Male-killing virus in a noctuid moth Spodoptera litura

Author:

Nagamine Keisuke12ORCID,Kanno Yoshiaki1ORCID,Sahara Ken3ORCID,Fujimoto Toshiaki3,Yoshido Atsuo34ORCID,Ishikawa Yukio5ORCID,Terao Misato1ORCID,Kageyama Daisuke2ORCID,Shintani Yoshinori1

Affiliation:

1. Department of Environmental and Horticultural Sciences, Minami Kyushu University, Miyakonojo, Miyazaki 885-0035, Japan

2. Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-0851, Japan

3. Faculty of Agriculture, Iwate University, Morioka, Iwate 020-8550, Japan

4. Institute of Entomology, Biology Centre of the Czech Academy of Sciences, České Budějovice 370 05, Czech Republic

5. Faculty of Agriculture, Setsunan University, Hirakata, Osaka 573-0101, Japan

Abstract

A female-biased sex ratio is considered advantageous for the cytoplasmic elements that inhabit sexually reproducing organisms. There are numerous examples of bacterial symbionts in the arthropod cytoplasm that bias the host sex ratio toward females through various means, including feminization and male killing. Recently, maternally inherited RNA viruses belonging to the family Partitiviridae were found to cause male killing in moths and flies, but it was unknown whether male-killing viruses were restricted to Partitiviridae or could be found in other taxa. Here, we provide compelling evidence that a maternally inherited RNA virus, Spodoptera litura male-killing virus (SlMKV), selectively kills male embryos of the tobacco caterpillar Spodoptera litura , resulting in all-female broods. SlMKV injected into uninfected S. litura can also be inherited maternally and causes male killing. SlMKV has five genomic segments encoding seven open reading frames, has no homolog of known male-killing genes, and belongs to an unclassified group of arthropod-specific viruses closely related to Tolivirales. When transinfected into larvae, both male and female recipients allow SlMKV to proliferate, but only males die at the pupal stage. The viral RNA levels in embryonic and pupal male killing suggest that the mechanism of male killing involves the constitutive expression of viral products that are specifically lethal to males, rather than the male-specific expression of viral products. Our results, together with recent findings on male-killing partiti-like viruses, suggest that diverse viruses in arthropods tend to acquire male killing independently and that such viruses may be important components of intragenomic conflict in arthropods.

Funder

MEXT | Japan Society for the Promotion of Science

NARO | Bio-oriented Technology Research Advancement Institution

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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