Abstract
Accurate knowledge of the mutation rate provides a base line for inferring expected rates of evolution, for testing evolutionary hypotheses and for estimation of key parameters. Advances in sequencing technology now permit direct estimates of the mutation rate from sequencing of close relatives. Within insects there have been three prior such estimates, two in nonsocial insects (Drosophila: 2.8 × 10−9 per bp per haploid genome per generation; Heliconius: 2.9 × 10−9) and one in a social species, the honeybee (3.4 × 10−9). Might the honeybee’s rate be ∼20% higher because it has an exceptionally high recombination rate and recombination may be directly or indirectly mutagenic? To address this possibility, we provide a direct estimate of the mutation rate in the bumblebee (Bombus terrestris), this being a close relative of the honeybee but with a much lower recombination rate. We confirm that the crossover rate of the bumblebee is indeed much lower than honeybees (8.7 cM/Mb vs. 37 cM/Mb). Importantly, we find no significant difference in the mutation rates: we estimate for bumblebees a rate of 3.6 × 10−9 per haploid genome per generation (95% confidence intervals 2.38 × 10−9 and 5.37 × 10−9) which is just 5% higher than the estimate that of honeybees. Both genomes have approximately one new mutation per haploid genome per generation. While we find evidence for a direct coupling between recombination and mutation (also seen in honeybees), the effect is so weak as to leave almost no footprint on any between-species differences. The similarity in mutation rates suggests an approximate constancy of the mutation rate in insects.
Highlights
Accurate estimation of the mutation rate is necessary for establishing a base rate for molecular evolution in the absence of biased gene conversion or natural selection
To address the above hypothesis and, more generally the possibility that honeybees may have a high mutation rate because they have a high recombination rate, we estimate the mutation rate in the honeybees’ close relative, the relatively primitively social bumblebee (Bombus terrestris), by deep sequencing the whole genome of 32 drones, 22 of them from a same queen defined as colony I, 10 of them from another queen as colony II
We could confirm that the recombination rate of the bumblebee is considerably lower than that of the honeybees, the precise magnitude of difference being dependent on the marker density (7.5: 20 cM/Mb at low density, 8.7: 37 cM/Mb at higher densities)
Summary
Accurate estimation of the mutation rate is necessary for establishing a base rate for molecular evolution in the absence of biased gene conversion or natural selection. To address the above hypothesis and, more generally the possibility that honeybees may have a high mutation rate because they have a high recombination rate, we estimate the mutation rate in the honeybees’ close relative, the relatively primitively social bumblebee (Bombus terrestris), by deep sequencing the whole genome of 32 drones, 22 of them from a same queen defined as colony I, 10 of them from another queen as colony II We cannot exclude the hypothesis that all insects, regardless of sociality or recombination rate, have approximately the same mutation rate
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