Social Epigenetics Lab
Our research: Genomic imprinting in social insects
Genomic imprinting (GI) is the inactivation of one allele in diploid individuals, with inactivation being dependent upon the sex of the parent from which it was derived. Most harmful mutations require only a single good copy of the gene for the organism to survive. Why then do organisms sometimes silence one copy when they benefit from a spare? The leading explanation for the evolution of imprinting is conflict theory.
Matrigenes and patrigenes in the same organism can have different interests. In species with multiple paternity, a patrigene has a lower probability of being present in siblings that are progeny of the same mother than does a matrigene. As a result, a patrigene will value more the survival of the organism it is in, compared to the survival of siblings. The matrigene values them equally. In mammals and flowering plants, this conflict is played out during offspring provisioning with maternal resources. Conflict theory hypothesises that imprinting evolved to silence genes during provisioning. Consider a hypothetical gene causing resource transfer from mother to embryo. The matrigene should be imprinted as this will share resources more equally among embryos increasing the number of copies of the matrigene through siblings' survival.
Mammals and flowering plants inspired Haig's conflict theory. The only data to test the theory has thus far come from these same taxa. Eusocial Hymenoptera (ants, bees and wasps) provide an ideal model for making independent tests of the theory. Hymenoptera are haplodiploid, with diploid females (queens and workers) arising from fertilised eggs and haploid males arising from unfertilised eggs. This genetic system and social insects' reproductive division of labour results in novel predictions for conflict theory.
Until recently, a problem in using eusocial Hymenoptera to test conflict theory was that they were not known to have the mechanisms required for GI. In 2006, it was shown that the honeybee has a methylation system. DNA methylation is one of the major mechanisms of GI in mammals and flowering plants. It has since been found that this form of methylation exists generally in the hymenoptera and transmits epigenetic information.
To test the conflict theory it is necessary to investigate a trait that can be quantified both at the phenotypic and the gene expression levels, and for which the theory predicts conflict between an individual's matrigenes and patrigenes. Worker reproduction in bumblebees is such a trait. Workers will lay male eggs if a colony becomes queenless. Within these workers, the matrigenes and patrigenes of reproduction genes have different selectional pressures. A matrigene in a given worker has a 50% chance of ending up in that worker's son, but only a 25% chance of being in a different worker's son. The equivalent patrigene is equally likely to be in either son (50%). This asymmetry stems from the fact that there is only one patrigene in the colony (haploid father), but there are two potential matrigenes (diploid mother). For a patrigene, it is of equal value if its worker reproduces or the worker's siblings reproduce, for a matrigene it is twice as beneficial if the worker herself reproduces. The conflict theory predicts that genes whose upregulation is associated with worker reproduction should be expressed if matrigenes but not if patrigenes, i.e. patrigenes should be imprinted.
We have recently shown that methylation status corresponds to reproductive status in bumblebees. We have also removed methylation causing workers to begin reproduction (paper, press release and media coverage). This work is now being extended by an RRBS approach. Also using NGS approaches we are currently investigating if monoallelic expression is associated with differentially methylated alleles.