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Stolle, E.

Publications and source records attributed to Stolle, E..

11 recordsLinked to original sources

A chromosome-level genome assembly and resequencing data reveal low DNA methylation and reduced diversity in the solitary bee pollinator Osmia cornuta

Bees provide essential pollination services that contribute to ecosystem stability, as well as the sustainability of economic crop yields. Due to concerns over global and local declines, improving our understanding of these ecologically and commercially important species is crucial for determining their capacity to respond and adapt to environmental challenges. The European orchard bee (Osmia cornuta) is a solitary bee of increasing agricultural importance due to its role in the pollination of fruit crops, yet lacks genomic resources. Using cost-effective Nanopore-only long-read sequencing, we report the first genome assembly for O. cornuta, spanning 647.56Mb across 727 contigs (N50=3.94Mb) at a high level of completeness (99.88% BUSCO complete). In line with the expected number of chromosomes in this species, 16 major scaffolds were assembled to chromosome-level. Also, we provisionally investigated the epigenomic architecture of O. cornuta, finding low numbers of CG dinucleotides that were either 5-methylated or 5-hydroxymethylated, providing additional evidence for the limited role methylation plays in gene regulation in Hymenopterans. To generate improved gene annotations, we combined transcriptomic- and orthology-based approaches, leading to the prediction of 12,144 genes and 25,964 proteins, showing exceptionally high BUSCO completeness (99.64%). Lastly, through whole-genome resequencing of a representative dataset, we provisionally find patterns of reduced nucleotide diversity and lower recombination rates within O. cornuta compared to other bee species. Collectively, our study provides a novel insight into the genome architecture of a key pollinator, providing an important resource to facilitate further genomic studies. Significance statementSolitary bees are crucial pollinators for crops and wild plants, but scientists have lacked the genetic blueprints needed to understand how these species might adapt to environmental threats like climate change and habitat loss. Using modern and cost-effective technologies, we generated the complete genome of the European orchard bee, an economically important fruit pollinator. This comprehensive genetic resource provides the foundation for future research on solitary bee biology and conservation, necessary to understand their adaptive potential in the face of environmental challenges. In line with this, we analysed this species genetic variation across populations in Germany using a small, representative dataset and found surprisingly low genetic diversity and limited evidence of gene recombination during reproduction, which are factors that could restrict its capacity to evolve in response to environmental challenges.

genomics↗

Reference genome sequence of the solitary bee Camptopoeum friesei Mocsary, 1894 (Hymenoptera, Andrenidae)

Bees are major pollinators of flowering plants and thus are important ecosystem service providers for natural habitats and crops. Evolution led to a wide range of adaptations in behaviors, morphology and ecological traits. Many plants rely on specialized bee species for pollination events, and so this interdependence can make them increasingly vulnerable to ongoing threats of habitat loss and pesticide exposure. Studying the genomes of bee species across different life histories and ecological specializations can help understand the evolution of these traits more generally, but also inform conservation efforts for Camptopoeum friesei specifically. Here, we present the reference genome of the solitary bee Camptopoeum friesei (Arthropoda; Insecta; Hymenoptera; Andrenidae). C. friesei is highly dependent on steppe habitats where it nests in saline soils. Further, it is highly specialized (oligolectic) on a few Asteraceae: Centaurea and Cirsium, in particular on Centaurea stoebe. As a consequence of its high specialization level, it is of its ecological niche with an extremely scattered and rare habitat, C. friesei is highly threatened in central Europe, albeit local aggregations can be rich in individuals. The high-quality genome assembly for the colourful bee Camptopoeum friesei was generated using long-read PacBio HiFi in combination with chromatin conformation capture (Hi-C) sequencing. The genome spans 367.7 megabases (Mb), N50 of 25.2 Mb. The majority of the assembly is scaffolded into 10 chromosomes and harbours [~]40% repeats. Species taxonomyEukaryota; Opisthokonta; Metazoa; Eumetazoa; Bilateria; Protostomia; Ecdysozoa; Panarthropoda; Arthropoda; Mandibulata; Pancrustacea; Hexapoda; Insecta; Dicondylia; Pterygota; Neoptera; Endopterygota; Hymenoptera; Apocrita; Aculeata; Apoidea; Anthophila; Andrenidae; Panurginae; Panurgini; Camptopoeum friesei Mocsary, 1894 (NCBI:txid2918745)

zoology↗

No supergene despite social polymorphism in the big-headed ant Pheidole pallidula

Ant colonies ancestrally contained one queen and her non-reproductive workers. This is also the case for many but not all colonies of the Mediterranean big-headed ant Pheidole pallidula. Indeed, this species also has a derived form of social organization with multiple reproductive queens in the colony. The co-existence of two social forms also independently evolved in three other lineages of ants. In each of those lineages, variants of a supergene region of suppressed recombination determine social form. This is likely because supergene regions can link advantageous combinations of alleles from multiple loci. We thus hypothesized that a supergene region also determines colony queen number in the big-headed ant. To test this, we performed extensive population genetic analyses and genomic comparisons. We find no evidence of a supergene-like region with differentiation between single- and multiple-queen colonies. Our results show that a complex social polymorphism can evolve and be maintained without supergenes.

evolutionary biology↗

Bee core venom genes predominantly originated before aculeate stingers evolved

Venoms, which have evolved numerous times in animals, are ideal models of convergent trait evolution. However, detailed genomic studies of toxin-encoding genes exist for only a few animal groups. The hyper-diverse hymenopteran insects are the most speciose venomous clade, but investigation of the origin of their venom genes has been largely neglected. Utilising a combination of genomic and proteo-transcriptomic data, we investigated the origin of 11 toxin genes in 29 published and three new hymenopteran genomes and compiled an up-to-date list of prevalent bee venom proteins. Observed patterns indicate that bee venom genes predominantly originate through single gene co-option with gene duplication contributing to subsequent diversification. Most Hymenoptera venom genes are shared by all members of the clade and only melittin and the new venom protein family anthophilin1 appear unique to the bee lineage. Most venom proteins thus predate the mega-radiation of hymenopterans and the evolution of the aculeate stinger.

evolutionary biology↗

Parameter exploration improves the accuracy of long-read genome assembly

Long-molecule sequencing is now routinely applied to generate high-quality reference genome assemblies. However, datasets differ in repeat composition, heterozygosity, read lengths and error profiles. The assembly parameters that provide the best results could thus differ across datasets. By integrating four complementary and biologically meaningful metrics, we show that simple fine-tuning of assembly parameters can substantially improve the quality of long-read genome assemblies. In particular, modifying estimates of sequencing error rates improves some metrics more than two-fold. We provide a flexible software, CompareGenomeQualities, that automates comparisons of assembly qualities for researchers wanting a straightforward mechanism for choosing among multiple assemblies.

bioinformatics↗

Recurring adaptive introgression of a supergene that determines social organization

Introgression has been proposed as an essential source of adaptive genetic variation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. This barrier might be overcome in supergene regions, where suppressed recombination leads to joint inheritance across many loci. Here, we study the evolution of a large supergene region that determines a major social and ecological trait in Solenopsis fire ants: whether colonies have one queen or multiple queens. Using coalescent-based phylogenies built from the genomes of 365 haploid fire ant males, we show that the supergene variant responsible for multiple-queen colonies evolved in one species and repeatedly spread to other species through introgressive hybridization. This finding highlights how supergene architecture can enable a complex adaptive phenotype to recurrently permeate species boundaries.

evolutionary biology↗

Transcriptomic signatures of ageing vary in solitary and social forms of an orchid bee

Eusocial insect queens are remarkable in their ability to maximise both fecundity and longevity, thus escaping the typical trade-off between these two traits. In species exhibiting complex eusocial behaviour, several mechanisms have been proposed to underlie the remoulding of the trade-off, such as reshaping of the juvenile hormone pathway, or caste-specific susceptibility to oxidative stress. However, it remains a challenge to disentangle the molecular mechanisms underlying the remoulding of the trade-off in eusocial insects from caste-specific physiological attributes that have subsequently arisen due to their different life histories. Socially plastic species such as the orchid bee Euglossa viridissima represent excellent models to address the role of sociality per se in longevity as they allow direct comparisons of solitary and social individuals within a common genetic background. We present data on gene expression and juvenile hormone levels from young and old bees, from both solitary and social nests. We found 940 genes to be differentially expressed with age in solitary females, versus only 14 genes in social dominant females, and seven genes in subordinate females. We performed a weighted gene co-expression network analysis to further highlight candidate genes related to ageing in this species. Primary "ageing gene" candidates were related to protein synthesis, gene expression, immunity and venom production. Remarkably, juvenile hormone titres did not vary with age or social status. These results represent an important step in understanding the proximate mechanisms underlying the remodeling of the fecundity/longevity trade-off that accompanies the evolutionary transition from solitary life to eusociality. Significance statementThe remarkably long lifespan of the queens of eusocial insects despite their high reproductive output suggests that they are not subject to the widespread trade-off between fecundity and longevity that governs solitary animal life histories, yet surprisingly little is known of the molecular mechanisms underpinning their longevity. Using a socially plastic bee in which some individuals of a population are social whilst others are solitary, we identified hundreds of candidate genes and related gene networks that are involved in the remoulding of the fecundity/longevity tradeoff. As well as identifying candidate ageing genes, our data suggest that even in incipient stages of sociality there is a marked reprogramming of ageing; long live the queen.

evolutionary biology↗

Genomic architecture and evolutionary conflict drive allele-specific expression in the social supergene of the red fire ant

Supergenes are genomic regions of suppressed recombination that underlie complex polymorphisms. Despite the importance of such regions, our empirical understanding of their early evolution is limited. The young "social" supergene of the fire ant Solenopsis invicta provides a powerful system for disentangling the roles of evolutionary conflict and the implications of suppressed recombination. We used population genomics to identify genetic differences between supergene variants and gene expression analyses across different populations, castes and body parts to characterize allelic expression differences for the hundreds of genes in the supergene. We find that the expression of most genes is independent of social form or supergene variant, in line with the young age of this system. Many of the genes with allelic expression differences, however, show a pattern consistent with gene degeneration due to suppressed recombination. In contrast, a small portion of the genes has the signature of evolutionary conflict between social forms.

molecular biology↗

Brain microRNA expression associated with social evolution in bees

Evolutionary transitions to a social lifestyle in insects are associated with lineage-specific changes in gene expression, but the key nodes that drive these regulatory changes are unknown. We examined the relationship between social organization and lineage-specific microRNAs (miRNAs). Genome scans across 12 bee species showed that miRNA copy-number is mostly conserved and not associated with sociality. However, deep sequencing of small RNAs in six bee species revealed a substantial proportion (20-35%) of detected miRNAs had lineage-specific expression in the brain, 24-72% of which did not have homologs in other species. Lineage-specific miRNAs disproportionately target lineage-specific genes, and have lower expression levels than shared miRNAs. The predicted targets of lineage-specific miRNAs are not enriched for genes with caste-biased expression or genes under positive selection in social species. Together, these results suggest that novel miRNAs may coevolve with novel genes, and thus contribute to lineage-specific patterns of evolution in bees, but do not appear to have significant influence on social evolution. Our analyses also support the hypothesis that many new miRNAs are purged by selection due to deleterious effects on mRNA targets, and suggest genome structure is not as influential in regulating bee miRNA evolution as has been shown for mammalian miRNAs.

genomics↗

Draft genome assembly and population genetics of an agricultural pollinator, the solitary alkali bee (Halictidae: Nomia melanderi)

Alkali bees (Nomia melanderi) are solitary relatives of the halictine bees, which have become an important model for the evolution of social behavior, but for which few solitary comparisons exist. These ground-nesting bees defend their developing offspring against pathogens and predators, and thus exhibit some of the key traits that preceded insect sociality. Alkali bees are also efficient native pollinators of alfalfa seed, which is a crop of major economic value in the United States. We sequenced, assembled, and annotated a high-quality draft genome of 299.6 Mbp for this species. Repetitive content makes up more than one-third of this genome, and previously uncharacterized transposable elements are the most abundant type of repetitive DNA. We predicted 10,847 protein coding genes, and identify 479 of these undergoing positive directional selection with the use of population genetic analysis based on low-coverage whole genome sequencing of 19 individuals. We found evidence of recent population bottlenecks, but no significant evidence of population structure. We also identify 45 genes enriched for protein translation and folding, transcriptional regulation, and triglyceride metabolism evolving slower in alkali bees compared to other halictid bees. These resources will be useful for future studies of bee comparative genomics and pollinator health research.

genomics↗

Degenerative expansion of a young supergene

Suppressed recombination ultimately leads to gene loss, as demonstrated by the depauperate Y chromosomes of long-established XY pairs. To understand the shorter term effects, we used high-resolution optical mapping and k-mer distribution analysis on a young non-recombining region of fire ant social chromosomes. Instead of shrinking, the region has increased in length by more than 30%. This demonstrates that degenerative expansion can occur during the early evolution of non-recombining regions.

evolutionary biology↗