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 alleles in diploid individuals, with the expression being dependent on 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 honey bees 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 genes. The most highly biased genes were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honey bee, suggesting rapid evolution of genomic imprinting in Hymenoptera.

How does epigenetics influence the course of evolution?

“…In mammals and plants, 'imprints' typically involve sexspecific DNA methylation of the promoter regions of the relevant genes [67,68]. In insects, parent-specific allele expression levels are repeatedly observed [69][70][71][72]. However, the underlying molecular mechanisms of the imprinting that cause parent-specific gene expression (PSGE) in insects have not been conclusively established [43].…”

A novel method for using RNA‐seq data to identify imprinted genes in social Hymenoptera with multiply mated queens

“…Social Hymenoptera with a life‐time unmated worker caste are predicted to utilize genomic imprinting in multiple situations of reproductive conflicts, although some of the theory was more confident (Queller, 2003) than other assessments (Kronauer, 2008). However, compared to mammals, there are few systematic searches for imprinted genes in social insects and all are restricted to either honeybees or bumblebees (Galbraith et al., 2016; Kocher et al, 2015; Lonsdale et al., 2017; Marshall et al., 2020; Smith et al., 2020), predominantly due to the difficulty of maintaining and breeding other social insect species under laboratory conditions. Here, we developed a general method to search for imprinted genes in social hymenopteran species without requiring reciprocal crosses, and we demonstrated the utility of this technique using the leaf‐cutting ant Acromyrmex echinatior .…”

“…Only five social insect studies have attempted to directly identify putatively imprinting-induced ASE with genome-wide searches based on high-throughput sequencing: three in the honeybee (Galbraith et al, 2016;Kocher et al, 2015;Smith et al, 2020) and two in a bumblebee (Lonsdale et al, 2017;Marshall et al, 2020).…”

“…Only five social insect studies have attempted to directly identify putatively imprinting‐induced ASE with genome‐wide searches based on high‐throughput sequencing: three in the honeybee (Galbraith et al., 2016; Kocher et al, 2015; Smith et al., 2020) and two in a bumblebee (Lonsdale et al., 2017; Marshall et al., 2020). These studies adopted techniques successfully applied in other (diploid) organisms, where two genotypes are reciprocally crossed and offspring RNA sequenced to find genes where the relative proportion of the two RNA alleles is dependent on the direction of the cross while differing significantly from the 1:1 null expectation (Babak et al, 2015, Coolon et al, 2012, Gehring et al, 2011, Gregg et al, 2010, Wang et al., 2008).…”

Sexual antagonism in haplodiploids

“…Finally, a further intragenomic conflict that may emerge over sexual antagonism is that between maternal-origin and paternal-origin genes (Haig 2002). The asymmetric transmission genetics that defines haplodiploidy may subsequently generate differences between maternal-origin and paternal-origin genes in how they value males and females, and also their relatedness to the males and females with whom they interact (Haig 1992;Queller and Strassmann 2002;Queller 2003;Wild and West 2009;Rautiala and Gardner 2016;Marshall et al 2020). In the simplest case, with full outbreeding, we find that if a gene is of maternal-origin it places equal value upon males and females, under diploidy, arrhenotoky and PGE.…”