Originally published as Genetics Published Articles Ahead of Print on December 1, 2005.

Genetics, Vol. 172, 1655-1663, March 2006, Copyright © 2006
doi:10.1534/genetics.105.053173

Patterns of Diversity and Linkage Disequilibrium Within the Cosmopolitan Inversion In(3R)Payne in Drosophila melanogaster Are Indicative of Coadaptation

W. Jason Kennington*,{dagger},{ddagger},1, Linda Partridge{dagger} and Ary A. Hoffmann{ddagger}

* School of Animal Biology, University of Western Australia, Crawley, Western Australia 6009, Australia, {dagger} Department of Biology, University College, London WC1E 2BT, United Kingdom and {ddagger} Centre for Environmental Stress and Adaptation Research, Department of Genetics, University of Melbourne, Victoria 3010, Australia

1 Corresponding author: School of Animal Biology, University of Western Australia, Crawley, WA 6009, Australia. 
E-mail: wjk{at}cyllene.uwa.edu.au

The cosmopolitan inversion In(3R)Payne in Drosophila melanogaster decreases in frequency with increasing distance from the equator on three continents, indicating it is subject to strong natural selection. We investigated patterns of genetic variation and linkage disequilibrium (LD) in 24 molecular markers located within and near In(3R)Payne to determine if different parts of the inversion responded to selection the same way. We found reduced variation in the markers we used compared to others distributed throughout the genome, consistent with the inversion having a relatively recent origin (<Ne generations). LD between markers and In(3R)Payne varied significantly among markers within the inversion, with regions of high association interspersed by regions of low association. Several factors indicate that these patterns were not due to demographic factors such as admixture and bottlenecks associated with colonization, but instead reflected strong epistatic selection. Furthermore, we found that nonadjacent regions with high association to the inversion contained markers with the strongest clinal patterns in allele frequency; in most cases, the level of clinal variation was beyond what could be explained by hitchhiking with In(3R)Payne, indicating that genes within these regions are targets of selection. Our results provide some support for the hypothesis that inversions persist in natural populations because they hold together favorable combinations of alleles that act together to facilitate adaptive shifts.




This article has been cited by other articles:


Home page
 Mol Biol EvolHome page
C. Nobrega, M. Khadem, M. Aguade, and C. Segarra
Genetic Exchange versus Genetic Differentiation in a Medium-Sized Inversion of Drosophila: The A2/Ast Arrangements of Drosophila subobscura
Mol. Biol. Evol., August 1, 2008; 25(8): 1534 - 1543.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
T. L. Turner, M. T. Levine, M. L. Eckert, and D. J. Begun
Genomic Analysis of Adaptive Differentiation in Drosophila melanogaster
Genetics, May 1, 2008; 179(1): 455 - 473.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
M. T. Levine and D. J. Begun
Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila melanogaster
Genetics, May 1, 2008; 179(1): 475 - 485.
[Abstract] [Full Text] [PDF]

Home page
 GeneticsHome page
W. J. Kennington, A. A. Hoffmann, and L. Partridge
Mapping Regions Within Cosmopolitan Inversion In(3R)Payne Associated With Natural Variation in Body Size in Drosophila melanogaster
Genetics, September 1, 2007; 177(1): 549 - 556.
[Abstract] [Full Text] [PDF]

Home page
 Proc. Natl. Acad. Sci. USAHome page
K. A. Dyer, B. Charlesworth, and J. Jaenike
Chromosome-wide linkage disequilibrium as a consequence of meiotic drive
PNAS, January 30, 2007; 104(5): 1587 - 1592.
[Abstract] [Full Text] [PDF]