Karl M. Glastad

Molecular traces of alternative social organization in a termite genome

Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.

DNA methylation in insects: on the brink of the epigenomic era.

DNA methylation plays an important role in gene regulation in animals. However, the evolution and function of DNA methylation has only recently emerged as the subject of widespread study in insects. In this review we profile the known distribution of DNA methylation systems across insect taxa and synthesize functional inferences from studies of DNA methylation in insects and vertebrates. Unlike vertebrate genomes, which tend to be globally methylated, DNA methylation is primarily targeted to genes in insects. Nevertheless, mounting evidence suggests that a specialized role exists for genic methylation in the regulation of transcription, and possibly mRNA splicing, in both insects and mammals. Investigations in several insect taxa further reveal that DNA methylation is preferentially targeted to ubiquitously expressed genes and may play a key role in the regulation of phenotypic plasticity. We suggest that insects are particularly amenable to advancing our understanding of the biological functions of DNA methylation, because insects are evolutionarily diverse, display several lineage‐specific losses of DNA methylation and possess tractable patterns of DNA methylation in moderately sized genomes.

Genomic signatures of evolutionary transitions from solitary to group living

For bees, many roads lead to social harmony Eusociality, where workers sacrifice their reproductive rights to support the colony, has evolved repeatedly and represents the most evolved form of social evolution in insects. Kapheim et al. looked across the genomes of 10 bee species with varying degrees of sociality to determine the underlying genomic contributions. No one genomic path led to eusociality, but similarities across genomes were seen in features such as increases in gene regulation and methylation. It also seems that selection pressures relaxed after the emergence of complex sociality. Science, this issue p. 1139 Social evolution in bees has followed diverse genomic paths but shares genomic patterns. The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.

Patterning and Regulatory Associations of DNA Methylation Are Mirrored by Histone Modifications in Insects

Epigenetic information is an important mediator of the relationship between genotype and phenotype in eukaryotic organisms. One of the most important and widely conserved forms of epigenetic information is the methylation of genes. However, the function of intragenic DNA methylation remains poorly understood. The goal of this study was to gain greater understanding of the nature of intragenic methylation by determining its role in the multilayered epigenetic landscape of insects. We first investigated the evolutionary lability of DNA methylation by examining whether methylation patterns were conserved in the fire ant and honey bee. We found that DNA methylation was targeted to largely overlapping sets of orthologs in both species. Next, we compared intragenic DNA methylation levels in the fire ant and honey bee to comprehensive epigenetic and gene-regulatory data from Drosophila melanogaster orthologs. We observed striking evidence of a conserved association between DNA methylation in fire ants and honey bees, and several active histone modifications, constitutive gene expression, and “broad” promoter architecture in D. melanogaster. Overall, our study illustrates that DNA methylation is a single component of a conserved, integrated, multilayered epigenetic and regulatory landscape in insect genomes.

Genome, transcriptome and methylome sequencing of a primitively eusocial wasp reveal a greatly reduced DNA methylation system in a social insect

Comparative genomics of social insects has been intensely pursued in recent years with the goal of providing insights into the evolution of social behaviour and its underlying genomic and epigenomic basis. However, the comparative approach has been hampered by a paucity of data on some of the most informative social forms (e.g. incipiently and primitively social) and taxa (especially members of the wasp family Vespidae) for studying social evolution. Here, we provide a draft genome of the primitively eusocial model insect Polistes dominula, accompanied by analysis of caste‐related transcriptome and methylome sequence data for adult queens and workers. Polistes dominula possesses a fairly typical hymenopteran genome, but shows very low genomewide GC content and some evidence of reduced genome size. We found numerous caste‐related differences in gene expression, with evidence that both conserved and novel genes are related to caste differences. Most strikingly, these –omics data reveal a major reduction in one of the major epigenetic mechanisms that has been previously suggested to be important for caste differences in social insects: DNA methylation. Along with a conspicuous loss of a key gene associated with environmentally responsive DNA methylation (the de novo DNA methyltransferase Dnmt3), these wasps have greatly reduced genomewide methylation to almost zero. In addition to providing a valuable resource for comparative analysis of social insect evolution, our integrative –omics data for this important behavioural and evolutionary model system call into question the general importance of DNA methylation in caste differences and evolution in social insects.

Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface

BackgroundRelatively little is known about the genomic basis and evolution of wood-feeding in beetles. We undertook genome sequencing and annotation, gene expression assays, studies of plant cell wall degrading enzymes, and other functional and comparative studies of the Asian longhorned beetle, Anoplophora glabripennis, a globally significant invasive species capable of inflicting severe feeding damage on many important tree species. Complementary studies of genes encoding enzymes involved in digestion of woody plant tissues or detoxification of plant allelochemicals were undertaken with the genomes of 14 additional insects, including the newly sequenced emerald ash borer and bull-headed dung beetle.ResultsThe Asian longhorned beetle genome encodes a uniquely diverse arsenal of enzymes that can degrade the main polysaccharide networks in plant cell walls, detoxify plant allelochemicals, and otherwise facilitate feeding on woody plants. It has the metabolic plasticity needed to feed on diverse plant species, contributing to its highly invasive nature. Large expansions of chemosensory genes involved in the reception of pheromones and plant kairomones are consistent with the complexity of chemical cues it uses to find host plants and mates.ConclusionsAmplification and functional divergence of genes associated with specialized feeding on plants, including genes originally obtained via horizontal gene transfer from fungi and bacteria, contributed to the addition, expansion, and enhancement of the metabolic repertoire of the Asian longhorned beetle, certain other phytophagous beetles, and to a lesser degree, other phytophagous insects. Our results thus begin to establish a genomic basis for the evolutionary success of beetles on plants.

The Function of Intragenic DNA Methylation: Insights from Insect Epigenomes

Epigenetic inheritance plays a fundamentally important role in mediating gene regulation and phenotypic plasticity. DNA methylation, in particular, has been the focus of many recent studies aimed at understanding the function of epigenetic information in insects. An understanding of DNA methylation, however, requires knowledge of its context in relation to other epigenetic modifications. Here, we review recent insights into the localization of DNA methylation in insect genomes and further discuss the functional significance of these insights in the context of the greater eukaryotic epigenome. In particular, we highlight the complementarity of the eukaryotic epigenetic landscape. We focus on the importance of DNA methylation to nucleosome stability, which may explain the context-dependent associations of DNA methylation with gene expression. Ultimately, we suggest that the integration of diverse epigenetic modifications in studies of insects will greatly advance our understanding of the evolution of epigenetic systems and epigenetic contributions to developmental regulation.

Evidence of a conserved functional role for DNA methylation in termites.

Many organisms are capable of developing distinct phenotypes from the same genotype. This developmental plasticity is particularly prevalent in insects, which can produce alternate adaptive forms in response to distinct environmental cues. The ability to develop divergent phenotypes from the same genotype often relies on epigenetic information, which affects gene function and is transmitted through cell divisions. One of the most important epigenetic marks, DNA methylation, has been lost in several insect lineages, yet its taxonomic distribution and functional conservation remain uninvestigated in many taxa. In the present study, we demonstrate that the signature of high levels of DNA methylation exists in the expressed genes of two termites, Reticulitermes flavipes and Coptotermes formosanus. Further, we show that DNA methylation is preferentially targeted to genes with ubiquitous expression among morphs. Functional associations of DNA methylation are also similar to those observed in other invertebrate taxa with functional DNA methylation systems. Finally, we demonstrate an association between DNA methylation and the long‐term evolutionary conservation of genes. Overall, our findings strongly suggest DNA methylation is present at particularly high levels in termites and may play similar roles to those found in other insects.

The Genome and Methylome of a Subsocial Small Carpenter Bee, Ceratina calcarata.

Understanding the evolution of animal societies, considered to be a major transition in evolution, is a key topic in evolutionary biology. Recently, new gateways for understanding social evolution have opened up due to advances in genomics, allowing for unprecedented opportunities in studying social behavior on a molecular level. In particular, highly eusocial insect species (caste-containing societies with nonreproductives that care for siblings) have taken center stage in studies of the molecular evolution of sociality. Despite advances in genomic studies of both solitary and eusocial insects, we still lack genomic resources for early insect societies. To study the genetic basis of social traits requires comparison of genomes from a diversity of organisms ranging from solitary to complex social forms. Here we present the genome of a subsocial bee, Ceratina calcarata. This study begins to address the types of genomic changes associated with the earliest origins of simple sociality using the small carpenter bee. Genes associated with lipid transport and DNA recombination have undergone positive selection in C. calcarata relative to other bee lineages. Furthermore, we provide the first methylome of a noneusocial bee. Ceratina calcarata contains the complete enzymatic toolkit for DNA methylation. As in the honey bee and many other holometabolous insects, DNA methylation is targeted to exons. The addition of this genome allows for new lines of research into the genetic and epigenetic precursors to complex social behaviors.

Epigenetic inheritance and genome regulation: is DNA methylation linked to ploidy in haplodiploid insects?

Organisms show great variation in ploidy level. For example, chromosome copy number varies among cells, individuals and species. One particularly widespread example of ploidy variation is found in haplodiploid taxa, wherein males are typically haploid and females are typically diploid. Despite the prevalence of haplodiploidy, the regulatory consequences of having separate haploid and diploid genomes are poorly understood. In particular, it remains unknown whether epigenetic mechanisms contribute to regulatory compensation for genome dosage. To gain greater insights into the importance of epigenetic information to ploidy compensation, we examined DNA methylation differences among diploid queen, diploid worker, haploid male and diploid male Solenopsis invicta fire ants. Surprisingly, we found that morphologically dissimilar diploid males, queens and workers were more similar to one another in terms of DNA methylation than were morphologically similar haploid and diploid males. Moreover, methylation level was positively associated with gene expression for genes that were differentially methylated in haploid and diploid castes. These data demonstrate that intragenic DNA methylation levels differ among individuals of distinct ploidy and are positively associated with levels of gene expression. Thus, these results suggest that epigenetic information may be linked to ploidy compensation in haplodiploid insects. Overall, this study suggests that epigenetic mechanisms may be important to maintaining appropriate patterns of gene regulation in biological systems that differ in genome copy number.