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

Abstract

Kin selection may act differently on genes inherited from parents (matrigenes and patrigenes), resulting in intragenomic conflict. This conflict can be observed as differential expression of matrigenes and patrigenes, or parent‐specific gene expression (PSGE). In honey bees (Apis mellifera), intragenomic conflict is hypothesized to occur in multiple social contexts. Previously, we found that patrigene‐biased expression in reproductive tissues was associated with increased reproductive potential in worker honey bees, consistent with the prediction that patrigenes are selected to promote selfish behaviour in this context. Here, we examined brain gene expression patterns to determine if PSGE is also found in other tissues. As before, the number of transcripts showing patrigene expression bias was significantly greater in the brains of reproductive vs. sterile workers, while the number of matrigene‐biased transcripts was not significantly different. Twelve transcripts out of the 374 showing PSGE in either tissue showed PSGE in both brain and reproductive tissues; this overlap was significantly greater than expected by chance. However, the majority of transcripts show PSGE only in one tissue, suggesting the epigenetic mechanisms mediating PSGE exhibit plasticity between tissues. There was no significant overlap between transcripts that showed PSGE and transcripts that were significantly differentially expressed. Weighted gene correlation network analysis identified modules which were significantly enriched in both types of transcripts, suggesting that these genes may influence each other through gene networks. Our results provide further support for the kin selection theory of intragenomic conflict, and provide valuable insights into the mechanisms which may mediate this process.

Examining parent-of-origin effects on transcription and RNA methylation in mediating aggressive behavior in honey bees (Apis mellifera)

“…This study provides evidence for the role of intragenomic con ict in mediating aggression and colony defense in worker honey bees. When coupled with previous studies that demonstrated how intragenomic con ict shapes worker reproduction [17,19,21,22], our results suggest that intragenomic con ict and parent-speci c transcription may be important factors in shaping the individual variation seen within the context of social behavior in honey bees, and potentially other species [24,32]. We examined whether RNA m6A and/or alternative splicing play a role in intragenomic con ict in honey bees and did not nd evidence to suggest that either are associated with parent-speci c transcription in this species.…”

“…For each transcript, all positions were required to exhibit the same direction of parent-or lineage-speci c bias at previously established thresholds for p1 (the proportion of reads mapping to the AHB allele in offspring from the EHB queen and AHB drone cross) and p2 (the proportion of reads mapping to the AHB allele in offspring from the AHB queen and EHB drone cross) for the transcript to be reported as exhibiting bias. Additionally, a GLIMMIX [17,21,22] was t for each transcript, separately, to test for an effect of parent, lineage, and their interaction. Test results were FDR corrected, and only transcripts with a signi cant effect of parent or lineage, but not their interaction, were considered to exhibit bias.…”

“…Previous studies in honey bees have found evidence for parent-of-origin related variation in reproductive morphology, physiology, transcription [8,[16][17][18][19][20][21][22], and aggressive behavior [14,23], all of which are consistent with the kinship theory of intragenomic con ict [6,24]. These studies evaluated workers from reciprocal crosses of "Africanized" honey bees (AHBs, which are derived from the subspecies A. m. scutellata) and European honey bees (EHBs, which are derived from subspecies from Europe, such as A. m. ligustica) -two strains of honey bee that vary in their genotype, physiology, and behavior [25,26].…”

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].…”

Caste- and sex-specific DNA methylation in a bumblebee is associated with codon degeneracy

“…The function of DNA methylation in insects is largely unknown and thought to be variable based on the range of overall levels between taxonomic orders (Provataris et al ., 2018). However, multiple insect species have now been show to display parent-of-origin gene expression, including the mealybug Planococcus citri (de la Filia et al ., 2021) and two Hymenopteran species, the bumblebee, Bombus terrestris (Marshall et al ., 2020b) and the honeybee Apis mellifera (Kocher et al ., 2015; Galbraith et al ., 2016; Smith et al ., 2020; Galbraith et al ., 2021). In Hymenoptera, DNA methylation has been associated with caste differences in various species (Lyko et al ., 2010; Bonasio et al ., 2012; Amarasinghe et al ., 2014; Glastad et al ., 2016).…”