BackgroundThe shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.ResultsWe report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.ConclusionsThese two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0623-3) contains supplementary material, which is available to authorized users.

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.

BackgroundUnderstanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution.ResultsWe sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways.ConclusionsThese genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.

Division of labor is fundamental to the success of all societies. The most striking examples are the physically polymorphic worker castes in social insects with clear morphological adaptations to different roles. These polymorphic worker castes have previously been thought to be a classic example of nongentically controlled polymorphism, being mediated entirely by environmental cues. Here we show that worker caste development in the leaf-cutting ant Acromyrmex echinatior has a significant genetic component. Individuals of different patrilines within the same colony differ in their propensities to develop into minor or major workers. The mechanism appears to be plastic, with caste destiny resulting from interplay between nurture and nature. Unlike the few other recently discovered examples of a genetic influence on caste determination, the present result does not relate to any rare or exceptional circumstances, such as interspecific hybridization. The results suggest that a significant role of genetics may have been overlooked in our understanding of other complex polymorphisms of social insects.

S.. 2017. Bumblebee family lineage survival is enhanced in high-quality landscapes. Nature, 543 (7646). 547-549. 10.1038/nature21709Contact CEH NORA team at noraceh@ceh.ac.ukThe NERC and CEH trademarks and logos ('the Trademarks') are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. 1Bumblebee family lineage survival is enhanced in high quality landscapes Main textThe loss of semi-natural habitats and floral resources within intensively managed agricultural landscapes has been identified as a major driver of declines in insect pollinators 3,9,10 , with negative consequences for crop pollination 11 . Habitat restoration (e.g. the planting of flowering hedgerows, meadows or flower strips along field margins under agri-environment schemes 12 )can mitigate these effects, increasing local pollinator abundance and species richness 13-15 and enhancing rates of persistence and colonization at the community level 16 . However, we lack understanding of the effects of restoration on key aspects of pollinator biology that may explain the mechanisms behind these responses. In particular, improving habitat quality might be expected to enhance the prospects of successful reproduction and between-year survival in targeted areas, but whether this occurs is unknown.3 Bumblebees (Bombus spp.) are key pollinators of wild flowers and commercial crops 17,18 .Following a eusocial, annual colony cycle, new queens enter hibernation in the autumn and emerge in spring to search for a nest site and found a colony. Each colony may produce up to several hundred 'daughter' workers, which forage from spring to summer at flowers for nectar and pollen to rear new daughter queens and males 19 . The survival and dispersal patterns of bumblebee queens during hibernation and nest-searching periods are critical to overall population persistence, but remain undescribed in wild populations 8,20,21 . In addition, although the availability of floral resources within foraging distance of the nest has been shown to increase numbers of workers and males produced per colony, effects on queen production have been less clear 22 and there is no evidence regarding how queen production, survival and dispersal may be linked with underlying habitat quality and land-use 23 .Here, we investigated the effects of habitat quality and land-use on bumblebee survival and dispersal between colony cycle stages across two years. We first tested whether colonies located within or near high-value foraging habitats had a greater probability of producing daughter queens that survive the winter hibernation and spring emergence stages, henceforth termed 'family lineage survival'. Second, we tested whether the distances travelled by queens between hibernation and nest-searching periods (as a measure of minimum relative queen dispersal distances within our study landscape) were affected by the proportion of high quality habitat surrounding their natal colony. We sampled DNA non-lethally from...

Kin-selection theory underlies our basic understanding of social evolution [1, 2]. Nest drifting in eusocial insects (where workers move between nests) presents a challenge to this paradigm, since a worker should remain as a helper on her natal colony, rather than visit other colonies to which she is less closely related. Here we reveal nest drifting as a strategy by which workers may maximize their indirect fitness by helping on several related nests, preferring those where the marginal return from their help is greatest. By using a novel monitoring technique, radio frequency identification (RFID) tagging, we provide the first accurate estimate of drifting in a eusocial insect: 56% of females drifted in a natural population of the eusocial paper wasp Polistes canadensis, exceeding previous records of drifting in natural populations by more than 30-fold. We demonstrate that drifting cannot be explained through social parasitism, queen succession, mistakes in nest identity, or methodological bias. Instead, workers appear to gain indirect fitness benefits by helping on several related colonies in a viscous population structure. The potential importance of this strategy as a component of the kin-selected benefits for a social insect worker has previously been overlooked because of methodological difficulties in quantifying and studying drifting.

The origin and maintenance of eusociality is a central problem in evolutionary biology. Eusocial groups contain individuals that forfeit their own reproduction in order to help others reproduce. In facultatively eusocial taxa, offspring can choose whether to found new nests or become helpers in their natal groups. In many facultatively eusocial insects, offspring need continuous care during development, but adult carers have life expectancies shorter than the developmental period. When a lone foundress dies, her partly reared brood are usually doomed. Here, we show that helpers in a tropical hover wasp (Liostenogaster flavolineata) have an insurance-based advantage over lone foundresses because after a helper dies, most of the brood that she has partly reared will be brought to maturity by surviving nest-mates. After some of the helpers are experimentally removed from a multi-female nest, the reduced group is left with more brood than it would normally rear. We found that larger, more valuable extra brood were reared through to maturity, but not smaller, less valuable brood. Smaller brood may be sacrificed to feed larger brood, and reduced groups probably benefited from increased short-term helper recruitment. Rearing extra brood did not increase adult mortality or brood development time.

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.