Biology subjects

Obbard, D. J.

Publications and source records attributed to Obbard, D. J..

18 recordsLinked to original sources

bioRxiv2025

Estimating the additive genetic variance for relative fitness from changes in allele frequency

The rate of adaptation is equal to the additive genetic variance for relative fitness (VA) in the population. Estimating VA typically involves obtaining suitable measures of fitness on a large number of individuals with known pairwise relatedness. Such data are hard to collect and the results are often sensitive to the definition of fitness used. Here, we present a new method for estimating VA that does not involve making measurements of fitness on individuals, but instead tracks changes in the genetic composition of the population. First, we show that VA can readily be expressed as a function of the genome-wide diversity/linkage disequilibrium matrix and genome-wide expected change in allele frequency due to selection. We then show how independent experimental replicates can be used to infer the expected change in allele frequency due to selection and then estimate VA via a linear mixed model. Finally, using individual-based simulations, we demonstrate that our approach yields precise and accurate estimates over a range of biologically plausible scenarios. Article summaryConventional approaches for estimating the heritable component of fitness variation (VA) have steep methodological, statistical, and even definitional challenges. Here, the authors present a new method that overcomes many of these issue by modelling VA using selection-induced changes to a populations genetic composition. The authors develop novel mathematical theory and an inference approach that uses independent experimental populations derived from the same ancestral population. Individual based simulations show that this method provides unbiased and precise estimates of VA. This opens the door for future studies investigating the genomic distribution of VA, a key factor driving Darwinian evolution.

evolutionary biology↗

bioRxiv2024

Footprints of worldwide adaptation in structured populations of D. melanogaster through the expanded DEST 2.0 genomic resource

Large scale genomic resources can place genetic variation into an ecologically informed context. To advance our understanding of the population genetics of the fruit fly Drosophila melanogaster, we present an expanded release of the community-generated population genomics resource Drosophila Evolution over Space and Time (DEST 2.0; https://dest.bio/). This release includes 530 high-quality pooled libraries from flies collected across six continents over more than a decade (2009-2021), most at multiple time points per year; 211 of these libraries are sequenced and shared here for the first time. We used this enhanced resource to elucidate several aspects of the species demographic history and identify novel signs of adaptation across spatial and temporal dimensions. We showed that patterns of secondary contact, originally characterized in North America, are replicated in South America and Australia. We also found that the spatial genetic structure of populations is stable over time, but that drift due to seasonal contractions of population size causes populations to diverge over time. We identified signals of adaptation that vary between continents in genomic regions associated with xenobiotic resistance, consistent with independent adaptation to common pesticides. Moreover, by analyzing samples collected during spring and fall across Europe, we provide new evidence for seasonal adaptation related to loci associated with pathogen response. Furthermore, we have also released an updated version of the DEST genome browser. This is a useful tool for studying spatio-temporal patterns of genetic variation in this classic model system.

evolutionary biology↗

bioRxiv2024

Variable prevalence of protective Spiroplasma infection over time in two natural populations of Drosophila hydei

The temporal dynamics of protective symbionts have rarely been characterized outside of aphid hosts. Here, we determine the prevalence of Spiroplasma in two populations of D. hydei where Spiroplasma infection had been previously recorded (UK and Japan). We observe that infection in both populations is variable over time and confirm the persistence of Spiroplasma in the UK population for 9 years. Thus, variable prevalence over time appears to be a common feature of these symbioses.

ecology↗

bioRxiv2024

A diverse gut virome from Drosophila melanogaster

Drosophila melanogaster is not only one of the most important models of antiviral immunity in invertebrates, but is also a powerful model for research of the gut microbiome. Although recent studies have continued to improve our knowledge of the fly gut microbiota, the viral component of the microbiome has remained unexplored. Here we explore the viral component of the Drosophila melanogaster gut microbiome using deep metagenomic DNA sequencing. We recovered 3035 phage sequences, resulting in 167 viral Metagenome-Assembled Genomes. The majority of these sequences are potentially novel bacteriophages from the order Caudovirales, which mainly target major gut bacteria of D. melanogaster, including Lactobacillus, Acetobacter, and Gluconobacter. Our functional annotation and discovery of auxiliary metabolic genes showed that these bacteriophages have the potential to influence microbial metabolism and genetic information processing. We also identified evidence of known fly pathogens Drosophila Kallithea nudivirus, Vesanto bidna-like virus, and Viltain densovirus, some of which were common in our studied populations. Our findings reveal a complex and diverse phage community in the D. melanogaster gut microbiome, paving the way to study host-phage related research in the natural microbial communities.

microbiology↗

bioRxiv2023

Single-fly assemblies fill major phylogenomic gaps across the Drosophilidae Tree of Life

Long-read sequencing is driving rapid progress in genome assembly across all major groups of life, including species of the family Drosophilidae, a longtime model system for genetics, genomics, and evolution. We previously developed a cost-effective hybrid Oxford Nanopore (ONT) long-read and Illumina short-read sequencing approach and used it to assemble 101 drosophilid genomes from laboratory cultures, greatly increasing the number of genome assemblies for this taxonomic group. The next major challenge is to address the laboratory culture bias in taxon sampling by sequencing genomes of species that cannot easily be reared in the lab. Here, we build upon our previous methods to perform amplification-free ONT sequencing of single wild flies obtained either directly from the field or from ethanol-preserved specimens in museum collections, greatly improving the representation of lesser studied drosophilid taxa in whole-genome data. Using Illumina Novaseq X Plus and ONT P2 sequencers with R10.4.1 chemistry, we set a new benchmark for inexpensive hybrid genome assembly at US $150 per genome while assembling genomes from as little as 35 ng of genomic DNA from a single fly. We present 183 new genome assemblies for 179 species as a resource for drosophilid systematics, phylogenetics, and comparative genomics. Of these genomes, 62 are from pooled lab strains and 121 from single adult flies. Despite the sample limitations of working with small insects, most single-fly diploid assemblies are comparable in contiguity (>1Mb contig N50), completeness (>98% complete dipteran BUSCOs), and accuracy (>QV40 genome-wide with ONT R10.4.1) to assemblies from inbred lines. We present a well-resolved multi-locus phylogeny for 360 drosophilid and 4 outgroup species encompassing all publicly available (as of August 2023) genomes for this group. Finally, we present a Progressive Cactus whole-genome, reference-free alignment built from a subset of 298 suitably high-quality drosophilid genomes. The new assemblies and alignment, along with updated laboratory protocols and computational pipelines, are released as an open resource and as a tool for studying evolution at the scale of an entire insect family.

evolutionary biology↗

bioRxiv2023

Naturally occurring viruses of Drosophila reduce offspring number and lifespan

Drosophila remains a pre-eminent insect model system for host-virus interaction, but the host range and fitness consequences of the drosophilid virome are poorly understood. Metagenomic studies have reported over 160 viruses associated with Drosophilidae, but few isolates are available to characterise the Drosophila immune response, and most characterisation has relied on injection and systemic infection. Here we use a more natural infection route to characterise the fitness effects of infection and to study a wider range of viruses. We exposed laboratory D. melanogaster to 23 naturally occurring viruses from wild-collected drosophilids. We recorded transmission rates along with two components of female fitness: survival and the lifetime number of adult offspring produced. Nine different viruses transmitted during contact with laboratory D. melanogaster, although for the majority, rates of transmission were less than 20%. Five virus infections led to a significant decrease in lifespan (D. melanogaster nora virus, D. immigrans nora virus, Muthill virus, galbut virus and Prestney Burn virus), and three led to a reduction in the total number of offspring. Our findings demonstrate the utility of the Drosophila model for community-level studies of host-virus interactions, and suggest that viral infection could be a substantial fitness burden on wild flies.

evolutionary biology↗

bioRxiv2023

Experimental estimates of germline mutation rate in eukaryotes: a phylogenetic meta-analysis

Mutation is the ultimate source of all genetic variation, and over the last ten years the ready availability of whole-genome sequencing has permitted direct estimation of mutation rate for many non-model species across the tree of life. In this meta-analysis we make a comprehensive search of the literature for mutation rate estimates in eukaryotes, identifying 140 mutation accumulation (MA) and parent-offspring (PO) sequencing studies covering 134 species. Based on these data, we revisit differences in single nucleotide mutation (SNM) rate between different phylogenetic lineages and update the known relationships between mutation rate and generation time, genome size, and nucleotide diversity--while accounting for phylogenetic non-independence. We do not find a significant difference between MA and PO in estimated mutation rates, but we confirm that mammal and plant lineages have higher mutation rates than arthropods, and that unicellular eukaryotes have the lowest mutation rates. We find that mutation rates are higher in species with longer generation times and larger genome sizes, even when accounting for phylogenetic relationships. Moreover, although nucleotide diversity is positively correlated with mutation rate, the gradient of the relationship is significantly less than one (on a logarithmic scale), consistent with higher mutation rates in populations with smaller effective size. For the 29 species for which data are available, we find that indel mutation rates are positively correlated with nucleotide mutation rates, and that short deletions are generally more common than short insertions. Nevertheless, despite recent progress, no estimates of either SNM or indel mutation rates are available for the majority of deeply-branching eukaryotic lineages--or even for most animal phyla. Even among charismatic megafauna, experimental mutation rate estimates remain unknown for amphibia and scarce for reptiles and fish. Lay SummaryOver the past decade, the sequencing revolution has led to an ever-increasing number of mutation-rate estimates from mutation accumulation or parent-offspring sequencing studies in eukaryotes. However, studies rarely quantify to what extent the mutation rate varies among these species. Also, despite strong predictions as to how mutation rate should vary with (e.g.) generation time, there have been few recent or wide-ranging analyses of such predictors while accounting for the inherent similarity between closely-related species. Of particular note, there has been surprisingly little effort to robustly test the drift barrier hypothesis that mutation rates should decrease with increasing effective population size. In this study, we used a comprehensive literature search to identify all the available experimental estimates of mutation rate in eukaryotes and subject them to phylogenetic mixed-model analyses. We find that per-nucleotide per-generation mutation rates differ by orders of magnitude among species: plants and mammals tend to have higher mutation rates than arthropods, and unicellular organisms have the lowest mutation rates. Our analysis also shows that mutation rates increase significantly with increasing generation time and genome size, and nucleotide diversity increases with mutation rate with a gradient less than one--as predicted by the drift-barrier hypothesis.

evolutionary biology↗

bioRxiv2022

Variation in mutation, recombination, and transposition rates in Drosophila melanogaster and Drosophila simulans

Mutation, recombination, and transposition occurring during meiosis provide the variation on which natural selection can act and the rates at which they occur are important parameters in models of evolution. The de novo mutation rate determines levels of genetic diversity, responses to ongoing selection, and levels of genetic load. Recombination breaks up haplotypes and reduces the effects of linkage, helping to spread beneficial alleles and purge deleterious ones. Transposable elements (TE) selfishly replicate themselves through the genome, imposing fitness costs on the host and introducing complex mutations that can affect gene expression and give rise to new genes. However, even for key evolutionary models such as Drosophila melanogaster and D. simulans few estimates of these parameters are available, and we have little idea of how rates vary between individuals, sexes, populations, or species. Here, we provide direct estimates of mutation, recombination, and transposition rates and their variation in a West African and a European population of D. melanogaster and a European population of D. simulans. Across 89 flies, we observe 58 single nucleotide mutations, 286 crossovers, and 89 TE insertions. Compared to the European D. melanogaster, we find the West African population has a lower mutation rate (1.67 vs. 4.86 x 10-9 site-1 gen-1) and transposition rate (8.99 vs. 23.36 x 10-5 copy-1 gen-1), but a higher recombination rate (3.44 vs. 2.06 cM/Mb). The European D. simulans population has a similar mutation rate to European D. melanogaster but a significantly higher recombination rate and a lower but not significantly different transposition rate. Overall, we find paternal-derived mutations are more frequent than maternal ones in both species. HighlightsO_LIDe novo mutation rates are 1.67 x 10-9 site-1 gen-1 (95% HPD CI: 0.54 - 3.14 x 10-9), 4.86 x 10-9 site-1 gen-1 (2.11 - 8.02 x 10-9), and 4.51 x 10-9 site-1 gen-1 (1.94 - 7.75 x 10-9) for the West African D. melanogaster, the European D. melanogaster and the European D. simulans population, respectively. C_LIO_LIIn females, recombination rates in the absence of large genomic inversions are 3.44 cM/Mb (2.72 - 4.18), 2.06 cM/Mb (1.57 - 2.57), and 3.04 cM/Mb (2.45 - 3.73) for the three populations, respectively. There was no strong evidence of recombination observed in males. C_LIO_LIMutations (SNMs and indels) are male-biased. C_LIO_LIThe West African D. melanogaster population has a lower TE activity than the other populations and CMC-Transib is the dominant active TE. The European D. melanogaster population has multiple active TEs: Gypsy, CMC-Transib, Pao, Jockey and hAT-hobo; while in European D. simulans, they are Gypsy, CMC-Transib, Pao, hAT-hobo, Copia and TcMar-Mariner. C_LI

evolutionary biology↗

bioRxiv2021

Predictors of virus prevalence and diversity across a wild bumblebee community

Viruses are key regulators of natural populations. Despite this, we have limited knowledge of the diversity and ecology of viruses that lack obvious fitness effects on their host. This is even the case in wild host populations that provide ecosystem services, where small fitness effects may have major ecological and financial impacts in aggregate. One such group of hosts are the bumblebees, which have a major role in the pollination of food crops and have suffered population declines and range contractions in recent decades. In this study, we used a multivariate generalised linear mixed model to investigate the ecological factors that determine the prevalence of four recently discovered bumblebee viruses (Mayfield virus 1, Mayfield virus 2, River Liunaeg virus and Loch Morlich virus), and two previously known viruses that infect both wild bumblebees and managed honeybees (Acute bee paralysis virus and Slow bee paralysis virus). We show that the recently discovered bumblebee viruses were more genetically diverse than the viruses shared with honeybees, potentially due to spillover dynamics of shared viruses. We found evidence for ecological drivers of prevalence in our samples, with relatively weak evidence for a positive effect of precipitation on the prevalence of River Luinaeg virus. Coinfection is potentially important in shaping prevalence: we found a strong positive association between River Liunaeg virus and Loch Morlich virus presence after controlling for host species, location and other relevant ecological variables. This study represents a first step in the description of predictors of bumblebee infection in the wild not driven by spillover from honeybees.

microbiology↗

bioRxiv2020

The discovery, distribution and diversity of DNA viruses associated with Drosophila melanogaster in Europe

Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the Drosophila virome. Here we report fourteen DNA viruses detected in a metagenomic analysis of approximately 6500 pool-sequenced Drosophila, sampled from 47 European locations between 2014 and 2016. These include three new Nudiviruses, a new and divergent Entomopox virus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy virus. We also find an endogenous genomic copy of Galbut virus, a dsRNA Partitivirus, segregating at very low frequency. Remarkably, we find that Drosophila Vesanto virus, a small DNA virus previously described as a Bidnavirus, may be composed of up to 12 segments and represent a new lineage of segmented DNA viruses. Two of the DNA viruses, Drosophila Kallithea nudivirus and Drosophila Vesanto virus are relatively common, found in 2% or more of wild flies. The others are rare, with many likely to be represented by a single infected fly. We find that virus prevalence in Europe reflects the prevalence seen in publicly-available datasets, with Drosophila Kallithea nudivirus and Drosophila Vesanto virus the only ones commonly detectable in public data from wild-caught flies and large population cages, and the other viruses being rare or absent. These analyses suggest that DNA viruses are at lower prevalence than RNA viruses in D. melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redressing an earlier bias toward RNA virus studies in Drosophila, and lay the foundation needed to harness the power of Drosophila as a model system for the study of DNA viruses.

microbiology↗

bioRxiv2019

A new lineage of segmented RNA viruses infecting animals

Metagenomic sequencing has revolutionised our knowledge of virus diversity, with new virus sequences being reported faster than ever before. However, virus discovery from metagenomic sequencing usually depends on detectable homology: without a sufficiently close relative, so-called dark virus sequences remain unrecognisable. An alternative approach is to use virus-identification methods that do not depend on detecting homology, such as virus recognition by host antiviral immunity. For example, virus-derived small RNAs have previously been used to propose dark virus sequences associated with the Drosophilidae (Diptera). Here we combine published Drosophila data with a comprehensive search of transcriptomic sequences and selected meta-transcriptomic datasets to identify a completely new lineage of segmented positive-sense single-stranded RNA viruses that we provisionally refer to as the Quenyaviruses. Each of the five segments contains a single open reading frame, with most encoding proteins showing no detectable similarity to characterised viruses, and one sharing a small number of residues with the RNA-dependent RNA polymerases of single- and double-stranded RNA viruses. Using these sequences, we identify close relatives in approximately 20 arthropods, including insects, crustaceans, spiders and a myriapod. Using a more conserved sequence from the putative polymerase, we further identify relatives in meta-transcriptomic datasets from gut, gill, and lung tissues of vertebrates, reflecting infections of vertebrates or of their associated parasites. Our data illustrate the utility of small RNAs to detect viruses with limited sequence conservation, and provide robust evidence for a new deeply divergent and phylogenetically distinct RNA virus lineage.

evolutionary biology↗

bioRxiv2018

Host evolutionary history predicts virus prevalence across bumblebee species

Why a pathogen associates with one host but not another is one of the most important questions in disease ecology. Here we use transcriptome sequencing of wild-caught bumblebees from 13 species to describe their natural viruses, and to quantify the impact of evolutionary history on the realised associations between viruses and their pollinator hosts. We present 37 novel virus sequences representing at least 30 different viruses associated with bumblebees. We verified 17 of them by PCR and estimate their prevalence across species in the wild. Through small RNA sequencing, we demonstrate that at least 10 of these viruses form active infections in wild individuals. Using a phylogenetic mixed model approach, we show that the evolutionary history of the host shapes the current distribution of virus/bumblebee associations. Specifically, we find that related hosts share viral assemblages, viruses differ in their prevalence averaged across hosts and the prevalence of infection in individual virus-host pairings depends on precise characteristics of that pairing. Authors SummaryDespite the importance of disease in the regulation of animal populations, our understanding of the distribution of pathogen burden across wild communities remains in its infancy. In this study, we investigated the distribution of viruses across natural populations of 13 different bumblebee species in Scotland. We first searched for viruses using a metatranscriptomic approach, finding at least 30 new viruses of bumblebees, and assayed a subset of them for their presence and absence in different host species. Then, in the first application of these methods to an animal-virus system, we used co-phylogenetic mixed models to investigate the factors that lead to species being having different prevalences for a subset of these viruses. While much of the variation in the prevalence of the viruses can be explained by the idiosyncrasies of individual bumblebee-virus pairings, there is a phylogenetic signal with related bumblebee species being infected at similar frequencies by the same sets of viruses. Consistent with previous work, our study indicates that, while in general the interaction between a host and a virus may be unpredictable, closely related species are more likely to exhibit similar patterns of infection.

evolutionary biology↗

bioRxiv2018

Induction and suppression of NF-κB signalling by a DNA virus of Drosophila

Interactions between the insect immune system and RNA viruses have been best studied in Drosophila, where RNA interference, NF-O_SCPLOWKC_SCPLOWB and JAK-STAT pathways underlie antiviral immunity. In response to these immune mechanisms, insect viruses have convergently evolved suppressors of RNA interference that act by diverse mechanisms to permit viral replication. However, interactions between the insect immune system and DNA viruses have received less attention, primarily because few Drosophila-infecting DNA virus isolates are available. Here, we use a recently-isolated DNA virus of Drosophila melanogaster, Kallithea virus, to probe known antiviral immune responses and virus evasion tactics in the context of DNA virus infection. We find that fly mutants for RNA interference and Immune deficiency (Imd), but not Toll, pathways are more susceptible to Kallithea virus infection. We identify the Kallithea virus-encoded protein gp83 as a potent inhibitor of Toll signalling, strongly suggesting that Toll mediates antiviral responses during Kallithea virus infection, but that it is suppressed by the virus. Further, we find that Kallithea gp83 inhibits Toll signalling either through NF-O_SCPLOWKC_SCPLOWB transcription factor regulation, or transcriptionally. Together, these results provide a broad description of known antiviral pathways in the context of DNA virus infection and identify the first Toll pathway inhibitor in a Drosophila virus, extending the known diversity of insect virus-encoded immune inhibitors.

microbiology↗

bioRxiv2017

Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses

Drosophila melanogaster has played a key role in our understanding of invertebrate immunity. However, both functional and evolutionary studies of host-virus interaction in Drosophila have been limited by a dearth of native virus isolates. In particular, despite a long history of virus research, DNA viruses of D. melanogaster have only recently been described, and none have been available for experimental study. Here we report the isolation and comprehensive characterisation of Kallithea virus, a large double-stranded DNA virus, and the first DNA virus to have been reported from wild populations of D. melanogaster. We find that Kallithea virus infection is costly for adult flies, reaching high titres in both sexes and disproportionately reducing survival in males and movement and late fecundity in females. Using the Drosophila Genetic Reference Panel, we quantify host genetic variance for virus-induced mortality and viral titre and identify candidate host genes that may underlie this variation, including Cdc42-interacting protein 4. Using full transcriptome sequencing of infected males and females, we examine the transcriptional response of flies to Kallithea virus infection, and describe differential regulation of virus-responsive genes. This work establishes Kallithea virus as a new tractable model to study the natural interaction between D. melanogaster and DNA viruses, and we hope it will serve as a basis for future studies of immune responses to DNA viruses in insects.\n\nAuthor SummaryThe fruit fly Drosophila melanogaster is a useful model species to study host-virus interaction and innate immunity. However, few natural viruses of Drosophila have been available for experiments, and no natural DNA viruses of Drosophila melanogaster have been available at all. Although infecting flies with viruses from other insects has been useful to uncover general immune mechanisms, viruses that naturally infect wild flies could help us to learn more about the coevolutionary process, and more about the genes that underlie the host-virus interaction. Here we present an isolate of a DNA virus (named Kallithea Virus) that naturally infects the model species Drosophila melanogaster in the wild. We describe the basic biology of infection by this virus, finding that both male and females flies die from infection, but females are more tolerant of infection than males, while laying lay fewer eggs than uninfected females. We quantify genetic variation for virus resistance in the flies, and we use RNA sequencing to see which genes are expressed in male and female flies in response to infection. These results will form the basis for further research to understand how insects defend themselves against infection by DNA viruses, and how DNA viruses can overcome antiviral defence.

microbiology↗

bioRxiv2017

The virome of Drosophila suzukii, an invasive pest of soft fruit

Drosophila suzukii (Matsumura) is one of the most damaging and costly pests to invade temperate horticultural regions in recent history. Conventional control of this pest is challenging, and an environmentally benign microbial biopesticide is highly desirable. A thorough exploration of the pathogens infecting this pest is not only the first step on the road to the development of an effective biopesticide, but also provides a valuable comparative dataset for the study of viruses in the model family Drosophilidae. Here we use a metatransciptomic approach to identify viruses infecting this fly in both its native (Japanese) and invasive (British and French) ranges. We describe 18 new RNA viruses, including members of the Picornavirales, Mononegavirales, Bunyavirales, Chuviruses, Nodaviridae, Tombusviridae, Reoviridae, and Nidovirales, and discuss their phylogenetic relationships with previously known viruses. We also detect 18 previously described viruses of other Drosophila species that appear to be associated with D. suzukii in the wild.

microbiology↗

bioRxiv2017

Metagenomic sequencing suggests arthropod antiviral RNA interference is highly derived, and identifies novel viral small RNAs in a mollusc and a brown alga

RNA interference (RNAi)-related pathways target viruses and transposable element (TE) transcripts in plants, fungi, and ecdysozoans (nematodes and arthropods), giving protection against infection and transmission. In each case, this produces abundant TE and virus-derived 20-30nt small RNAs, which provide a characteristic signature of RNAi-mediated defence. The broad phylogenetic distribution of the Argonaute and Dicer-family genes that mediate these pathways suggests that defensive RNAi is ancient and probably shared by most animal (metazoan) phyla. Indeed, while vertebrates had been thought an exception, it has recently been argued that mammals also possess an antiviral RNAi pathway, although its immunological relevance is currently uncertain and the viral small RNAs are not detectably under natural conditions. Here we use a metagenomic approach to test for the presence of virus-derived small RNAs in five divergent animal phyla (Porifera, Cnidaria, Echinodermata, Mollusca, and Annelida), and in a brown alga--which represents an independent origin of multicellularity from plants, fungi, and animals. We use metagenomic RNA sequencing to identify around 80 virus-like contigs in these lineages, and small RNA sequencing to identify small RNAs derived from those viruses. Contrary to our expectations, we were unable to identify canonical (i.e. Drosophila-, nematode- or plant-like) viral small RNAs in any of these organisms, despite the widespread presence of abundant micro-RNAs, and transposon-derived somatic Piwi-interacting piRNAs in the animals. Instead, we identified a distinctive group of virus-derived small RNAs in the mollusc, which have a piRNA-like length distribution but lack key signatures of piRNA biogenesis, and a group of 21U virus-derived small RNAs in the brown alga. We also identified primary piRNAs derived from putatively endogenous copies of DNA viruses in the cnidarian and the echinoderm, and an endogenous RNA virus in the mollusc. The absence of canonical virus-derived small RNAs from our samples may suggest that the majority of animal phyla lack an antiviral RNAi response. Alternatively, these phyla could possess an antiviral RNAi response resembling that reported for vertebrates, which is not detectable through simple metagenomic sequencing of wild-type individuals. In either case, our findings suggest that the current antiviral RNAi responses of arthropods and nematodes are highly diverged from the ancestral metazoan state, and that antiviral RNAi may even have evolved independently on multiple occasions.\n\nAuthor summaryThe presence of abundant virus-derived small RNAs in infected plants, fungi, nematodes, and arthropods suggests that Dicer-dependent antiviral RNAi is an ancient and conserved defence. Using metagenomic sequencing from wild-caught organisms we show that antiviral RNAi is highly variable across animals. We identify a distinctive group of virus-derived small RNAs in a mollusc, which have a piRNA-like length distribution but lack key signatures of piRNA biogenesis. We also report a group of 21U virus-derived small RNAs in a brown alga, which represents an origin of multicellularity separate from that of plants, fungi, and animals. The absence of virus-derived small RNAs from our samples may suggest that the majority of animal phyla lack an antiviral RNAi response or that these phyla could possess an antiviral RNAi response resembling that reported for vertebrates, which is not detectable through simple metagenomic sequencing of wild-type individuals. In addition, we report abundant somatic piRNAs across anciently divergent animals suggesting that this is the ancestral state in Bilateria. Our study challenges the widely-held assumption that most invertebrates possess an antiviral RNAi pathway likely similar to that seen in Drosophila, other arthropods, and nematodes.

evolutionary biology↗

bioRxiv2017

RNA interference pathways display high rates of adaptive protein evolution across multiple invertebrates

Conflict between organisms can lead to reciprocal adaptation that manifests itself as an increased evolutionary rate in the genes mediating the conflict. This adaptive signature has been observed in RNA interference (RNAi) pathway genes involved in the suppression of viruses and transposable elements in Drosophila melanogaster, suggesting that a subset of Drosophila RNAi genes may be locked into an arms race with these parasites. However, it is not known whether rapid evolution of RNAi genes is a general phenomenon across invertebrates, or which RNAi genes generally evolve adaptively. Here we use population genomic data from eight invertebrate species to infer rates of adaptive sequence evolution, and to test for past and ongoing selective sweeps in RNAi genes. We assess rates of adaptive protein evolution across species by using a formal meta-analytic framework to combine data across species, and by implementing a multispecies generalised linear mixed model of mutation counts. In all species, we find that RNAi genes display a greater rate of adaptive protein substitution than other genes, and that this is primarily mediated by positive selection acting on the subset of genes that are most likely to defend against viruses and transposable elements. In contrast, evidence for recent selective sweeps is broadly spread across functional classes of RNAi genes and differs substantially among species. Finally, we identify genes that exhibit elevated adaptive evolution across the analysed insect species combined, perhaps due to concurrent parasite-mediated arms races.

evolutionary biology↗

bioRxiv2016

Vertically transmitted rhabdoviruses are found across three insect families and have dynamic interactions with their hosts

A small number of free-living viruses have been found to be obligately vertically transmitted, but it remains uncertain how widespread vertically transmitted viruses are and how quickly they can spread through host populations. Recent metagenomic studies have found several insects to be infected with sigma viruses (Rhabdoviridae). Here, we report that sigma viruses that infect Mediterranean fruit flies (Ceratitis capitata), Drosophila immigrans, and speckled wood butterflies (Pararge aegeria) are all vertically transmitted. We find patterns of vertical transmission that are consistent with those seen in Drosophila sigma viruses, with high rates of maternal transmission, and lower rates of paternal transmission. This mode of transmission allows them to spread rapidly in populations, and using viral sequence data we found the viruses in D. immigrans and C. capitata had both recently swept through host populations. The viruses were common in nature, with mean prevalences of 12% in C. capitata, 38% in D. immigrans and 74% in P. aegeria. We conclude that vertically transmitted rhabdoviruses may be widespread in insects, and that these viruses can have dynamic interactions with their hosts.

evolutionary biology↗