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Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp.

ABSTRACT: Self-sacrifice is very rare among organisms. Here, we report a new and astonishing case of adaptive self-sacrifice in a polyembryonic parasitic wasp, Copidosoma floridanum. This wasp is unique in terms of its larval cloning and soldier larvae. Male clone larvae have been found to be killed by female soldier larvae, which suggests intersexual conflict between male and female larvae. However, we show here that mass killing is adaptive to all the killed males as well as the female soldiers that have conducted the killing because the killing increases their indirect fitness by promoting the reproduction of their clone sibs. We construct a simple model that shows that the optimal number of surviving males for both male and female larvae is very small but not zero. We then compare this prediction with the field data. These data agree quite well with the model predictions, showing an optimal killing rate of approximately 94-98% of the males in a mixed brood. The underlying mechanism of this mass kill is almost identical to the local competition for mates that occurs in other wasp species. The maternal control of the sex ratio during oviposition, which is well known in other hymenopterans, is impossible in this polyembryonic wasp. Thus, this mass kill is necessary to maximize the fitness of the female killers and male victims, which can be seen as an analogy of programmed cell death in multicellular organisms.

SUBMITTER: Otsuki T

PROVIDER: S-EPMC6517382 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Publications

Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp.

Otsuki Takahiro T Uka Daisuke D Ito Hiromu H Ichinose Genki G Nii Momoka M Morita Satoru S Sakamoto Takuma T Nishiko Maaya M Tabunoki Hiroko H Kobayashi Kazuya K Matsuura Kenji K Iwabuchi Kikuo K Yoshimura Jin J

Scientific reports 20190514 1

Self-sacrifice is very rare among organisms. Here, we report a new and astonishing case of adaptive self-sacrifice in a polyembryonic parasitic wasp, Copidosoma floridanum. This wasp is unique in terms of its larval cloning and soldier larvae. Male clone larvae have been found to be killed by female soldier larvae, which suggests intersexual conflict between male and female larvae. However, we show here that mass killing is adaptive to all the killed males as well as the female soldiers that hav ...[more]

PMID: 31089143

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Project description: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 x 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 x 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 x 10(-5) for NSRO and 3 x 10(-4) for NSRO-A.

Dataset Information

Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp.

Publications

Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp.

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