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Social insects, particularly honey bees, have exceptionally high genomic frequencies of genetic recombination. This phenomenon and underlying mechanisms are poorly understood. To characterise the patterns of crossovers and gene conversion in the honey bee genome, a recombination map of 187 honey bee brothers was generated by whole-genome resequencing. Recombination events were heterogeneously distributed without many true hotspots. The tract lengths between phase shifts were bimodally distributed, indicating distinct crossover and gene conversion events. While crossovers predominantly occurred in G/C-rich regions and seemed to cause G/C enrichment, the gene conversions were found predominantly in A/T-rich regions. The nucleotide composition of sequences involved in gene conversions that were associated with or distant from crossovers corresponded to the differences between crossovers and gene conversions. These combined results suggest two types of DNA double-strand break repair during honey bee meiosis: non-canonical homologous recombination, leading to gene conversion and A/T enrichment of the genome, and the canonical homologous recombination based on completed double Holliday Junctions, which can result in gene conversion or crossover and is associated with G/C bias. This G/C bias may be selected for to balance the A/T-rich base composition of eusocial hymenopteran genomes. The lack of evidence for a preference of the canonical homologous recombination for double-strand break repair suggests that the high genomic recombination rate of honey bees is mainly the consequence of a high rate of double-strand breaks, which could in turn result from the life history of honey bees and their A/T-rich genome., (© 2024 The Author(s). Insect Molecular Biology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.)

De novo genes emerge from noncoding regions of genomes via succession of mutations. Among others, such mutations activate transcription and create a new open reading frame (ORF). Although the mechanisms underlying ORF emergence are well documented, relatively little is known about the mechanisms enabling new transcription events. Yet, in many species a continuum between absent and very prominent transcription has been reported for essentially all regions of the genome. In this study, we searched for de novo transcripts by using newly assembled genomes and transcriptomes of seven inbred lines of Drosophila melanogaster, originating from six European and one African population. This setup allowed us to detect sample specific de novo transcripts, and compare them to their homologous nontranscribed regions in other samples, as well as genic and intergenic control sequences. We studied the association with transposable elements (TEs) and the enrichment of transcription factor motifs upstream of de novo emerged transcripts and compared them with regulatory elements. We found that de novo transcripts overlap with TEs more often than expected by chance. The emergence of new transcripts correlates with regions of high guanine-cytosine content and TE expression. Moreover, upstream regions of de novo transcripts are highly enriched with regulatory motifs. Such motifs are more enriched in new transcripts overlapping with TEs, particularly DNA TEs, and are more conserved upstream de novo transcripts than upstream their 'nontranscribed homologs'. Overall, our study demonstrates that TE insertion is important for transcript emergence, partly by introducing new regulatory motifs from DNA TE families., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

Genome sequencing quality, in terms of both read length and accuracy, is constantly improving. By combining long-read sequencing technologies with various scaffolding techniques, chromosome-level genome assemblies are now achievable at an affordable price for non-model organisms. Insects represent an exciting taxon for studying the genomic underpinnings of evolutionary innovations, due to ancient origins, immense species-richness, and broad phenotypic diversity. Here we summarize some of the most important methods for carrying out a comparative genomics study on insects. We describe available tools and offer concrete tips on all stages of such an endeavor from DNA extraction through genome sequencing, annotation, and several evolutionary analyses. Along the way we describe important insect-specific aspects, such as DNA extraction difficulties or gene families that are particularly difficult to annotate, and offer solutions. We describe results from several examples of comparative genomics analyses on insects to illustrate the fascinating questions that can now be addressed in this new age of genomics research., (© 2024. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.)

Live birth (viviparity) has arisen repeatedly and independently among animals. We sequenced the genome and transcriptome of the viviparous Pacific beetle-mimic cockroach and performed comparative analyses with two other viviparous insect lineages, tsetse flies and aphids, to unravel the basis underlying the transition to viviparity in insects. We identified pathways undergoing adaptive evolution for insects, involved in urogenital remodeling, tracheal system, heart development, and nutrient metabolism. Transcriptomic analysis of cockroach and tsetse flies revealed that uterine remodeling and nutrient production are increased and the immune response is altered during pregnancy, facilitating structural and physiological changes to accommodate and nourish the progeny. These patterns of convergent evolution of viviparity among insects, together with similar adaptive mechanisms identified among vertebrates, highlight that the transition to viviparity requires changes in urogenital remodeling, enhanced tracheal and heart development (corresponding to angiogenesis in vertebrates), altered nutrient metabolism, and shifted immunity in animal systems., Competing Interests: The authors declare no competing interest., (© 2023 The Author(s).)

(1) Unravelling the molecular basis underlying major evolutionary transitions can shed light on how complex phenotypes arise. The evolution of eusociality, a major evolutionary transition, has been demonstrated to be accompanied by enhanced gene regulation. Numerous pieces of evidence suggest the major impact of transposon insertion on gene regulation and its role in adaptive evolution. Transposons have been shown to be play a role in gene duplication involved in the eusocial transition in termites. However, evidence of the molecular basis underlying the eusocial transition in Blattodea remains scarce. Could transposons have facilitated the eusocial transition in termites through shifts of gene expression? (2) Using available cockroach and termite genomes and transcriptomes, we investigated if transposons insert more frequently in genes with differential expression in queens and workers and if those genes could be linked to specific functions essential for eusocial transition. (3) The insertion rate of transposons differs among differentially expressed genes and displays opposite trends between termites and cockroaches. The functions of termite transposon-rich queen- and worker-biased genes are related to reproduction and ageing and behaviour and gene expression, respectively. (4) Our study provides further evidence on the role of transposons in the evolution of eusociality, potentially through shifts in gene expression.

The technology of long reads substantially improved the contingency of the genome assembly, particularly resolving contiguity of the repetitive regions. By integrating the interactive fragment using Hi-C, and the HiFi technique, a solid genome of the honeybee Apis mellifera carnica was assembled at the chromosomal level. A distinctive pattern of genes involved in social evolution was found by comparing it with social and solitary bees. A positive selection was identified in genes involved with cold tolerance, which likely underlies the adaptation of this European honeybee subspecies in the north hemisphere. The availability of this new high-quality genome will foster further studies and advances on genome variation during subspeciation, honeybee breeding and comparative genomics.

In contrast to the western honey bee, Apis mellifera , other honey bee species have been largely neglected despite their importance and diversity. The genetic basis of the evolutionary diversification of honey bees remains largely unknown. Here, we provide a genome-wide comparison of three honey bee species, each representing one of the three subgenera of honey bees, namely the dwarf ( Apis florea ), giant ( A. dorsata ), and cavity-nesting ( A. mellifera ) honey bees with bumblebees as an outgroup. Our analyses resolve the phylogeny of honey bees with the dwarf honey bees diverging first. We find that evolution of increased eusocial complexity in Apis proceeds via increases in the complexity of gene regulation, which is in agreement with previous studies. However, this process seems to be related to pathways other than transcriptional control. Positive selection patterns across Apis reveal a trade-off between maintaining genome stability and generating genetic diversity, with a rapidly evolving piRNA pathway leading to genomes depleted of transposable elements, and a rapidly evolving DNA repair pathway associated with high recombination rates in all Apis species. Diversification within Apis is accompanied by positive selection in several genes whose putative functions present candidate mechanisms for lineage-specific adaptations, such as migration, immunity, and nesting behavior., (© 2021 Fouks et al.; Published by Cold Spring Harbor Laboratory Press.)

Pollinators use multiple cues whilst foraging including direct cues from flowers and indirect cues from other pollinators. The use of indirect social cues is common in social insects, such as honeybees and bumblebees, where a social environment facilitates the ability to use such cues. Bumblebees use cues to forage on flowers according to previous foraging experiences. Flowers are an essential food source for pollinators but also pose a high risk of parasite infection through the shared use of flowers leading to parasite spillover. Nevertheless, bumblebees have evolved behavioral defense mechanisms to limit parasite infection by avoiding contaminated flowers. Mechanisms underlying the avoidance of contaminated flowers by bumblebees are poorly understood. Bumblebees were recorded having the choice to forage on non-contaminated flowers and flowers contaminated by a trypan osome gut parasite, Crithidia bombi . The use of different treatments with presence or absence of conspecifics on both contaminated and non-contaminated flowers allowed to investigate the role of social visual cues on their pathogen avoidance behavior. Bumblebees are expected to use social visual cues to avoid contaminated flowers. Our study reveals that the presence of a conspecific on flowers either contaminated or not does not help bumblebee foragers avoiding contaminated flowers. Nevertheless, bumblebees whereas gaining experience tend to avoid their conspecific when placed on contaminated flower and copy it when on the non-contaminated flower. Our experiment suggests a detrimental impact of floral scent on disease avoidance behavior.

The main selective force driving floral evolution and diversity is plant-pollinator interactions. Pollinators use floral signals and indirect cues to assess flower reward, and the ensuing flower choice has major implications for plant fitness. While many pollinator behaviors have been described, the impact of parasites on pollinator foraging decisions and plant-pollinator interactions have been largely overlooked. Growing evidence of the transmission of parasites through the shared-use of flowers by pollinators demonstrate the importance of behavioral immunity (altered behaviors that enhance parasite resistance) to pollinator health. During foraging bouts, pollinators can protect themselves against parasites through self-medication, disease avoidance, and grooming. Recent studies have documented immune behaviors in foraging pollinators, as well as the impacts of such behaviors on flower visitation. Because pollinator parasites can affect flower choice and pollen dispersal, they may ultimately impact flower fitness. Here, we discuss how pollinator immune behaviors and floral traits may affect the presence and transmission of pollinator parasites, as well as how pollinator parasites, through these immune behaviors, can impact plant-pollinator interactions. We further discuss how pollinator immune behaviors can impact plant fitness, and how floral traits may adapt to optimize plant fitness in response to pollinator parasites. We propose future research directions to assess the role of pollinator parasites in plant-pollinator interactions and evolution, and we propose better integration of the role of pollinator parasites into research related to pollinator optimal foraging theory, floral diversity and agricultural practices., Competing Interests: None declared.

Western honey bees (Apis mellifera) far exceed the commonly observed 1–2 meiotic recombination events per chromosome and exhibit the highest Metazoan recombination rate (20 cM/Mb) described thus far. However, the reasons for this exceptional rate of recombination are not sufficiently understood. In a comparative study, we report on the newly constructed genomic linkage maps of Apis florea and Apis dorsata that represent the two honey bee lineages without recombination rate estimates so far. Each linkage map was generated de novo, based on SNP genotypes of haploid male offspring of a single female. The A. florea map spans 4,782 cM with 1,279 markers in 16 linkage groups. The A. dorsata map is 5,762 cM long and contains 1,189 markers in 16 linkage groups. Respectively, these map sizes result in average recombination rate estimates of 20.8 and 25.1 cM/Mb. Synteny analyses indicate that frequent intra-chromosomal rearrangements but no translocations among chromosomes accompany the high rates of recombination during the independent evolution of the three major honey bee lineages. Our results imply a common cause for the evolution of very high recombination rates in Apis. Our findings also suggest that frequent homologous recombination during meiosis might increase ectopic recombination and rearrangements within but not between chromosomes. It remains to be investigated whether the resulting inversions may have been important in the evolutionary differentiation between honey bee species.

Background: The 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., Results: We 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., Conclusions: These 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.

A key feature for the success of social insects is division of labour, allowing colony members to specialize on different tasks. Nest defence is a defining task for social insects since it is crucial for colony integrity. A particularly impressive and well-known case of worker specialization in complex hymenopteran societies is found in leaf-cutting ants of the genera Atta and Acromyrmex. We hypothesized that three morphological worker castes of Acromyrmex echinatior differ in their likelihood to attack intruders, and show that major workers are more aggressive towards non-nestmate workers than medium and minor workers. Moreover, minors do not discriminate between nestmate and non-nestmate brood, while larger workers do. We further show that A. echinatior ants use cuticular chemical compounds for nestmate recognition. We took advantage of the natural variation in the cuticular compounds between colonies to investigate the proximate factors that may have led to the observed caste differences in aggression. We infer that major workers differ from medium workers in their general propensity to attack intruders (the "action component" of the nestmate recognition system), while minors seem to be less sensitive to foreign odours ("perception component"). Our results highlight the importance of proximate mechanisms underlying social insect behaviour, and encourage an appreciation of intra-colony variation when analysing colony-level traits such as nest defence., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Foraging is a result of innate and acquired mechanisms, and is optimized in order to increase fitness. During foraging, an animal faces many threats, such as predation and infection. The uptake of parasites and diseases while foraging is common and an individual should be adapted to detect and avoid such threats, using cues from either the abiotic environment or the parasite. Social animals possess an additional cue to detect such contaminated food sources: information provided by conspecifics. Bumblebees avoid contaminated flowers, but the cues used by the bees to distinguish contamination remain unknown. Under controlled laboratory conditions, we tested the use of scent marks derived from other foragers in choosing between a contaminated (by Crithidia bombi) and an uncontaminated flower. As a positive control we tested the bee's choice between two flowers, one scented with geraniol and containing a highly rewarding sugar solution, and the other not scented and containing a poorer reward. The bees mainly chose the uncontaminated and the rewarding scented flowers. Scent marks did not increase the efficiency of the bumblebees in choosing the better flower. The bees from both experiments behaved similarly, showing that the main and most relevant cue used to choose the uncontaminated flower is the odour from the parasite itself. The adaptation of bumblebees to avoid flowers contaminated by C. bombi arose from the long-term host-parasite interaction between these species. This strong adaptation results in an innate behaviour of bees and a detection and aversion of the odour of contaminated flower nectar.

Bumblebee colonies are founded by a single-mated queen. Due to this life history trait, bumblebees are more susceptible to parasites and diseases than polyandrous and/or polygynous social insects. A greater resistance towards parasites is shown when the genetic variability within a colony is increased. The parasite resistance may be divided into different levels regarding the step of the parasite infection (e.g. parasite uptake, parasite intake, parasite's establishment in the nest, parasite transmission). We investigate the prophylactic behaviour of bumblebees. Bumblebees were observed during their foraging flights on two artificial flowers; one of these was contaminated by Crithidia bombi, a naturally occurring gut parasite of bumblebees (in a control experiment the non-specific pathogen Escherichia coli was used). For C. bombi, bumblebees were preferentially observed feeding on the non-contaminated flower. Whereas for E. coli, the number of visits between flowers was the same, bumblebees spent more time feeding on the non-contaminated flower. These results demonstrate the ability of bumblebees to recognise the contamination of food sources. In addition, bumblebees have a stronger preference for the non-contaminated flower when C. bombi is present in the other flower than with E. coli which might be explained as an adaptive behaviour of bumblebees towards this specific gut parasite. It seems that the more specific the parasite is, the more it reduces the reward of the flower.