Variation in mutation, recombination, and transposition rates in Drosophila melanogaster and Drosophila simulans

Abstract

Mutation, recombination, and transposition occurring during meiosis provide the variation on which natural selection can act and the rates at which they occur are important parameters in models of evolution. The de novo mutation rate determines levels of genetic diversity, responses to ongoing selection, and levels of genetic load. Recombination breaks up haplotypes and reduces the effects of linkage, helping to spread beneficial alleles and purge deleterious ones. Transposable elements (TE) selfishly replicate themselves through the genome, imposing fitness costs on the host and introducing complex mutations that can affect gene expression and give rise to new genes. However, even for key evolutionary models such as Drosophila melanogaster and D. simulans few estimates of these parameters are available, and we have little idea of how rates vary between individuals, sexes, populations, or species. Here, we provide direct estimates of mutation, recombination, and transposition rates and their variation in a West African and a European population of D. melanogaster and a European population of D. simulans. Across 89 flies, we observe 58 single nucleotide mutations, 286 crossovers, and 89 TE insertions. Compared to the European D. melanogaster, we find the West African population has a lower mutation rate (1.67 vs. 4.86 x 10-9 site-1 gen-1) and transposition rate (8.99 vs. 23.36 x 10-5 copy-1 gen-1), but a higher recombination rate (3.44 vs. 2.06 cM/Mb). The European D. simulans population has a similar mutation rate to European D. melanogaster but a significantly higher recombination rate and a lower but not significantly different transposition rate. Overall, we find paternal-derived mutations are more frequent than maternal ones in both species. HighlightsO_LIDe novo mutation rates are 1.67 x 10-9 site-1 gen-1 (95% HPD CI: 0.54 - 3.14 x 10-9), 4.86 x 10-9 site-1 gen-1 (2.11 - 8.02 x 10-9), and 4.51 x 10-9 site-1 gen-1 (1.94 - 7.75 x 10-9) for the West African D. melanogaster, the European D. melanogaster and the European D. simulans population, respectively. C_LIO_LIIn females, recombination rates in the absence of large genomic inversions are 3.44 cM/Mb (2.72 - 4.18), 2.06 cM/Mb (1.57 - 2.57), and 3.04 cM/Mb (2.45 - 3.73) for the three populations, respectively. There was no strong evidence of recombination observed in males. C_LIO_LIMutations (SNMs and indels) are male-biased. C_LIO_LIThe West African D. melanogaster population has a lower TE activity than the other populations and CMC-Transib is the dominant active TE. The European D. melanogaster population has multiple active TEs: Gypsy, CMC-Transib, Pao, Jockey and hAT-hobo; while in European D. simulans, they are Gypsy, CMC-Transib, Pao, hAT-hobo, Copia and TcMar-Mariner. C_LI