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Low Temperature Reveals Genetic Variability Against Male-Killing Spiroplasma in Drosophila melanogaster Natural Populations

  • Host Microbe Interactions
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Abstract

Spiroplasma endosymbionts are maternally inherited microorganisms which infect many arthropod species. In some Drosophila species, it acts as a reproductive manipulator, spreading in populations by killing the sons of infected mothers. Distinct Drosophila melanogaster populations from Brazil exhibit variable male-killing Spiroplasma prevalences. In this study, we investigated the presence of variability for the male-killing phenotype among Drosophila and/or Spiroplasma strains and verified if it correlates with the endosymbiont prevalence in natural populations. For that, we analyzed the male-killing expression when Spiroplasma strains from different populations were transferred to a standard D. melanogaster line (Canton-S) and when a common Spiroplasma strain was transferred to different wild-caught D. melanogaster lines, both at optimal and challenging temperatures for the bacteria. No variation was observed in the male-killing phenotype induced by different Spiroplasma strains. No phenotypic variability among fly lines was detected at optimal temperature (23 °C), as well. Conversely, significant variation in the male-killing expression was revealed among D. melanogaster lines at 18.5 °C, probably caused by imperfect transmission of the endosymbiont. Distinct lines differed in their average sex ratios as well as in the pattern of male-killing expression as the infected females aged. Greater variation occurred among lines from one locality, although there was no clear correlation between the male-killing intensity and the endosymbiont prevalence in each population. Imperfect transmission or male killing may also occur in the field, thus helping to explain the low or intermediate prevalences reported in nature. We discuss the implications of our results for the dynamics of male-killing Spiroplasma in natural populations.

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Acknowledgments

We thank Ayana Martins and Lyes Assis Garcia for collections in Salvador and Rio de Janeiro, Klélia Carvalho and Claudete Couto for their technical support, Horácio Montenegro for statistical help, Espaço da Escrita (Unicamp) for reviewing the English version of the manuscript, John Pool for providing lines from Uganda, and anonymous reviewers for their suggestions. This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and Fundo de Apoio ao Ensino, à Pesquisa e à Extensão—Unicamp (FAEPEX).

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The authors declare no conflict of interest.

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Authors and Affiliations

  1. Departamento de Genética, Evolução e Bioagentes, Instituto de Biologia, Universidade Estadual de Campinas, Unicamp, Cx. 6109, Campinas, 13083-970, São Paulo, Brazil

    Iuri Matteuzzo Ventura, Thais Costa & Louis Bernard Klaczko

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  1. Iuri Matteuzzo Ventura
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  2. Thais Costa
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  3. Louis Bernard Klaczko
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Correspondence to Louis Bernard Klaczko.

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Data Archiving

Data are available in the Dryad Digital Repository: doi:10.5061/dryad.qh113.

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Table S1

Average proprotions of females and standard errors for each strain, during the days 3–10. (XLSX 10 kb)

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Ventura, I.M., Costa, T. & Klaczko, L.B. Low Temperature Reveals Genetic Variability Against Male-Killing Spiroplasma in Drosophila melanogaster Natural Populations. Microb Ecol 67, 229–235 (2014). https://doi.org/10.1007/s00248-013-0295-z

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  • DOI: https://doi.org/10.1007/s00248-013-0295-z

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