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. 2009 May 26;106(21):8465-70.
doi: 10.1073/pnas.0901389106. Epub 2009 May 13.

Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea

Eugene V Ryabov  1 , Gary Keane, Neil Naish, Carol Evered, Doreen Winstanley
Affiliations

Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea

Eugene V Ryabov et al. Proc Natl Acad Sci U S A. .

Abstract

Winged morphs of aphids are essential for their dispersal and survival. We discovered that the production of the winged morph in asexual clones of the rosy apple aphid, Dysaphis plantaginea, is dependent on their infection with a DNA virus, Dysaphis plantaginea densovirus (DplDNV). Virus-free clones of the rosy apple aphid, or clones infected singly with an RNA virus, rosy apple aphid virus (RAAV), did not produce the winged morph in response to crowding and poor plant quality. DplDNV infection results in a significant reduction in aphid reproduction rate, but such aphids can produce the winged morph, even at low insect density, which can fly and colonize neighboring plants. Aphids infected with DplDNV produce a proportion of virus-free aphids, which enables production of virus-free clonal lines after colonization of a new plant. Our data suggest that a mutualistic relationship exists between the rosy apple aphid and its viruses. Despite the negative impact of DplDNV on rosy apple aphid reproduction, this virus contributes to their survival by inducing wing development and promoting dispersal.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
RAAV and DplDNV in the rosy apple aphid. (A) Genetically identical aphids infected with different virus combinations. (B) Accumulation of RAAV and DplDNV in individual aphids. Clone WS was originated from a single doubly infected aphid; clones 2D, R3, and 10A were produced by selecting progeny of clone WS. Clone Inj-9 was produced from a virus-free aphid of clone 2D following injection with a DplDNV virus preparation from clone 10A.
Fig. 2.
Fig. 2.
DplDNV-induced wing development in asexual clones of the rosy apple aphid. Scanning electron microscopy. (A) Adult aphid from clone 2D (virus free). (D) Adult aphid from clone R3 (RAAV infected). Aphids from clone 10A (DplDNV infected): (B) fourth instar with wing buds and (C) winged adult. Aphids from the clone WS (DplDNV and RAAV infections): (E) fourth instar with wing buds and (F) winged adult. Wing buds are indicated with arrows. (Scale bar: 1 mm.) (G) Accumulation of DplDNV DNA in individual light, dark (with wing buds), and winged aphids. ND, nondetectable levels of DplDNV DNA; n/a, not applicable. Clone Inj-9 was produced from a single aphid from clone 2D injected with a DplDNV virus preparation; the progeny was sampled 4 weeks postinjection. Bars depict the accumulation of DplDNV DNA (mean ± standard error) in individual aphids. Numbers of the sampled aphids are shown in parentheses. Values without significant difference (ANOVA) are indicated with asterisks (*).
Fig. 3.
Fig. 3.
Dispersal of DplDNV-infected aphids. Plantain 2 weeks postinfestation with 10 aphids from clones (A) R3 (localized) and (B and C) WS (dispersed). (Scale bars: 1 cm.)
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