Publications by category
Journal articles
Hayward A, Baril T (In Press). A draft genome sequence of the elusive giant squid, Architeuthis dux. GigaScience
Dupeyron M, Singh K, Bass C, Hayward A (In Press). Evolution of Mutator transposable elements across eukaryotic diversity. Mobile DNA
Hayward A, Kolm N, Kotrschal A, Løvlie H, Cornwallis CK, Zidar J, Buechel SD, Tsuboi M (In Press). Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids. Journal of Evolutionary Biology
Baril T, Hayward A (In Press). Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, Danaus plexippus.
Mobile DNAAbstract:
Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, Danaus plexippus
Background
Lepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly is available for the monarch butterfly (Danaus plexippus), but it lacks an in-depth transposable element (TE) annotation, presenting an opportunity to explore monarch TE dynamics and the impact of TEs on shaping the monarch genome.
Results
We find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1- 2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes.
Conclusions
We provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.
Abstract.
Qu Z, Nong W, So WL, Barton-Owen T, Li Y, Li C, Leung TCN, Baril T, Wong AYP, Swale T, et al (In Press). Millipede genomes reveal unique adaptation of genes and microRNAs during myriapod evolution.
Abstract:
Millipede genomes reveal unique adaptation of genes and microRNAs during myriapod evolution
AbstractThe Myriapoda including millipedes and centipedes is of major importance in terrestrial ecology and nutrient recycling. Here, we sequenced and assembled two chromosomal-scale genomes of millipedes Helicorthomorpha holstii (182 Mb, N50 18.11 Mb mainly on 8 pseudomolecules) and Trigoniulus corallinus (449 Mb, N50 26.78 Mb mainly on 15 pseudomolecules). Unique defense systems, genomic features, and patterns of gene regulation in millipedes, not observed in other arthropods, are revealed. Millipedes possesses a unique ozadene defensive gland unlike the venomous forcipules in centipedes. Sets of genes associated with anti-microbial activity are identified with proteomics, suggesting that the ozadene gland is not primarily an antipredator adaptation (at least in T. corallinus). Macro-synteny analyses revealed highly conserved genomic blocks between centipede and the two millipedes. Tight Hox and the first loose ecdysozoan ParaHox homeobox clusters are identified, and a myriapod-specific genomic rearrangement including Hox3 is also observed. The Argonaute proteins for loading small RNAs are duplicated in both millipedes, but unlike insects, an argonaute duplicate has become a pseudogene. Evidence of post-transcriptional modification in small RNAs, including species-specific microRNA arm switching that provide differential gene regulation is also obtained. Millipede genomes reveal a series of unique genomic adaptations and microRNA regulation mechanisms have occurred in this major lineage of arthropod diversity. Collectively, the two millipede genomes shed new light on this fascinating but poorly understood branch of life, with a highly unusual body plan and novel adaptations to their environment.
Abstract.
Hayward A (In Press). Origin of the Retroviruses: when, where, and how?.
Current Opinion in VirologyAbstract:
Origin of the Retroviruses: when, where, and how?
Retroviruses are a virus family of considerable medical and veterinary importance. Additionally, it is now clear that endogenous retroviruses (ERVs) comprise significant portions of vertebrate genomes. Until recently, very little was known about the deep evolutionary origins of retroviruses. However, advances in genomics and informatics have opened the way for great strides in understanding. Recent research employing a wide variety of bioinformatic approaches has demonstrated that retroviruses evolved during the early Palaeozoic Era, between 460-550 million years ago, providing the oldest inferred date estimate for any virus group. This finding presents an important framework to investigate the evolutionary transitions that led to the emergence of the retroviruses, offering potential insights into the infectious origins of a major group of pathogenic viruses.
Abstract.
Mackintosh A, Laetsch D, Hayward A, Charlesworth B, Waterfall M, Vila R, Lohse K (In Press). The determinants of genetic diversity in butterflies. Nature Communications
Brekke TD, Papadopulos AST, Julià E, Fornas O, Fu B, Yang F, de la Fuente R, Page J, Baril T, Hayward A, et al (2023). A new chromosome-assigned Mongolian gerbil genome allows characterization of complete centromeres and a fully heterochromatic chromosome.
Mol Biol EvolAbstract:
A new chromosome-assigned Mongolian gerbil genome allows characterization of complete centromeres and a fully heterochromatic chromosome.
Chromosome-scale genome assemblies based on ultra-long read sequencing technologies are able to illuminate previously intractable aspects of genome biology such as fine-scale centromere structure and large-scale variation in genome features such as heterochromatin, GC content, recombination rate, and gene content. We present here a new chromosome-scale genome of the Mongolian gerbil (Meriones unguiculatus) which includes the complete sequence of all centromeres. Gerbils are thus the one of the first vertebrates to have their centromeres completely sequenced. Gerbil centromeres are composed of four different repeats of length 6pb, 37
bp, 127
bp, or 1747bp which occur in simple alternating arrays and span 1-6Mb. Gerbil genomes have both an extensive set of GC-rich genes and chromosomes strikingly enriched for constitutive heterochromatin. We sought to determine if there was a link between these two phenomena and found that the two heterochromatic chromosomes of the Mongolian gerbil have distinct underpinnings: Chromosome 5 has a large block of intra-arm heterochromatin as the result of a massive expansion of centromeric repeats, while chromosome 13 is comprised of extremely large (>150
kb) repeated sequences. In addition to characterizing centromeres, our results demonstrate the importance of including karyotypic features such as chromosome number and the locations of centromeres in the interpretation of genome sequence data, and highlight novel patterns involved in the evolution of chromosomes.
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Author URL.
Mackintosh A, Vila R, Laetsch DR, Hayward A, Martin SH, Lohse K (2023). Chromosome Fissions and Fusions Act as Barriers to Gene Flow between Brenthis Fritillary Butterflies.
Mol Biol Evol,
40(3).
Abstract:
Chromosome Fissions and Fusions Act as Barriers to Gene Flow between Brenthis Fritillary Butterflies.
Chromosome rearrangements are thought to promote reproductive isolation between incipient species. However, it is unclear how often, and under what conditions, fission and fusion rearrangements act as barriers to gene flow. Here we investigate speciation between two largely sympatric fritillary butterflies, Brenthis daphne and Brenthis ino. We use a composite likelihood approach to infer the demographic history of these species from whole-genome sequence data. We then compare chromosome-level genome assemblies of individuals from each species and identify a total of nine chromosome fissions and fusions. Finally, we fit a demographic model where effective population sizes and effective migration rate vary across the genome, allowing us to quantify the effects of chromosome rearrangements on reproductive isolation. We show that chromosomes involved in rearrangements experienced less effective migration since the onset of species divergence and that genomic regions near rearrangement points have a further reduction in effective migration rate. Our results suggest that the evolution of multiple rearrangements in the B. daphne and B. ino populations, including alternative fusions of the same chromosomes, have resulted in a reduction in gene flow. Although fission and fusion of chromosomes are unlikely to be the only processes that have led to speciation between these butterflies, this study shows that these rearrangements can directly promote reproductive isolation and may be involved in speciation when karyotypes evolve quickly.
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Author URL.
Vila R, Lohse K, Hayward A, Laetsch DR, Wright C (2023). The genome sequence of the Chalkhill Blue, Lysandra coridon (Poda, 1761). Wellcome Open Research, 8
Lohse K, Hayward A, Vila R, Carvalho APS, Kawahara AY (2023). The genome sequence of the Large Skipper, Ochlodes sylvanus, (Esper, 1777). Wellcome Open Research, 8
Lohse K, Hayward A, Laetsch DR, Marques V, Vila R, Tyler-Smith C (2023). The genome sequence of the Mazarine Blue, Cyaniris semiargus (Rottemburg, 1775). Wellcome Open Research, 8
Galbraith JD, Hayward A (2023). The influence of transposable elements on animal colouration.
Trends GenetAbstract:
The influence of transposable elements on animal colouration.
Transposable elements (TEs) are mobile genetic sequences present within host genomes. TEs can contribute to the evolution of host traits, since transposition is mutagenic and TEs often contain host regulatory and protein coding sequences. We review cases where TEs influence animal colouration, reporting major patterns and outstanding questions. TE-induced colouration phenotypes typically arise via introduction of novel regulatory sequences and splice sites, affecting pigment cell development or pigment synthesis. We discuss if particular TE types may be more frequently involved in the evolution of colour variation in animals, given that examples involving long terminal repeat (LTR) elements appear to dominate. Currently, examples of TE-induced colouration phenotypes in animals mainly concern model and domesticated insect and mammal species. However, several influential recent examples, coupled with increases in genome sequencing, suggest cases reported from wild species will increase considerably.
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Lear L, Padfield D, Dowsett T, Jones M, Kay S, Hayward A, Vos M (2022). Bacterial colonisation dynamics of household plastics in a coastal environment.
Sci Total Environ,
838(Pt 4).
Abstract:
Bacterial colonisation dynamics of household plastics in a coastal environment.
Accumulation of plastics in the marine environment has widespread detrimental consequences for ecosystems and wildlife. Marine plastics are rapidly colonised by a wide diversity of bacteria, including human pathogens, posing potential risks to health. Here, we investigate the effect of polymer type, residence time and estuarine location on bacterial colonisation of common household plastics, including pathogenic bacteria. We submerged five main household plastic types: low-density PE (LDPE), high-density PE (HDPE), polypropylene (PP), polyvinyl chloride (PVC) and polyethylene terephthalate (PET) at an estuarine site in Cornwall (U.K.) and tracked bacterial colonisation dynamics. Using both culture-dependent and culture-independent approaches, we found that bacteria rapidly colonised plastics irrespective of polymer type, reaching culturable densities of up to 1000 cells cm3 after 7 weeks. Community composition of the biofilms changed over time, but not among polymer types. The presence of pathogenic bacteria, quantified using the insect model Galleria mellonella, increased dramatically over a five-week period, with Galleria mortality increasing from 4% in week one to 65% in week five. No consistent differences in virulence were observed between polymer types. Pathogens isolated from plastic biofilms using Galleria enrichment included Serratia and Enterococcus species and they harboured a wide range of antimicrobial resistance genes. Our findings show that plastics in coastal waters are rapidly colonised by a wide diversity of bacteria independent of polymer type. Further, our results show that marine plastic biofilms become increasingly associated with virulent bacteria over time.
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Law STS, Nong W, So WL, Baril T, Swale T, Chan CB, Tobe SS, Kai Z-P, Bendena WG, Hayward A, et al (2022). Chromosomal-level reference genome of the moth Heortia vitessoides (Lepidoptera: Crambidae), a major pest of agarwood-producing trees.
Genomics,
114(4).
Abstract:
Chromosomal-level reference genome of the moth Heortia vitessoides (Lepidoptera: Crambidae), a major pest of agarwood-producing trees.
The moth Heortia vitessoides Moore (Lepidoptera: Crambidae) is a major pest of ecologically, commercially and culturally important agarwood-producing trees in the genus Aquilaria. In particular, H. vitessoides is one of the most destructive defoliating pests of the incense tree Aquilaria sinesis, which produces a valuable fragrant wood used as incense and in traditional Chinese medicine [33]. Nevertheless, a genomic resource for H. vitessoides is lacking. Here, we present a chromosomal-level assembly for H. vitessoides, consisting of a 517 megabase (Mb) genome assembly with high physical contiguity (scaffold N50 of 18.2 Mb) and high completeness (97.9% complete BUSCO score). To aid gene annotation, 8 messenger RNA transcriptomes from different developmental stages were generated, and a total of 16,421 gene models were predicted. Expansion of gene families involved in xenobiotic metabolism and development were detected, including duplications of cytosolic sulfotransferase (SULT) genes shared among lepidopterans. In addition, small RNA sequencing of 5 developmental stages of H. vitessoides facilitated the identification of 85 lepidopteran conserved microRNAs, 94 lineage-specific microRNAs, as well as several microRNA clusters. A large proportion of the H. vitessoides genome consists of repeats, with a 29.12% total genomic contribution from transposable elements, of which long interspersed nuclear elements (LINEs) are the dominant component (17.41%). A sharp decrease in the genome-wide percentage of LINEs with lower levels of genetic distance to family consensus sequences suggests that LINE activity has peaked in H. vitessoides. In contrast, opposing patterns suggest a substantial recent increase in DNA and LTR element activity. Together with annotations of essential sesquiterpenoid hormonal pathways, neuropeptides, microRNAs and transposable elements, the high-quality genomic and transcriptomic resources we provide for the economically important moth H. vitessoides provide a platform for the development of genomic approaches to pest management, and contribute to addressing fundamental research questions in Lepidoptera.
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Nong W, Yu Y, Aase-Remedios ME, Xie Y, So WL, Li Y, Wong CF, Baril T, Law STS, Lai SY, et al (2022). Genome of the ramshorn snail Biomphalaria straminea-an obligate intermediate host of schistosomiasis.
Gigascience,
11Abstract:
Genome of the ramshorn snail Biomphalaria straminea-an obligate intermediate host of schistosomiasis.
BACKGROUND: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. FINDINGS: Using a combination of Illumina short-read, 10X Genomics linked-read, and Hi-C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. CONCLUSION: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.
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Author URL.
Doyle T, Jimenez-Guri E, Hawkes WLS, Massy R, Mantica F, Permanyer J, Cozzuto L, Hermoso Pulido T, Baril T, Hayward A, et al (2022). Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.
Mol Ecol,
31(16), 4332-4350.
Abstract:
Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.
Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.
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Castledine M, Sierocinski P, Inglis M, Kay S, Hayward A, Buckling A, Padfield D (2022). Greater Phage Genotypic Diversity Constrains Arms-Race Coevolution. Frontiers in Cellular and Infection Microbiology, 12
So WL, Nong W, Xie Y, Baril T, Ma H-Y, Qu Z, Haimovitz J, Swale T, Gaitan-Espitia JD, Lau KF, et al (2022). Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes.
Nat Commun,
13(1).
Abstract:
Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes.
Animals display a fascinating diversity of body plans. Correspondingly, genomic analyses have revealed dynamic evolution of gene gains and losses among animal lineages. Here we sequence six new myriapod genomes (three millipedes, three centipedes) at key phylogenetic positions within this major but understudied arthropod lineage. We combine these with existing genomic resources to conduct a comparative analysis across all available myriapod genomes. We find that millipedes generally have considerably smaller genomes than centipedes, with the repeatome being a major contributor to genome size, driven by independent large gains of transposons in three centipede species. In contrast to millipedes, centipedes gained a large number of gene families after the subphyla diverged, with gains contributing to sensory and locomotory adaptations that facilitated their ecological shift to predation. We identify distinct horizontal gene transfer (HGT) events from bacteria to millipedes and centipedes, with no identifiable HGTs shared among all myriapods. Loss of juvenile hormone O-methyltransferase, a key enzyme in catalysing sesquiterpenoid hormone production in arthropods, was also revealed in all millipede lineages. Our findings suggest that the rapid evolution of distinct genomic pathways in centipede and millipede lineages following their divergence from the myriapod ancestor, was shaped by differing ecological pressures.
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Jaitly R, Ehrnsten E, Hedlund J, Cant M, Lehmann P, Hayward A (2022). The evolution of predator avoidance in cephalopods: a case of brain over brawn?. Frontiers in Marine Science, 9
Lohse K, Hayward A, Vila R, programme WSITOL, collective WSISODP, collective TOLCI, Howe C, Consortium DTOL (2022). The genome sequence of the Adonis blue, Lysandra bellargus (Rottemburg, 1775). Wellcome Open Research, 7
Lohse K, Hayward A, Laetsch DR, Vila R, Lucek K (2022). The genome sequence of the Arran brown, Erebia ligea (Linnaeus, 1758). Wellcome Open Research, 7
Ebdon S, Mackintosh A, Lohse K, Hayward A, Arif S, Whitla R (2022). The genome sequence of the black-veined white butterfly, Aporia crataegi (Linnaeus, 1758). Wellcome Open Research, 7
Lohse K, Hayward A, Laetsch DR, Vila R, Yumnam T (2022). The genome sequence of the common yellow swallowtail, Papilio machaon (Linnaeus, 1758). Wellcome Open Research, 7
Hayward A, Vila R, Lohse K, Laetsch D, Darwin Tree of Life Barcoding collective, Wellcome Sanger Institute Tree of Life programme, Wellcome Sanger Institute Scientific Operations: DNA Pipelines collective, Tree of Life Core Informatics collective, Darwin Tree of Life Consortium (2022). The genome sequence of the grizzled skipper, Pyrgus malvae (Linnaeus, 1758).
Wellcome Open Res,
7Abstract:
The genome sequence of the grizzled skipper, Pyrgus malvae (Linnaeus, 1758).
We present a genome assembly from an individual male Pyrgus malvae (the grizzled skipper; Arthropoda; Insecta; Lepidoptera; Hesperiidae). The genome sequence is 725 megabases in span. The majority (99.97%) of the assembly is scaffolded into 31 chromosomal pseudomolecules, with the Z sex chromosome assembled.
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Author URL.
Lohse K, Vila R, Hayward A, Laetsch DR, Wahlberg N (2022). The genome sequence of the high brown fritillary, Fabriciana adippe (Dennis & Schiffermüller, 1775). Wellcome Open Research, 7
Mackintosh A, Laetsch DR, Baril T, Foster RG, Dincă V, Vila R, Hayward A, Lohse K (2022). The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.
G3 (Bethesda),
12(6).
Abstract:
The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.
The lesser marbled fritillary, Brenthis ino (Rottemburg, 1775), is a species of Palearctic butterfly. Male Brenthis ino individuals have been reported to have between 12 and 14 pairs of chromosomes, a much-reduced chromosome number than is typical in butterflies. Here, we present a chromosome-level genome assembly for Brenthis ino, as well as gene and transposable element annotations. The assembly is 411.8 Mb in length with a contig N50 of 9.6 Mb and a scaffold N50 of 29.5 Mb. We also show evidence that the male individual from which we generated HiC data was heterozygous for a neo-Z chromosome, consistent with inheriting 14 chromosomes from one parent and 13 from the other. This genome assembly will be a valuable resource for studying chromosome evolution in Lepidoptera, as well as for comparative and population genomics more generally.
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Vila R, Lohse K, Hayward A, Laetsch D, Lab NHMGA, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL, et al (2022). The genome sequence of the marbled white butterfly, Melanargia galathea (Linnaeus, 1758). Wellcome Open Research, 7
Mackintosh A, Laetsch DR, Baril T, Ebdon S, Jay P, Vila R, Hayward A, Lohse K (2022). The genome sequence of the scarce swallowtail, Iphiclides podalirius.
G3 (Bethesda),
12(9).
Abstract:
The genome sequence of the scarce swallowtail, Iphiclides podalirius.
The scarce swallowtail, Iphiclides podalirius (Linnaeus, 1758), is a species of butterfly in the family Papilionidae. Here, we present a chromosome-level genome assembly for Iphiclides podalirius as well as gene and transposable element annotations. We investigate how the density of genomic features differs between the 30 Iphiclides podalirius chromosomes. We find that shorter chromosomes have higher heterozygosity at four-fold-degenerate sites and a greater density of transposable elements. While the first result is an expected consequence of differences in recombination rate, the second suggests a counter-intuitive relationship between recombination and transposable element evolution. This high-quality genome assembly, the first for any species in the tribe Leptocircini, will be a valuable resource for population genomics in the genus Iphiclides and comparative genomics more generally.
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Author URL.
Hayward A, Lohse K, Laetsch DR, Vila R, programme WSITOL, collective WSISODP, collective TOLCI, Taluy E, Consortium DTOL (2022). The genome sequence of the silver-studded blue, Plebejus argus (Linnaeus, 1758). Wellcome Open Research, 7
Hayward A, Biscocho R (2022). The genome sequence of the small skipper, Thymelicus sylvestris (Poda, 1761). Wellcome Open Research, 7
Vila R, Lohse K, Hayward A, Laetsch DR, Wahlberg N (2022). The genome sequence of the white admiral, Limenitis camilla (Linnaeus, 1764). Wellcome Open Research, 7
Hayward A, Gilbert C (2022). Transposable elements.
Curr Biol,
32(17), R904-R909.
Abstract:
Transposable elements.
Transposable elements are known by many names, including 'transposons', 'interspersed repeats', 'selfish genetic elements', 'jumping genes', and 'parasitic DNA', but here we will refer to them simply as transposable elements. Many biologists will have heard of transposable elements and their ability to transpose (change position) within the genome. But fewer may be aware of their varied influences on host biology, including contributions to the evolution of diverse host traits such as internal gestation, memory, colouration, and adaptive immunity. Transposable elements are a near ubiquitous feature of eukaryotic genomes, and they often comprise a substantial proportion of total genomic content. Consequently, transposable element genes are considered among the most abundant coding sequences in nature. Recent advances in genome sequencing have ushered in a golden age for transposable-element research, providing opportunities to greatly improve our understanding of the effects of transposable elements on host evolution and disease. However, our ability to detect and analyse transposable elements still faces significant challenges, impairing efforts to decipher their evolution, characterise their diversity, and elucidate their myriad host influences. Below, we summarise key aspects of transposable element biology in eukaryotes and discuss major outstanding research questions.
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Hayward A, Poulin R, Nakagawa S (2021). A broadscale analysis of host-symbiont cophylogeny reveals the drivers of phylogenetic congruence.
ECOLOGY LETTERS,
24(8), 1681-1696.
Author URL.
Singh KS, Cordeiro EMG, Troczka BJ, Pym A, Mackisack J, Mathers TC, Duarte A, Legeai F, Robin S, Bielza P, et al (2021). Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae.
Commun Biol,
4(1).
Abstract:
Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae.
The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host-plant associations, uncovering the widespread co-option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.
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Nong W, Qu Z, Li Y, Barton-Owen T, Wong AYP, Yip HY, Lee HT, Narayana S, Baril T, Swale T, et al (2021). Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication.
Commun Biol,
4(1).
Abstract:
Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication.
Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7 Gb, N50 = 90.2 Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7 Gb, N50 = 109.7 Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD. Comparison of C. rotundicauda and T. tridentatus genomes from populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for improving our understanding of invertebrate WGD events on the evolutionary fates of genes and microRNAs, at both the individual and population level. We also provide improved genomic resources for horseshoe crabs, of applied value for breeding programs and conservation of this fascinating and unusual invertebrate lineage.
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Troczka BJ, Singh KS, Zimmer CT, Vontas J, Nauen R, Hayward A, Bass C (2021). Molecular innovations underlying resistance to nicotine and neonicotinoids in the aphid Myzus persicae.
Pest Manag Sci,
77(12), 5311-5320.
Abstract:
Molecular innovations underlying resistance to nicotine and neonicotinoids in the aphid Myzus persicae.
The green peach aphid, Myzus persicae, is a globally distributed highly damaging crop pest. This species has demonstrated an exceptional ability to evolve resistance to both synthetic insecticides used for control, and natural insecticides produced by certain plants as a chemical defense against insect attack. Here we review work characterizing the evolution of resistance in M. persicae to the natural insecticide nicotine and the structurally related class of synthetic neonicotinoid insecticides. We outline how research on this topic has provided insights into long-standing questions of both evolutionary and applied importance. These include questions pertaining to the origins of novel traits, the number and nature of mutational events or 'adaptive steps' underlying the evolution of new phenotypes, and whether host plant adaptations can be co-opted to confer resistance to synthetic insecticides. Finally, research on the molecular mechanisms underlying insecticide resistance in M. persicae has generated several outstanding questions on the genetic architecture of resistance to both natural and synthetic xenobiotics, and we conclude by identifying key knowledge gaps for future research. © 2021 the Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
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Blasco-Costa I, Hayward A, Poulin R, Balbuena JA (2021). Next-generation cophylogeny: unravelling eco-evolutionary processes.
Trends in Ecology and Evolution,
36(10), 907-918.
Abstract:
Next-generation cophylogeny: unravelling eco-evolutionary processes
A fundamental question in evolutionary biology is how microevolutionary processes translate into species diversification. Cophylogeny provides an appropriate framework to address this for symbiotic associations, but historically has been primarily limited to unveiling patterns. We argue that it is essential to integrate advances from ecology and evolutionary biology into cophylogeny, to gain greater mechanistic insights and transform cophylogeny into a platform to advance understanding of interspecific interactions and diversification more widely. We discuss key directions, such as incorporating trait reconstruction and considering multiple scales of network organization, and highlight recent developments for implementation. A new quantitative framework is proposed to allow integration of relevant information, such as quantitative traits and assessment of the contribution of individual mechanisms to cophylogenetic patterns.
Abstract.
Ebdon S, Laetsch DR, Dapporto L, Hayward A, Ritchie MG, Dincӑ V, Vila R, Lohse K (2021). The Pleistocene species pump past its prime: Evidence from European butterfly sister species.
Mol Ecol,
30(14), 3575-3589.
Abstract:
The Pleistocene species pump past its prime: Evidence from European butterfly sister species.
The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. While it is clear that the contact zones that have been described for many sister taxa are secondary and have formed in the current interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here, we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases, species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post-divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the initial stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial divergence and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact zone pairs.
Abstract.
Author URL.
Vila R, Hayward A, Lohse K, Wright C, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL (2021). The genome sequence of the Glanville fritillary, Melitaea cinxia (Linnaeus, 1758). Wellcome Open Research, 6
Ebdon S, Mackintosh A, Hayward A, Wotton K, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL (2021). The genome sequence of the clouded yellow, Colias crocea (Geoffroy, 1785). Wellcome Open Research, 6
Hayward A, Vila R, Laetsch DR, Lohse K, Baril T (2021). The genome sequence of the heath fritillary, Melitaea athalia (Rottemburg, 1775).
Wellcome Open Research,
6, 304-304.
Abstract:
The genome sequence of the heath fritillary, Melitaea athalia (Rottemburg, 1775)
We present a genome assembly from an individual female Melitaea athalia (also known as Mellicta athalia; the heath fritillary; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 610 megabases in span. In total, 99.98% of the assembly is scaffolded into 32 chromosomal pseudomolecules, with the W and Z sex chromosome assembled. Gene annotation of this assembly on Ensembl has identified 12,824 protein coding genes.
Abstract.
Hayward A, Wright C, Darwin Tree of Life Barcoding collective, Wellcome Sanger Institute Tree of Life programme, Wellcome Sanger Institute Scientific Operations: DNA Pipelines collective, Tree of Life Core Informatics collective, Darwin Tree of Life Consortium (2021). The genome sequence of the holly blue, Celastrina argiolus (Linnaeus, 1758).
Wellcome Open Res,
6Abstract:
The genome sequence of the holly blue, Celastrina argiolus (Linnaeus, 1758).
We present a genome assembly from an individual male Celastrina argiolus) (the holly blue; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequence is 499 megabases in span. The majority (99.99%) of the assembly is scaffolded into 26 chromosomal pseudomolecules, with the Z sex chromosome assembled. Gene annotation of this assembly on Ensembl has identified 12,199 protein coding genes.
Abstract.
Author URL.
Lohse K, Hayward A, Ebdon S (2021). The genome sequences of the male and female green-veined white, Pieris napi (Linnaeus, 1758).
Wellcome Open Research,
6, 288-288.
Abstract:
The genome sequences of the male and female green-veined white, Pieris napi (Linnaeus, 1758)
We present genome assemblies from a male and female Pieris napi (the green-veined white; Arthropoda; Insecta; Lepidoptera; Pieridae). The genome sequences of the male and female are 320 and 319 megabases in span, respectively. The majority of the assembly (99.79% of the male assembly, 99.88% of the female) is scaffolded into 24 autosomal pseudomolecules, with the Z sex chromosome assembled for the male and Z and W chromosomes assembled for the female. Gene annotation of the male assembly on Ensembl has identified 13,221 protein coding genes.
Abstract.
Panini M, Chiesa O, Troczka BJ, Mallott M, Manicardi GC, Cassanelli S, Cominelli F, Hayward A, Mazzoni E, Bass C, et al (2021). Transposon-mediated insertional mutagenesis unmasks recessive insecticide resistance in the aphid Myzus persicae.
Proc Natl Acad Sci U S A,
118(23).
Abstract:
Transposon-mediated insertional mutagenesis unmasks recessive insecticide resistance in the aphid Myzus persicae.
The evolution of resistance to insecticides threatens the sustainable control of many of the world's most damaging insect crop pests and disease vectors. To effectively combat resistance, it is important to understand its underlying genetic architecture, including the type and number of genetic variants affecting resistance and their interactions with each other and the environment. While significant progress has been made in characterizing the individual genes or mutations leading to resistance, our understanding of how genetic variants interact to influence its phenotypic expression remains poor. Here, we uncover a mechanism of insecticide resistance resulting from transposon-mediated insertional mutagenesis of a genetically dominant but insecticide-susceptible allele that enables the adaptive potential of a previously unavailable recessive resistance allele to be unlocked. Specifically, we identify clones of the aphid pest Myzus persicae that carry a resistant allele of the essential voltage-gated sodium channel (VGSC) gene with the recessive M918T and L1014F resistance mutations, in combination with an allele lacking these mutations but carrying a Mutator-like element transposon insertion that disrupts the coding sequence of the VGSC. This results in the down-regulation of the dominant susceptible allele and monoallelic expression of the recessive resistant allele, rendering the clones resistant to the insecticide bifenthrin. These findings are a powerful example of how transposable elements can provide a source of evolutionary potential that can be revealed by environmental and genetic perturbation, with applied implications for the control of highly damaging insect pests.
Abstract.
Author URL.
Nong W, Law STS, Wong AYP, Baril T, Swale T, Chu LM, Hayward A, Lau DTW, Hui JHL (2020). Chromosomal‐level reference genome of the incense tree. <i>Aquilaria sinensis</i>. Molecular Ecology Resources, 20(4), 971-979.
Qu Z, Nong W, Yu Y, Baril T, Yip HY, Hayward A, Hui JHL (2020). Genome of the four-finger threadfin Eleutheronema tetradactylum (Perciforms: Polynemidae).
BMC Genomics,
21(1).
Abstract:
Genome of the four-finger threadfin Eleutheronema tetradactylum (Perciforms: Polynemidae)
Background: Teleost fish play important roles in aquatic ecosystems and aquaculture. Threadfins (Perciformes: Polynemidae) show a range of interesting biology, and are of considerable importance for both wild fisheries and aquaculture. Additionally, the four-finger threadfin Eleutheronema tetradactylum is of conservation relevance since its populations are considered to be in rapid decline and it is classified as endangered. However, no genomic resources are currently available for the threadfin family Polynemidae. Results: We sequenced and assembled the first threadfin fish genome, the four-finger threadfin E. tetradactylum. We provide a genome assembly for E. tetradactylum with high contiguity (scaffold N50 = 56.3 kb) and high BUSCO completeness at 96.5%. The assembled genome size of E. tetradactylum is just 610.5 Mb, making it the second smallest perciform genome assembled to date. Just 9.07–10.91% of the genome sequence was found to consist of repetitive elements (standard RepeatMasker analysis vs custom analysis), making this the lowest repeat content identified to date for any perciform fish. A total of 37,683 protein-coding genes were annotated, and we include analyses of developmental transcription factors, including the Hox, ParaHox, and Sox families. MicroRNA genes were also annotated and compared with other chordate lineages, elucidating the gains and losses of chordate microRNAs. Conclusions: the four-finger threadfin E. tetradactylum genome presented here represents the first available genome sequence for the ecologically, biologically, and commercially important clade of threadfin fish. Our findings provide a useful genomic resource for future research into the interesting biology and evolution of this valuable group of food fish.
Abstract.
Qu Z, Nong W, So WL, Barton-Owen T, Li Y, Leung TCN, Li C, Baril T, Wong AYP, Swale T, et al (2020). Millipede genomes reveal unique adaptations during myriapod evolution.
PLoS Biol,
18(9).
Abstract:
Millipede genomes reveal unique adaptations during myriapod evolution.
The Myriapoda, composed of millipedes and centipedes, is a fascinating but poorly understood branch of life, including species with a highly unusual body plan and a range of unique adaptations to their environment. Here, we sequenced and assembled 2 chromosomal-level genomes of the millipedes Helicorthomorpha holstii (assembly size = 182 Mb; shortest scaffold/contig length needed to cover 50% of the genome [N50] = 18.11 Mb mainly on 8 pseudomolecules) and Trigoniulus corallinus (assembly size = 449 Mb, N50 = 26.78 Mb mainly on 17 pseudomolecules). Unique genomic features, patterns of gene regulation, and defence systems in millipedes, not observed in other arthropods, are revealed. Both repeat content and intron size are major contributors to the observed differences in millipede genome size. Tight Hox and the first loose ecdysozoan ParaHox homeobox clusters are identified, and a myriapod-specific genomic rearrangement including Hox3 is also observed. The Argonaute (AGO) proteins for loading small RNAs are duplicated in both millipedes, but unlike in insects, an AGO duplicate has become a pseudogene. Evidence of post-transcriptional modification in small RNAs-including species-specific microRNA arm switching-providing differential gene regulation is also obtained. Millipedes possesses a unique ozadene defensive gland unlike the venomous forcipules found in centipedes. We identify sets of genes associated with the ozadene that play roles in chemical defence as well as antimicrobial activity. Macro-synteny analyses revealed highly conserved genomic blocks between the 2 millipedes and deuterostomes. Collectively, our analyses of millipede genomes reveal that a series of unique adaptations have occurred in this major lineage of arthropod diversity. The 2 high-quality millipede genomes provided here shed new light on the conserved and lineage-specific features of millipedes and centipedes. These findings demonstrate the importance of the consideration of both centipede and millipede genomes-and in particular the reconstruction of the myriapod ancestral situation-for future research to improve understanding of arthropod evolution, and animal evolutionary genomics more widely.
Abstract.
Author URL.
Hedlund J, Ehrnsten E, Hayward C, Lehmann P, Hayward A (2020). New records of the Paleotropical migrant <i>Hemianax ephippiger</i> in the Caribbean and a review of its status in the Neotropics. International Journal of Odonatology, 23(4), 315-325.
Dupeyron M, Baril T, Bass C, Hayward A (2020). Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements.
Mob DNA,
11Abstract:
Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements.
BACKGROUND: Tc1/mariner transposons are widespread DNA transposable elements (TEs) that have made important contributions to the evolution of host genomic complexity in metazoans. However, the evolution and diversity of the Tc1/mariner superfamily remains poorly understood. Following recent developments in genome sequencing and the availability of a wealth of new genomes, Tc1/mariner TEs have been identified in many new taxa across the eukaryotic tree of life. To date, the majority of studies focussing on Tc1/mariner elements have considered only a single host lineage or just a small number of host lineages. Thus, much remains to be learnt about the evolution of Tc1/mariner TEs by performing analyses that consider elements that originate from across host diversity. RESULTS: We mined the non-redundant database of NCBI using BLASTp searches, with transposase sequences from a diverse set of reference Tc1/mariner elements as queries. A total of 5158 Tc1/mariner elements were retrieved and used to reconstruct evolutionary relationships within the superfamily. The resulting phylogeny is well resolved and includes several new groups of Tc1/mariner elements. In particular, we identify a new family of plant-genome restricted Tc1/mariner elements, which we call PlantMar. We also show that the pogo family is much larger and more diverse than previously appreciated, and we review evidence for a potential revision of its status to become a separate superfamily. CONCLUSIONS: Our study provides an overview of Tc1-mariner phylogeny and summarises the impressive diversity of Tc1-mariner TEs among sequenced eukaryotes. Tc1/mariner TEs are successful in a wide range of eukaryotes, especially unikonts (the taxonomic supergroup containing Amoebozoa, Opisthokonta, Breviatea, and Apusomonadida). In particular, ecdysozoa, and especially arthropods, emerge as important hosts for Tc1/mariner elements (except the PlantMar family). Meanwhile, the pogo family, which is by far the largest Tc1/mariner family, also includes many elements from fungal and chordate genomes. Moreover, there is evidence of the repeated exaptation of pogo elements in vertebrates, including humans, in addition to the well-known example of CENP-B. Collectively, our findings provide a considerable advancement in understanding of Tc1/mariner elements, and more generally they suggest that much work remains to improve understanding of the diversity and evolution of DNA TEs.
Abstract.
Author URL.
Li Y, Nong W, Baril T, Yip HY, Swale T, Hayward A, Ferrier DEK, Hui JHL (2020). Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome.
BMC Genomics,
21(1).
Abstract:
Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome
Background: Homeobox-containing genes encode crucial transcription factors involved in animal, plant and fungal development, and changes to homeobox genes have been linked to the evolution of novel body plans and morphologies. In animals, some homeobox genes are clustered together in the genome, either as remnants from ancestral genomic arrangements, or due to coordinated gene regulation. Consequently, analyses of homeobox gene organization across animal phylogeny provide important insights into the evolution of genome organization and developmental gene control, and their interaction. However, homeobox gene organization remains to be fully elucidated in several key animal ancestors, including those of molluscs, lophotrochozoans and bilaterians. Results: Here, we present a high-quality chromosome-level genome assembly of the Hong Kong oyster, Magallana hongkongensis (2n = 20), for which 93.2% of the genomic sequences are contained on 10 pseudomolecules (~ 758 Mb, scaffold N50 = 72.3 Mb). Our genome assembly was scaffolded using Hi-C reads, facilitating a larger scaffold size compared to the recently published M. hongkongensis genome of Peng et al. (Mol Ecol Resources, 2020), which was scaffolded using the Crassostrea gigas assembly. A total of 46,963 predicted gene models (45,308 protein coding genes) were incorporated in our genome, and genome completeness estimated by BUSCO was 94.6%. Homeobox gene linkages were analysed in detail relative to available data for other mollusc lineages. Conclusions: the analyses performed in this study and the accompanying genome sequence provide important genetic resources for this economically and culturally valuable oyster species, and offer a platform to improve understanding of animal biology and evolution more generally. Transposable element content is comparable to that found in other mollusc species, contrary to the conclusion of another recent analysis. Also, our chromosome-level assembly allows the inference of ancient gene linkages (synteny) for the homeobox-containing genes, even though a number of the homeobox gene clusters, like the Hox/ParaHox clusters, are undergoing dispersal in molluscs such as this oyster.
Abstract.
Singh KS, Troczka BJ, Duarte A, Balabanidou V, Trissi N, Carabajal Paladino LZ, Nguyen P, Zimmer CT, Papapostolou KM, Randall E, et al (2020). The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses.
Science Advances,
6(19).
Abstract:
The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses
A complex series of mutational events protected a mutualistic symbiosis during the shift of an insect to a toxic host plant.
Abstract.
Tsuboi M, Kotrschal A, Hayward A, Buechel SD, Zidar J, Løvlie H, Kolm N (2016). Evolution of brain-body allometry in Lake Tanganyika cichlids. Evolution, 70(7), 1559-1568.
Ács Z, Hayward A, Sugár L (2016). Genetic diversity and population genetics of large lungworms (Dictyocaulus, Nematoda) in wild deer in Hungary.
Parasitol Res,
115(9), 3295-3312.
Abstract:
Genetic diversity and population genetics of large lungworms (Dictyocaulus, Nematoda) in wild deer in Hungary.
Dictyocaulus nematode worms live as parasites in the lower airways of ungulates and can cause significant disease in both wild and farmed hosts. This study represents the first population genetic analysis of large lungworms in wildlife. Specifically, we quantify genetic variation in Dictyocaulus lungworms from wild deer (red deer, fallow deer and roe deer) in Hungary, based on mitochondrial cytochrome c oxidase subunit 1 (cox1) sequence data, using population genetic and phylogenetic analyses. The studied Dictyocaulus taxa display considerable genetic diversity. At least one cryptic species and a new parasite-host relationship are revealed by our molecular study. Population genetic analyses for Dictyocaulus eckerti revealed high gene flow amongst weakly structured spatial populations that utilise the three host deer species considered here. Our results suggest that D. eckerti is a widespread generalist parasite in ungulates, with a diverse genetic backround and high evolutionary potential. In contrast, evidence of cryptic genetic structure at regional geographic scales was observed for Dictyocaulus capreolus, which infects just one host species, suggesting it is a specialist within the studied area. D. capreolus displayed lower genetic diversity overall, with only moderate gene flow compared to the closely related D. eckerti. We suggest that the differing vagility and dispersal behaviour of hosts are important contributing factors to the population structure of lungworms, and possibly other nematode parasites with single-host life cycles. Our findings are of relevance for the management of lungworms in deer farms and wild deer populations.
Abstract.
Author URL.
Mcmahon DP, Hayward A (2016). Why grow up? a perspective on insect strategies to avoid metamorphosis.
Ecological Entomology,
41(5), 505-515.
Abstract:
Why grow up? a perspective on insect strategies to avoid metamorphosis
1. Insects with complete metamorphosis (holometaboly) are extremely successful, constituting over 60% of all described animal species. Complete metamorphosis confers significant advantages because it enables organisms to optimise life-history components through temporal partitioning, and thereby to exploit multiple ecological niches. Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis. 2. In this review, we discuss different strategies that have evolved that result in the loss of complete metamorphosis (type I and type II paedomorphosis). In addition, the ecological pressures and developmental modifications that facilitate this avoidance are considered, as well as the importance of life cycle complexity in life-history evolution. 3. Interestingly, only female holometabolous insects have entirely avoided complete metamorphosis, and it is always the ancestrally juvenile morphology that is retained. These findings point to a strong sex-biased trade-off between investment in reproduction and development. While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described. 4. Thus, complete metamorphosis, which originated only once in insects, appears to have been almost fully retained. This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.
Abstract.
Hayward A, Katzourakis A (2015). Endogenous retroviruses. Current Biology, 25(15), R644-R646.
Kenny NJ, Sin YW, Hayward A, Paps J, Chu KH, Hui JHL (2015). The phylogenetic utility and functional constraint of microRNA flanking sequences.
Proceedings of the Royal Society B: Biological Sciences,
282(1803), 20142983-20142983.
Abstract:
The phylogenetic utility and functional constraint of microRNA flanking sequences
. MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transcriptional regulation of gene expression. miRNA genes have been posited as highly conserved in the clades in which they exist. Consequently, miRNAs have been used as rare genome change characters to estimate phylogeny by tracking their gain and loss. However, their short length (21–23 bp) has limited their perceived utility in sequenced-based phylogenetic inference. Here, using reference taxa with established phylogenetic relationships, we demonstrate that miRNA sequences are of high utility in quantitative, rather than in qualitative, phylogenetic analysis. The clear orthology among miRNA genes from different species makes it straightforward to identify and align these sequences from even fragmentary datasets. We also identify significant sequence conservation in the regions directly flanking miRNA genes, and show that this too is of utility in phylogenetic analysis, as well as highlighting conserved regions that will be of interest to other fields. Employing miRNA sequences from 12 sequenced drosophilid genomes, together with a
. Tribolium castaneum
. outgroup, we demonstrate that this approach is robust using Bayesian and maximum-likelihood methods. The utility of these characters is further demonstrated in the rhabditid nematodes and primates. As next-generation sequencing makes it more cost-effective to sequence genomes and small RNA libraries, this methodology provides an alternative data source for phylogenetic analysis. The approach allows rapid resolution of relationships between both closely related and rapidly evolving species, and provides an additional tool for investigation of relationships within the tree of life.
.
Abstract.
Tsuboi M, Husby A, Kotrschal A, Hayward A, Buechel SD, Zidar J, Løvlie H, Kolm N (2014). Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids. Evolution, 69(1), 190-200.
Erezyilmaz DF, Hayward A, Huang Y, Paps J, Acs Z, Delgado JA, Collantes F, Kathirithamby J (2014). Expression of the Pupal Determinant broad during Metamorphic and Neotenic Development of the Strepsipteran Xenos vesparum Rossi. PLoS ONE, 9(4), e93614-e93614.
Hayward A, Cornwallis CK, Jern P (2014). Pan-vertebrate comparative genomics unmasks retrovirus macroevolution.
Proceedings of the National Academy of Sciences,
112(2), 464-469.
Abstract:
Pan-vertebrate comparative genomics unmasks retrovirus macroevolution
Significance
. For millions of years retroviruses, such as HIV in humans, have attacked vertebrates. Occasionally retroviruses infiltrate germ cells, incorporate themselves into the host’s genome, and transmit vertically to the host’s offspring as endogenous retroviruses (ERVs). Consequently, ERVs make up large portions of vertebrate genomes and represent a record of past host–retrovirus interactions. We developed pan-vertebrate ERV analyses to provide an overview of host–retrovirus interactions, generating insights into retroviral evolution, diversity, host-switching, and the factors influencing retroviral transmission. Astoundingly, we found over 36,000 ERV lineages across our sample of vertebrate diversity. The results provide knowledge about host–retrovirus coevolution, suggesting an unprecedented ability of retroviruses to switch between distantly related vertebrates and implying existence of additional, yet unidentified retroviruses.
Abstract.
Hayward A, Grabherr M, Jern P (2013). Broad-scale phylogenomics provides insights into retrovirus–host evolution.
Proceedings of the National Academy of Sciences,
110(50), 20146-20151.
Abstract:
Broad-scale phylogenomics provides insights into retrovirus–host evolution
Significance
. Retroviruses, such as HIV, are important pathogens of vertebrates, including humans. They are capable of crossing species barriers to infect new hosts, but knowledge about the evolutionary history of retroviruses is limited. However, genomic traces of past retrovirus activities known as “endogenous retroviruses” can be screened from sequenced genomes and analyzed to improve understanding of retrovirus evolution. Here we use a unique approach to address the evolution of one group of retroviruses in a screen of 60 diverse vertebrate host genomes. We find evidence of rampant host-switching across mammalian orders by members of this group throughout their evolutionary history. We also find evidence that the spread of infective retroviruses from this group may be facilitated by rats.
Abstract.
Hayward A, Ghazal A, Andersson G, Andersson L, Jern P (2013). ZBED Evolution: Repeated Utilization of DNA Transposons as Regulators of Diverse Host Functions. PLoS ONE, 8(3), e59940-e59940.
Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens H-J, et al (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491(7424), 393-398.
HAYWARD A, MCMAHON DP, KATHIRITHAMBY J (2011). Cryptic diversity and female host specificity in a parasitoid where the sexes utilize hosts from separate orders. Molecular Ecology, 20(7), 1508-1528.
McMahon DP, Hayward A, Kathirithamby J (2011). Strepsiptera. Current Biology, 21(8), R271-R272.
McMahon DP, Hayward A, Kathirithamby J (2011). The First Molecular Phylogeny of Strepsiptera (Insecta) Reveals an Early Burst of Molecular Evolution Correlated with the Transition to Endoparasitism. PLoS ONE, 6(6), e21206-e21206.
Nicholls JA, Fuentes-Utrilla P, Hayward A, Melika G, Csóka G, Nieves-Aldrey J-L, Pujade-Villar J, Tavakoli M, Schönrogge K, Stone GN, et al (2010). Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts.
BMC Evol Biol,
10Abstract:
Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts.
BACKGROUND: Biological invasions provide a window on the process of community assembly. In particular, tracking natural enemy recruitment to invading hosts can reveal the relative roles of co-evolution (including local adaptation) and ecological sorting. We use molecular data to examine colonisation of northern Europe by the parasitoid Megastigmus stigmatizans following invasions of its herbivorous oak gallwasp hosts from the Balkans. Local host adaptation predicts that invading gallwasp populations will have been tracked primarily by sympatric Balkan populations of M. stigmatizans (Host Pursuit Hypothesis). Alternatively, ecological sorting allows parasitoid recruitment from geographically distinct populations with no recent experience of the invading hosts (Host Shift Hypothesis). Finally, we test for long-term persistence of parasitoids introduced via human trade of their hosts' galls (Introduction Hypothesis). RESULTS: Polymorphism diagnostic of different southern refugial regions was present in both mitochondrial and nuclear microsatellite markers, allowing us to identify the origins of northern European invaded range M. stigmatizans populations. As with their hosts, some invaded range populations showed genetic variation diagnostic of Balkan sources, supporting the Host Pursuit Hypothesis. In contrast, other invading populations had an Iberian origin, unlike their hosts in northern Europe, supporting the Host Shift Hypothesis. Finally, both British and Italian M. stigmatizans populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources. CONCLUSIONS: These data reveal the continental scale of multi-trophic impacts of anthropogenic disturbance and highlight the fact that herbivores and their natural enemies may face very different constraints on range expansion. The ability of natural enemies to exploit ecologically-similar hosts with which they have had no historical association supports a major role for ecological sorting processes in the recent assembly of these communities. The multitude of origins of invading natural enemy populations in this study emphasises the diversity of mechanisms requiring consideration when predicting consequences of other biological invasions or biological control introductions.
Abstract.
Author URL.
Hayward A, Takahashi T, Bendena WG, Tobe SS, Hui JHL (2010). Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in metazoans. FEBS Letters, 584(6), 1273-1278.
Nicholls JA, Preuss S, Hayward A, Melika G, Csóka G, Nieves-Aldrey J-L, Askew RR, Tavakoli M, Schönrogge K, Stone GN, et al (2010). Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes.
Mol Ecol,
19(3), 592-609.
Abstract:
Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes.
Little is known about the evolutionary history of most complex multi-trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host-tracking) or later divergence in higher trophic levels (Delayed Host-tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species-level divergence at both 8-9 and 4-5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host-tracking Hypothesis for community evolution.
Abstract.
Author URL.
HAYWARD A (2010). Cryptic diversity and patterns of host specificity in trematode flatworms. Molecular Ecology, 19(13), 2602-2604.
Hui JHL, Hayward A, Bendena WG, Takahashi T, Tobe SS (2010). Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects. Peptides, 31(3), 451-455.
Ács Z, Challis RJ, Bihari P, Blaxter M, Hayward A, Melika G, Csóka G, Pénzes Z, Pujade-Villar J, Nieves-Aldrey J-L, et al (2010). Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic. Molecular Phylogenetics and Evolution, 55(1), 210-225.
KATHIRITHAMBY J, HAYWARD A, MCMAHON DP, FERREIRA RS, ANDREAZZE R, ALMEIDA ANDRADE HTD, FRESNEAU D (2009). Conspecifics of a heterotrophic heteronomous species of Strepsiptera (Insecta) are matched by molecular characterization. Systematic Entomology, 35(2), 234-242.
McMahon DP, Hayward A, Kathirithamby J (2009). The mitochondrial genome of the 'twisted-wing parasite' Mengenilla australiensis (Insecta, Strepsiptera): a comparative study. BMC Genomics, 10(1), 603-603.
STONE GN, ATKINSON RJ, ROKAS A, ALDREY J-LN, MELIKA G, Ács ZOLTAN, CSÓKA G, HAYWARD A, BAILEY R, BUCKEE C, et al (2007). Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps. Molecular Ecology, 17(2), 652-665.
STONE GN, CHALLIS RJ, ATKINSON RJ, CSÓKA G, HAYWARD A, MELIKA G, MUTUN S, PREUSS S, ROKAS A, SADEGHI E, et al (2007). The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari. Molecular Ecology, 16(13), 2768-2781.
HAYWARD A, STONE GN (2005). Comparative phylogeography across two trophic levels: the oak gall wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology, 15(2), 479-489.
Hayward A, Stone GN (2005). Oak gall wasp communities: Evolution and ecology. Basic and Applied Ecology, 6(5), 435-443.
Publications by year
In Press
Hayward A, Baril T (In Press). A draft genome sequence of the elusive giant squid, Architeuthis dux. GigaScience
Baril T, Imrie RM, Hayward A (In Press). Earl Grey: a fully automated user-friendly transposable element annotation and analysis pipeline.
Abstract:
Earl Grey: a fully automated user-friendly transposable element annotation and analysis pipeline
ABSTRACTBackgroundTransposable elements (TEs) are found in nearly all eukaryotic genomes and are implicated in a range of evolutionary processes. Despite considerable research attention on TEs, their annotation and characterisation remain challenging, particularly for non-specialists. Current methods of automated TE annotation are subject to several issues that can reduce their overall quality: (i) fragmented and overlapping TE annotations may lead to erroneous estimates of TE count and coverage; (ii) repeat models may represent small proportions of their total length, where 5’ and 3’ regions are poorly captured; (iii) resultant libraries may contain redundancy, with the same TE family represented more than once. Existing pipelines can also be challenging to install, run, and extract data from. To address these issues, we present Earl Grey: a fully automated transposable element annotation pipeline designed for the user-friendly curation and annotation of TEs in eukaryotic genome assemblies.ResultsUsing a simulated genome, three model genome assemblies, and three non-model genome assemblies, Earl Grey outperforms current widely used TE annotation methodologies in ameliorating the issues mentioned above by producing longer TE consensus sequences in non-redundant TE libraries, which are then used to produce less fragmented TE annotations without the presence of overlaps. Earl Grey scores highly in benchmarking for TE annotation (MCC: 0.99) and classification (97% correctly classified) in comparison to existing software.ConclusionsEarl Grey provides a comprehensive and fully automated TE annotation toolkit that provides researchers with paper-ready summary figures and outputs in standard formats compatible with other bioinformatics tools. Earl Grey has a modular format, with great scope for the inclusion of additional modules focussed on further quality control aspects and tailored analyses in future releases.
Abstract.
Baril T, Imrie RM, Hayward A (In Press). Earl Grey: a fully automated user-friendly transposable element annotation and analysis pipeline.
Abstract:
Earl Grey: a fully automated user-friendly transposable element annotation and analysis pipeline
Abstract
. Background
Transposable elements (TEs) are found in nearly all eukaryotic genomes and are implicated in a range of evolutionary processes. Despite considerable research attention on TEs, their annotation and characterisation remain challenging, particularly for non-specialists. Current methods of automated TE annotation are subject to several issues that can reduce their overall quality: (i) fragmented and overlapping TE annotations may lead to erroneous estimates of TE count and coverage; (ii) repeat models may represent small proportions of their total length, where 5’ and 3’ regions are poorly captured; (iii) resultant libraries may contain redundancy, with the same TE family represented more than once. Existing pipelines can also be challenging to install, run, and extract data from. To address these issues, we present Earl Grey: a fully automated transposable element annotation pipeline designed for the user-friendly curation and annotation of TEs in eukaryotic genome assemblies.
Results
Using a simulated genome, three model genome assemblies, and three non-model genome assemblies, Earl Grey outperforms current widely used TE annotation methodologies in ameliorating the issues mentioned above by producing longer TE consensus sequences in non-redundant TE libraries, which are then used to produce less fragmented TE annotations without the presence of overlaps. Earl Grey scores highly in benchmarking for TE annotation (MCC: 0.99) and classification (97% correctly classified) in comparison to existing software.
Conclusions
Earl Grey provides a comprehensive and fully automated TE annotation toolkit that provides researchers with paper-ready summary figures and outputs in standard formats compatible with other bioinformatics tools. Earl Grey has a modular format, with great scope for the inclusion of additional modules focussed on further quality control aspects and tailored analyses in future releases.
Abstract.
Dupeyron M, Singh K, Bass C, Hayward A (In Press). Evolution of Mutator transposable elements across eukaryotic diversity. Mobile DNA
Hayward A, Kolm N, Kotrschal A, Løvlie H, Cornwallis CK, Zidar J, Buechel SD, Tsuboi M (In Press). Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids. Journal of Evolutionary Biology
Baril T, Hayward A (In Press). Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, <i>Danaus plexippus</i>.
Abstract:
Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, Danaus plexippus
AbstractBackgroundLepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly is available for the monarch butterfly (Danaus plexippus), but it lacks an in-depth transposable element (TE) annotation, presenting an opportunity to explore monarch TE dynamics and the impact of TEs on shaping the monarch genome.ResultsWe find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1- 2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes.ConclusionsWe provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.
Abstract.
Baril T, Hayward A (In Press). Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, Danaus plexippus.
Mobile DNAAbstract:
Migrators Within Migrators: Exploring Transposable Element Dynamics in the Monarch Butterfly, Danaus plexippus
Background
Lepidoptera (butterflies and moths) are an important model system in ecology and evolution. A high-quality chromosomal genome assembly is available for the monarch butterfly (Danaus plexippus), but it lacks an in-depth transposable element (TE) annotation, presenting an opportunity to explore monarch TE dynamics and the impact of TEs on shaping the monarch genome.
Results
We find 6.21% of the monarch genome is comprised of TEs, a reduction of 6.85% compared to the original TE annotation performed on the draft genome assembly. Monarch TE content is low compared to two closely related species with available genomes, Danaus chrysippus (33.97% TE) and Danaus melanippus (11.87% TE). The biggest TE contributions to genome size in the monarch are LINEs and Penelope-like elements, and three newly identified families, r2-hero_dPle (LINE), penelope-1_dPle (Penelope-like), and hase2-1_dPle (SINE), collectively contribute 34.92% of total TE content. We find evidence of recent TE activity, with two novel Tc1 families rapidly expanding over recent timescales (tc1-1_dPle, tc1- 2_dPle). LINE fragments show signatures of genomic deletions indicating a high rate of TE turnover. We investigate associations between TEs and wing colouration and immune genes and identify a three-fold increase in TE content around immune genes compared to other host genes.
Conclusions
We provide a detailed TE annotation and analysis for the monarch genome, revealing a considerably smaller TE contribution to genome content compared to two closely related Danaus species with available genome assemblies. We identify highly successful novel DNA TE families rapidly expanding over recent timescales, and ongoing signatures of both TE expansion and removal highlight the dynamic nature of repeat content in the monarch genome. Our findings also suggest that insect immune genes are promising candidates for future interrogation of TE-mediated host adaptation.
Abstract.
Qu Z, Nong W, So WL, Barton-Owen T, Li Y, Li C, Leung TCN, Baril T, Wong AYP, Swale T, et al (In Press). Millipede genomes reveal unique adaptation of genes and microRNAs during myriapod evolution.
Abstract:
Millipede genomes reveal unique adaptation of genes and microRNAs during myriapod evolution
AbstractThe Myriapoda including millipedes and centipedes is of major importance in terrestrial ecology and nutrient recycling. Here, we sequenced and assembled two chromosomal-scale genomes of millipedes Helicorthomorpha holstii (182 Mb, N50 18.11 Mb mainly on 8 pseudomolecules) and Trigoniulus corallinus (449 Mb, N50 26.78 Mb mainly on 15 pseudomolecules). Unique defense systems, genomic features, and patterns of gene regulation in millipedes, not observed in other arthropods, are revealed. Millipedes possesses a unique ozadene defensive gland unlike the venomous forcipules in centipedes. Sets of genes associated with anti-microbial activity are identified with proteomics, suggesting that the ozadene gland is not primarily an antipredator adaptation (at least in T. corallinus). Macro-synteny analyses revealed highly conserved genomic blocks between centipede and the two millipedes. Tight Hox and the first loose ecdysozoan ParaHox homeobox clusters are identified, and a myriapod-specific genomic rearrangement including Hox3 is also observed. The Argonaute proteins for loading small RNAs are duplicated in both millipedes, but unlike insects, an argonaute duplicate has become a pseudogene. Evidence of post-transcriptional modification in small RNAs, including species-specific microRNA arm switching that provide differential gene regulation is also obtained. Millipede genomes reveal a series of unique genomic adaptations and microRNA regulation mechanisms have occurred in this major lineage of arthropod diversity. Collectively, the two millipede genomes shed new light on this fascinating but poorly understood branch of life, with a highly unusual body plan and novel adaptations to their environment.
Abstract.
Hayward A (In Press). Origin of the Retroviruses: when, where, and how?.
Current Opinion in VirologyAbstract:
Origin of the Retroviruses: when, where, and how?
Retroviruses are a virus family of considerable medical and veterinary importance. Additionally, it is now clear that endogenous retroviruses (ERVs) comprise significant portions of vertebrate genomes. Until recently, very little was known about the deep evolutionary origins of retroviruses. However, advances in genomics and informatics have opened the way for great strides in understanding. Recent research employing a wide variety of bioinformatic approaches has demonstrated that retroviruses evolved during the early Palaeozoic Era, between 460-550 million years ago, providing the oldest inferred date estimate for any virus group. This finding presents an important framework to investigate the evolutionary transitions that led to the emergence of the retroviruses, offering potential insights into the infectious origins of a major group of pathogenic viruses.
Abstract.
Mackintosh A, Laetsch D, Hayward A, Charlesworth B, Waterfall M, Vila R, Lohse K (In Press). The determinants of genetic diversity in butterflies. Nature Communications
2023
Brekke TD, Papadopulos AST, Julià E, Fornas O, Fu B, Yang F, de la Fuente R, Page J, Baril T, Hayward A, et al (2023). A new chromosome-assigned Mongolian gerbil genome allows characterization of complete centromeres and a fully heterochromatic chromosome.
Mol Biol EvolAbstract:
A new chromosome-assigned Mongolian gerbil genome allows characterization of complete centromeres and a fully heterochromatic chromosome.
Chromosome-scale genome assemblies based on ultra-long read sequencing technologies are able to illuminate previously intractable aspects of genome biology such as fine-scale centromere structure and large-scale variation in genome features such as heterochromatin, GC content, recombination rate, and gene content. We present here a new chromosome-scale genome of the Mongolian gerbil (Meriones unguiculatus) which includes the complete sequence of all centromeres. Gerbils are thus the one of the first vertebrates to have their centromeres completely sequenced. Gerbil centromeres are composed of four different repeats of length 6pb, 37
bp, 127
bp, or 1747bp which occur in simple alternating arrays and span 1-6Mb. Gerbil genomes have both an extensive set of GC-rich genes and chromosomes strikingly enriched for constitutive heterochromatin. We sought to determine if there was a link between these two phenomena and found that the two heterochromatic chromosomes of the Mongolian gerbil have distinct underpinnings: Chromosome 5 has a large block of intra-arm heterochromatin as the result of a massive expansion of centromeric repeats, while chromosome 13 is comprised of extremely large (>150
kb) repeated sequences. In addition to characterizing centromeres, our results demonstrate the importance of including karyotypic features such as chromosome number and the locations of centromeres in the interpretation of genome sequence data, and highlight novel patterns involved in the evolution of chromosomes.
Abstract.
Author URL.
Mackintosh A, Vila R, Laetsch DR, Hayward A, Martin SH, Lohse K (2023). Chromosome Fissions and Fusions Act as Barriers to Gene Flow between Brenthis Fritillary Butterflies.
Mol Biol Evol,
40(3).
Abstract:
Chromosome Fissions and Fusions Act as Barriers to Gene Flow between Brenthis Fritillary Butterflies.
Chromosome rearrangements are thought to promote reproductive isolation between incipient species. However, it is unclear how often, and under what conditions, fission and fusion rearrangements act as barriers to gene flow. Here we investigate speciation between two largely sympatric fritillary butterflies, Brenthis daphne and Brenthis ino. We use a composite likelihood approach to infer the demographic history of these species from whole-genome sequence data. We then compare chromosome-level genome assemblies of individuals from each species and identify a total of nine chromosome fissions and fusions. Finally, we fit a demographic model where effective population sizes and effective migration rate vary across the genome, allowing us to quantify the effects of chromosome rearrangements on reproductive isolation. We show that chromosomes involved in rearrangements experienced less effective migration since the onset of species divergence and that genomic regions near rearrangement points have a further reduction in effective migration rate. Our results suggest that the evolution of multiple rearrangements in the B. daphne and B. ino populations, including alternative fusions of the same chromosomes, have resulted in a reduction in gene flow. Although fission and fusion of chromosomes are unlikely to be the only processes that have led to speciation between these butterflies, this study shows that these rearrangements can directly promote reproductive isolation and may be involved in speciation when karyotypes evolve quickly.
Abstract.
Author URL.
Baril T, Pym A, Bass C, Hayward A (2023). Patterns of transposable element accumulation at resistance loci: a comparative genomic analysis in aphids.
Vila R, Lohse K, Hayward A, Laetsch DR, Wright C (2023). The genome sequence of the Chalkhill Blue, Lysandra coridon (Poda, 1761). Wellcome Open Research, 8
Lohse K, Hayward A, Vila R, Carvalho APS, Kawahara AY (2023). The genome sequence of the Large Skipper, Ochlodes sylvanus, (Esper, 1777). Wellcome Open Research, 8
Lohse K, Hayward A, Laetsch DR, Marques V, Vila R, Tyler-Smith C (2023). The genome sequence of the Mazarine Blue, Cyaniris semiargus (Rottemburg, 1775). Wellcome Open Research, 8
Galbraith JD, Hayward A (2023). The influence of transposable elements on animal colouration.
Trends GenetAbstract:
The influence of transposable elements on animal colouration.
Transposable elements (TEs) are mobile genetic sequences present within host genomes. TEs can contribute to the evolution of host traits, since transposition is mutagenic and TEs often contain host regulatory and protein coding sequences. We review cases where TEs influence animal colouration, reporting major patterns and outstanding questions. TE-induced colouration phenotypes typically arise via introduction of novel regulatory sequences and splice sites, affecting pigment cell development or pigment synthesis. We discuss if particular TE types may be more frequently involved in the evolution of colour variation in animals, given that examples involving long terminal repeat (LTR) elements appear to dominate. Currently, examples of TE-induced colouration phenotypes in animals mainly concern model and domesticated insect and mammal species. However, several influential recent examples, coupled with increases in genome sequencing, suggest cases reported from wild species will increase considerably.
Abstract.
Author URL.
2022
Brekke TD, Papadopulos AST, Julià E, Fornas O, Fu B, Yang F, de la Fuente R, Page J, Baril T, Hayward A, et al (2022). A chromosome-assigned Mongolian gerbil genome with sequenced centromeres provides evidence of a new chromosome.
Lear L, Padfield D, Dowsett T, Jones M, Kay S, Hayward A, Vos M (2022). Bacterial colonisation dynamics of household plastics in a coastal environment.
Sci Total Environ,
838(Pt 4).
Abstract:
Bacterial colonisation dynamics of household plastics in a coastal environment.
Accumulation of plastics in the marine environment has widespread detrimental consequences for ecosystems and wildlife. Marine plastics are rapidly colonised by a wide diversity of bacteria, including human pathogens, posing potential risks to health. Here, we investigate the effect of polymer type, residence time and estuarine location on bacterial colonisation of common household plastics, including pathogenic bacteria. We submerged five main household plastic types: low-density PE (LDPE), high-density PE (HDPE), polypropylene (PP), polyvinyl chloride (PVC) and polyethylene terephthalate (PET) at an estuarine site in Cornwall (U.K.) and tracked bacterial colonisation dynamics. Using both culture-dependent and culture-independent approaches, we found that bacteria rapidly colonised plastics irrespective of polymer type, reaching culturable densities of up to 1000 cells cm3 after 7 weeks. Community composition of the biofilms changed over time, but not among polymer types. The presence of pathogenic bacteria, quantified using the insect model Galleria mellonella, increased dramatically over a five-week period, with Galleria mortality increasing from 4% in week one to 65% in week five. No consistent differences in virulence were observed between polymer types. Pathogens isolated from plastic biofilms using Galleria enrichment included Serratia and Enterococcus species and they harboured a wide range of antimicrobial resistance genes. Our findings show that plastics in coastal waters are rapidly colonised by a wide diversity of bacteria independent of polymer type. Further, our results show that marine plastic biofilms become increasingly associated with virulent bacteria over time.
Abstract.
Author URL.
Law STS, Nong W, So WL, Baril T, Swale T, Chan CB, Tobe SS, Kai Z-P, Bendena WG, Hayward A, et al (2022). Chromosomal-Level Reference Genome of the Moth Heortia Vitessoides (Lepidoptera: Crambidae), a Major Pest of Agarwood-Producing Trees.
Law STS, Nong W, So WL, Baril T, Swale T, Chan CB, Tobe SS, Kai Z-P, Bendena WG, Hayward A, et al (2022). Chromosomal-level reference genome of the moth Heortia vitessoides (Lepidoptera: Crambidae), a major pest of agarwood-producing trees.
Genomics,
114(4).
Abstract:
Chromosomal-level reference genome of the moth Heortia vitessoides (Lepidoptera: Crambidae), a major pest of agarwood-producing trees.
The moth Heortia vitessoides Moore (Lepidoptera: Crambidae) is a major pest of ecologically, commercially and culturally important agarwood-producing trees in the genus Aquilaria. In particular, H. vitessoides is one of the most destructive defoliating pests of the incense tree Aquilaria sinesis, which produces a valuable fragrant wood used as incense and in traditional Chinese medicine [33]. Nevertheless, a genomic resource for H. vitessoides is lacking. Here, we present a chromosomal-level assembly for H. vitessoides, consisting of a 517 megabase (Mb) genome assembly with high physical contiguity (scaffold N50 of 18.2 Mb) and high completeness (97.9% complete BUSCO score). To aid gene annotation, 8 messenger RNA transcriptomes from different developmental stages were generated, and a total of 16,421 gene models were predicted. Expansion of gene families involved in xenobiotic metabolism and development were detected, including duplications of cytosolic sulfotransferase (SULT) genes shared among lepidopterans. In addition, small RNA sequencing of 5 developmental stages of H. vitessoides facilitated the identification of 85 lepidopteran conserved microRNAs, 94 lineage-specific microRNAs, as well as several microRNA clusters. A large proportion of the H. vitessoides genome consists of repeats, with a 29.12% total genomic contribution from transposable elements, of which long interspersed nuclear elements (LINEs) are the dominant component (17.41%). A sharp decrease in the genome-wide percentage of LINEs with lower levels of genetic distance to family consensus sequences suggests that LINE activity has peaked in H. vitessoides. In contrast, opposing patterns suggest a substantial recent increase in DNA and LTR element activity. Together with annotations of essential sesquiterpenoid hormonal pathways, neuropeptides, microRNAs and transposable elements, the high-quality genomic and transcriptomic resources we provide for the economically important moth H. vitessoides provide a platform for the development of genomic approaches to pest management, and contribute to addressing fundamental research questions in Lepidoptera.
Abstract.
Author URL.
Mackintosh A, Vila R, Laetsch DR, Hayward A, Martin SH, Lohse K (2022). Chromosome fissions and fusions act as barriers to gene flow between Brenthis fritillary butterflies.
Mitchell C (2022). Evolutionary and ecological immunology of. Toll-like receptors in mammals: patterns of selection within and across taxa.
Abstract:
Evolutionary and ecological immunology of. Toll-like receptors in mammals: patterns of selection within and across taxa
Infection from pathogens is consequential in host survival and fitness. Genetic differences in immune components can provide benefits in defending a host from pathogens. The Toll-like receptors (TLRs) are a family on innate immune receptors which detect pathogen components and have been found to show signs of positive selection across taxa. Genetic variation within TLRs has also been shown to relate to susceptibility to infection. In the first chapter I examine signatures of positive selection across the order Carnivora. The chapter aims to look for trends within and between TLRs using tests for selection, location of positively selected codons (PSCs), and TLR cellular location. I also investigate strength of selection over each species’ evolutionary history to find relationships with ecological and life history characteristics. The majority of TLRs show robust evidence of positive selection, with PSCs located within areas of biological significance for pathogen interaction. Stronger signs of positive selection were found in extra-cellular receptors than intra-cellular. Significant relationships between strength of selection and ecological characteristics and life history traits were found in multiples TLRs. Most notably, these were with the reproductive traits of gestation length, interbirth interval, and litter size, which potentially illustrate theories of life history trade off in investment between reproduction and immune function. The second chapter of this thesis focuses on genetic and behavioural defences which are crucial in host-pathogen relationships but not often combined into one study. This study looks at population-level TLR polymorphism in the bank vole (Myodes glareolus) and boldness and exploration personality scores. The haplotypes of the voles formed three clusters (A, B and C) but no significant relationships were found between the clusters and personality. However, there was a trend between B cluster haplotypes and increased explorations scores. These prospective relationships have implications in the maintenance of personality and genetic variation within populations and their roles in the spread of disease. The study highlights the importance of considering multiple aspects of host immune defence and their interactions rather than individualising the components. Overall, interaction with pathogens plays a large role in patterns in selection seen across taxa and within species. This thesis shows how the inclusion and consideration of ecological and behavioural factors into immunogenetics can provide a more representative idea of the complex interactions that are at work in host immune defences.
Abstract.
Nong W, Yu Y, Aase-Remedios ME, Xie Y, So WL, Li Y, Wong CF, Baril T, Law STS, Lai SY, et al (2022). Genome of the ramshorn snail Biomphalaria straminea-an obligate intermediate host of schistosomiasis.
Gigascience,
11Abstract:
Genome of the ramshorn snail Biomphalaria straminea-an obligate intermediate host of schistosomiasis.
BACKGROUND: Schistosomiasis, or bilharzia, is a parasitic disease caused by trematode flatworms of the genus Schistosoma. Infection by Schistosoma mansoni in humans results when cercariae emerge into water from freshwater snails in the genus Biomphalaria and seek out and penetrate human skin. The snail Biomphalaria straminea is native to South America and is now also present in Central America and China, and represents a potential vector host for spreading schistosomiasis. To date, genomic information for the genus is restricted to the neotropical species Biomphalaria glabrata. This limits understanding of the biology and management of other schistosomiasis vectors, such as B. straminea. FINDINGS: Using a combination of Illumina short-read, 10X Genomics linked-read, and Hi-C sequencing data, our 1.005 Gb B. straminea genome assembly is of high contiguity, with a scaffold N50 of 25.3 Mb. Transcriptomes from adults were also obtained. Developmental homeobox genes, hormonal genes, and stress-response genes were identified, and repeat content was annotated (40.68% of genomic content). Comparisons with other mollusc genomes (including Gastropoda, Bivalvia, and Cephalopoda) revealed syntenic conservation, patterns of homeobox gene linkage indicative of evolutionary changes to gene clusters, expansion of heat shock protein genes, and the presence of sesquiterpenoid and cholesterol metabolic pathway genes in Gastropoda. In addition, hormone treatment together with RT-qPCR assay reveal a sesquiterpenoid hormone responsive system in B. straminea, illustrating that this renowned insect hormonal system is also present in the lophotrochozoan lineage. CONCLUSION: This study provides the first genome assembly for the snail B. straminea and offers an unprecedented opportunity to address a variety of phenomena related to snail vectors of schistosomiasis, as well as evolutionary and genomics questions related to molluscs more widely.
Abstract.
Author URL.
Doyle T, Jimenez-Guri E, Hawkes WLS, Massy R, Mantica F, Permanyer J, Cozzuto L, Hermoso Pulido T, Baril T, Hayward A, et al (2022). Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.
Mol Ecol,
31(16), 4332-4350.
Abstract:
Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration.
Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.
Abstract.
Author URL.
Castledine M, Sierocinski P, Inglis M, Kay S, Hayward A, Buckling A, Padfield D (2022). Greater Phage Genotypic Diversity Constrains Arms-Race Coevolution. Frontiers in Cellular and Infection Microbiology, 12
So WL, Nong W, Xie Y, Baril T, Ma H-Y, Qu Z, Haimovitz J, Swale T, Gaitan-Espitia JD, Lau KF, et al (2022). Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes.
Nat Commun,
13(1).
Abstract:
Myriapod genomes reveal ancestral horizontal gene transfer and hormonal gene loss in millipedes.
Animals display a fascinating diversity of body plans. Correspondingly, genomic analyses have revealed dynamic evolution of gene gains and losses among animal lineages. Here we sequence six new myriapod genomes (three millipedes, three centipedes) at key phylogenetic positions within this major but understudied arthropod lineage. We combine these with existing genomic resources to conduct a comparative analysis across all available myriapod genomes. We find that millipedes generally have considerably smaller genomes than centipedes, with the repeatome being a major contributor to genome size, driven by independent large gains of transposons in three centipede species. In contrast to millipedes, centipedes gained a large number of gene families after the subphyla diverged, with gains contributing to sensory and locomotory adaptations that facilitated their ecological shift to predation. We identify distinct horizontal gene transfer (HGT) events from bacteria to millipedes and centipedes, with no identifiable HGTs shared among all myriapods. Loss of juvenile hormone O-methyltransferase, a key enzyme in catalysing sesquiterpenoid hormone production in arthropods, was also revealed in all millipede lineages. Our findings suggest that the rapid evolution of distinct genomic pathways in centipede and millipede lineages following their divergence from the myriapod ancestor, was shaped by differing ecological pressures.
Abstract.
Author URL.
Jaitly R, Ehrnsten E, Hedlund J, Cant M, Lehmann P, Hayward A (2022). The evolution of predator avoidance in cephalopods: a case of brain over brawn?. Frontiers in Marine Science, 9
Lohse K, Hayward A, Vila R, programme WSITOL, collective WSISODP, collective TOLCI, Howe C, Consortium DTOL (2022). The genome sequence of the Adonis blue, Lysandra bellargus (Rottemburg, 1775). Wellcome Open Research, 7
Lohse K, Hayward A, Laetsch DR, Vila R, Lucek K (2022). The genome sequence of the Arran brown, Erebia ligea (Linnaeus, 1758). Wellcome Open Research, 7
Ebdon S, Mackintosh A, Lohse K, Hayward A, Arif S, Whitla R (2022). The genome sequence of the black-veined white butterfly, Aporia crataegi (Linnaeus, 1758). Wellcome Open Research, 7
Lohse K, Hayward A, Laetsch DR, Vila R, Yumnam T (2022). The genome sequence of the common yellow swallowtail, Papilio machaon (Linnaeus, 1758). Wellcome Open Research, 7
Hayward A, Vila R, Lohse K, Laetsch D, Darwin Tree of Life Barcoding collective, Wellcome Sanger Institute Tree of Life programme, Wellcome Sanger Institute Scientific Operations: DNA Pipelines collective, Tree of Life Core Informatics collective, Darwin Tree of Life Consortium (2022). The genome sequence of the grizzled skipper, Pyrgus malvae (Linnaeus, 1758).
Wellcome Open Res,
7Abstract:
The genome sequence of the grizzled skipper, Pyrgus malvae (Linnaeus, 1758).
We present a genome assembly from an individual male Pyrgus malvae (the grizzled skipper; Arthropoda; Insecta; Lepidoptera; Hesperiidae). The genome sequence is 725 megabases in span. The majority (99.97%) of the assembly is scaffolded into 31 chromosomal pseudomolecules, with the Z sex chromosome assembled.
Abstract.
Author URL.
Lohse K, Vila R, Hayward A, Laetsch DR, Wahlberg N (2022). The genome sequence of the high brown fritillary, Fabriciana adippe (Dennis & Schiffermüller, 1775). Wellcome Open Research, 7
Mackintosh A, Laetsch DR, Baril T, Foster RG, Dincă V, Vila R, Hayward A, Lohse K (2022). The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.
G3 (Bethesda),
12(6).
Abstract:
The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.
The lesser marbled fritillary, Brenthis ino (Rottemburg, 1775), is a species of Palearctic butterfly. Male Brenthis ino individuals have been reported to have between 12 and 14 pairs of chromosomes, a much-reduced chromosome number than is typical in butterflies. Here, we present a chromosome-level genome assembly for Brenthis ino, as well as gene and transposable element annotations. The assembly is 411.8 Mb in length with a contig N50 of 9.6 Mb and a scaffold N50 of 29.5 Mb. We also show evidence that the male individual from which we generated HiC data was heterozygous for a neo-Z chromosome, consistent with inheriting 14 chromosomes from one parent and 13 from the other. This genome assembly will be a valuable resource for studying chromosome evolution in Lepidoptera, as well as for comparative and population genomics more generally.
Abstract.
Author URL.
Vila R, Lohse K, Hayward A, Laetsch D, Lab NHMGA, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL, et al (2022). The genome sequence of the marbled white butterfly, Melanargia galathea (Linnaeus, 1758). Wellcome Open Research, 7
Mackintosh A, Laetsch DR, Baril T, Ebdon S, Jay P, Vila R, Hayward A, Lohse K (2022). The genome sequence of the scarce swallowtail, Iphiclides podalirius.
Mackintosh A, Laetsch DR, Baril T, Ebdon S, Jay P, Vila R, Hayward A, Lohse K (2022). The genome sequence of the scarce swallowtail, Iphiclides podalirius.
G3 (Bethesda),
12(9).
Abstract:
The genome sequence of the scarce swallowtail, Iphiclides podalirius.
The scarce swallowtail, Iphiclides podalirius (Linnaeus, 1758), is a species of butterfly in the family Papilionidae. Here, we present a chromosome-level genome assembly for Iphiclides podalirius as well as gene and transposable element annotations. We investigate how the density of genomic features differs between the 30 Iphiclides podalirius chromosomes. We find that shorter chromosomes have higher heterozygosity at four-fold-degenerate sites and a greater density of transposable elements. While the first result is an expected consequence of differences in recombination rate, the second suggests a counter-intuitive relationship between recombination and transposable element evolution. This high-quality genome assembly, the first for any species in the tribe Leptocircini, will be a valuable resource for population genomics in the genus Iphiclides and comparative genomics more generally.
Abstract.
Author URL.
Hayward A, Lohse K, Laetsch DR, Vila R, programme WSITOL, collective WSISODP, collective TOLCI, Taluy E, Consortium DTOL (2022). The genome sequence of the silver-studded blue, Plebejus argus (Linnaeus, 1758). Wellcome Open Research, 7
Hayward A, Biscocho R (2022). The genome sequence of the small skipper, Thymelicus sylvestris (Poda, 1761). Wellcome Open Research, 7
Vila R, Lohse K, Hayward A, Laetsch DR, Wahlberg N (2022). The genome sequence of the white admiral, Limenitis camilla (Linnaeus, 1764). Wellcome Open Research, 7
Hayward A, Gilbert C (2022). Transposable elements.
Curr Biol,
32(17), R904-R909.
Abstract:
Transposable elements.
Transposable elements are known by many names, including 'transposons', 'interspersed repeats', 'selfish genetic elements', 'jumping genes', and 'parasitic DNA', but here we will refer to them simply as transposable elements. Many biologists will have heard of transposable elements and their ability to transpose (change position) within the genome. But fewer may be aware of their varied influences on host biology, including contributions to the evolution of diverse host traits such as internal gestation, memory, colouration, and adaptive immunity. Transposable elements are a near ubiquitous feature of eukaryotic genomes, and they often comprise a substantial proportion of total genomic content. Consequently, transposable element genes are considered among the most abundant coding sequences in nature. Recent advances in genome sequencing have ushered in a golden age for transposable-element research, providing opportunities to greatly improve our understanding of the effects of transposable elements on host evolution and disease. However, our ability to detect and analyse transposable elements still faces significant challenges, impairing efforts to decipher their evolution, characterise their diversity, and elucidate their myriad host influences. Below, we summarise key aspects of transposable element biology in eukaryotes and discuss major outstanding research questions.
Abstract.
Author URL.
2021
Hayward A, Poulin R, Nakagawa S (2021). A broadscale analysis of host-symbiont cophylogeny reveals the drivers of phylogenetic congruence.
ECOLOGY LETTERS,
24(8), 1681-1696.
Author URL.
Lear L, Padfield D, Dowsett T, Jones M, Kay S, Hayward A, Vos M (2021). Bacterial colonisation dynamics of household plastics in a coastal environment.
Dupeyron M, Baril T, Hayward A (2021). Broadscale evolutionary analysis of eukaryotic DDE transposons.
Singh KS, Cordeiro EMG, Troczka BJ, Pym A, Mackisack J, Mathers TC, Duarte A, Legeai F, Robin S, Bielza P, et al (2021). Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae.
Commun Biol,
4(1).
Abstract:
Global patterns in genomic diversity underpinning the evolution of insecticide resistance in the aphid crop pest Myzus persicae.
The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host-plant associations, uncovering the widespread co-option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.
Abstract.
Author URL.
Nong W, Qu Z, Li Y, Barton-Owen T, Wong AYP, Yip HY, Lee HT, Narayana S, Baril T, Swale T, et al (2021). Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication.
Commun Biol,
4(1).
Abstract:
Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication.
Whole genome duplication (WGD) has occurred in relatively few sexually reproducing invertebrates. Consequently, the WGD that occurred in the common ancestor of horseshoe crabs ~135 million years ago provides a rare opportunity to decipher the evolutionary consequences of a duplicated invertebrate genome. Here, we present a high-quality genome assembly for the mangrove horseshoe crab Carcinoscorpius rotundicauda (1.7 Gb, N50 = 90.2 Mb, with 89.8% sequences anchored to 16 pseudomolecules, 2n = 32), and a resequenced genome of the tri-spine horseshoe crab Tachypleus tridentatus (1.7 Gb, N50 = 109.7 Mb). Analyses of gene families, microRNAs, and synteny show that horseshoe crabs have undergone three rounds (3R) of WGD. Comparison of C. rotundicauda and T. tridentatus genomes from populations from several geographic locations further elucidates the diverse fates of both coding and noncoding genes. Together, the present study represents a cornerstone for improving our understanding of invertebrate WGD events on the evolutionary fates of genes and microRNAs, at both the individual and population level. We also provide improved genomic resources for horseshoe crabs, of applied value for breeding programs and conservation of this fascinating and unusual invertebrate lineage.
Abstract.
Author URL.
Troczka BJ, Singh KS, Zimmer CT, Vontas J, Nauen R, Hayward A, Bass C (2021). Molecular innovations underlying resistance to nicotine and neonicotinoids in the aphid Myzus persicae.
Pest Manag Sci,
77(12), 5311-5320.
Abstract:
Molecular innovations underlying resistance to nicotine and neonicotinoids in the aphid Myzus persicae.
The green peach aphid, Myzus persicae, is a globally distributed highly damaging crop pest. This species has demonstrated an exceptional ability to evolve resistance to both synthetic insecticides used for control, and natural insecticides produced by certain plants as a chemical defense against insect attack. Here we review work characterizing the evolution of resistance in M. persicae to the natural insecticide nicotine and the structurally related class of synthetic neonicotinoid insecticides. We outline how research on this topic has provided insights into long-standing questions of both evolutionary and applied importance. These include questions pertaining to the origins of novel traits, the number and nature of mutational events or 'adaptive steps' underlying the evolution of new phenotypes, and whether host plant adaptations can be co-opted to confer resistance to synthetic insecticides. Finally, research on the molecular mechanisms underlying insecticide resistance in M. persicae has generated several outstanding questions on the genetic architecture of resistance to both natural and synthetic xenobiotics, and we conclude by identifying key knowledge gaps for future research. © 2021 the Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
Abstract.
Author URL.
Blasco-Costa I, Hayward A, Poulin R, Balbuena JA (2021). Next-generation cophylogeny: unravelling eco-evolutionary processes.
Trends in Ecology and Evolution,
36(10), 907-918.
Abstract:
Next-generation cophylogeny: unravelling eco-evolutionary processes
A fundamental question in evolutionary biology is how microevolutionary processes translate into species diversification. Cophylogeny provides an appropriate framework to address this for symbiotic associations, but historically has been primarily limited to unveiling patterns. We argue that it is essential to integrate advances from ecology and evolutionary biology into cophylogeny, to gain greater mechanistic insights and transform cophylogeny into a platform to advance understanding of interspecific interactions and diversification more widely. We discuss key directions, such as incorporating trait reconstruction and considering multiple scales of network organization, and highlight recent developments for implementation. A new quantitative framework is proposed to allow integration of relevant information, such as quantitative traits and assessment of the contribution of individual mechanisms to cophylogenetic patterns.
Abstract.
Ebdon S, Laetsch DR, Dapporto L, Hayward A, Ritchie MG, Dincӑ V, Vila R, Lohse K (2021). The Pleistocene species pump past its prime: Evidence from European butterfly sister species.
Mol Ecol,
30(14), 3575-3589.
Abstract:
The Pleistocene species pump past its prime: Evidence from European butterfly sister species.
The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. While it is clear that the contact zones that have been described for many sister taxa are secondary and have formed in the current interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here, we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases, species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post-divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the initial stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial divergence and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact zone pairs.
Abstract.
Author URL.
Vila R, Hayward A, Lohse K, Wright C, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL (2021). The genome sequence of the Glanville fritillary, Melitaea cinxia (Linnaeus, 1758). Wellcome Open Research, 6
Ebdon S, Mackintosh A, Hayward A, Wotton K, collective DTOLB, programme WSITOL, collective WSISODP, collective TOLCI, Consortium DTOL (2021). The genome sequence of the clouded yellow, Colias crocea (Geoffroy, 1785). Wellcome Open Research, 6
Hayward A, Vila R, Laetsch DR, Lohse K, Baril T (2021). The genome sequence of the heath fritillary, Melitaea athalia (Rottemburg, 1775).
Wellcome Open Research,
6, 304-304.
Abstract:
The genome sequence of the heath fritillary, Melitaea athalia (Rottemburg, 1775)
We present a genome assembly from an individual female Melitaea athalia (also known as Mellicta athalia; the heath fritillary; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 610 megabases in span. In total, 99.98% of the assembly is scaffolded into 32 chromosomal pseudomolecules, with the W and Z sex chromosome assembled. Gene annotation of this assembly on Ensembl has identified 12,824 protein coding genes.
Abstract.
Hayward A, Wright C, Darwin Tree of Life Barcoding collective, Wellcome Sanger Institute Tree of Life programme, Wellcome Sanger Institute Scientific Operations: DNA Pipelines collective, Tree of Life Core Informatics collective, Darwin Tree of Life Consortium (2021). The genome sequence of the holly blue, Celastrina argiolus (Linnaeus, 1758).
Wellcome Open Res,
6Abstract:
The genome sequence of the holly blue, Celastrina argiolus (Linnaeus, 1758).
We present a genome assembly from an individual male Celastrina argiolus) (the holly blue; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequence is 499 megabases in span. The majority (99.99%) of the assembly is scaffolded into 26 chromosomal pseudomolecules, with the Z sex chromosome assembled. Gene annotation of this assembly on Ensembl has identified 12,199 protein coding genes.
Abstract.
Author URL.
Mackintosh A, Laetsch DR, Baril T, Foster R, Dincă V, Vila R, Hayward A, Lohse K (2021). The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.
Lohse K, Hayward A, Ebdon S (2021). The genome sequences of the male and female green-veined white, Pieris napi (Linnaeus, 1758).
Wellcome Open Research,
6, 288-288.
Abstract:
The genome sequences of the male and female green-veined white, Pieris napi (Linnaeus, 1758)
We present genome assemblies from a male and female Pieris napi (the green-veined white; Arthropoda; Insecta; Lepidoptera; Pieridae). The genome sequences of the male and female are 320 and 319 megabases in span, respectively. The majority of the assembly (99.79% of the male assembly, 99.88% of the female) is scaffolded into 24 autosomal pseudomolecules, with the Z sex chromosome assembled for the male and Z and W chromosomes assembled for the female. Gene annotation of the male assembly on Ensembl has identified 13,221 protein coding genes.
Abstract.
Panini M, Chiesa O, Troczka BJ, Mallott M, Manicardi GC, Cassanelli S, Cominelli F, Hayward A, Mazzoni E, Bass C, et al (2021). Transposon-mediated insertional mutagenesis unmasks recessive insecticide resistance in the aphid Myzus persicae.
Proc Natl Acad Sci U S A,
118(23).
Abstract:
Transposon-mediated insertional mutagenesis unmasks recessive insecticide resistance in the aphid Myzus persicae.
The evolution of resistance to insecticides threatens the sustainable control of many of the world's most damaging insect crop pests and disease vectors. To effectively combat resistance, it is important to understand its underlying genetic architecture, including the type and number of genetic variants affecting resistance and their interactions with each other and the environment. While significant progress has been made in characterizing the individual genes or mutations leading to resistance, our understanding of how genetic variants interact to influence its phenotypic expression remains poor. Here, we uncover a mechanism of insecticide resistance resulting from transposon-mediated insertional mutagenesis of a genetically dominant but insecticide-susceptible allele that enables the adaptive potential of a previously unavailable recessive resistance allele to be unlocked. Specifically, we identify clones of the aphid pest Myzus persicae that carry a resistant allele of the essential voltage-gated sodium channel (VGSC) gene with the recessive M918T and L1014F resistance mutations, in combination with an allele lacking these mutations but carrying a Mutator-like element transposon insertion that disrupts the coding sequence of the VGSC. This results in the down-regulation of the dominant susceptible allele and monoallelic expression of the recessive resistant allele, rendering the clones resistant to the insecticide bifenthrin. These findings are a powerful example of how transposable elements can provide a source of evolutionary potential that can be revealed by environmental and genetic perturbation, with applied implications for the control of highly damaging insect pests.
Abstract.
Author URL.
2020
Nong W, Law STS, Wong AYP, Baril T, Swale T, Chu LM, Hayward A, Lau DTW, Hui JHL (2020). Chromosomal-level reference genome of the incense tree Aquilaria sinensis.
Nong W, Law STS, Wong AYP, Baril T, Swale T, Chu LM, Hayward A, Lau DTW, Hui JHL (2020). Chromosomal‐level reference genome of the incense tree. <i>Aquilaria sinensis</i>. Molecular Ecology Resources, 20(4), 971-979.
Qu Z, Nong W, Yu Y, Baril T, Yip HY, Hayward A, Hui JHL (2020). Genome of the four-finger threadfin Eleutheronema tetradactylum (Perciforms: Polynemidae).
BMC Genomics,
21(1).
Abstract:
Genome of the four-finger threadfin Eleutheronema tetradactylum (Perciforms: Polynemidae)
Background: Teleost fish play important roles in aquatic ecosystems and aquaculture. Threadfins (Perciformes: Polynemidae) show a range of interesting biology, and are of considerable importance for both wild fisheries and aquaculture. Additionally, the four-finger threadfin Eleutheronema tetradactylum is of conservation relevance since its populations are considered to be in rapid decline and it is classified as endangered. However, no genomic resources are currently available for the threadfin family Polynemidae. Results: We sequenced and assembled the first threadfin fish genome, the four-finger threadfin E. tetradactylum. We provide a genome assembly for E. tetradactylum with high contiguity (scaffold N50 = 56.3 kb) and high BUSCO completeness at 96.5%. The assembled genome size of E. tetradactylum is just 610.5 Mb, making it the second smallest perciform genome assembled to date. Just 9.07–10.91% of the genome sequence was found to consist of repetitive elements (standard RepeatMasker analysis vs custom analysis), making this the lowest repeat content identified to date for any perciform fish. A total of 37,683 protein-coding genes were annotated, and we include analyses of developmental transcription factors, including the Hox, ParaHox, and Sox families. MicroRNA genes were also annotated and compared with other chordate lineages, elucidating the gains and losses of chordate microRNAs. Conclusions: the four-finger threadfin E. tetradactylum genome presented here represents the first available genome sequence for the ecologically, biologically, and commercially important clade of threadfin fish. Our findings provide a useful genomic resource for future research into the interesting biology and evolution of this valuable group of food fish.
Abstract.
Qu Z, Nong W, So WL, Barton-Owen T, Li Y, Leung TCN, Li C, Baril T, Wong AYP, Swale T, et al (2020). Millipede genomes reveal unique adaptations during myriapod evolution.
PLoS Biol,
18(9).
Abstract:
Millipede genomes reveal unique adaptations during myriapod evolution.
The Myriapoda, composed of millipedes and centipedes, is a fascinating but poorly understood branch of life, including species with a highly unusual body plan and a range of unique adaptations to their environment. Here, we sequenced and assembled 2 chromosomal-level genomes of the millipedes Helicorthomorpha holstii (assembly size = 182 Mb; shortest scaffold/contig length needed to cover 50% of the genome [N50] = 18.11 Mb mainly on 8 pseudomolecules) and Trigoniulus corallinus (assembly size = 449 Mb, N50 = 26.78 Mb mainly on 17 pseudomolecules). Unique genomic features, patterns of gene regulation, and defence systems in millipedes, not observed in other arthropods, are revealed. Both repeat content and intron size are major contributors to the observed differences in millipede genome size. Tight Hox and the first loose ecdysozoan ParaHox homeobox clusters are identified, and a myriapod-specific genomic rearrangement including Hox3 is also observed. The Argonaute (AGO) proteins for loading small RNAs are duplicated in both millipedes, but unlike in insects, an AGO duplicate has become a pseudogene. Evidence of post-transcriptional modification in small RNAs-including species-specific microRNA arm switching-providing differential gene regulation is also obtained. Millipedes possesses a unique ozadene defensive gland unlike the venomous forcipules found in centipedes. We identify sets of genes associated with the ozadene that play roles in chemical defence as well as antimicrobial activity. Macro-synteny analyses revealed highly conserved genomic blocks between the 2 millipedes and deuterostomes. Collectively, our analyses of millipede genomes reveal that a series of unique adaptations have occurred in this major lineage of arthropod diversity. The 2 high-quality millipede genomes provided here shed new light on the conserved and lineage-specific features of millipedes and centipedes. These findings demonstrate the importance of the consideration of both centipede and millipede genomes-and in particular the reconstruction of the myriapod ancestral situation-for future research to improve understanding of arthropod evolution, and animal evolutionary genomics more widely.
Abstract.
Author URL.
Hedlund J, Ehrnsten E, Hayward C, Lehmann P, Hayward A (2020). New records of the Paleotropical migrant <i>Hemianax ephippiger</i> in the Caribbean and a review of its status in the Neotropics. International Journal of Odonatology, 23(4), 315-325.
Dupeyron M, Baril T, Bass C, Hayward A (2020). Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements.
Mob DNA,
11Abstract:
Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements.
BACKGROUND: Tc1/mariner transposons are widespread DNA transposable elements (TEs) that have made important contributions to the evolution of host genomic complexity in metazoans. However, the evolution and diversity of the Tc1/mariner superfamily remains poorly understood. Following recent developments in genome sequencing and the availability of a wealth of new genomes, Tc1/mariner TEs have been identified in many new taxa across the eukaryotic tree of life. To date, the majority of studies focussing on Tc1/mariner elements have considered only a single host lineage or just a small number of host lineages. Thus, much remains to be learnt about the evolution of Tc1/mariner TEs by performing analyses that consider elements that originate from across host diversity. RESULTS: We mined the non-redundant database of NCBI using BLASTp searches, with transposase sequences from a diverse set of reference Tc1/mariner elements as queries. A total of 5158 Tc1/mariner elements were retrieved and used to reconstruct evolutionary relationships within the superfamily. The resulting phylogeny is well resolved and includes several new groups of Tc1/mariner elements. In particular, we identify a new family of plant-genome restricted Tc1/mariner elements, which we call PlantMar. We also show that the pogo family is much larger and more diverse than previously appreciated, and we review evidence for a potential revision of its status to become a separate superfamily. CONCLUSIONS: Our study provides an overview of Tc1-mariner phylogeny and summarises the impressive diversity of Tc1-mariner TEs among sequenced eukaryotes. Tc1/mariner TEs are successful in a wide range of eukaryotes, especially unikonts (the taxonomic supergroup containing Amoebozoa, Opisthokonta, Breviatea, and Apusomonadida). In particular, ecdysozoa, and especially arthropods, emerge as important hosts for Tc1/mariner elements (except the PlantMar family). Meanwhile, the pogo family, which is by far the largest Tc1/mariner family, also includes many elements from fungal and chordate genomes. Moreover, there is evidence of the repeated exaptation of pogo elements in vertebrates, including humans, in addition to the well-known example of CENP-B. Collectively, our findings provide a considerable advancement in understanding of Tc1/mariner elements, and more generally they suggest that much work remains to improve understanding of the diversity and evolution of DNA TEs.
Abstract.
Author URL.
Li Y, Nong W, Baril T, Yip HY, Swale T, Hayward A, Ferrier DEK, Hui JHL (2020). Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome.
BMC Genomics,
21(1).
Abstract:
Reconstruction of ancient homeobox gene linkages inferred from a new high-quality assembly of the Hong Kong oyster (Magallana hongkongensis) genome
Background: Homeobox-containing genes encode crucial transcription factors involved in animal, plant and fungal development, and changes to homeobox genes have been linked to the evolution of novel body plans and morphologies. In animals, some homeobox genes are clustered together in the genome, either as remnants from ancestral genomic arrangements, or due to coordinated gene regulation. Consequently, analyses of homeobox gene organization across animal phylogeny provide important insights into the evolution of genome organization and developmental gene control, and their interaction. However, homeobox gene organization remains to be fully elucidated in several key animal ancestors, including those of molluscs, lophotrochozoans and bilaterians. Results: Here, we present a high-quality chromosome-level genome assembly of the Hong Kong oyster, Magallana hongkongensis (2n = 20), for which 93.2% of the genomic sequences are contained on 10 pseudomolecules (~ 758 Mb, scaffold N50 = 72.3 Mb). Our genome assembly was scaffolded using Hi-C reads, facilitating a larger scaffold size compared to the recently published M. hongkongensis genome of Peng et al. (Mol Ecol Resources, 2020), which was scaffolded using the Crassostrea gigas assembly. A total of 46,963 predicted gene models (45,308 protein coding genes) were incorporated in our genome, and genome completeness estimated by BUSCO was 94.6%. Homeobox gene linkages were analysed in detail relative to available data for other mollusc lineages. Conclusions: the analyses performed in this study and the accompanying genome sequence provide important genetic resources for this economically and culturally valuable oyster species, and offer a platform to improve understanding of animal biology and evolution more generally. Transposable element content is comparable to that found in other mollusc species, contrary to the conclusion of another recent analysis. Also, our chromosome-level assembly allows the inference of ancient gene linkages (synteny) for the homeobox-containing genes, even though a number of the homeobox gene clusters, like the Hox/ParaHox clusters, are undergoing dispersal in molluscs such as this oyster.
Abstract.
Ebdon S, Laetsch DR, Dapporto L, Hayward A, Ritchie MG, Dincă V, Vila R, Lohse K (2020). The Pleistocene species pump past its prime: evidence from European butterfly sister species.
Singh KS, Troczka BJ, Duarte A, Balabanidou V, Trissi N, Carabajal Paladino LZ, Nguyen P, Zimmer CT, Papapostolou KM, Randall E, et al (2020). The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses.
Science Advances,
6(19).
Abstract:
The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses
A complex series of mutational events protected a mutualistic symbiosis during the shift of an insect to a toxic host plant.
Abstract.
2019
Mackintosh A, Laetsch DR, Hayward A, Charlesworth B, Waterfall M, Vila R, Lohse K (2019). The determinants of genetic diversity in butterflies – Lewontin’s paradox revisited.
2016
Tsuboi M, Kotrschal A, Hayward A, Buechel SD, Zidar J, Løvlie H, Kolm N (2016). Evolution of brain-body allometry in Lake Tanganyika cichlids. Evolution, 70(7), 1559-1568.
Ács Z, Hayward A, Sugár L (2016). Genetic diversity and population genetics of large lungworms (Dictyocaulus, Nematoda) in wild deer in Hungary.
Parasitol Res,
115(9), 3295-3312.
Abstract:
Genetic diversity and population genetics of large lungworms (Dictyocaulus, Nematoda) in wild deer in Hungary.
Dictyocaulus nematode worms live as parasites in the lower airways of ungulates and can cause significant disease in both wild and farmed hosts. This study represents the first population genetic analysis of large lungworms in wildlife. Specifically, we quantify genetic variation in Dictyocaulus lungworms from wild deer (red deer, fallow deer and roe deer) in Hungary, based on mitochondrial cytochrome c oxidase subunit 1 (cox1) sequence data, using population genetic and phylogenetic analyses. The studied Dictyocaulus taxa display considerable genetic diversity. At least one cryptic species and a new parasite-host relationship are revealed by our molecular study. Population genetic analyses for Dictyocaulus eckerti revealed high gene flow amongst weakly structured spatial populations that utilise the three host deer species considered here. Our results suggest that D. eckerti is a widespread generalist parasite in ungulates, with a diverse genetic backround and high evolutionary potential. In contrast, evidence of cryptic genetic structure at regional geographic scales was observed for Dictyocaulus capreolus, which infects just one host species, suggesting it is a specialist within the studied area. D. capreolus displayed lower genetic diversity overall, with only moderate gene flow compared to the closely related D. eckerti. We suggest that the differing vagility and dispersal behaviour of hosts are important contributing factors to the population structure of lungworms, and possibly other nematode parasites with single-host life cycles. Our findings are of relevance for the management of lungworms in deer farms and wild deer populations.
Abstract.
Author URL.
Mcmahon DP, Hayward A (2016). Why grow up? a perspective on insect strategies to avoid metamorphosis.
Ecological Entomology,
41(5), 505-515.
Abstract:
Why grow up? a perspective on insect strategies to avoid metamorphosis
1. Insects with complete metamorphosis (holometaboly) are extremely successful, constituting over 60% of all described animal species. Complete metamorphosis confers significant advantages because it enables organisms to optimise life-history components through temporal partitioning, and thereby to exploit multiple ecological niches. Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis. 2. In this review, we discuss different strategies that have evolved that result in the loss of complete metamorphosis (type I and type II paedomorphosis). In addition, the ecological pressures and developmental modifications that facilitate this avoidance are considered, as well as the importance of life cycle complexity in life-history evolution. 3. Interestingly, only female holometabolous insects have entirely avoided complete metamorphosis, and it is always the ancestrally juvenile morphology that is retained. These findings point to a strong sex-biased trade-off between investment in reproduction and development. While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described. 4. Thus, complete metamorphosis, which originated only once in insects, appears to have been almost fully retained. This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.
Abstract.
2015
Hayward A, Katzourakis A (2015). Endogenous retroviruses. Current Biology, 25(15), R644-R646.
Kenny NJ, Sin YW, Hayward A, Paps J, Chu KH, Hui JHL (2015). The phylogenetic utility and functional constraint of microRNA flanking sequences.
Proceedings of the Royal Society B: Biological Sciences,
282(1803), 20142983-20142983.
Abstract:
The phylogenetic utility and functional constraint of microRNA flanking sequences
. MicroRNAs (miRNAs) have recently risen to prominence as novel factors responsible for post-transcriptional regulation of gene expression. miRNA genes have been posited as highly conserved in the clades in which they exist. Consequently, miRNAs have been used as rare genome change characters to estimate phylogeny by tracking their gain and loss. However, their short length (21–23 bp) has limited their perceived utility in sequenced-based phylogenetic inference. Here, using reference taxa with established phylogenetic relationships, we demonstrate that miRNA sequences are of high utility in quantitative, rather than in qualitative, phylogenetic analysis. The clear orthology among miRNA genes from different species makes it straightforward to identify and align these sequences from even fragmentary datasets. We also identify significant sequence conservation in the regions directly flanking miRNA genes, and show that this too is of utility in phylogenetic analysis, as well as highlighting conserved regions that will be of interest to other fields. Employing miRNA sequences from 12 sequenced drosophilid genomes, together with a
. Tribolium castaneum
. outgroup, we demonstrate that this approach is robust using Bayesian and maximum-likelihood methods. The utility of these characters is further demonstrated in the rhabditid nematodes and primates. As next-generation sequencing makes it more cost-effective to sequence genomes and small RNA libraries, this methodology provides an alternative data source for phylogenetic analysis. The approach allows rapid resolution of relationships between both closely related and rapidly evolving species, and provides an additional tool for investigation of relationships within the tree of life.
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Abstract.
2014
Tsuboi M, Husby A, Kotrschal A, Hayward A, Buechel SD, Zidar J, Løvlie H, Kolm N (2014). Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids. Evolution, 69(1), 190-200.
Erezyilmaz DF, Hayward A, Huang Y, Paps J, Acs Z, Delgado JA, Collantes F, Kathirithamby J (2014). Expression of the Pupal Determinant broad during Metamorphic and Neotenic Development of the Strepsipteran Xenos vesparum Rossi. PLoS ONE, 9(4), e93614-e93614.
Hayward A, Cornwallis CK, Jern P (2014). Pan-vertebrate comparative genomics unmasks retrovirus macroevolution.
Proceedings of the National Academy of Sciences,
112(2), 464-469.
Abstract:
Pan-vertebrate comparative genomics unmasks retrovirus macroevolution
Significance
. For millions of years retroviruses, such as HIV in humans, have attacked vertebrates. Occasionally retroviruses infiltrate germ cells, incorporate themselves into the host’s genome, and transmit vertically to the host’s offspring as endogenous retroviruses (ERVs). Consequently, ERVs make up large portions of vertebrate genomes and represent a record of past host–retrovirus interactions. We developed pan-vertebrate ERV analyses to provide an overview of host–retrovirus interactions, generating insights into retroviral evolution, diversity, host-switching, and the factors influencing retroviral transmission. Astoundingly, we found over 36,000 ERV lineages across our sample of vertebrate diversity. The results provide knowledge about host–retrovirus coevolution, suggesting an unprecedented ability of retroviruses to switch between distantly related vertebrates and implying existence of additional, yet unidentified retroviruses.
Abstract.
2013
Hayward A, Grabherr M, Jern P (2013). Broad-scale phylogenomics provides insights into retrovirus–host evolution.
Proceedings of the National Academy of Sciences,
110(50), 20146-20151.
Abstract:
Broad-scale phylogenomics provides insights into retrovirus–host evolution
Significance
. Retroviruses, such as HIV, are important pathogens of vertebrates, including humans. They are capable of crossing species barriers to infect new hosts, but knowledge about the evolutionary history of retroviruses is limited. However, genomic traces of past retrovirus activities known as “endogenous retroviruses” can be screened from sequenced genomes and analyzed to improve understanding of retrovirus evolution. Here we use a unique approach to address the evolution of one group of retroviruses in a screen of 60 diverse vertebrate host genomes. We find evidence of rampant host-switching across mammalian orders by members of this group throughout their evolutionary history. We also find evidence that the spread of infective retroviruses from this group may be facilitated by rats.
Abstract.
Hayward A, Ghazal A, Andersson G, Andersson L, Jern P (2013). ZBED Evolution: Repeated Utilization of DNA Transposons as Regulators of Diverse Host Functions. PLoS ONE, 8(3), e59940-e59940.
2012
Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens H-J, et al (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491(7424), 393-398.
2011
HAYWARD A, MCMAHON DP, KATHIRITHAMBY J (2011). Cryptic diversity and female host specificity in a parasitoid where the sexes utilize hosts from separate orders. Molecular Ecology, 20(7), 1508-1528.
McMahon DP, Hayward A, Kathirithamby J (2011). Strepsiptera. Current Biology, 21(8), R271-R272.
McMahon DP, Hayward A, Kathirithamby J (2011). The First Molecular Phylogeny of Strepsiptera (Insecta) Reveals an Early Burst of Molecular Evolution Correlated with the Transition to Endoparasitism. PLoS ONE, 6(6), e21206-e21206.
2010
Nicholls JA, Fuentes-Utrilla P, Hayward A, Melika G, Csóka G, Nieves-Aldrey J-L, Pujade-Villar J, Tavakoli M, Schönrogge K, Stone GN, et al (2010). Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts.
BMC Evol Biol,
10Abstract:
Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts.
BACKGROUND: Biological invasions provide a window on the process of community assembly. In particular, tracking natural enemy recruitment to invading hosts can reveal the relative roles of co-evolution (including local adaptation) and ecological sorting. We use molecular data to examine colonisation of northern Europe by the parasitoid Megastigmus stigmatizans following invasions of its herbivorous oak gallwasp hosts from the Balkans. Local host adaptation predicts that invading gallwasp populations will have been tracked primarily by sympatric Balkan populations of M. stigmatizans (Host Pursuit Hypothesis). Alternatively, ecological sorting allows parasitoid recruitment from geographically distinct populations with no recent experience of the invading hosts (Host Shift Hypothesis). Finally, we test for long-term persistence of parasitoids introduced via human trade of their hosts' galls (Introduction Hypothesis). RESULTS: Polymorphism diagnostic of different southern refugial regions was present in both mitochondrial and nuclear microsatellite markers, allowing us to identify the origins of northern European invaded range M. stigmatizans populations. As with their hosts, some invaded range populations showed genetic variation diagnostic of Balkan sources, supporting the Host Pursuit Hypothesis. In contrast, other invading populations had an Iberian origin, unlike their hosts in northern Europe, supporting the Host Shift Hypothesis. Finally, both British and Italian M. stigmatizans populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources. CONCLUSIONS: These data reveal the continental scale of multi-trophic impacts of anthropogenic disturbance and highlight the fact that herbivores and their natural enemies may face very different constraints on range expansion. The ability of natural enemies to exploit ecologically-similar hosts with which they have had no historical association supports a major role for ecological sorting processes in the recent assembly of these communities. The multitude of origins of invading natural enemy populations in this study emphasises the diversity of mechanisms requiring consideration when predicting consequences of other biological invasions or biological control introductions.
Abstract.
Author URL.
Hayward A, Takahashi T, Bendena WG, Tobe SS, Hui JHL (2010). Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in metazoans. FEBS Letters, 584(6), 1273-1278.
Nicholls JA, Preuss S, Hayward A, Melika G, Csóka G, Nieves-Aldrey J-L, Askew RR, Tavakoli M, Schönrogge K, Stone GN, et al (2010). Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes.
Mol Ecol,
19(3), 592-609.
Abstract:
Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes.
Little is known about the evolutionary history of most complex multi-trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host-tracking) or later divergence in higher trophic levels (Delayed Host-tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species-level divergence at both 8-9 and 4-5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host-tracking Hypothesis for community evolution.
Abstract.
Author URL.
HAYWARD A (2010). Cryptic diversity and patterns of host specificity in trematode flatworms. Molecular Ecology, 19(13), 2602-2604.
Hui JHL, Hayward A, Bendena WG, Takahashi T, Tobe SS (2010). Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects. Peptides, 31(3), 451-455.
Ács Z, Challis RJ, Bihari P, Blaxter M, Hayward A, Melika G, Csóka G, Pénzes Z, Pujade-Villar J, Nieves-Aldrey J-L, et al (2010). Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the Western Palaearctic. Molecular Phylogenetics and Evolution, 55(1), 210-225.
2009
KATHIRITHAMBY J, HAYWARD A, MCMAHON DP, FERREIRA RS, ANDREAZZE R, ALMEIDA ANDRADE HTD, FRESNEAU D (2009). Conspecifics of a heterotrophic heteronomous species of Strepsiptera (Insecta) are matched by molecular characterization. Systematic Entomology, 35(2), 234-242.
McMahon DP, Hayward A, Kathirithamby J (2009). The mitochondrial genome of the 'twisted-wing parasite' Mengenilla australiensis (Insecta, Strepsiptera): a comparative study. BMC Genomics, 10(1), 603-603.
2007
STONE GN, ATKINSON RJ, ROKAS A, ALDREY J-LN, MELIKA G, Ács ZOLTAN, CSÓKA G, HAYWARD A, BAILEY R, BUCKEE C, et al (2007). Evidence for widespread cryptic sexual generations in apparently purely asexual Andricus gallwasps. Molecular Ecology, 17(2), 652-665.
STONE GN, CHALLIS RJ, ATKINSON RJ, CSÓKA G, HAYWARD A, MELIKA G, MUTUN S, PREUSS S, ROKAS A, SADEGHI E, et al (2007). The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari. Molecular Ecology, 16(13), 2768-2781.
2005
HAYWARD A, STONE GN (2005). Comparative phylogeography across two trophic levels: the oak gall wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology, 15(2), 479-489.
Hayward A, Stone GN (2005). Oak gall wasp communities: Evolution and ecology. Basic and Applied Ecology, 6(5), 435-443.
