Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Abstract

Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…4b and Supplementary Table 16). These results show strong parallels to findings for eusocial Hymenoptera [40][41][42][43] . This is in stark contrast to the non-eusocial cockroach, B. germanica, where there was only a very weak relationship between CpG o/e and differential expression between nymphs and adult females (r = 0.14), nor were any large differences apparent in enriched GO terms between putatively methylated and non-methylated genes (Fig.…”

Queen pheromones modulate DNA methyltransferase activity in bee and ant workers

“…Caste fate is typically environmentally determined [5] and may be regulated epigenetically, for example by histone modification [6] and DNA methylation [7]. Unlike some insect taxa, many social Hymenoptera possess a full set of genes for DNA methylation and demethylation, including one or more orthologues of the 'maintenance' DNA methyltransferase dnmt1 and the 'de novo' DNA methyltransferase dnmt 3 [8]. Insect DNA methylation has been linked to alternative splicing [9] and is mostly found in the exons of highly expressed genes [8], implying that it affects both the type and amount of transcript produced.…”

“…Unlike some insect taxa, many social Hymenoptera possess a full set of genes for DNA methylation and demethylation, including one or more orthologues of the 'maintenance' DNA methyltransferase dnmt1 and the 'de novo' DNA methyltransferase dnmt 3 [8]. Insect DNA methylation has been linked to alternative splicing [9] and is mostly found in the exons of highly expressed genes [8], implying that it affects both the type and amount of transcript produced. In honeybees, DNA methylation was found to be caste-specific in initial studies [10,11], though not in a subsequent study [2].…”

Genetic architecture of key social trait differs significantly between primitive and advanced eusocial species

“…Patalano et al (7) show that the changes in the genetic architecture during the transition from solitary to eusocial lifestyle were mostly subtle and did not require the recruitment of massive genetic or epigenetic regulatory mechanisms that characterize advanced eusocial societies.…”

“…For example, in some highly derived ant species, workers emerge with no or nonfunctional ovaries and thus are true "somatic cells" of a superorganism (6). In PNAS, Patalano et al (7) sequenced the genomes, brain transcriptomes, and methylomes of two eusocial species in which caste determination is still highly plastic (Polistes) or has reversed from a caste determination with a dedicated reproductive caste (queens) to the ancestral state with omnipotent individuals competing for reproductive rights by evolutionarily "losing" the queen phenotype (Dinoponera). Hence, this study gives us a rare glimpse into the genome organization and molecular mechanisms that represent or resemble the earliest stages in social evolution where reproductive castes were not yet fixed or morphologically differentiated, like in most species of the highly advanced eusocial species of ants, social bees, and termites.…”