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Genetic and Evolutionary Correlates of Fine-Scale Recombination Rate Variation in Drosophila persimilis

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Abstract

Recombination is fundamental to meiosis in many species and generates variation on which natural selection can act, yet fine-scale linkage maps are cumbersome to construct. We generated a fine-scale map of recombination rates across two major chromosomes in Drosophila persimilis using 181 SNP markers spanning two of five major chromosome arms. Using this map, we report significant fine-scale heterogeneity of local recombination rates. However, we also observed “recombinational neighborhoods,” where adjacent intervals had similar recombination rates after excluding regions near the centromere and telomere. We further found significant positive associations of fine-scale recombination rate with repetitive element abundance and a 13-bp sequence motif known to associate with human recombination rates. We noted strong crossover interference extending 5–7 Mb from the initial crossover event. Further, we observed that fine-scale recombination rates in D. persimilis are strongly correlated with those obtained from a comparable study of its sister species, D. pseudoobscura. We documented a significant relationship between recombination rates and intron nucleotide sequence diversity within species, but no relationship between recombination rate and intron divergence between species. These results are consistent with selection models (hitchhiking and background selection) rather than mutagenic recombination models for explaining the relationship of recombination with nucleotide diversity within species. Finally, we found significant correlations between recombination rate and GC content, supporting both GC-biased gene conversion (BGC) models and selection-driven codon bias models. Overall, this genome-enabled map of fine-scale recombination rates allowed us to confirm findings of broader-scale studies and identify multiple novel features that merit further investigation.

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Acknowledgments

Funding was provided by NIH GM076051, NIH GM086445, and NSF DEB 0715484 to MAFN. We thank S. Bennett for technical support, R. Kulathinal for generating the alignment of the D. persimilis 454 sequence traces to the other sequences, and the Noor lab, R. Kliman, L. Loewe and D. Lowry for comments on the manuscript. We thank C. Fitzpatrick for preliminary interference analysis on D. pseudoobscura data. We also thank F. Dietrich for help in developing the scripts to design genotyping markers, and C. Jones and T. Mitchell-Olds for valuable input on data analysis.

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Stevison, L.S., Noor, M.A.F. Genetic and Evolutionary Correlates of Fine-Scale Recombination Rate Variation in Drosophila persimilis . J Mol Evol 71, 332–345 (2010). https://doi.org/10.1007/s00239-010-9388-1

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