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Common and unique strategies of male killing evolved in two distinct Drosophila symbionts.
Proc Biol Sci 2018; 285(1875)PB

Abstract

Male killing is a selfish reproductive manipulation caused by symbiotic bacteria, where male offspring of infected hosts are selectively killed. The underlying mechanisms and the process of their evolution are of great interest not only in terms of fundamental biology, but also their potential applications. The two bacterial Drosophila symbionts, Wolbachia and Spiroplasma, have independently evolved male-killing ability. This raises the question whether the underlying mechanisms share some similarities or are specific to each bacterial species. Here, we analyse pathogenic phenotypes of D. bifasciata infected with its natural male-killing Wolbachia strain and compare them with those of D. melanogaster infected with male-killing Spiroplasma We show that male progeny infected with the Wolbachia strain die during embryogenesis with abnormal apoptosis. Interestingly, male-killing Wolbachia infection induces DNA damage and segregation defects in the dosage-compensated chromosome in male embryos, which are reminiscent of the phenotypes caused by male-killing Spiroplasma in D. melanogaster By contrast, host neural development seems to proceed normally unlike male-killing Spiroplasma infection. Our results demonstrate that the dosage-compensated chromosome is a common target of two distinct male killers, yet Spiroplasma uniquely evolved the ability to damage neural tissue of male embryos.

Authors+Show Affiliations

Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Station 19, CH-1015 Lausanne, Switzerland toshiyuki.harumoto@epfl.ch.Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan.Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne (EPFL), Station 19, CH-1015 Lausanne, Switzerland bruno.lemaitre@epfl.ch.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29563258

Citation

Harumoto, Toshiyuki, et al. "Common and Unique Strategies of Male Killing Evolved in Two Distinct Drosophila Symbionts." Proceedings. Biological Sciences, vol. 285, no. 1875, 2018.
Harumoto T, Fukatsu T, Lemaitre B. Common and unique strategies of male killing evolved in two distinct Drosophila symbionts. Proc Biol Sci. 2018;285(1875).
Harumoto, T., Fukatsu, T., & Lemaitre, B. (2018). Common and unique strategies of male killing evolved in two distinct Drosophila symbionts. Proceedings. Biological Sciences, 285(1875), doi:10.1098/rspb.2017.2167.
Harumoto T, Fukatsu T, Lemaitre B. Common and Unique Strategies of Male Killing Evolved in Two Distinct Drosophila Symbionts. Proc Biol Sci. 2018 03 28;285(1875) PubMed PMID: 29563258.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Common and unique strategies of male killing evolved in two distinct Drosophila symbionts. AU - Harumoto,Toshiyuki, AU - Fukatsu,Takema, AU - Lemaitre,Bruno, PY - 2017/09/28/received PY - 2018/02/26/accepted PY - 2018/3/23/entrez PY - 2018/3/23/pubmed PY - 2019/6/4/medline KW - Drosophila KW - Spiroplasma KW - Wolbachia KW - male killing KW - symbiosis JF - Proceedings. Biological sciences JO - Proc. Biol. Sci. VL - 285 IS - 1875 N2 - Male killing is a selfish reproductive manipulation caused by symbiotic bacteria, where male offspring of infected hosts are selectively killed. The underlying mechanisms and the process of their evolution are of great interest not only in terms of fundamental biology, but also their potential applications. The two bacterial Drosophila symbionts, Wolbachia and Spiroplasma, have independently evolved male-killing ability. This raises the question whether the underlying mechanisms share some similarities or are specific to each bacterial species. Here, we analyse pathogenic phenotypes of D. bifasciata infected with its natural male-killing Wolbachia strain and compare them with those of D. melanogaster infected with male-killing Spiroplasma We show that male progeny infected with the Wolbachia strain die during embryogenesis with abnormal apoptosis. Interestingly, male-killing Wolbachia infection induces DNA damage and segregation defects in the dosage-compensated chromosome in male embryos, which are reminiscent of the phenotypes caused by male-killing Spiroplasma in D. melanogaster By contrast, host neural development seems to proceed normally unlike male-killing Spiroplasma infection. Our results demonstrate that the dosage-compensated chromosome is a common target of two distinct male killers, yet Spiroplasma uniquely evolved the ability to damage neural tissue of male embryos. SN - 1471-2954 UR - https://www.unboundmedicine.com/medline/citation/29563258/Common_and_unique_strategies_of_male_killing_evolved_in_two_distinct_Drosophila_symbionts_ L2 - https://royalsocietypublishing.org/doi/full/10.1098/rspb.2017.2167?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -