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Social insect colony size is correlated with rates of molecular evolution

Abstract

Larger numbers of germline cell divisions can increase the number of mutations inherited by offspring. Therefore, in systems where the number of offspring is dependent on the number of germline cell divisions, a higher overall rate of molecular evolution may be expected. Here, I examine whether colony size in social insects, which varies from tens to millions, influences molecular evolutionary rates via this mechanism. Comparative analyses of whole genomes from three clades of social insects, including eight species in the ant genus Pseudomyrmex, seven fungus-growing ants, and 11 bees, reveal that rates of molecular evolution are positively correlated with colony size. The additional germline cell divisions necessary to maintain large colony sizes may lead to mutation accumulation in the germlines of queens of these species, a process similar to that which occurs in aging human males. Among species with large colonies, I also find a weak signal of intensified constraint on DNA repair genes. This pattern suggests the intriguing possibility that the additional mutations that occur in these taxa may increase selective pressure for replication fidelity. Finally, I find that colony size is negatively associated with GC-content in five highly conserved genes across 115 ant genera, a pattern consistent with a positive relationship between substitution rate and colony size. Colony size, a fundamental facet of eusociality, appears to play a previously unappreciated role in genome evolution.

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Data availability statement

Genome sequences have been deposited in the NCBI genomes database under BioProject number PRJNA268384.

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Acknowledgements

I thank Lindell Bromham, Paul Durst, Deren Eaton, Wynn Meyer, Corrie Moreau, Luisa Pallares, Tom Stewart, and Benjamin Winger for providing analytical insights and valuable feedback on earlier versions of this manuscript. I thank members of the Kocher Lab at Princeton University for their input. This work was supported by postdoctoral fellowship Grant No. 2018-67012-28085 from the USDA National Institute of Food and Agriculture.

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Correspondence to B. E. R. Rubin.

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Significance statement: The causes of genomic change are manifold and difficult to diagnose. Here, I find that colony size, a fundamental facet of insect sociality, is positively correlated with rates of molecular evolution, genome-wide. In social insect taxa with the largest colonies, a queen may produce hundreds of millions of offspring, requiring vastly more divisions in germline stem cells than in taxa with small colonies, leading to mutation accumulation. In addition, genes involved in DNA repair experience increased purifying selection in taxa with large colony sizes, suggesting that selective pressures work to compensate for the inherent change in substitution rate. These findings reveal a fundamental force in genome evolution which may serve to cap the size and complexity of social insect colonies.

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Rubin, B.E.R. Social insect colony size is correlated with rates of molecular evolution. Insect. Soc. 69, 147–157 (2022). https://doi.org/10.1007/s00040-022-00859-3

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  • DOI: https://doi.org/10.1007/s00040-022-00859-3

Keywords

  • Molecular evolution
  • Mutation rate
  • DNA repair
  • Social insects
  • Colony size
  • Hymenoptera