheritance property, these reproductive distortions are regarded as selfish strategies of the facultative symbionts whereby the frequency of infected females increases in host populations, sometimes at the expense of host fitness (18,86).…”

Heritable Endosymbionts of Drosophila

“…Examples of sex ratio bias or male killing have been reported for a few other Drosophila species (reviewed in Anbutsu and Fukatsu 2003), but the causative agents have not been identified. Other bacterial groups, including the Gammaproteobacteria (e.g., Moran et al 2005a) and the phylum Bacteroidetes (Zchori-Fein and Perlman 2004), are also common as opportunistic heritable symbionts of insects, having major effects on reproduction, but their extent in Drosophila is not known.…”