Gene Duplication in the Honeybee: Patterns of DNA Methylation, Gene Expression, and Genomic Environment

Abstract

Gene duplication serves a critical role in evolutionary adaptation by providing genetic raw material to the genome. The evolution of duplicated genes may be influenced by epigenetic processes such as DNA methylation, which affects gene function in some taxa. However, the manner in which DNA methylation affects duplicated genes is not well understood. We studied duplicated genes in the honeybee Apis mellifera, an insect with a highly sophisticated social structure, to investigate whether DNA methylation was associated with gene duplication and genic evolution. We found that levels of gene body methylation were significantly lower in duplicate genes than in single-copy genes, implicating a possible role of DNA methylation in postduplication gene maintenance. Additionally, we discovered associations of gene body methylation with the location, length, and time since divergence of paralogous genes. We also found that divergence in DNA methylation was associated with divergence in gene expression in paralogs, although the relationship was not completely consistent with a direct link between DNA methylation and gene expression. Overall, our results provide further insight into genic methylation and how its association with duplicate genes might facilitate evolutionary processes and adaptation.

The impact of epigenetic information on genome evolution

“…Gene body methylation, which is the most common form of DNA methylation in invertebrates, is known to be positively associated with gene expression [4]. Interestingly, duplicated genes have lower levels of gene body methylation than singletons in honeybees [99], which is consistent with the idea that DNA methylation may affect duplicate gene function. Data from plants also support the idea that divergence of gene body methylation correlates with expression divergence [100].…”

“…Data from other species such as zebrafish [97] are consistent with this model. Data from invertebrates and plants also support the role of DNA methylation in regulating duplicate genes [98,99]. Gene body methylation, which is the most common form of DNA methylation in invertebrates, is known to be positively associated with gene expression [4].…”

Honeybee (Apis mellifera) Maternal Effect Causes Alternation of DNA Methylation Regulating Queen Development

“…Only 3 of 1456 DMGs were mapped to our previous DEGs data (Fig S2). Evidence showed that honeybee DNA methylation has an association with alternative splicing and gene duplication (Elango et al, 2009;Dyson & Goodisman, 2020), but there isn't a completely direct link between DNA methylation and gene expression. The present study and our previous study showed a same pattern that QE/2L comparison had more DMGs and DEGs than QE/ WE and WE/2L comparisons (see Fig 3 from this study and Fig 3 from Wei et al, 2019).…”

Expansion and accelerated evolution of 9-exon odorant receptors inPolistespaper wasps

“…Increased copy number of 9-exon ORs may not only expand the qualitative range of compounds perceived by paper wasps, but also the quantitative olfactory space, since wasps may be able to discern unique concentration differences between CHC blends as a result of the combined action of 9-exon ORs with various response thresholds. Gene duplication can also promote regulatory diversification (Kucharski et al 2016;Dyson & Goodisman 2020). Between castes and across stages of the colony cycle, CHCs vary in P. metricus (Toth et al 2014).…”