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Cytonuclear Epistasis Controls the Density of Symbiont Wolbachia pipientis in Nongonadal Tissues of Mosquito Culex quinquefasciatus

Kevin J. Emerson and Robert L. Glaser
G3: Genes, Genomes, Genetics August 1, 2017 vol. 7 no. 8 2627-2635; https://doi.org/10.1534/g3.117.043422
Kevin J. Emerson
Department of Biology, St. Mary’s College of Maryland, Maryland 20686-3001
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Robert L. Glaser
Wadsworth Center, New York State Department of Health, Albany, New York 12201-0509Department of Biomedical Sciences, University at Albany, New York 12222
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  • For correspondence: robert.glaser@health.ny.gov
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Abstract

Wolbachia pipientis, a bacterial symbiont infecting arthropods and nematodes, is vertically transmitted through the female germline and manipulates its host’s reproduction to favor infected females. Wolbachia also infects somatic tissues where it can cause nonreproductive phenotypes in its host, including resistance to viral pathogens. Wolbachia-mediated phenotypes are strongly associated with the density of Wolbachia in host tissues. Little is known, however, about how Wolbachia density is regulated in native or heterologous hosts. Here, we measure the broad-sense heritability of Wolbachia density among families in field populations of the mosquito Culex pipiens, and show that densities in ovary and nongonadal tissues of females in the same family are not correlated, suggesting that Wolbachia density is determined by distinct mechanisms in the two tissues. Using introgression analysis between two different strains of the closely related species C. quinquefasciatus, we show that Wolbachia densities in ovary tissues are determined primarily by cytoplasmic genotype, while densities in nongonadal tissues are determined by both cytoplasmic and nuclear genotypes and their epistatic interactions. Quantitative-trait-locus mapping identified two major-effect quantitative-trait loci in the C. quinquefasciatus genome explaining a combined 23% of variance in Wolbachia density, specifically in nongonadal tissues. A better understanding of how Wolbachia density is regulated will provide insights into how Wolbachia density can vary spatiotemporally in insect populations, leading to changes in Wolbachia-mediated phenotypes such as viral pathogen resistance.

  • cytonuclear epistasis
  • Wolbachia pipientis
  • Culex quinquefasciatus
  • Wolbachia density
  • QTL mapping
  • Received May 17, 2017.
  • Accepted June 5, 2017.
  • Copyright © 2017 Emerson, Glaser

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Volume 7 Issue 8, August 2017

G3: Genes|Genomes|Genetics: 7 (8)

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Cytonuclear Epistasis Controls the Density of Symbiont Wolbachia pipientis in Nongonadal Tissues of Mosquito Culex quinquefasciatus

Kevin J. Emerson and Robert L. Glaser
G3: Genes, Genomes, Genetics August 1, 2017 vol. 7 no. 8 2627-2635; https://doi.org/10.1534/g3.117.043422
Kevin J. Emerson
Department of Biology, St. Mary’s College of Maryland, Maryland 20686-3001
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert L. Glaser
Wadsworth Center, New York State Department of Health, Albany, New York 12201-0509Department of Biomedical Sciences, University at Albany, New York 12222
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: robert.glaser@health.ny.gov
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Citation

Cytonuclear Epistasis Controls the Density of Symbiont Wolbachia pipientis in Nongonadal Tissues of Mosquito Culex quinquefasciatus

Kevin J. Emerson and Robert L. Glaser
G3: Genes, Genomes, Genetics August 1, 2017 vol. 7 no. 8 2627-2635; https://doi.org/10.1534/g3.117.043422
Kevin J. Emerson
Department of Biology, St. Mary’s College of Maryland, Maryland 20686-3001
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Robert L. Glaser
Wadsworth Center, New York State Department of Health, Albany, New York 12201-0509Department of Biomedical Sciences, University at Albany, New York 12222
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: robert.glaser@health.ny.gov

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