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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’.

 

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.

 

Deciphering processes that contribute to genetic differentiation and divergent selection of natural populations is useful for evaluating the adaptive potential and resilience of organisms faced with various anthropogenic stressors. Insect pollinator species, including wild bees, provide critical ecosystem services but are highly susceptible to biodiversity declines. Here, we use population genomics to infer the genetic structure and test for evidence of local adaptation in an economically important native pollinator, the small carpenter bee (Ceratina calcarata).Using genome‐wide SNP data (n = 8302), collected from specimens across the species' entire distribution, we evaluated population differentiation and genetic diversity and identified putative signatures of selection in the context of geographic and environmental variation. Results of the analyses of principal component and Bayesian clustering were concordant with the presence of two to three genetic clusters, associated with landscape features and inferred phylogeography of the species. All populations examined in our study demonstrated a heterozygote deficit, along with significant levels of inbreeding. We identified 250 robust outlier SNPs, corresponding to 85 annotated genes with known functional relevance to thermoregulation, photoperiod, and responses to various abiotic and biotic stressors. Taken together, these data provide evidence for local adaptation in a wild bee and highlight genetic responses of native pollinators to landscape and climate features.

 

Many insects show plasticity in the area of the brain called the mushroom bodies (MB) with foraging and social experience. MBs are paired neuropils associated with learning and memory. MB volume is typically greater in mature foragers relative to young and/or inexperienced individuals. Long-term studies show that extended experience may further increase MB volume, but long-term studies have only been performed on non-reproductive social insect workers. Here we use the subsocial beeCeratina calcaratato test the effect of extended foraging experience on MB volume among reproductive females.Ceratina calcaratafemales forage to provision their immature offspring in the spring, and then again to provision their adult daughters in the late summer. We measured the volume of the MB calyces and peduncle, antennal lobes (AL), optic lobes (OL), central complex (CX), and whole brains of three groups of bees: newly emerged females, reproductive females in spring (foundresses), and post-reproductive mothers feeding their adult daughters in late summer. Post-reproductive late summer mothers had smaller MB calyces and ALs than foundresses. Moreover, among late mothers (but not other bees), wing wear, which is a measure of foraging experience, negatively correlated with both MB and OL volume. This is contrary to previously studied non-reproductive social insect workers in which foraging experience correlates postiviely with MB volume, and suggests that post-reproductive bees may reduce neural investment near the end of their lives.

 

As urbanization continues to increase, it is expected that two‐thirds of the human population will reside in cities by 2050. Urbanization fragments and degrades natural landscapes, threatening wildlife including economically important species such as bees. In this study, we employ whole genome sequencing to characterize the population genetics, metagenome and microbiome, and environmental stressors of a common wild bee,Ceratina calcarata. Population genomic analyses revealed the presence of low genetic diversity and elevated levels of inbreeding. Through analyses of isolation by distance, resistance, and environment across urban landscapes, we found that green spaces including shrubs and scrub were the most optimal pathways for bee dispersal, and conservation efforts should focus on preserving these land traits to maintain high connectivity across sites for wild bees. Metagenomic analyses revealed landscape sites exhibiting urban heat island effects, such as high temperatures and development but low precipitation and green space, had the highest taxa alpha diversity across all domains even when isolating for potential pathogens. Notably, the integration of population and metagenomic data showed that reduced connectivity in urban areas is not only correlated with lower relatedness among individuals but is also associated with increased pathogen diversity, exposing vulnerable urban bees to more pathogens. Overall, our combined population and metagenomic approach found significant environmental variation in bee microbiomes and nutritional resources even in the absence of genetic differentiation, as well as enabled the potential early detection of stressors to bee health.

 

Bees collect pollen from flowers for their offspring, and by doing so contribute critical pollination services for our crops and ecosystems. Unlike many managed bee species, wild bees are thought to obtain much of their microbiome from the environment. However, we know surprisingly little about what plant species bees visit and the microbes associated with the collected pollen. Here, we addressed the hypothesis that the pollen and microbial components of bee diets would change across the range of the bee, by amplicon sequencing pollen provisions of a widespread small carpenter bee, Ceratina calcarata, across three populations. Ceratina calcarata was found to use a diversity of floral resources across its range, but the bacterial genera associated with pollen provisions were very consistent. Acinetobacter, Erwinia, Lactobacillus, Sodalis, Sphingomonas and Wolbachia were among the top ten bacterial genera across all sites. Ceratina calcarata uses both raspberry (Rubus) and sumac (Rhus) stems as nesting substrates, however nests within these plants showed no preference for host plant pollen. Significant correlations in plant and bacterial co-occurrence differed between sites, indicating that many of the most common bacterial genera have either regional or transitory floral associations. This range-wide study suggests microbes present in brood provisions are conserved within a bee species, rather than mediated by climate or pollen composition. Moving forward, this has important implications for how these core bacteria affect larval health and whether these functions vary across space and diet. These data increase our understanding of how pollinators interact with and adjust to their changing environment. 

Conserving bees are critical both ecologically and economically. Genetic tools are valuable for monitoring these vital pollinators since tracking these small, fast‐flying insects by traditional means is difficult. By surveying the current state of the literature, this review discusses how recent advances in landscape genetic and genomic research are elucidating how wild bees respond to anthropogenic threats. Current literature suggests that there may be geographic differences in the vulnerability of bee species to landscape changes. Populations of temperate bee species are becoming more isolated and more genetically depauperate as their landscape becomes more fragmented, but tropical bee species appear unaffected. These differences may be an artifact of historical differences in land‐use, or it suggests that different management plans are needed for temperate and tropical bee species. Encouragingly, genetic studies on invasive bee species indicate that low levels of genetic diversity may not lead to rapid extinction in bees as once predicted. Additionally, next‐generation sequencing has given researchers the power to identify potential genes under selection, which are likely critical to species’ survival in their rapidly changing environment. While genetic studies provide insights into wild bee biology, more studies focusing on a greater phylogenetic and life‐history breadth of species are needed. Therefore, caution should be taken when making broad conservation decisions based on the currently few species examined.

 

Anthropogenic activities are rapidly changing the environment, and species that do not respond face a higher risk of extinction. Species may respond to environmental changes by modifying their behaviors, shifting their distributions, or changing their morphology. Recent morphological responses are often measured by changes in body size. Changes in body size are often attributed to climate change, but may instead be due to differences in available resources associated with changes in local land‐use. The effects of temperature and land‐use can be uncoupled in populations of the small carpenter beeCeratina calcarata, which have experienced changes in agricultural and urban cover independent of climate change. We studied how the morphology of this bee has changed over the past 118 years (1902–2019) in relation to climate change and the past 45 years (1974–2019) in relation to agricultural and urban cover. Over this time, summer temperatures increased. We found that male and female size decreased with increasing temperature. Male size also decreased with agricultural expansion. Female size, however, increased with agricultural expansion. These results suggest that rising temperatures correlate with a decrease in female body size, while, opposite to predicted, agricultural land‐use may select for increased female body size. These opposing pressures act concurrently and may result in bee extirpation from agricultural habitats if selection for large sizes is unsustainable as temperatures continue to increase. Furthermore, this study emphasizes the need to consider multiple environmental stressors when examining the effects of climate change due to their interactions.