Eusociality has arisen independently at least 11 times in insects. Despite this convergence, there are striking differences among eusocial lifestyles, ranging from species living in small colonies with overt conflict over reproduction to species in which colonies contain hundreds of thousands of highly specialized sterile workers produced by one or a few queens. Although the evolution of eusociality has been intensively studied, the genetic changes involved in the evolution of eusociality are relatively unknown. We examined patterns of molecular evolution across three independent origins of eusociality by sequencing transcriptomes of nine socially diverse bee species and combining these data with genome sequence from the honey bee Apis mellifera to generate orthologous sequence alignments for 3,647 genes. We found a shared set of 212 genes with a molecular signature of accelerated evolution across all eusocial lineages studied, as well as unique sets of 173 and 218 genes with a signature of accelerated evolution specific to either highly or primitively eusocial lineages, respectively. These results demonstrate that convergent evolution can involve a mosaic pattern of molecular changes in both shared and lineage-specific sets of genes. Genes involved in signal transduction, gland development, and carbohydrate metabolism are among the most prominent rapidly evolving genes in eusocial lineages. These findings provide a starting point for linking specific genetic changes to the evolution of eusociality. social evolution | social insects | sociogenomics | molecular phylogenetics

Many insects sequester nutrients during developmentally programmed periods, which they metabolize during subsequent life history stages. During these periods, failure to store adequate nutrients can have persistent effects on fitness. Here, we examined a critical but under-studied nutrient storage period in queen bumble bees: the first days of adult life, which are followed by a diapause period typically coinciding with winter. We experimentally manipulated availability of pollen (the primary dietary source of lipids and protein) and the sugar concentration of artificial nectar (the primary source of carbohydrates) for laboratory-reared queens during this period and examined three nutritional phenomena: (i) diet impacts on nutritional status, (ii) the timescale upon which nutrient sequestration occurs and (iii) the fitness consequences of nutrient sequestration, specifically related to survival across the life cycle. We found evidence that pollen and nectar starvation negatively impact lipid storage, whereas nectar sugar concentration impacts stored carbohydrates. The majority of nutrients were stored during the first ~ 3 days of adult life. Nutrients derived from pollen during this period appear to be more critical for surviving earlier life stages, whereas nutrients sequestered from nectar become more important for surviving the diapause and post-diapause periods. Negative impacts of a poor diet during early life persisted in our experiment, even when pollen and a relatively high (50%) nectar sugar concentration were provided post-diapause. Based on these findings, we posit that the nutritional environment during the early adult life of queens has both immediate and persistent impacts on fitness. These findings underscore the importance of examining effects of stage-specific nutritional limitations on physiology and life history traits in this social insect group. Moreover, the findings may shed light on how declining food resources are contributing to the decline of wild bumble bee populations.

As increasingly large molecular data sets are collected for phylogenomics, the conflicting phylogenetic signal among gene trees poses challenges to resolve some difficult nodes of the Tree of Life. Among these nodes, the phylogenetic position of the honey bees (Apini) within the corbiculate bee group remains controversial, despite its considerable importance for understanding the emergence and maintenance of eusociality. Here, we show that this controversy stems in part from pervasive phylogenetic conflicts among GC-rich gene trees. GC-rich genes typically have a high nucleotidic heterogeneity among species, which can induce topological conflicts among gene trees. When retaining only the most GC-homogeneous genes or using a nonhomogeneous model of sequence evolution, our analyses reveal a monophyletic group of the three lineages with a eusocial lifestyle (honey bees, bumble bees, and stingless bees). These phylogenetic relationships strongly suggest a single origin of eusociality in the corbiculate bees, with no reversal to solitary living in this group. To accurately reconstruct other important evolutionary steps across the Tree of Life, we suggest removing GC-rich and GC-heterogeneous genes from large phylogenomic data sets. Interpreted as a consequence of genome-wide variations in recombination rates, this GC effect can affect all taxa featuring GC-biased gene conversion, which is common in eukaryotes.

The social insects live in extraordinarily complex and cohesive societies, where many individuals sacrifice their personal reproduction to become helpers in the colony. Identifying adaptive molecular changes involved in eusocial evolution in insects is important for understanding the mechanisms underlying transitions from solitary to social living, as well as the maintenance and elaboration of social life. Here, we review recent advances made in this area of research in several insect groups: the ants, bees, wasps, and termites. Drawing from whole-genome comparisons, candidate gene approaches, and a genome-scale comparative analysis of protein-coding sequence, we highlight novel insights gained for five major biological processes: chemical signaling, brain development and function, immunity, reproduction, and metabolism and nutrition. Lastly, we make comparisons across these diverse approaches and social insect lineages and discuss potential common themes of eusocial evolution, as well as challenges and prospects for future research in the field.comparative genomics | molecular evolution | social evolution | sociogenomics

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