Publications by category
Journal articles
Hayward A, Baril T (In Press). A draft genome sequence of the elusive giant squid, Architeuthis dux.
GigaScience Full text.
Dupeyron M, Singh K, Bass C, Hayward A (In Press). Evolution of Mutator transposable elements across eukaryotic diversity.
Mobile DNA Full text.
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 Full text.
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.
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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 Full text.
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.
Molecular Ecology Resources,
20(4), 971-979.
Full text.
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)
© 2020, the Author(s). 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.
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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.
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Hedlund J, Ehrnsten E, Hayward C, Lehmann P, Hayward A (2020). New records of the Paleotropical migrant Hemianax ephippiger in the Caribbean and a review of its status in the Neotropics.
International Journal of Odonatology,
23(4), 315-325.
Full text.
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.
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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
© 2020, the Author(s). 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.
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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), eaba1070-eaba1070.
Abstract:
The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses
Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.
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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.
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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
© 2016 the Royal Entomological Society 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.
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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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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.
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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.
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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
Although extensive research has demonstrated host-retrovirus microevolutionary dynamics, it has been difficult to gain a deeper understanding of the macroevolutionary patterns of host–retrovirus interactions. Here we use recent technological advances to infer broad patterns in retroviral diversity, evolution, and host–virus relationships by using a large-scale phylogenomic approach using endogenous retroviruses (ERVs). Retroviruses insert a proviral DNA copy into the host cell genome to produce new viruses. ERVs are provirus insertions in germline cells that are inherited down the host lineage and consequently present a record of past host–viral associations. By mining ERVs from 65 host genomes sampled across vertebrate diversity, we uncover a great diversity of ERVs, indicating that retroviral sequences are much more prevalent and widespread across vertebrates than previously appreciated. The majority of ERV clades that we recover do not contain known retroviruses, implying either that retroviral lineages are highly transient over evolutionary time or that a considerable number of retroviruses remain to be identified. By characterizing the distribution of ERVs, we show that no major vertebrate lineage has escaped retroviral activity and that retroviruses are extreme host generalists, having an unprecedented ability for rampant host switching among distantly related vertebrates. In addition, we examine whether the distribution of ERVs can be explained by host factors predicted to influence viral transmission and find that internal fertilization has a pronounced effect on retroviral colonization of host genomes. By capturing the mode and pattern of retroviral evolution and contrasting ERV diversity with known retroviral diversity, our study provides a cohesive framework to understand host–virus coevolution better.
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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.
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.
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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.
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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 Full text.
Dupeyron M, Singh K, Bass C, Hayward A (In Press). Evolution of Mutator transposable elements across eukaryotic diversity.
Mobile DNA Full text.
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 Full text.
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.
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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 Full text.
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.
Molecular Ecology Resources,
20(4), 971-979.
Full text.
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)
© 2020, the Author(s). 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.
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Hedlund J, Ehrnsten E, Hayward C, Lehmann P, Hayward A (2020). New records of the Paleotropical migrant Hemianax ephippiger in the Caribbean and a review of its status in the Neotropics.
International Journal of Odonatology,
23(4), 315-325.
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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.
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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
© 2020, the Author(s). 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), eaba1070-eaba1070.
Abstract:
The genetic architecture of a host shift: an adaptive walk protected an aphid and its endosymbiont from plant chemical defenses
Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.
Abstract.
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.
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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
© 2016 the Royal Entomological Society 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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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.
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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.
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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
Although extensive research has demonstrated host-retrovirus microevolutionary dynamics, it has been difficult to gain a deeper understanding of the macroevolutionary patterns of host–retrovirus interactions. Here we use recent technological advances to infer broad patterns in retroviral diversity, evolution, and host–virus relationships by using a large-scale phylogenomic approach using endogenous retroviruses (ERVs). Retroviruses insert a proviral DNA copy into the host cell genome to produce new viruses. ERVs are provirus insertions in germline cells that are inherited down the host lineage and consequently present a record of past host–viral associations. By mining ERVs from 65 host genomes sampled across vertebrate diversity, we uncover a great diversity of ERVs, indicating that retroviral sequences are much more prevalent and widespread across vertebrates than previously appreciated. The majority of ERV clades that we recover do not contain known retroviruses, implying either that retroviral lineages are highly transient over evolutionary time or that a considerable number of retroviruses remain to be identified. By characterizing the distribution of ERVs, we show that no major vertebrate lineage has escaped retroviral activity and that retroviruses are extreme host generalists, having an unprecedented ability for rampant host switching among distantly related vertebrates. In addition, we examine whether the distribution of ERVs can be explained by host factors predicted to influence viral transmission and find that internal fertilization has a pronounced effect on retroviral colonization of host genomes. By capturing the mode and pattern of retroviral evolution and contrasting ERV diversity with known retroviral diversity, our study provides a cohesive framework to understand host–virus coevolution better.
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.
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.
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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.
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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.
