Parent of origin gene expression in the bumblebee, Bombus terrestris, supports Haig’s kinship theory for the evolution of genomic imprinting

Abstract

Genomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Haig’s kinship theory hypothesizes that genomic imprinting is due to an evolutionary conflict of interest between alleles from the mother and father. In social insects, it has been suggested that genomic imprinting should be widespread. One recent study identified parent-of-origin expression in honeybees and found evidence supporting the kinship theory. However, little is known about genomic imprinting in insects and multiple theoretical predictions must be tested to avoid single-study confirmation bias. We, therefore, tested for parent-of-origin expression in a primitively eusocial bee. We found equal numbers of maternally and paternally biased expressed alleles. The most highly biased alleles were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honeybee, suggesting rapid evolution of genomic imprinting in Hymenoptera.Impact summaryGenomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Genomic imprinting is an evolutionary paradox. Natural selection is expected to favour expression of both alleles in order to protect against recessive mutations that render a gene ineffective. What then is the benefit of silencing one copy of a gene, making the organism functionally haploid at that locus? Several explanations for the evolution of genomic imprinting have been proposed. Haig’s kinship theory is the most developed and best supported.Haig’s theory is based on the fact that maternally (matrigene) and paternally (patrigene) inherited genes in the same organism can have different interests. For example, in a 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 be selected to value the survival of the organism it is in more highly, compared to the survival of siblings. This is not the case for a matrigene.Kinship theory is central to our evolutionary understanding of imprinting effects in human health and plant breeding. Despite this, it still lacks a robust, independent test. Colonies of social bees consist of diploid females (queens and workers) and haploid males created from unfertilised eggs. This along with their social structures allows for novel predictions of Haig’s theory.In this paper, we find parent of origin allele specific expression in the important pollinator, the buff-tailed bumblebee. We also find, as predicted by Haig’s theory, a balanced number of genes showing matrigenic or patrigenic bias with the most extreme bias been found in matrigenically biased genes.

Tissue‐specific transcription patterns support the kinship theory of intragenomic conflict in honey bees (Apis mellifera)

“…Finally, genes showing PSGE were also in modules enriched in genes involved in post‐transcriptional processing, suggesting that they may influence physiology and behaviour through these pathways. As genomic resources expand and methods for manipulating gene expression and gene sequences become more sophisticated, it will be important to evaluate these mechanisms in other bee species (Grozinger & Zayed, 2020), particularly those where the predictions of patrigene vs. matrigene expression bias in mediating worker reproduction may differ (see Marshall, van Zweden, et al, 2020).…”

Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

“…2016 ; Smith et al. 2020 ) and bumblebees ( Marshall et al. 2020 ) and there has been speculation that DNA methylation may act as an imprinting mark.…”

Kr-h1 maintains distinct caste-specific neurotranscriptomes in response to socially regulated hormones

“…We analyzed previously published RNA-seq data from ant species with fixed queen-worker (Solenopsis invicta and Monomorium pharaonis) or queenless social systems (Dinoponera quadriceps and Ooceraea biroi). We also analyzed two species of wasps (Polistes dominula and Polistes canadensis) and bees (Bombus terrestris and Megalopta genalis) (Chandra et al, 2018;Kapheim et al, 2020;Marshall et al, 2020;Patalano et al, 2015;Standage et al, 2016;Wang et al, 2020). In all cases, genes differentially expressed between non-reproductive and reproductive individuals overlapped significantly with genes regulated by JH3 and 20E in Harpegnathos neuronal cultures (Figure S3, Venn diagrams).…”