A male-killing gene encoded by a symbiotic virus of Drosophila

Abstract

In most eukaryotes, biparentally inherited nuclear genomes and maternally inherited cytoplasmic genomes have different evolutionary interests. Strongly female-biased sex ratios that are repeatedly observed in various arthropods often result from the male-specific lethality (male-killing) induced by maternally inherited symbiotic bacteria such as Spiroplasma and Wolbachia. However, despite some plausible case reports wherein viruses are raised as male-killers, it is not well understood how viruses, having much smaller genomes than bacteria, are capable of inducing male-killing. Here we show that a maternally inherited double-stranded RNA (dsRNA) virus belonging to the family Partitiviridae (designated DbMKPV1) induces male-killing in Drosophila. DbMKPV1 localizes in the cytoplasm and possesses only four genes, i.e., one gene in each of the four genomic segments (dsRNA1−dsRNA4), in contrast to ca. 1000 or more genes possessed by Spiroplasma or Wolbachia. We also show that a protein (designated PVMKp1; 330 amino acids in size), encoded by a gene on the dsRNA4 segment, is necessary and sufficient for inducing male-killing. Our results imply that male-killing genes can be easily acquired by symbiotic viruses through reassortment and that symbiotic viruses are hidden players in arthropod evolution. We anticipate that host-manipulating genes possessed by symbiotic viruses can be utilized for controlling arthropods.

Transcriptome Analysis Reveals a Diverse Range of Novel Viruses in Australian Sugarcane Soldier Fly (Inopus flavus) Larvae

“…From a pest control point of view, it is important to note that a partitivirus related to SFaPV, Drosophila male-killing partitivirus, was found to encode a gene which favours female selection by elimination of males [ 42 ]. These new findings indicate that male killing by these viruses may be prevalent among insect species and could be potentially utilised to suppress host population.…”

Two male-killing Wolbachia from Drosophila birauraia that are closely related but distinct in genome structure

“…The sex ratios of the lines derived from field-collected females were determined at the adult stage. The normal sex ratio (NSR) isofemale line SP11-20 [ 23 ] was maintained for more than 70 generations. The all-female matrilines (W1 and W2), each derived from a single female, were maintained by crossing with males of the SP11-20 line.…”

“…The all-female matrilines (W1 and W2), each derived from a single female, were maintained by crossing with males of the SP11-20 line. Wolbachia and the MK partiti-like virus DbMKPV1 infections were detected by PCR, as described previously [ 22 , 23 ].…”

“…Egg-hatching rates were estimated by counting the number of hatched and unhatched larvae. A total of 50–100 females of either W1 or NSR (SP11-20) were allowed to oviposit on grape juice agar medium for 1 day [ 23 ]. The eggs were collected and maintained in phosphate-buffered saline with Tween 20 (PBST; 137 mmol l −1 NaCl, 8.1 mmol l −1 Na 2 HPO 4 , 2.68 mmol l −1 KCl, 1.47 mmol l −1 KH 2 PO 4 , 0.02% Tween 20, pH7.4) for 4 days.…”

“…Further, we compared their genomes with the partiti-like virus DbMKPV1, which induces MK during the late embryonic stage (i.e. early MK) in D. biauraria [22,23], to clarify the evolutionary origin of MK in this fly species. We determined the sex of embryos and hatchlings by PCR targeting a male-specific Y chromosome marker.…”