Using citizen science data to assess the population genetic structure of the common yellowjacket wasp, Vespula vulgaris.

Monitoring insect genetic diversity and population structure has never been more important to manage the biodiversity crisis. Citizen science has become an increasingly popular tool to gather ecological data affordably across a wide range of spatial and temporal scales. To date, most insect-related citizen science initiatives have focused on occurrence and abundance data. Here, we show that poorly preserved insect samples collected by citizen scientists can yield population genetic information, providing new insights into population connectivity, genetic diversity and dispersal behaviour of little-studied insects. We analysed social wasps collected by participants of the Big Wasp Survey, a citizen science project that aims to map the diversity and distributions of vespine wasps in the UK. Although Vespula vulgaris is a notorious invasive species around the world, it remains poorly studied in its native range. We used these data to assess the population genetic structure of the common yellowjacket V. vulgaris at different spatial scales. We found a single, panmictic population across the UK with little evidence of population genetic structuring; the only possible limit to gene flow is the Irish sea, resulting in significant differentiation between the Northern Ireland and mainland UK populations. Our results suggest that queens disperse considerable distances from their natal nests to found new nests, resulting in high rates of gene flow and thus little differentiation across the landscape. Citizen science data has made it feasible to perform this study, and we hope that it will encourage future projects to adopt similar practices in insect population monitoring.

Putting hornets on the genomic map.

Hornets are the largest of the social wasps, and are important regulators of insect populations in their native ranges. Hornets are also very successful as invasive species, with often devastating economic, ecological and societal effects. Understanding why these wasps are such successful invaders is critical to managing future introductions and minimising impact on native biodiversity. Critical to the management toolkit is a comprehensive genomic resource for these insects. Here we provide the annotated genomes for two hornets, Vespa crabro and Vespa velutina. We compare their genomes with those of other social Hymenoptera, including the northern giant hornet Vespa mandarinia. The three hornet genomes show evidence of selection pressure on genes associated with reproduction, which might facilitate the transition into invasive ranges. Vespa crabro has experienced positive selection on the highest number of genes, including those putatively associated with molecular binding and olfactory systems. Caste-specific brain transcriptomic analysis also revealed 133 differentially expressed genes, some of which are associated with olfactory functions. This report provides a spring-board for advancing our understanding of the evolution and ecology of hornets, and opens up opportunities for using molecular methods in the future management of both native and invasive populations of these over-looked insects.

Social complexity, life-history and lineage influence the molecular basis of castes in vespid wasps.

A key mechanistic hypothesis for the evolution of division of labour in social insects is that a shared set of genes co-opted from a common solitary ancestral ground plan (a genetic toolkit for sociality) regulates caste differentiation across levels of social complexity. Using brain transcriptome data from nine species of vespid wasps, we test for overlap in differentially expressed caste genes and use machine learning models to predict castes using different gene sets. We find evidence of a shared genetic toolkit across species representing different levels of social complexity. We also find evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that are related to level of social complexity, lineage and of colony founding. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality.

Molecular patterns and processes in evolving sociality: lessons from insects.

Social insects have provided some of the clearest insights into the origins and evolution of collective behaviour. Over 20 years ago, Maynard Smith and Szathmáry defined the most complex form of insect social behaviour-superorganismality-among the eight major transitions in evolution that explain the emergence of biological complexity. However, the mechanistic processes underlying the transition from solitary life to superorganismal living in insects remain rather elusive. An overlooked question is whether this major transition arose via incremental or step-wise modes of evolution. We suggest that examination of the molecular processes underpinning different levels of social complexity represented across the major transition from solitary to complex sociality can help address this question. We present a framework for using molecular data to assess to what extent the mechanistic processes that take place in the major transition to complex sociality and superorganismality involve nonlinear (implying step-wise evolution) or linear (implying incremental evolution) changes in the underlying molecular mechanisms. We assess the evidence for these two modes using data from social insects and discuss how this framework can be used to test the generality of molecular patterns and processes across other major transitions. This article is part of a discussion meeting issue 'Collective behaviour through time'.

Co-expression Gene Networks and Machine-learning Algorithms Unveil a Core Genetic Toolkit for Reproductive Division of Labour in Rudimentary Insect Societies.

The evolution of eusociality requires that individuals forgo some or all their own reproduction to assist the reproduction of others in their group, such as a primary egg-laying queen. A major open question is how genes and genetic pathways sculpt the evolution of eusociality, especially in rudimentary forms of sociality-those with smaller cooperative nests when compared with species such as honeybees that possess large societies. We lack comprehensive comparative studies examining shared patterns and processes across multiple social lineages. Here we examine the mechanisms of molecular convergence across two lineages of bees and wasps exhibiting such rudimentary societies. These societies consist of few individuals and their life histories range from facultative to obligately social. Using six species across four independent origins of sociality, we conduct a comparative meta-analysis of publicly available transcriptomes. Standard methods detected little similarity in patterns of differential gene expression in brain transcriptomes among reproductive and non-reproductive individuals across species. By contrast, both supervised machine learning and consensus co-expression network approaches uncovered sets of genes with conserved expression patterns among reproductive and non-reproductive phenotypes across species. These sets overlap substantially, and may comprise a shared genetic "toolkit" for sociality across the distantly related taxa of bees and wasps and independently evolved lineages of sociality. We also found many lineage-specific genes and co-expression modules associated with social phenotypes and possible signatures of shared life-history traits. These results reveal how taxon-specific molecular mechanisms complement a core toolkit of molecular processes in sculpting traits related to the evolution of eusociality.

Sequenceserver: A Modern Graphical User Interface for Custom BLAST Databases.

Comparing newly obtained and previously known nucleotide and amino-acid sequences underpins modern biological research. BLAST is a well-established tool for such comparisons but is challenging to use on new data sets. We combined a user-centric design philosophy with sustainable software development approaches to create Sequenceserver, a tool for running BLAST and visually inspecting BLAST results for biological interpretation. Sequenceserver uses simple algorithms to prevent potential analysis errors and provides flexible text-based and visual outputs to support researcher productivity. Our software can be rapidly installed for use by individuals or on shared servers.

The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera.

A phylogenetic tree at the species level is still far off for highly diverse insect orders, including the Coleoptera, but the taxonomic breadth of public sequence databases is growing. In addition, new types of data may contribute to increasing taxon coverage, such as metagenomic shotgun sequencing for assembly of mitogenomes from bulk specimen samples. The current study explores the application of these techniques for large-scale efforts to build the tree of Coleoptera. We used shotgun data from 17 different ecological and taxonomic datasets (5 unpublished) to assemble a total of 1942 mitogenome contigs of >3000 bp. These sequences were combined into a single dataset together with all mitochondrial data available at GenBank, in addition to nuclear markers widely used in molecular phylogenetics. The resulting matrix of nearly 16,000 species with two or more loci produced trees (RAxML) showing overall congruence with the Linnaean taxonomy at hierarchical levels from suborders to genera. We tested the role of full-length mitogenomes in stabilizing the tree from GenBank data, as mitogenomes might link terminals with non-overlapping gene representation. However, the mitogenome data were only partly useful in this respect, presumably because of the purely automated approach to assembly and gene delimitation, but improvements in future may be possible by using multiple assemblers and manual curation. In conclusion, the combination of data mining and metagenomic sequencing of bulk samples provided the largest phylogenetic tree of Coleoptera to date, which represents a summary of existing phylogenetic knowledge and a defensible tree of great utility, in particular for studies at the intra-familial level, despite some shortcomings for resolving basal nodes.

Genes and genomic processes underpinning the social lives of ants.

The >15000 ant species are all highly social and show great variation in colony organization, complexity and behavior. The mechanisms by which such sociality evolved, as well as those underpinning the elaboration of ant societies since their ∼140 million year old common ancestor, have long been pondered. Here, we review recent insights generated using various genomic approaches. This includes understanding the molecular mechanisms underlying caste differentiation and the diversity of social structures, studying the impact of eusociality on genomic evolutionary rates, and investigating gene expression changes associated with differences in lifespan between castes. Furthermore, functional studies involving RNAi and CRISPR have recently been successfully applied to ants, opening the door to exciting research that promises to revolutionize the understanding of the evolution and diversification of social living.

The rectal valve in Curculionoidea (Insecta: Coleoptera).

A rectal valve is known from Bostrichiformia (e.g. Dermestidae, Bostrichidae, Ptinidae), Cucujiformia (e.g. Chrysmeloidea, Cleridae, Curculionoidea, Endomychidae, Tenebrionidae) and Buprestidae, associated with the cryptonephridial system for water recovery from fecal matter. The valve is probably homologous in at least the Bostrichiformia and Cucujiformia although the form it takes may not be. It comprises a sclerotized band lying in the wall of the rectum where this meets the perinephric membrane. The valve is plesiomorphically a narrow crimped ring, probably acting as a sphincter to retain fecal matter for water extraction. Apomorphically it extends longitudinally along the rectum and supports the perinephric chamber; this state has probably arisen independently several times. Larval and adult morphology may be similar or different. Within the Curculionoidea different apomorphic forms suggest monophyly of groups within the Anthribidae and Dryophthoridae, and within the curculionid subfamilies Entiminae, Mesoptiliinae, Molytinae and Cossoninae + Scolytinae, although limited weight should be placed on a single character. No support is provided for a relationship between the Platypodinae and Scolytinae. The genera Cylindrotypetes Zimmerman 1942 and Edaphotrypetes Morimoto 1995 are transferred from Molytinae: Phoenicobatini to Cossoninae: Pentrarthini.