Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster

Ye, Yixin H., Chenoweth, Stephen F. and McGraw, Elizabeth A. (2009) Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. PLoS Pathogens, 5 4: e1000385.1-e1000385.9. doi:10.1371/journal.ppat.1000385


Author Ye, Yixin H.
Chenoweth, Stephen F.
McGraw, Elizabeth A.
Title Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster
Formatted title
Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster
Journal name PLoS Pathogens   Check publisher's open access policy
ISSN 1553-7366
1553-7374
Publication date 2009-04-01
Year available 2009
Sub-type Article (original research)
DOI 10.1371/journal.ppat.1000385
Open Access Status DOI
Volume 5
Issue 4
Start page e1000385.1
End page e1000385.9
Total pages 9
Editor Kasturi Haldar
Place of publication San Francisco, CA, United States
Publisher Public Library of Science
Language eng
Subject C1
060307 Host-Parasite Interactions
970106 Expanding Knowledge in the Biological Sciences
Abstract Drosophila harbor substantial genetic variation for antibacterial defense, and investment in immunity is thought to involve a costly trade-off with life history traits, including development, life span, and reproduction. To understand the way in which insects invest in fighting bacterial infection, we selected for survival following systemic infection with the opportunistic pathogen Pseudomonas aeruginosa in wild-caught Drosophila melanogaster over 10 generations. We then examined genome-wide changes in expression in the selected flies relative to unselected controls, both of which had been infected with the pathogen. This powerful combination of techniques allowed us to specifically identify the genetic basis of the evolved immune response. In response to selection, population-level survivorship to infection increased from 15% to 70%. The evolved capacity for defense was costly, however, as evidenced by reduced longevity and larval viability and a rapid loss of the trait once selection pressure was removed. Counter to expectation, we observed more rapid developmental rates in the selected flies. Selection-associated changes in expression of genes with dual involvement in developmental and immune pathways suggest pleiotropy as a possible mechanism for the positive correlation. We also found that both the Toll and the Imd pathways work synergistically to limit infectivity and that cellular immunity plays a more critical role in overcoming P. aeruginosa infection than previously reported. This work reveals novel pathways by which Drosophila can survive infection with a virulent pathogen that may be rare in wild populations, however, due to their cost.
Formatted abstract
Drosophila harbor substantial genetic variation for antibacterial defense, and investment in immunity is thought to involve a
costly trade-off with life history traits, including development, life span, and reproduction. To understand the way in which
insects invest in fighting bacterial infection, we selected for survival following systemic infection with the opportunistic
pathogen Pseudomonas aeruginosa in wild-caught Drosophila melanogaster over 10 generations. We then examined
genome-wide changes in expression in the selected flies relative to unselected controls, both of which had been infected
with the pathogen. This powerful combination of techniques allowed us to specifically identify the genetic basis of the
evolved immune response. In response to selection, population-level survivorship to infection increased from 15% to 70%.
The evolved capacity for defense was costly, however, as evidenced by reduced longevity and larval viability and a rapid loss
of the trait once selection pressure was removed. Counter to expectation, we observed more rapid developmental rates in
the selected flies. Selection-associated changes in expression of genes with dual involvement in developmental and
immune pathways suggest pleiotropy as a possible mechanism for the positive correlation. We also found that both the Toll
and the Imd pathways work synergistically to limit infectivity and that cellular immunity plays a more critical role in
overcoming P. aeruginosa infection than previously reported. This work reveals novel pathways by which Drosophila can
survive infection with a virulent pathogen that may be rare in wild populations, however, due to their cost.
Keyword Pseudomonas-aeruginosa
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ
Additional Notes Article no. e1000385

Document type: Journal Article
Sub-type: Article (original research)
Collections: 2010 Higher Education Research Data Collection
ERA 2012 Admin Only
School of Biological Sciences Publications
 
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Created: Thu, 03 Sep 2009, 18:06:02 EST by Mr Andrew Martlew on behalf of School of Biological Sciences