Biology subjects

Mallon, E. B.

Publications and source records attributed to Mallon, E. B..

12 recordsLinked to original sources

bioRxiv2025

Larval diapause slows adult epigenetic ageing in an insect model, Nasonia vitripennis

Epigenetic clocks based on DNA methylation provide robust biomarkers of biological age, yet the mechanistic basis and functional significance of slowing these clocks remain unclear. Progress has been limited by the lack of short-lived, genetically tractable model organisms with functional DNA methylation systems. The jewel wasp, Nasonia vitripennis, offers a unique solution. It combines a functional DNA methylation system with a short lifespan and established tools for experimental manipulation. We previously developed an epigenetic clock in Nasonia, but whether this clock reflects plastic, environmentally driven ageing processes was unknown. Here, we test this directly by experimentally inducing larval diapause, a naturally occurring developmental arrest triggered by environmental cues. Diapause extended median adult lifespan by 36% and significantly slowed the rate of epigenetic ageing. Using whole-genome bisulfite sequencing across multiple adult timepoints, we show that while adults that have passed through diapause as larvae initially emerge epigenetically older, their subsequent epigenetic ageing proceeds 29% more slowly than non-diapaused controls. Clock CpGs were enriched for gene ontology terms related to conserved nutrient-sensing and developmental pathways, including insulin/IGF signaling and mTOR, supporting the established mechanistic link between development and epigenetic ageing. These findings demonstrate that epigenetic ageing is plastic in Nasonia and can be experimentally modulated by early-life environment, establishing this animal model as a tractable system for dissecting the causal mechanisms of epigenetic ageing.

genetics↗

bioRxiv2024

Developmental DNA Methylation in the Parasitoid Wasp Nasonia vitripennis

DNA methylation is a crucial epigenetic mark the development of many insect species, being essential for fertility and the progression of development in a range of organisms. However, the mechanisms underpinning the role of DNA methylation in insect development remains elusive. Furthermore, the patterns of methylation in different species can be varied. Here we aim to profile methylation across metamorphosis in the insect DNA methylation model Nasonia vitripennis for the first time. We find DNA methylation is at the highest in the embryo, and at the lowest in the larva. We find that the gene expression levels of NvTet and NvDnmt enzymes compliment the observed methylation patterns. Performing differential methylation analysis we find enriched GO terms for developmentally specific processes and find sites with differential methylation are share homology with developmentally linked transcription factors. Additionally, we identify sites uniquely methylated in each developmental stage, many of which also share homology with developmentally linked transcription factors. In all, we find that methylation is variable in its global methylation levels and site specific methylation throughout Nasonia vitripennis development, but find no obvious link with gene expression.

genetics↗

bioRxiv2023

Air pollution modifies key colonization factors of the beneficial bee gut symbiont Snodgrassella alvi and disrupts the bumblebee (Bombus terrestris) gut microbiome.

Air pollution is the worlds largest environmental health risk. Particulate pollutants, a major component of air pollution, are detrimental to human health and a significant risk to wildlife and ecosystems globally. Black carbon, a by-product of fossil fuel and biomass burning, is a key constituent of air pollution with levels continuing to increase worldwide. Here we describe the effects of black carbon on the beneficial gut microbiome of an important global insect pollinator, the buff-tailed bumblebee (Bombus terrestris). Our data shows that exposure to black carbon particulates alters the biofilm structure, gene expression and initial adhesion of beneficial bee gut coloniser, Snodgrassella alvi in vitro. Additionally, our results show that black carbon disrupts adult Bombus terrestris gut microbiome composition, a vital component to bee health. Exposure to black carbon increased bees viable gut bacteria and significantly altered the abundance of beneficial core bacteria Gilliamella and Bombilactobacillus in the microbiome. These findings demonstrate that exposure to black carbon air pollution has direct, measurable effects on bees beneficial gut commensal bacteria and microbiome. Together these data highlight that particulate pollutants are an underexplored risk for the health of insect pollinators.

microbiology↗

bioRxiv2023

A role for DNA methylation in bumblebee morphogenesis hints at female-specific developmental erasure.

Epigenetic mechanisms, such as DNA methylation, are crucial factors in animal development. In some mammals almost all DNA methylation is erased during embryo development and re-established in a sex- and cell-specific manner. This erasure and re-establishment is thought to primarily be a vertebrate-specific trait. Insects are particularly interesting in terms of development as many species often undergo remarkable morphological changes en route to maturity, i.e. morphogenesis. However, little is known about the role of epigenetic mechanisms in this process across species. We have used whole genome bisulfite sequencing to track genome-wide DNA methylation changes through the development of an economically and environmentally important pollinator species, the bumblebee Bombus terrestris. We find overall levels of DNA methylation vary throughout development and we find developmentally relevant differentially methylated genes throughout. Intriguingly, we have identified a depletion of DNA methylation in ovaries and an enrichment in sperm. We suggest this could represent a sex-specific DNA methylation erasure event. To our knowledge this is the first suggestion of possible developmental DNA methylation erasure in an insect species. This study lays the required groundwork for functional experimental work to determine if there is a causal-nature to the DNA methylation differences identified. Additionally, the application of single-cell methylation sequencing to this system will enable more accurate identification of when/if DNA methylation is erased during development.

developmental biology↗

bioRxiv2023

Lack of paternal silencing and ecotype-specific expression in head and body lice hybrids.

Paternal genome elimination (PGE) is a non-Mendelian inheritance system in which males develop from fertilised eggs but their paternally-inherited chromosomes are eliminated before or during spermatogenesis. Therefore, PGE males only transmit their maternally inherited set of chromosomes to their offspring. PGE has been described in numerous arthropod species, many of which are pests or parasites, posing a severe economic burden on crop production and/or with implications for human health. In order to understand how PGE has evolved on the molecular level, to potentially develop novel control strategies, we need to examine species which display basal forms of PGE. The human louse, Pediculus humanus, represents an ideal model system to understand the molecular underpinnings of PGE. In this study we analysed parent-of-origin allele specific expression patterns in male offspring of crosses between head and body lice ecotypes. We have shown that hybrid adult males of P. humanus display biparental gene expression, which constitutes the first known case of a species with PGE in which genetic activity of paternal chromosomes in the soma is not affected by embryonic heterochromatinization or (partial or complete) elimination. We have also identified maternally-biased genes (potentially imprinted genes) which may be involved in the elimination of paternal chromosomes during spermatogenesis. Finally, we have identified genes which show ecotype-specific expression bias. Given the low genetic diversity between ecotypes this is suggestive for a role of epigenetic processes in ecotype differences. These findings have implications for models of pediculicide resistance in human lice and for the development of novel epigenetic-mediated control strategies.

evolutionary biology↗

bioRxiv2023

An epigenetic clock in an insect model system

BackgroundThe ageing process is a multifaceted phenomenon marked by the gradual deterioration of cellular and organismal functions, accompanied by an elevated susceptibility to diseases. The intricate interplay between genetic and environmental factors complicates research, particularly in complex mammalian models. In this context, simple invertebrate organisms have been pivotal, but the current models lack detectable DNA methylation limiting the exploration of this critical epigenetic ageing mechanism. This study introduces Nasonia vitripennis, the jewel wasp, as an innovative invertebrate model for investigating the epigenetics of ageing. Leveraging its advantages as a model organism and possessing a functional DNA methylation system, Nasonia emerges as a valuable addition to ageing research. ResultsWhole-genome bisulfite sequencing unveiled dynamic alterations in DNA methylation, with differentially methylated CpGs between distinct time points in both male and female wasps. These changes were associated with numerous genes, enriching for functions related to telomere maintenance, histone methylation, and mRNA catabolic processes. Additionally, other CpGs were found to be variably methylated at each timepoint. Sex-specific effects on epigenetic entropy were observed, indicating differential patterns in the loss of epigenetic stability over time. Constructing an epigenetic clock containing 19 CpGs revealed a robust correlation between epigenetic age and chronological age. ConclusionsNasonia vitripennis emerges as a promising model for investigating the epigenetics of ageing, shedding light on the intricate dynamics of DNA methylation and their implications for age-related processes. This research not only expands the repertoire of ageing models but also opens avenues for deeper exploration of epigenetic mechanisms in the context of ageing.

genomics↗

bioRxiv2021

Parent of origin DNA methylation as a potential mechanism for genomic imprinting in bees.

Social insects display extreme phenotypic differences between sexes and castes even though the underlying genome can be almost identical. Epigenetic processes have been proposed as a possible mechanism for mediating these phenotypic differences. Using whole genome bisulfite sequencing of queens, males and reproductive female workers we have characterised the sex- and caste-specific methylome of the bumblebee Bombus terrestris. We have identified a potential role for DNA methylation in histone modification processes which may influence sex and caste phenotypic differences. We also find differentially methylated genes generally show low levels of DNA methylation which may suggest a separate function for lowly methylated genes in mediating transcriptional plasticity. Unlike highly methylated genes which are usually involved in housekeeping functions. We also examined the relationship between the underlying genome and the methylome using whole genome re-sequencing of the same queens and males. We find DNA methylation is enriched at zero-fold degenerate sites. We suggest DNA methylation may be acting as a mutagen at these sites thereby providing substrate for selection via changes in gene transcription mediated by the underlying genotype. However, we did not see any relationship between DNA methylation and rates of positive selection in our samples. In order to fully assess a possible role for DNA methylation in adaptive processes a specifically designed study using natural population data is needed.

evolutionary biology↗

bioRxiv2021

Sexual morph specialisation in a trioecious nematode balances opposing selective forces.

The coexistence of different mating strategies, whereby a species can reproduce both by selfing and outcrossing, is an evolutionary enigma that has long intrigued biologists (Darwin, 1877). Theory predicts only two stable mating states : outcrossing with strong inbreeding depression or selfing with weak inbreeding depression. As these two mating strategies are subject to opposing selective forces, mixed breeding systems are thought to be a rare transitory state, yet they have been found to persist even after multiple speciation events. We hypothesise that if each mating strategy plays a distinctive role during the species life history, opposing selective pressures could be balanced, permitting the stable co-existence of selfing and outcrossing sexual morphs. In this scenario, we would expect each sexual morph to be specialised in their respective roles. Here we show, using a combination of behavioural, physiological and gene expression studies, that the selfing (hermaphrodite) and outcrossing (female) sexual morphs of the trioecious nematode Auanema freiburgensis have distinct adaptations optimised for their different roles during the life cycle. A. freiburgensis hermaphrodites are produced under stressful conditions, are specialised for dispersal to new habitat patches and exhibit metabolic and intestinal changes that enable them to meet the energetic cost of dispersal and reproduction. In contrast, A. freiburgensis females are produced in favourable conditions, facilitate rapid population growth and compensate for the lack of reproductive assurance by reallocating resources from intestinal development to robust mate-finding behaviour. The specialisation of each mating system for their role in the life cycle could balance opposing selective forces allowing the stable maintenance of both outcrossing and selfing mating systems in A. freiburgensis.

evolutionary biology↗

bioRxiv2020

Bumblebee worker castes show differences in allele-specific DNA methylation and allele-specific expression.

Allele-specific expression is when one allele of a gene shows higher levels of expression compared to the other allele, in a diploid organism. Genomic imprinting is an extreme example of this, where some genes exhibit allele-specific expression in a parent-of-origin manner. Recent work has identified potentially imprinted genes in species of Hymenoptera. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals DNA methylation is often associated with imprinted genes. DNA methylation systems have been described in species of Hymenoptera, providing a candidate imprinting mechanism. Using previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive castes and the proportion of allele-specific expression bias generally varies between colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both castes. There is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that DNA methylation does not directly drive genome-wide allele-specific expression in this species. Only a small number of the genes identified may be imprinted and it may be these genes which are associated with allele-specific DNA methylation. Future work utilising reciprocal crosses to identify parent-of-origin DNA methylation will further clarify the role of DNA methylation in parent-of-origin allele-specific expression.

evolutionary biology↗

bioRxiv2020

Genome-wide search for parent-of-origin allele specific expression in Bombus terrestris.

Genomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Haigs kinship theory hypothesizes that genomic imprinting is due to an evolutionary conflict of interest between alleles from the mother and father. In social insects, it has been suggested that genomic imprinting should be widespread. One recent study identified parent-of-origin expression in honeybees and found evidence supporting the kinship theory. However, little is known about genomic imprinting in insects and multiple theoretical predictions must be tested to avoid single-study confirmation bias. We, therefore, tested for parent-of-origin expression in a primitively eusocial bee. We found equal numbers of maternally and paternally biased expressed alleles. The most highly biased alleles were maternally expressed, offering support for the kinship theory. We also found low conservation of potentially imprinted genes with the honeybee, suggesting rapid evolution of genomic imprinting in Hymenoptera. Impact summaryGenomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. Genomic imprinting is an evolutionary paradox. Natural selection is expected to favour expression of both alleles in order to protect against recessive mutations that render a gene ineffective. What then is the benefit of silencing one copy of a gene, making the organism functionally haploid at that locus? Several explanations for the evolution of genomic imprinting have been proposed. Haigs kinship theory is the most developed and best supported. Haigs theory is based on the fact that maternally (matrigene) and paternally (patrigene) inherited genes in the same organism can have different interests. For example, in a species with multiple paternity, a patrigene has a lower probability of being present in siblings that are progeny of the same mother than does a matrigene. As a result, a patrigene will be selected to value the survival of the organism it is in more highly, compared to the survival of siblings. This is not the case for a matrigene. Kinship theory is central to our evolutionary understanding of imprinting effects in human health and plant breeding. Despite this, it still lacks a robust, independent test. Colonies of social bees consist of diploid females (queens and workers) and haploid males created from unfertilised eggs. This along with their social structures allows for novel predictions of Haigs theory. In this paper, we find parent of origin allele specific expression in the important pollinator, the buff-tailed bumblebee. We also find, as predicted by Haigs theory, a balanced number of genes showing matrigenic or patrigenic bias with the most extreme bias been found in matrigenically biased genes.

evolutionary biology↗

bioRxiv2019

The effects of the neonicotinoid imidacloprid on gene expression and DNA methylation in the buff-tailed bumblebee Bombus terrestris

Neonicotinoids are effective insecticides used on many important arable and horticultural crops. They are nicotinic acetylcholine receptor agonists which disrupt the function of insect neurons and cause paralysis and death. In addition to direct mortality, there are numerous sublethal effects of low doses of neonicotinoids on bees. We hypothesize that some of these large array of effects could be a consequence of epigenetic changes in bees induced by neonicotinoids. We compared whole methylome (BS-seq) and RNA-seq libraries of the brains of buff tailed bumblebee Bombus terrestris workers exposed to field realistic doses of the neonicotinoid imidacloprid to libraries from control workers. We found numerous genes which show differential expression between neonicotinoid treated bees and control bees, but no differentially methylated cytosines in any context. We found CpG methylation to be focused mainly in exons and associated with highly expressed genes. We discuss the implications of our results for future legislation.

ecology↗

bioRxiv2019

Methylation and Gene Expression Differences Between Reproductive Castes of Bumblebee Workers.

Phenotypic plasticity is the production of multiple phenotypes from a single genome and is notably observed in social insects. Multiple epigenetic mechanisms have been associated with social insect plasticity, with DNA methylation being explored to the greatest extent. DNA methylation is thought to play a role in caste determination in Apis mellifera, and other social insects, but there is limited knowledge on its role in other bee species. In this study we analysed whole genome bisulfite sequencing and RNA-seq data sets from head tissue of reproductive and sterile castes of the eusocial bumblebee Bombus terrestris. We found genome-wide methylation in B. terrestris is similar to other social insects and does not differ between reproductive castes. We did, however, find differentially methylated genes between castes, which are enriched for multiple biological processes including reproduction. However we found no relationship between differential methylation and differential gene expression or differential exon usage between castes. Our results also indicate high inter-colony variation in methylation. These findings suggest methylation is associated with caste differences but may serve an alternate function, other than direct caste determination in this species. This study provides the first insights into the nature of a bumblebee caste specific methylome as well as its interaction with gene expression and caste specific alternative splicing, providing greater understanding of the role of methylation in phenotypic plasticity within social bee species. Future experimental work is needed to determine the function of methylation and other epigenetic mechanisms in social insects.\n\nImpact SummarySocial insects, such as ants, termites, bees and wasps, can produce individuals with extreme physical and behavioural differences within the same colony known as castes (e.g. workers/soldiers/queens). These individuals have similar genomes and many studies have associated epigenetic mechanisms with the differences observed. Epigenetic modifications are changes that affect how genes are expressed without changing the underlying DNA code. Here we investigated differences in DNA methylation (a well researched modified base) between different reproductive castes of the bumblebee, Bombus terrestris, an economically and environmentally important pollinator species. We found B. terrestris has a similar methylation profile to other social insect species in terms of the distribution of methylation throughout the genome and the relationship between methylation and gene expression. Genes that have differences in methylation between reproductive castes are involved in multiple biological processes, including reproduction, suggesting methylation may hold multiple functions in this species. These differentially methylated genes are also different to differentially methylated genes identified between honeybee reproductive castes, again suggesting methylation may have a variable function. These findings provide greater understanding of the role of methylation in caste determination in social insect species.

evolutionary biology↗