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MBE Advance Access published online on February 22, 2006

Molecular Biology and Evolution, doi:10.1093/molbev/msj112
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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 January 30, 2006

Research Article

Genome-Wide Associations Between Hybrid Sterility QTL and Marker Transmission Ratio Distortion

Leonie C. Moyle 1 * and Elaine B. Graham 2

1 Center for Population Biology, University of California, Davis, USA 95616; Present Address: Department of Biology, Indiana University, Bloomington, IN 47405
2 Tomato Genetic Resource Center, University of California, Davis, USA 95616

* To whom correspondence should be addressed.
Leonie C. Moyle, E-mail: lmoyle{at}indiana.edu


   Abstract

Marker transmission ratio distortion (TRD) in genetic mapping populations is frequently ascribed to selection against allelic combinations that cause hybrid incompatibility. Accordingly, genomic regions of TRD should be non-randomly associated (co-located) with loci that underlie hybrid incompatibility. To directly test this hypothesis, we evaluated the genome-wide qualitative and quantitative agreement between chromosomal regions exhibiting marker TRD and those known to contain hybrid incompatibility QTL. Incompatibility data came from a near isogenic line (NIL) analysis of pollen and seed sterility in a cross between two Solanum (formerly Lycopersicon) species. We assessed (1) whether these incompatibility loci are co-located more frequently than expected by chance with markers that show significant TRD in two earlier generations preceding these introgression lines, and (2) whether the magnitude of marker distortion quantitatively matches the estimated strength of selection against each incompatibility locus. We found evidence that TRD regions are chromosomally co-located with hybrid incompatibility loci more frequently than is expected by chance: pollen sterility QTL were most closely associated with distorted heterozygote frequencies in later generation backcrosses. Nonetheless, there was no evidence for an association between TRD and seed sterility, and little evidence of a quantitative association between the magnitude of marker TRD and the fitness effects of heterospecific alleles at each chromosomal location. We propose and test a model (the ‘dance partner’ hypothesis) to explain several cases where regions of TRD are not associated with hybrid incompatibility loci. Under this model some NILs containing greater than one heterospecific introgression may not express hybrid incompatibility phenotypes because they carry both appropriate genetic ‘dance partners’ required for a fully functional interaction. Accordingly, negative interactions expressed in earlier BC generations are masked in these double-introgression NILs. Based on this model, we identify the location of several new putative pairwise interactors underlying hybrid incompatibility in this species cross.

Keywords: hybrid incompatibility; segregation; marker distortion; speciation; QTL mapping; NIL; Lycopersicon.
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