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MBE Advance Access published online on April 2, 2007

Molecular Biology and Evolution, doi:10.1093/molbev/msm066
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© The Author 2007. 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

Research Article

The Genetic Architecture of Ecological Speciation and the Association with Signatures of Selection in Natural Lake Whitefish (Coregonus sp. Salmonidae) Species Pairs

SM Rogers{dagger} and L Bernatchez

Québec Océan, Département de Biologie, Université Laval, Ste-Foy, Québec, Canada , G1K 7P4

{dagger} Present Address: Department of Zoology, University of British Columbia, #2370-6270 University Blvd. Vancouver, BC, V6T 1Z4, Canada, Ph: (604) 822-3383 Fx: (604) 822-2416, e-mail: srogers{at}zoology.ubc.ca

Received for publication February 23, 2007. Accepted for publication March 19, 2007.

Adaptive evolutionary change is contingent on variation and selection, thus understanding adaptative divergence and ultimately speciation requires information on both the genetic basis of adaptive traits as well as an understanding of the role of divergent natural selection on those traits. The lake whitefish (Coregonus clupeaformis) consists of several sympatric dwarf (limnetic) and normal (benthic) species pairs that co-inhabit northern postglacial lakes. These young species pairs have evolved independently and display parallelism in life-history, behavioral, and morphological divergence associated with the use of distinct trophic resources. We identified phenotype-environment associations and determined the genetic architecture and the role of selection modulating population genetic divergence in sympatric dwarf and normal lake whitefish. The genetic architecture of nine adaptive traits was analyzed in two hybrid backcrosses individually phenotyped throughout their life history. Significant QTL were associated with swimming behaviour (habitat selection, predator avoidance), growth rate, morphology (condition factor and gill rakers), and life history (onset of maturity and fecundity). Genome scans among four natural sympatric pairs, using loci segregating in the map, revealed a signature of selection for 24 loci. Loci exhibiting a signature of selection were associated with QTL relative to other regions of the genome more often than expected by chance alone. Two parallel QTL outliers for growth and condition factor exhibited segregation distortion in both mapping families, supporting the hypothesis that adaptive divergence contributing to parallel reductions of gene flow among natural populations may cause genetic incompatibilities. Overall, these findings offer evidence that the genetic architecture of ecological speciation is associated with signatures of selection in nature, providing strong support for the hypothesis that divergent natural selection is currently maintaining adaptive differentiation and promoting ecological speciation in lake whitefish species pairs.

Key Words: speciation • QTL • linkage • natural selection • Coregonus • genome scan


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