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You can't keep a good parasite down : Evolution of a male-killer suppressor uncovers cytoplasmic incompatibility

Hornett, Emily A. ; Duplouy, Anne M R LU ; Davies, Neil ; Roderick, George K. ; Wedell, Nina ; Hurst, Gregory D D and Charlat, Sylvain (2008) In Evolution 62(5). p.1258-1263
Abstract

Maternally inherited parasites are known to impose a wide variety of reproductive manipulations upon their host. These often produce strong selection on the host to suppress the parasite, resulting in a reduction in the frequency of the parasite. However, in the butterfly Hypolimnas bolina, infected with a Wolbachia bacterium, field data demonstrate that suppression of the male-killing phenotype does not depress parasite frequency. Here we test and verify one hypothesis to explain this apparent paradox - Wolbachia induces a second phenotype, Cytoplasmic Incompatibility (CI), in populations where host suppression has evolved. We further demonstrate that the capacity to induce CI has not evolved de novo, but instead is instantaneously... (More)

Maternally inherited parasites are known to impose a wide variety of reproductive manipulations upon their host. These often produce strong selection on the host to suppress the parasite, resulting in a reduction in the frequency of the parasite. However, in the butterfly Hypolimnas bolina, infected with a Wolbachia bacterium, field data demonstrate that suppression of the male-killing phenotype does not depress parasite frequency. Here we test and verify one hypothesis to explain this apparent paradox - Wolbachia induces a second phenotype, Cytoplasmic Incompatibility (CI), in populations where host suppression has evolved. We further demonstrate that the capacity to induce CI has not evolved de novo, but instead is instantaneously expressed upon the survival of infected males. The significance of these results is threefold: (1) multiple phenotypes can provide Wolbachia with the means to maintain itself in a host following suppression of a single manipulative phenotype; (2) the ability to induce CI can remain hidden in systems in which male-killing is observed, just as the ability to induce male-killing may be obscured in strains exhibiting CI; (3) the evolutionary maintenance of CI in a system in which it is not expressed suggests a functional link with male-killing or other traits under selection.

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author
; ; ; ; ; and
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Hypolimnas bolina, Male-killing, Suppression, Wolbachia
in
Evolution
volume
62
issue
5
pages
1258 - 1263
publisher
Wiley-Blackwell
external identifiers
  • scopus:43049127503
  • pmid:18298644
ISSN
0014-3820
DOI
10.1111/j.1558-5646.2008.00353.x
language
English
LU publication?
no
id
e8cfa064-ba2d-4cbc-b585-95d367ee48dc
date added to LUP
2018-11-16 15:54:32
date last changed
2024-06-26 03:08:22
@article{e8cfa064-ba2d-4cbc-b585-95d367ee48dc,
  abstract     = {{<p>Maternally inherited parasites are known to impose a wide variety of reproductive manipulations upon their host. These often produce strong selection on the host to suppress the parasite, resulting in a reduction in the frequency of the parasite. However, in the butterfly Hypolimnas bolina, infected with a Wolbachia bacterium, field data demonstrate that suppression of the male-killing phenotype does not depress parasite frequency. Here we test and verify one hypothesis to explain this apparent paradox - Wolbachia induces a second phenotype, Cytoplasmic Incompatibility (CI), in populations where host suppression has evolved. We further demonstrate that the capacity to induce CI has not evolved de novo, but instead is instantaneously expressed upon the survival of infected males. The significance of these results is threefold: (1) multiple phenotypes can provide Wolbachia with the means to maintain itself in a host following suppression of a single manipulative phenotype; (2) the ability to induce CI can remain hidden in systems in which male-killing is observed, just as the ability to induce male-killing may be obscured in strains exhibiting CI; (3) the evolutionary maintenance of CI in a system in which it is not expressed suggests a functional link with male-killing or other traits under selection.</p>}},
  author       = {{Hornett, Emily A. and Duplouy, Anne M R and Davies, Neil and Roderick, George K. and Wedell, Nina and Hurst, Gregory D D and Charlat, Sylvain}},
  issn         = {{0014-3820}},
  keywords     = {{Hypolimnas bolina; Male-killing; Suppression; Wolbachia}},
  language     = {{eng}},
  month        = {{05}},
  number       = {{5}},
  pages        = {{1258--1263}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Evolution}},
  title        = {{You can't keep a good parasite down : Evolution of a male-killer suppressor uncovers cytoplasmic incompatibility}},
  url          = {{http://dx.doi.org/10.1111/j.1558-5646.2008.00353.x}},
  doi          = {{10.1111/j.1558-5646.2008.00353.x}},
  volume       = {{62}},
  year         = {{2008}},
}