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Estimation of Fine-Scale Recombination Intensity Variation in the white–echinus Interval of D. melanogaster

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Abstract

Accurate assessment of local recombination rate variation is crucial for understanding the recombination process and for determining the impact of natural selection on linked sites. In Drosophila, local recombination intensity has been estimated primarily by statistical approaches, by estimating the local slope of the relationship between the physical and genetic maps. However, these estimates are limited in resolution and, as a result, the physical scale at which recombination intensity varies in Drosophila is largely unknown. Although there is some evidence suggesting as much as a 40-fold variation in crossover rate at a local scale in D. pseudoobscura, little is known about the fine-scale structure of recombination rate variation in D. melanogaster. Here we experimentally examine the fine-scale distribution of crossover events in a 1.2-Mb region on the D. melanogaster X chromosome using a classic genetic mapping approach. Our results show that crossover frequency is significantly heterogeneous within this region, varying approximately 3.5-fold. Simulations suggest that this degree of heterogeneity is sufficient to affect levels of standing nucleotide diversity, although the magnitude of this effect is small. We recover no statistical association between empirical estimates of nucleotide diversity and recombination intensity, which is likely due to the limited number of loci sampled in our population genetic data set. However, codon bias is significantly negatively correlated with fine-scale recombination intensity estimates, as expected. Our results shed light on the relevant physical scale to consider in evolutionary analyses relating to recombination rate and highlight the motivations to increase the resolution of the recombination map in Drosophila.

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Acknowledgments

The authors gratefully acknowledge everyone in the Clark and Aquadro laboratories (particularly S. Hackett and H. Flores)—along with B. P. Lazzaro, M. Hamblin, and J. G. Mezey—for their tireless fly sorting and scoring efforts. The authors also thank H. Flores, C. Pergueroles, A. Larracuente, and J. Werner for assistance with screening our experimental lines for inversions, and X. Wang for help with optimizing the pyrosequencing assays. R. Hernandez generously gave us permission to use the program SFS_CODE for our simulations, and the authors are also indebted to him for guidance in implementing this program. This work was supported in part by a National Institutes of Health National Research Service Award (Grant No. 1F32GM080944-01 to N. D. S., C. F. A., and A. G. C.).

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Correspondence to Nadia D. Singh.

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Singh, N.D., Aquadro, C.F. & Clark, A.G. Estimation of Fine-Scale Recombination Intensity Variation in the white–echinus Interval of D. melanogaster . J Mol Evol 69, 42–53 (2009). https://doi.org/10.1007/s00239-009-9250-5

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