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MBE Advance Access published online on November 21, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl176
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted November 15, 2006

Research Article

Restrictive Flamenco Alleles Are Maintained in Drosophila melanogaster Population Cages, Despite the Absence of Their Endogenous Gypsy Retroviral Targets

Alain Pélisson 1 *, Geneviève Payen-Groschêne 1, Christophe Terzian 2, and Alain Bucheton 1

1 Institut de Génétique Humaine, CNRS, 34396 Montpellier, Cedex 5, France
2 UMR5202, CNRS-MNHN-EPHE, 16 rue Buffon - CP39 -75005 Paris, France; Present address: UMR 754, INRA-ENVL-UCBL-EPHE, 50 Avenue Tony Garnier. 69366 Lyon cedex 07, France

* To whom correspondence should be addressed.
Alain Pélisson, E-mail: Alain.Pelisson{at}igh.cnrs.fr


  Abstract

The flamenco (flam) locus, located at 20A1-3 in the centromeric heterochromatin of the Drosophila melanogaster X chromosome, is a major regulator of the gypsy/mdg4 endogenous retrovirus. In restrictive strains, functional flam alleles maintain gypsy proviruses in a repressed state. By contrast, in permissive strains, proviral amplification results from infection of the female germline and subsequent insertions into the chromosomes of the progeny. A restrictive/permissive polymorphism prevails in natural and laboratory populations. This polymorphism was assumed to be maintained by the interplay of opposite selective forces : on one hand, the increase of genetic load caused by proviral insertions would favor restrictive flam alleles because they make flies resistant to these gypsy replicative transpositions; on the other, a hypothetical resistance cost would select against such alleles in the absence of the retrovirus. However, the population cage data presented in this paper do not fit with this simple resistance cost hypothesis, since restrictive alleles were not eliminated in the absence of functional gypsy proviruses: on the contrary, using two independent flam allelic pairs, the restrictive frequency rose to about ninety percent in every experimental population, whatever the pair of alleles and the allelic proportions in the initial inoculum. These data suggest that the flam polymorphism is maintained by some strong balancing selection that would act either on flam itself, independently of the deleterious effect of gypsy, or on a hypothetical flanking gene, in linkage desequilibrium with flam. Alternatively, restrictive flam alleles might also be resistant to some other retroelement(s) that would be still present in the cage populations, causing a positive selection for these alleles. Whatever the selective force(s) that maintain(s) high levels of restrictive alleles independently of gypsy, this unknown mechanism can set up an interesting kind of antiviral innate immunity, at the population level.

Keywords: Drosophila melanogaster; flamenco (flam); anti-gypsy resistance cost; natural and experimental populations; balancing selection; linkage desequilibrium.
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