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Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary life-cycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships, whereas incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. Our study reveals how bumblebee genes and genomes have evolved across the Bombus phylogeny and identifies variations potentially linked to key ecological and behavioral traits of these important pollinators.

The Hemiptera (aphids, cicadas, and true bugs) are a key insect order, with high diversity for feeding ecology and excellent experimental tractability for molecular genetics. Building upon recent sequencing of hemipteran pests such as phloem-feeding aphids and blood-feeding bed bugs, we present the genome sequence and comparative analyses centered on the milkweed bug Oncopeltus fasciatus, a seed feeder of the family Lygaeidae.

Small heat shock proteins (sHSPs) are an ubiquitous protein family found in archaea, bacteria and eukaryotes. In plants, as in other organisms, sHSPs are upregulated by stress and are proposed to act as molecular chaperones to protect other proteins from stress-induced damage. sHSPs share an ‘α-crystallin domain’ with a β-sandwich structure and a diverse N-terminal domain. Although sHSPs are 12–25 kDa polypeptides, most assemble into oligomers with ≥ 12 subunits. Plant sHSPs are particularly diverse and numerous; some species have as many as 40 sHSPs. In angiosperms this diversity comprises ≥ 11 sHSP classes encoding proteins targeted to the cytosol, nucleus, endoplasmic reticulum, chloroplasts, mitochondria and peroxisomes. The sHSPs underwent a lineage-specific gene expansion, diversifying early in land plant evolution, potentially in response to stress in the terrestrial environment, and expanded again in seed plants and again in angiosperms. Understanding the structure and evolution of plant sHSPs has progressed, and a model for their chaperone activity has been proposed. However, how the chaperone model applies to diverse sHSPs and what processes sHSPs protect are far from understood. As more plant genomes and transcriptomes become available, it will be possible to explore theories of the evolutionary pressures driving sHSP diversification.

Chemosensory-related gene (CRG) families have been studied extensively in insects, but their evolutionary history across the Arthropoda had remained relatively unexplored. Here, we address current hypotheses and prior conclusions on CRG family evolution using a more comprehensive data set. In particular, odorant receptors were hypothesized to have proliferated during terrestrial colonization by insects (hexapods), but their association with other pancrustacean clades and with independent terrestrial colonizations in other arthropod subphyla have been unclear. We also examine hypotheses on which arthropod CRG family is most ancient. Thus, we reconstructed phylogenies of CRGs, including those from new arthropod genomes and transcriptomes, and mapped CRG gains and losses across arthropod lineages. Our analysis was strengthened by including crustaceans, especially copepods, which reside outside the hexapod/branchiopod clade within the subphylum Pancrustacea. We generated the first high-resolution genome sequence of the copepod Eurytemora affinis and annotated its CRGs. We found odorant receptors and odorant binding proteins present only in hexapods (insects) and absent from all other arthropod lineages, indicating that they are not universal adaptations to land. Gustatory receptors likely represent the oldest chemosensory receptors among CRGs, dating back to the Placozoa. We also clarified and confirmed the evolutionary history of antennal ionotropic receptors across the Arthropoda. All antennal ionotropic receptors in E. affinis were expressed more highly in males than in females, suggestive of an association with male mate-recognition behavior. This study is the most comprehensive comparative analysis to date of CRG family evolution across the largest and most speciose metazoan phylum Arthropoda.

Eukaryotic protein kinases belong to a large superfamily with hundreds to thousands of copies and are components of essentially all cellular functions. The goals of this study are to classify protein kinases from 25 plant species and to assess their evolutionary history in conjunction with consideration of their molecular functions. The protein kinase superfamily has expanded in the flowering plant lineage, in part through recent duplications. As a result, the flowering plant protein kinase repertoire, or kinome, is in general significantly larger than other eukaryotes, ranging in size from 600 to 2500 members. This large variation in kinome size is mainly due to the expansion and contraction of a few families, particularly the receptor-like kinase/Pelle family. A number of protein kinases reside in highly conserved, low copy number families and often play broadly conserved regulatory roles in metabolism and cell division, although functions of plant homologues have often diverged from their metazoan counterparts. Members of expanded plant kinase families often have roles in plant-specific processes and some may have contributed to adaptive evolution. Nonetheless, non-adaptive explanations, such as kinase duplicate subfunctionalization and insufficient time for pseudogenization, may also contribute to the large number of seemingly functional protein kinases in plants.

We present a fast and flexible software package—SimPhy—for the simulation of multiple gene families evolving under incomplete lineage sorting, gene duplication and loss, horizontal gene transfer—all three potentially leading to species tree/gene tree discordance—and gene conversion. SimPhy implements a hierarchical phylogenetic model in which the evolution of species, locus, and gene trees is governed by global and local parameters (e.g., genome-wide, species-specific, locus-specific), that can be fixed or be sampled from a priori statistical distributions. SimPhy also incorporates comprehensive models of substitution rate variation among lineages (uncorrelated relaxed clocks) and the capability of simulating partitioned nucleotide, codon, and protein multilocus sequence alignments under a plethora of substitution models using the program INDELible. We validate SimPhy's output using theoretical expectations and other programs, and show that it scales extremely well with complex models and/or large trees, being an order of magnitude faster than the most similar program (DLCoal-Sim). In addition, we demonstrate how SimPhy can be useful to understand interactions among different evolutionary processes, conducting a simulation study to characterize the systematic overestimation of the duplication time when using standard reconciliation methods. SimPhy is available at https://github.com/adamallo/SimPhy, where users can find the source code, precompiled executables, a detailed manual and example cases.

Background Lichens, encompassing 20,000 known species, are symbioses between specialized fungi (mycobionts), mostly ascomycetes, and unicellular green algae or cyanobacteria (photobionts). Here we describe the first parallel genomic analysis of the mycobiont Cladonia grayi and of its green algal photobiont Asterochloris glomerata . We focus on genes/predicted proteins of potential symbiotic significance, sought by surveying proteins differentially activated during early stages of mycobiont and photobiont interaction in coculture, expanded or contracted protein families, and proteins with differential rates of evolution. Results A) In coculture, the fungus upregulated small secreted proteins, membrane transport proteins, signal transduction components, extracellular hydrolases and, notably, a ribitol transporter and an ammonium transporter, and the alga activated DNA metabolism, signal transduction, and expression of flagellar components. B) Expanded fungal protein families include heterokaryon incompatibility proteins, polyketide synthases, and a unique set of G-protein α subunit paralogs. Expanded algal protein families include carbohydrate active enzymes and a specific subclass of cytoplasmic carbonic anhydrases. The alga also appears to have acquired by horizontal gene transfer from prokaryotes novel archaeal ATPases and Desiccation-Related Proteins. Expanded in both symbionts are signal transduction components, ankyrin domain proteins and transcription factors involved in chromatin remodeling and stress responses. The fungal transportome is contracted, as are algal nitrate assimilation genes. C) In the mycobiont, slow-evolving proteins were enriched for components involved in protein translation, translocation and sorting. Conclusions The surveyed genes affect stress resistance, signaling, genome reprogramming, nutritional and structural interactions. The alga carries many genes likely transferred horizontally through viruses, yet we found no evidence of inter-symbiont gene transfer. The presence in the photobiont of meiosis-specific genes supports the notion that sexual reproduction occurs in Asterochloris while they are free-living, a phenomenon with implications for the adaptability of lichens and the persistent autonomy of the symbionts. The diversity of the genes affecting the symbiosis suggests that lichens evolved by accretion of many scattered regulatory and structural changes rather than through introduction of a few key innovations. This predicts that paths to lichenization were variable in different phyla, which is consistent with the emerging consensus that ascolichens could have had a few independent origins.

Abstract The repeated evolution of the same trait in different lineages provides powerful natural experiments to study the phenotypic and genotypic predictability of trait gain and loss. A fascinating example is the repeated evolution of hummingbird pollination in plant lineages in the Americas, a widespread and often unidirectional phenomenon. The spiral gingers in the genus Costus are ancestrally bee pollinated, and hummingbird pollination has evolved multiple times independently in the tropical Americas. These pollinator transitions are accompanied by predictable morphological and color changes, but the changes in floral scent have not been described. In this study, we describe the floral scent composition of 30 species of Costus sampled across the phylogeny to understand how floral scent has evolved across the genus with respect to pollinator transitions. We then combine transcriptomics and genomics to identify gene expression differences and gene family evolution associated with pollinator transitions. We show that hummingbird-pollinated species have mostly lost their floral scent, whereas bee-pollinated species exhibit either floral scent maintenance or, in some cases, gains of more diverse scent profiles. We find the floral scent loss appears to be due to gene downregulation rather than pseudogenization. The remarkable consistency of scent loss in hummingbird-pollinated species highlights the shared strong selection pressures experienced by these lineages. Even species with more recent transitions from bee to hummingbird pollination exhibit scent loss, highlighting the rapid breakdown of scent emission following pollinator transitions. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of floral scent genes.

Anthocyanin regulation can be fruitfully explored from a diverse perspective by studying distantly related model organisms. Land plants pioneers faced a huge evolutionary leap, involving substantial physiological and genetic changes. Anthocyanins have evolved alongside these changes, becoming versatile compounds capable of mitigating terrestrial challenges such as drought, salinity, extreme temperatures and high radiation. With the accessibility of whole-genome sequences from ancient plant lineages, deeper insights into the evolution of key metabolic pathways like phenylpropanoids have emerged. Despite understanding the function of anthocyanins under stress, gaps remain in uncovering the precise metabolic and regulatory mechanisms driving their overproduction under stressful conditions. For example, the regulatory effect of reactive oxygen species (ROS) on well-known transcription factors like MYBs is not fully elucidated. This manuscript presents an evolutionary analysis of the anthocyanin biosynthetic pathway to elucidate key genes. CINNAMATE 4-HYDROXYLASE ( C4H ) and CHALCONE ISOMERASE ( CHI2 ) received particular attention. C4H exposes remarkable differences between aquatic and land plants, while CHI2 demonstrates substantial variation in gene copy number and sequence similarity across species. The role of transcription factors, such as MYB, and the involvement of ROS in the regulation of anthocyanin biosynthesis are discussed. Complementary gene expression analyses under abiotic stress in Arabidopsis thaliana , Selaginella moellendorffii , and Marchantia polymorpha reveal intriguing gene-stress relationships. This study highlights evolutionary trends and the regulatory complexity of anthocyanin production under abiotic stress, providing insights and opening avenues for future research. Key message We propose that CHI2 is a distinctive gene in the anthocyanin biosynthetic pathway, with an unusual evolutionary pattern and a significant role in abiotic stress adaptation via bioinformatics analysis and reviewing current literature.

Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineages (e.g., Tetrahymena , Paramecium , Oxytricha , and Stylonychia ). Here, we focus on the uncultivable Karyorelictea and its understudied sister class Heterotrichea, which represent two extremes in genome architecture. Ciliates, a eukaryotic clade that is over 1 billion years old, are defined by division of genome function between transcriptionally inactive germline micronuclei and functional somatic macronuclei. To date, most analyses of gene family evolution have been limited to cultivable model lineages (e.g., Tetrahymena , Paramecium , Oxytricha , and Stylonychia ). Here, we focus on the uncultivable Karyorelictea and its understudied sister class Heterotrichea, which represent two extremes in genome architecture. Somatic macronuclei within the Karyorelictea are described as nearly diploid, while the Heterotrichea have hyperpolyploid somatic genomes. Previous analyses indicate that genome architecture impacts ciliate gene family evolution as the most diverse and largest gene families are found in lineages with extensively processed somatic genomes (i.e., possessing thousands of gene-sized chromosomes). To further assess ciliate gene family evolution, we analyzed 43 single-cell transcriptomes from 33 ciliate species representing 10 classes. Focusing on conserved eukaryotic genes, we use estimates of transcript diversity as a proxy for the number of paralogs in gene families among four focal clades: Karyorelictea, Heterotrichea, extensive fragmenters (with gene-size somatic chromosomes), and non-extensive fragmenters (with more traditional somatic chromosomes), the latter two within the subphylum Intramacronucleata. Our results show that (i) the Karyorelictea have the lowest average transcript diversity, while Heterotrichea are highest among the four groups; (ii) proteins in Karyorelictea are under the highest functional constraints, and the patterns of selection in ciliates may reflect genome architecture; and (iii) stop codon reassignments vary among members of the Heterotrichea and Spirotrichea but are conserved in other classes. IMPORTANCE To further our understanding of genome evolution in eukaryotes, we assess the relationship between patterns of molecular evolution within gene families and variable genome structures found among ciliates. We combine single-cell transcriptomics with bioinformatic tools, focusing on understudied and uncultivable lineages selected from across the ciliate tree of life. Our analyses show that genome architecture correlates with patterns of protein evolution as lineages with more canonical somatic genomes, such as the class Karyorelictea, have more conserved patterns of molecular evolution compared to other classes. This study showcases the power of single-cell transcriptomics for investigating genome architecture and evolution in uncultivable microbial lineages and provides transcriptomic resources for further research on genome evolution.