Biology subjects

Mathers, T. C.

Publications and source records attributed to Mathers, T. C..

At least 19 recordsLinked to original sources

bioRxiv2026

Widespread introgression and a potential role for a neo-sex chromosome in booby diversification and speciation

Speciation in marine taxa is dynamic and complex, often occurring in the absence of absolute geographic barriers to gene flow. Boobies comprise a clade of seven highly mobile seabird species with high diversity in the eastern Pacific Ocean, where no land barriers separate extant sister species and hybridization is widespread. They exhibit striking diversity in bare-part coloration, an important signal of mate quality, and possess a novel multiple sex chromosome system (Z1Z2Z1Z2 / Z1Z2W), likely resulting from a fusion between an ancestral autosomal microchromosome and the W chromosome. To understand speciation processes in the context of gene flow, we sequenced and analyzed 29 short-read booby genomes and assembled a reference northern gannet genome to (1) test for introgression, (2) characterize genomic patterns of divergence across species, and (3) investigate the gene content and evolution of the neo-sex chromosome. We found that divergence among eastern Pacific sister taxa is temporally associated with periods of glacial maxima. Between periods of glacial maxima, two pairs of sister species (blue-footed and Peruvian boobies; masked and Nazca boobies) exhibit strong signatures of episodic introgression, indicating that speciation has occurred over multiple periods of divergence followed by gene flow. However, in the third pair of sister species, genomic signatures showed higher divergence within brown booby populations than between brown and Cocos boobies. We also identified the epidermal differentiation complex - a gene cassette involved in skin, feather, beak, and claw development - on the neo-sex region of the W chromosome, where it spans the boundary between the putatively recombining and non-recombining regions, with interspecific variation in the exact recombination suppression boundary. We inferred that this complex may contribute to diversity in feather and bare part coloration across boobies. Together, these results reveal that diversification and speciation in a clade of highly mobile seabirds emerged from a complex evolutionary history involving historical climate dynamics, introgression, and sex chromosome evolution.

evolutionary biology↗

bioRxiv2026

Hybridisation and herbivory fuel Amazonian tree radiations

Tropical rainforests, and Amazonia in particular, contain more tree species than anywhere else, most of which arose through rapid evolutionary radiations 1-3. Rapid radiations are often catalysed by ecological opportunity 4-6, which in rainforest trees is presented by intense insect herbivore pressure, spurring the evolution of novel plant defence chemistry to escape it 7. However, we do not understand how long-lived trees can adapt quickly enough to keep pace with rapidly-evolving insect herbivores. Here we show that hybridisation in rainforest trees, which was considered rare, allows exchange of gene clusters used in chemical defence against herbivore attack, facilitating rapid adaptation and diversification. Using genome sequencing for 461 individuals from the genus Inga, a characteristic Amazonian tree radiation, we find that regional tree communities form syngameons - networks of closely related, co-occurring species connected by gene flow. Integrating these genomes with herbivore abundance data from the same communities across the tropical Americas, we show that herbivore compositional turnover coincides with local, recurrent interspecific transfer of defence gene clusters that are retained by balancing selection, consistent with fluctuating selective pressure imposed by shifting herbivore communities. Together, our results demonstrate that hybridisation allows long-lived tropical trees to rapidly evolve chemical defences, fuelling adaptation to the relentless insect herbivory that structures the worlds most species-rich forests.

evolutionary biology↗

bioRxiv2026

340 dipteran genomes reveal the origin of Muller elements and sex chromosomes in Diptera

Diptera genome evolution is traditionally viewed through the lens of Drosophila melanogaster. To provide an unbiased picture of chromosome evolution in Diptera, we reconstructed six ancestral linkage groups (ALGs) and their rearrangements using 340 chromosome-level genome assemblies from 59 dipteran Families and two outgroups. Notably, Diptera ALGs are conserved in many Nematoceran lineages, while emergence of Brachycera coincided with four chromosomal fissions, which subsequently fused in various combinations. In Schizophora and relatives, a stable karyotype of five metacentric chromosomes and a chromosome homologous to the dot emerged that is remarkably stable with the notable exception of Drosophila, where the metacentric chromosomes became acrocentric Muller elements. Furthermore, our reconstruction reveals an ancient sex chromosome system associated with a small and gene-poor ALG that frequently fused to other chromosomes.

genomics↗

bioRxiv2026

Rapidly evolving aphid gall effector proteins exhibit saposin-like folds

Many insects manipulate plants by injecting effector proteins. In one extreme example of this molecular "hijacking", Hormaphis cornu aphids inject bicycle proteins into Hamamelis virginiana, contributing to the development of novel organs called galls. Bicycle proteins share no amino acid sequence similarity with proteins of known function. Here, we report the crystal structures of two divergent bicycle proteins. Both proteins contain saposin-like folds: one with multiple disulfide bonds exhibits a swapped domain topology; the other has no disulfide bonds and possesses two distinct, tandem domains. To explore the structural evolution of bicycle proteins, we attempted to predict bicycle protein structures with Alphafold2 (AF2) and other deep learning programs. While AF2 did not recover the two experimental structures using existing databases, it succeeded when provided with multiple sequence alignments (MSAs) of protein sequences from newly sequenced closely related species. Using this approach, we generated 2400 high-confidence bicycle protein predictions from seven aphid species. While all aphid bicycle proteins contain predicted saposin-like folds, they display a vast diversity of structural and physicochemical properties. While this diversity thwarts prediction of conserved functions encoded in structure, it suggests that bicycle proteins have evolved to target diverse plant processes and/or to evade plant immune surveillance. Our extension of AF2 with custom MSAs of proteins from closely related species provides a generalizable, powerful approach for predicting structures of rapidly evolving protein families. Significance statementParasites introduce specialized "effector" proteins into hosts to suppress host immunity and to release nutrients. The molecular functions and structures of most effector proteins are unknown. Effector proteins often evolve rapidly and share no similarity with proteins of known function. Here, we demonstrate that machine learning algorithms can predict the structures of aphid "bicycle" effector proteins when supplemented with data from closely related species. We exploit this finding to generate predictions of 2400 bicycle protein structures. Aphid bicycle proteins exploit a common folding motif, yet exhibit topologically distinct structures that form separate structural clusters. Despite the clustering of these proteins in structure space, they occupy a nearly uniformly physicochemical space, suggesting that they encode a large diversity of molecular functions.

molecular biology↗

bioRxiv2026

High quality chromosomal genome assemblies of three human Plasmodium species directly from natural infections

Malaria, caused by mosquito-transmitted Plasmodium parasites, remains a major global health challenge. While P. falciparum accounts for most malaria deaths, the lesser-studied P. ovale spp. and P. malariae also contribute to disease burden across many endemic regions, typically causing milder but chronic infections. Here, we generated high-quality, chromosome-level reference genomes for P. ovale wallikeri, P. malariae, and P. falciparum directly from blood samples taken from natural infections. Using PacBio Ultra-Low-Input HiFi long-read sequencing and Hi-C chromatin conformation capture, we overcome limitations posed by low parasite biomass and the absence of in vitro culture for P. ovale wallikeri and P. malariae. These high quality reference genomes resolve previously inaccessible subtelomeric regions that include expanded gene families likely involved in host-parasite interactions, and they enhance our understanding of parasite persistence, transmission, immune evasion and comparative evolutionary studies. This work provides a critical foundation for including these neglected species in global malaria elimination efforts.

genomics↗

bioRxiv2025

Whole-Genome Population Genomics Reveals Lineage Structure and Adaptive Potential of Philaenus spumarius, the Principal Vector of Xylella fastidiosa in Europe

Philaenus spumarius (L.), the meadow spittlebug, is the principal European vector of Xylella fastidiosa. This xylem-feeding insect has a broad host range, ecological plasticity, and mobility, making it an efficient vector across diverse landscapes. Yet, major gaps remain in understanding its genetic diversity, migration patterns, and local adaptation, limiting effective control of X. fastidiosa outbreaks. To address these gaps, we worked with a global network of researchers and citizen scientists to assemble a geographically and ecologically diverse collection of P. spumarius samples. We generated a chromosome-level genome assembly for P. spumarius and high-quality assemblies for four related spittlebug species, providing a robust genomic framework for evolutionary and epidemiological studies. Resequencing 430 P. spumarius individuals from across the globe uncovered boreal, temperate, and semi-arid lineages shaped by geography and climate. The lineages vary in reproductive isolation and in the degree of mito-nuclear divergence. Iberian populations grouped with an individual identified as P. tesselatus contributing to regional genetic complexity. Genomic scans identified loci under selection in Apulian populations, including signatures in sulfotransferase (SULT) genes potentially linked to behavioural plasticity, host plant specialisation, or insecticide resistance in olive-growing regions. Migration analyses indicated limited long-distance dispersal but strong local connectivity, consistent with the rapid regional spread of X. fastidiosa. Together, these findings reveal the lineage structure and adaptive potential of P. spumarius, the key vector of X. fastidiosa in Europe. They underscore the importance of targeted surveillance of locally adapted populations and provide genomic tools for monitoring vector dynamics and mitigating emerging disease risks.

evolutionary biology↗

bioRxiv2025

Dynamic evolution of germ-line restricted chromosomes in three dark-winged fungus gnats (Sciaridae) revealed through chromosome level germline genomes.

Germline restricted chromosomes (GRCs) are an evolutionary mystery. While they seem to be important and perhaps indispensable in species they occur, they also show surprising variability in copy number and size. We are just beginning to understand the evolutionary significance of these chromosomes. One factor that impedes our understanding is that at present, few clades with these chromosomes have been studied in depth. We genomically investigate the GRCs in dark-winged fungus gnats (Sciaridae), a cosmopolitan and species-rich taxa which have harboured GRCs for at least 58 million years. Sciaridae species carry from 1-4 large GRCs which evolved through introgression from the Cecidomyiidae lineage. We produce the first male germline chromosome-scale genome assemblies for the sciarids Bradysia coprophila, B. impatiens, and Lycoriella ingenua. Comparing the GRCs both between and within species, we find that these chromosomes evolve in an extraordinarily dynamic fashion, with very little conservation of synteny or gene content. Puzzlingly, despite this variability, GRCs are gene rich and their genes are evolving under strong purifying selection. Additionally, we uncover evidence that somatic elimination of GRCs potentially occurs via a satellite mediated process. Our study sheds light on the mechanisms of meiosis, tissue restriction, chromosome elimination, and gives us a better appreciation for the diversity of genetic systems that not only persist, but thrive in nature. Significance statementGermline restricted chromosomes (GRCs) are a fascinating evolutionary puzzle. They are restricted to the germline early in development, have unusual transmission dynamics and are more variable than core chromosomes, but also seem to be indispensable in clades they occur in. We generate chromosome level GRC assemblies from three species of fungus gnats (Sciaridae, Diptera). We find that the GRCs, which originated via a cross-family hybridization event, are evolving much more dynamically than other chromosomes in the genome. The five GRCs we sequence are all large, gene-rich, and seem to carry functional genes, but contain mostly a non-overlapping gene set, suggesting that four of the five GRCs we sequenced did not evolve from the same original chromosome.

evolutionary biology↗

bioRxiv2025

Forty New Genomes Shed Light on Sexual Reproduction and the Origin of Tetraploidy in Microsporidia

Microsporidia are single-celled, obligately intracellular parasites with growing public health, agricultural, and economic importance. Despite this, Microsporidia remain relatively enigmatic, with many aspects of their biology and evolution unexplored. Key questions include whether Microsporidia undergo sexual reproduction, and the nature of the relationship between tetraploid and diploid lineages. While few high-quality microsporidian genomes currently exist to help answer such questions, large-scale biodiversity genomics initiatives, such as the Darwin Tree of Life project, can generate high-quality genome assemblies for microsporidian parasites when sequencing infected host species. Here, we present 40 new microsporidian genome assemblies from infected arthropod hosts that were sequenced to create reference genomes. Out of the 40, 32 are complete genomes, eight of which are chromosome-level, and eight are partial microsporidian genomes. We characterised 14 of these as polyploid and five as diploid. We found that tetraploid genome haplotypes are consistent with autopolyploidy, in that they coalesce more recently than species, and that they likely recombine. Within some genomes, we found large-scale rearrangements between the homeologous genomes. We also observed a high rate of rearrangement between genomes from different microsporidian groups, and a striking tolerance for segmental duplications. Analysis of chromatin conformation capture (Hi-C) data indicated that tetraploid genomes are likely organised into two diploid compartments, similar to dikaryotic cells in fungi, with evidence of recombination within and between compartments. Together, our results provide evidence for the existence of a sexual cycle in Microsporidia, and suggest a model for the microsporidian lifecycle that mirrors fungal reproduction.

genomics↗

bioRxiv2025

MicroFinder: Conserved gene-set mapping and assembly ordering for manual curation of bird microchromosomes

Obtaining chromosomally complete genome assemblies across the tree of life is a major goal of biodiversity genomics. However, some lineages remain recalcitrant to assembly despite recent advances in sequencing technologies and assembly tools. Birds present a substantial genome assembly challenge due to the presence of tiny, hard to assemble microchromosomes that are often highly fragmented or even missing in draft genome assemblies. As such, bird genomes require a large amount of expert manual curation effort via manipulation of genome-wide Hi-C contact maps and many current chromosome-level bird genome assemblies do not resolve the known karyotype. Microchromosomes have distinct genetic and epigenetic features. They are GC-biased, gene-rich, highly methylated, and have distinct spatial organisation in the centre of the nucleus. Importantly, they are conserved across avian evolution. Here, using a reference set of expert curated bird genomes, we have identified a set of conserved microchromosome genes and developed MicroFinder, a pipeline that uses this gene set to find small microchromosome fragments in draft genome assemblies to act as anchors for manual curation of microchromosomes. We demonstrate how MicroFinder can be used to improve the speed and accuracy of bird genome curation. Furthermore, we highlight the usefulness of MicroFinder by carrying out MicroFinder-enabled re-curation of 12 previously released chromosome-scale bird genome assemblies, increasing the sequence content of microchromosome models.

genomics↗

bioRxiv2024

Chromosome-level Assemblies of Three Candidatus Liberibacter solanacearum Vectors: Dyspersa apicalis, Dyspersa pallida, and Trioza urticae (Hemiptera: Psylloidea)

Psyllids are major vectors of plant diseases, including Candidatus Liberibacter solanacearum (CLso), the bacterial agent associated with zebra chip disease in potatoes and carrot yellows disease in carrot. Despite their agricultural significance, there is limited knowledge on the genome structure and genetic diversity of psyllids. In this study, we provide chromosome-level genome assemblies for three psyllid species known to transmit CLso: Dyspersa apicalis (carrot psyllid), Dyspersa pallida, and Trioza urticae (nettle psyllid). As D. apicalis is recognised as the primary vector of CLso by carrot growers in Northern Europe, we also resequenced populations of this species from Finland, Norway, and Austria. Genome assemblies were constructed using PacBio HiFi and Hi-C sequencing data, yielding genome sizes of: 594.01 Mbp for D. apicalis; 587.80 Mbp for D. pallida; and 655.58 Mbp for T. urticae. Over 90% of sequences anchored into 13 pseudo-chromosomes per species. The assemblies for D. apicalis and D. pallida exhibited high completeness, capturing over 92% of conserved Hemiptera single-copy orthologues, as assessed by Benchmarking Universal Single-Copy Orthologues (BUSCO) analysis. Furthermore, we identified sequences of the primary psyllid symbiont, Candidatus Carsonella ruddii, in all three species. Comparative genomic analyses demonstrated synteny with other psyllid species. Notably, we observed significant expansions in gene families, particularly those linked to potential insecticide detoxification, within the Dyspersa lineage. Resequencing efforts also revealed the existence of multiple subpopulations of D. apicalis across Europe. These high-quality genome resources will support future research on genome evolution, insect-plant-pest interactions, and strategies for disease management. SignificancePsyllid species are significant agricultural pests, known for transmitting plant diseases like Candidatus Liberibacter solanacearum (CLso), which causes zebra chip in potatoes and carrot yellows. However, genomic data on psyllids are limited. In this study, we present high-quality, chromosome-level genome assemblies for three psyllid species: Dyspersa apicalis, Dyspersa pallida, and Trioza urticae. We generated genome assemblies with over 90% of sequences anchored to 13 pseudo-chromosomes. Comparative analyses revealed gene expansions, particularly in detoxification pathways, suggesting adaptations within the Dyspersa lineage. Population resequencing of D. apicalis across Europe uncovered genetic subpopulations. These genomes will advance understanding of psyllid biology and inform disease management strategies.

genomics↗

bioRxiv2024

Genomes of two invasive Adelges species (hemlock woolly adelgid and pineapple gall adelgid) enable characterization of nicotinic acetylcholine receptors

Two invasive hemipteran adelgids are associated with widespread damage to several North American conifer species. Adelges tsugae, hemlock woolly adelgid, was introduced from Japan and reproduces parthenogenetically in North America, where it has rapidly decimated Tsuga canadensis and Tsuga caroliniana (the eastern and Carolina hemlocks, respectively). Adelges abietis, eastern spruce gall adelgid, introduced from Europe, forms distinctive pineapple-shaped galls on several native spruce species. While not considered a major forest pest, it weakens trees and increases susceptibility to additional stressors. Broad-spectrum insecticides that are often used to control adelgid populations can have off-target impacts on beneficial insects. Whole genome sequencing was performed on both species to aid in development of targeted solutions that may minimize ecological impact. Adelges abietis was sequenced using Illumina Linked-Read technology from 30 pooled individuals, with Hi-C scaffolding performed using data from a single individual collected from the same host plant. Adelges tsugae used Oxford Nanopore long-read sequencing from pooled nymphs. The assembled A. tsugae and A. abietis genomes, pooled from several parthenogenetic females, are 220.75 Mbp and 253.16 Mbp, respectively. Each consists of eight autosomal chromosomes, as well as two sex chromosomes (X1/X2), supporting the XX-XO sex determination system. The genomes are over 96% complete based on BUSCO assessment. Genome annotation identified 11,424 and 12,060 protein-coding genes in A. tsugae and A. abietis, respectively. Comparative analysis of proteins across 29 hemipteran species and 14 arthropod outgroups identified 31,666 putative gene families. Gene family evolution analysis with CAFE revealed lineage-specific expansions in immune-related aminopeptidases (ERAP1) and juvenile hormone binding proteins (JHBP), contractions in juvenile hormone acid methyltransferases (JHAMT), and conservation of nicotinic acetylcholine receptors (nAChR). These genes were explored as candidate families towards a long-term objective of developing adelgid-selective insecticides. Structural comparisons of proteins across seven focal species (Adelges tsugae, Adelges abietis, Adelges cooleyi, Rhopalosiphum maidis, Apis mellifera, Danaus plexippus, and Drosophila melanogaster) revealed high conservation of nAChR and ERAP1, while JHAMT exhibited species-specific structural divergence. The potential of JHAMT as a lineage-specific target for pest control was explored through virtual drug and pesticide screening.

genomics↗

bioRxiv2024

The conserved aphid saliva chemosensory protein effector Mp10 targets plant AMSH deubiquitinases at cellular membranes to suppress pattern-triggered immunity

Chemosensory proteins (CSPs) are a conserved family present in insects and other arthropods, recognized for their critical roles in both intra- and interspecies communication. However, the functional mechanisms of these proteins remain largely unexplored. In our previous research, we identified a CSP in aphid saliva, Mp10, from the peach-potato aphid Myzus persicae, which functions as an effector protein modulating host plant immunity. Mp10 suppresses pattern recognition receptor (PRR)-triggered immunity (PTI), the first layer of plant defence, while also inducing effector-triggered immunity (ETI). In this study, we elucidate the molecular mechanisms by which Mp10 suppresses PTI. Our findings reveal that Mp10 interacts with AMSH deubiquitinase enzymes in plants, as shown by yeast two-hybrid, co-immunoprecipitation (co-IP), and FRET-FLIM assays, with these interactions predominantly localized to intracellular membranes. Mp10 was found to modulate the dynamics of membrane-bound PRR receptor kinases in plant cells. Co-IP and mass spectrometry analyses demonstrated that Mp10 and AMSH2 associate with a range of PRR kinases, PRR-associated kinases, and proteins involved in the intracellular trafficking of membrane proteins. Mp10 reduces the accumulation of these kinases at the cell surface by promoting their internalization to internal membranes, thereby dampening PTI. Supporting this, a dominant-negative catalytically inactive variant of AMSH2 also inhibits PTI. Interestingly, Mp10 orthologues from other sap-feeding hemipteran insects exhibit similar immune-suppressive activities, and our findings show that their interaction with plant AMSH proteins is conserved, indicating this immune-suppression mechanism is evolutionarily ancient.

plant biology↗

bioRxiv2024

Genomics of Neotropical biodiversity indicators: two butterfly radiations with rampant chromosomal rearrangements and hybridisation

A major question in evolutionary biology is what drives the diversification of lineages. Rapid, recent radiations are ideal systems for addressing how new species arise because they still show key morphological and ecological adaptations associated with speciation. While most studied recent radiations have evolved in an insular environment, less research has been carried out on continental radiations with complex species interactions. Melinaea and Mechanitis butterflies (Nymphalidae: Ithomiini) have rapidly radiated in the Neotropics. They are classical models for Amazonian biogeography and colour pattern mimicry and have been proposed as biodiversity indicators. We generated reference genomes for five species of each genus, and whole-genome resequencing data of most species and subspecies covering a wide geographic range to assess phylogeographic relationships, patterns of hybridisation and chromosomal rearrangements. Our data help resolve the classification of these taxonomically challenging butterflies and reveal very high diversification rates. We find rampant evidence of historical hybridisation and putative hybrid species in both radiations, which may have facilitated their rapid diversification. Moreover, dozens of chromosomal fusions and fissions were identified between congeneric species, and even some within species. We conclude that interactions between geography, hybridisation and chromosomal rearrangements have contributed to these two rapid radiations in the highly diverse Neotropical region. We suggest that rapid radiations may be spurred by repeated periods of geographic isolation during Pleistocene climate oscillations, combined with lineage-specific rapid accumulation of incompatibilities during allopatric phases, followed by secondary contact with some gene exchange. Significance StatementUnderstanding factors contributing to rapid speciation is a key aim of evolutionary biology. Here we focus on two rapid radiations of Neotropical butterflies. Our genomic data with broad taxonomic and geographic coverage reveal rampant hybridisation and chromosomal rearrangements, each likely contributing to the high diversification rates. Our study highlights the use of genomic data to resolve taxonomically challenging species groups and elucidate drivers of diversification in rapid radiations. We show that for biodiversity hotspots with recent radiations, barcoding is insufficient to characterise species richness due to gene flow and recent speciation. The taxonomic implications of both introgression and karyotype diversity for species delimitation are important to consider during monitoring and management of biodiversity in these vulnerable habitats.

evolutionary biology↗

bioRxiv2023

Kinetochore and ionomic adaptation to whole genome duplication

Transforming genomic and cellular landscapes in a single generation, whole genome duplication (WGD) brings fundamental challenges, but is also associated with diversification. How is WGD tolerated, and what processes commonly evolve to stabilize the resulting polyploid? Here we study this in Cochlearia spp., which have experienced multiple WGDs in the last 300,000 years. We first generate a chromosome-scale genome and sequence 113 individuals from 33 diploid, tetraploid, hexaploid, and outgroup populations. We detect the clearest post-WGD selection signatures in functionally interacting kinetochore components and ion transporters. We structurally model these derived selected alleles, identifying striking WGD-relevant functional variation, and then compare these results to independent recent post-WGD selection in Arabidopsis arenosa and Cardamine amara. Most prominent in these results is genetic evidence of at least four functionally interacting kinetochore complex subunits in adaptation to WGD at the centromere among our very top selective sweep outliers. In addition, some of the same biological processes evolve in all three WGDs, but specific genes recruited are flexible. This points to a polygenic basis for modifying systems that control the kinetochore, meiotic crossover number, DNA repair, ion homeostasis, and cell cycle. Given that DNA management (especially repair) is the most salient category with the strongest selection signal, we speculate that the generation rate of structural genomic variants may be altered by WGD in young polyploids, contributing to their occasionally spectacular adaptability observed across kingdoms. Significance StatementWhole-genome duplication (WGD) occurs in all kingdoms and is linked to adaptation, speciation, domestication, and even cancer outcome. But WGD is a shock to the system, and commonly disrupts cell division due to increased DNA management burden and transformed cell physiology. Nevertheless, the hopeful monster that survives WGD is special, occasionally experiencing runaway success. Why do some thrive but others die? Here we introduce a powerful new model, Cochlearia, which has benefitted from multiple WGDs, and we provide the first genetic evidence of rapid adaptation of functionally interacting components of the cell division machinery, the kinetochore. We also compare which processes and genes evolve to stabilize the new polyploid in three independent cases and highlight common mechanisms.

evolutionary biology↗

bioRxiv2022

Hybridisation has shaped a recent radiation of grass-feeding aphids

Aphids are common crop pests. These insects reproduce by facultative parthenogenesis involving several rounds of clonal reproduction interspersed with an occasional sexual cycle. Furthermore, clonal aphids give birth to live apterous or winged young that are already pregnant. Together, these qualities enable rapid population growth and have facilitated the colonisation of crops globally. In several cases so-called "super clones" have come to dominate agricultural systems. However, the extent to which the sexual stage of the aphid life cycle has shaped global pest populations has remained largely unclear, as have the origins of successful lineages. Here, we used chromosome-scale genome assemblies to disentangle the evolution of two of the most significant global pests of cereals - the English (Sitobion avenae) and Indian (Sitobion miscanthi) grain aphids. We found that genome-wide divergence between S. avenae and S. miscanthi is low and that S. avenae sensu stricto is part of a larger cryptic species complex that includes multiple diverged S. miscanthi lineages. Moreover, comparison of haplotype-resolved assemblies reveals that the S. miscanthi isolate used for genome sequencing is likely a hybrid, with one of its diploid genome copies being closely related to S. avenae ([~]0.5% divergence) and the second being substantially more divergent (> 1%). Analyses of genotyping-by-sequencing (GBS) data of grain aphids from the UK and China revealed that S. avenae and S. miscanthi are part of a species complex with many highly differentiated lineages that predate the origins of agriculture. The complex consists of hybrid lineages that display a tangled history of hybridisation and genetic introgression. These data demonstrate that hybridisation has substantially contributed to grain aphid diversity, and hence, to the evolutionary potential of this important pest species.

evolutionary biology↗

bioRxiv2020

A chromosome-level genome assembly of the woolly apple aphid, Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae)

Woolly apple aphid (WAA, Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), is a major pest of apple trees (Malus domestica, order Rosales) and is critical to the economics of the apple industry in most parts of the world. Here, we generated a chromosome-level genome assembly of WAA - representing the first genome sequence from the aphid subfamily Eriosomatinae - using a combination of 10X Genomics linked-reads and in vivo Hi-C data. The final genome assembly is 327 Mb, with 91% of the assembled sequences anchored into six chromosomes. The contig and scaffold N50 values are 158 kb and 71 Mb, respectively, and we predicted a total of 28,186 protein-coding genes. The assembly is highly complete, including 97% of conserved arthropod single-copy orthologues based on BUSCO analysis. Phylogenomic analysis of WAA and nine previously published aphid genomes, spanning four aphid tribes and three subfamilies, reveals that the tribe Eriosomatini (represented by WAA) is recovered as a sister group to Aphidini + Macrosiphini (subfamily Aphidinae). We identified syntenic blocks of genes between our WAA assembly and the genomes of other aphid species and find that two WAA chromosomes (El5 and El6) map to the conserved Macrosiphini and Aphidini X chromosome. Our high-quality WAA genome assembly and annotation provides a valuable resource for research in a broad range of areas such as comparative and population genomics, insect-plant interactions and pest resistance management.

genomics↗

bioRxiv2020

Genome sequence of the banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) and its symbionts

The banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae), is a major pest of cultivated bananas (Musa spp., order Zingiberales), primarily due to its role as a vector of Banana bunchy top virus (BBTV), the most severe viral disease of banana worldwide. Here, we generated a highly complete genome assembly of P. nigronervosa using a single PCR-free Illumina sequencing library. Using the same sequence data, we also generated complete genome assemblies of the P. nigronervosa symbiotic bacteria Buchnera aphidicola and Wolbachia. To improve our initial assembly of P. nigronervos a we developed a k-mer based deduplication pipeline to remove genomic scaffolds derived from the assembly of haplotigs (allelic variants assembled as separate scaffolds). To demonstrate the usefulness of this pipeline, we applied it to the recently generated assembly of the aphid Myzus cerasi, reducing the duplication of conserved BUSCO genes by 25%. Phylogenomic analysis of P. nigronervos a, our improved M. cerasi assembly, and seven previously published aphid genomes, spanning three aphid tribes and two subfamilies, reveals that P. nigronervos a falls within the tribe Macrosiphini, but is an outgroup to other Macrosiphini sequenced so far. As such, the genomic resources reported here will be useful for understanding both the evolution of Macrosphini and for the study of P. nigronervosa. Furthermore, our approach using low cost, high-quality, Illumina short-reads to generate complete genome assemblies of understudied aphid species will help to fill in genomic black spots in the diverse aphid tree of life.

genomics↗

bioRxiv2020

Chromosome-scale genome assemblies of aphids reveal extensively rearranged autosomes and long-term conservation of the X chromosome

Large-scale chromosome rearrangements are arguably the most dramatic type of mutations, often leading to rapid evolution and speciation. However, chromosome dynamics have only been studied at the sequence level in a small number of model systems. In insects, Diptera (flies and mosquitoes) and Lepidoptera (butterflies and moths) have high levels of chromosome conservation. Whether this truly reflects the diversity of insect genome evolution is questionable given that many species exhibit rapid karyotype evolution. Here, we investigate chromosome evolution in aphids - an important group of hemipteran plant pests - using newly generated chromosome-scale genome assemblies of the green peach aphid (Myzus persicae) and the pea aphid (Acyrthosiphon pisum), and a previously published chromosome-scale assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganisation over the last 30 million years, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (M. persicae and A. pisum) and Aphidini (R. maidis). In contrast, gene content of the aphid sex (X) chromosome remained unchanged despite rapid sequence evolution, low gene expression and high transposable element load. To test whether rapid evolution of genome structure is a hallmark of Hemiptera, we compared our aphid assemblies to chromosome-level assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny and we detect only two chromosome fusion or fission events. The exceptional rate of structural evolution of aphid autosomes renders them an important emerging model system for studying the role of large-scale genome rearrangements in evolution.

genomics↗