A Search for Parent-of-Origin Effects on Honey Bee Gene Expression

Abstract

Parent-specific gene expression (PSGE) is little known outside of mammals and plants. PSGE occurs when the expression level of a gene depends on whether an allele was inherited from the mother or the father. Kin selection theory predicts that there should be extensive PSGE in social insects because social insect parents can gain inclusive fitness benefits by silencing parental alleles in female offspring. We searched for evidence of PSGE in honey bees using transcriptomes from reciprocal crosses between European and Africanized strains. We found 46 transcripts with significant parent-of-origin effects on gene expression, many of which overexpressed the maternal allele. Interestingly, we also found a large proportion of genes showing a bias toward maternal alleles in only one of the reciprocal crosses. These results indicate that PSGE may occur in social insects. The nonreciprocal effects could be largely driven by hybrid incompatibility between these strains. Future work will help to determine if these are indeed parent-of-origin effects that can modulate inclusive fitness benefits.

Testing the kinship theory of intragenomic conflict in honey bees ( Apis mellifera )

“…4; chi square with Yates correction, P < 0.0001 for both reproductive and sterile workers). Notably, a previous study of workers reared in the presence of a queen and brood did not show this patrigenic bias (10). Furthermore, we predicted that more transcripts would show a patrigenic bias in reproductive workers compared with sterile workers, and this prediction was also supported (chi square with Yates correction, P = 0.0259; Fig.…”

“…Each color represents a transcript that is significantly biased in both reciprocal crosses: green is maternal, red is paternal, blue is Africanized, purple is European, and gray is not significant. The significance was determined using an overlap between two statistical tests, a generalized linear interactive mixed model (GLIMMIX) (10), and a Storer-Kim test along with a cutoff threshold of <0.4 and >0.6 expression bias (note that 0.5 is equal expression of both allelic variants) (11).…”

“…This method has been used previously to identify parent-specific gene expression in honey bees (10). Parent of origin (maternal vs. paternal), race of origin (Africanized honey bee vs. European honey bee), and their interaction (parent × race) were included as fixed terms in the model, whereas SNP and replicate were considered as random factors.…”

“…We identified several gene ontology categories that were overrepresented in these sets of transcripts (Dataset S1). Finally, we used a previously established method (10,12) to quantify allele specific expression, using pyrosequencing to validate these results. We evaluated allelic expression levels of 12 genes, using 13 SNPs, in an independent sample of bees.…”

Differentially methylated obligatory epialleles modulate context-dependentLAMgene expression in the honeybeeApis mellifera

“…While parent-of-origin effects have been hinted for a number of traits in this organism, [24][25][26][27] there is currently no evidence that differentially methylated regions (DMRs) are associated with genomic imprinting. Given the extensive differential methylation that occurs in A. mellifera, and its association with complex traits, we wanted to investigate whether DMRs are associated with the underlying genetic sequence, the paternal or maternal inheritance of an allele, or whether they are primarily influenced by environmental cues.…”