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Harrison, M. C.

Publications and source records attributed to Harrison, M. C..

15 recordsLinked to original sources

Sociality in weevils is shaped by sheltering and convergent gene losses

Eusociality, characterized by overlapping generations, cooperative brood care, and reproductive division of labour, has arisen independently across diverse, phylogenetically distant insect orders, including Hymenoptera (ants, bees, and wasps), Blattodea (termites), and Coleoptera (weevils). While multiple studies have investigated the molecular evolution of sociality from solitary ancestors in Hymenoptera and Blattodea, so far little is known about the evolutionary signatures of social evolution in Coleoptera. Weevils (Curculionidae) provide an ideal system for addressing this question, as they cover the full spectrum of social complexity from parental care, through several origins of facultative eusociality to the only obligately eusocial beetle, Austroplatypus incompertus. We generated genome assemblies for A. incompertus and two facultatively eusocial weevil species, Xylosandrus germanus and Xyleborinus saxesenii, which together with 18 publicly available weevil genomes span two independent evolutionary origins of sociality. Our analyses reveal a genome-wide relaxation of purifying selection with increasing social complexity, which is most pronounced in A. incompertus. We find a significant excess of convergent gene family contractions in lineages where sociality evolved, and no evidence of elevated positive selection. These findings indicate that the molecular mechanisms of social evolution in weevils are primarily characterised by relaxed selection and gene loss, rather than adaptive innovation and gene family expansions. These observations are consistent with sheltering and reduced effective population size playing an important role, a pattern not previously observed in other clades.

evolutionary biology↗

Genome size, rather than sociality, predicts the turnover of duplicated genes in termites and hymenopterans

Gene duplication is a major source of genetic variation and is considered as an important driver of evolutionary novelties, including eusociality in insects, such as ants, wasps, bees, and termites. However, it remains unclear whether selection acts to increase gene copy number in social insects. Here, we studied the paranomes, namely, the whole set of paralogous genes in a genome, of Blattodea and Hymenoptera. We estimated the rates of gene duplication and loss using the distribution of synonymous substitution rate of paralogous genes and showed that regardless of sociality, duplicated genes were lost more rapidly than expected under random drift, indicating that negative selection on duplicated genes is prevalent across Blattodea and Hymenoptera. The rates of gene duplication and loss varied independently of sociality levels, but were positively related to genome size, suggesting the expansion/contraction of gene families can be a side effect of genome expansion/contraction. These results call for a reevaluation of adaptative gene duplications.

genomics↗

Rapid termite diversification is associated with increased transposable element activity

Termites are a lineage of social insects that originated during the Early Cretaceous [~]150 million years ago. They are the dominant decomposers in modern tropical and subtropical terrestrial ecosystems, a role they achieved through several phases of rapid diversification facilitated by unknown genetic mechanisms. Here, we investigated the link between termite diversification and the activity of transposable elements (TEs). We reconstructed the evolutionary history of TE replications using the genomes of 45 termite species and identified two waves of TE expansion that involved all major TE classes and superfamilies and took place synchronously across termite lineages. The first wave occurred around the end of the Cretaceous, and the second wave occurred during the Oligocene and Miocene, coinciding with the two major phases of termite diversification. We further estimated TE insertion/deletion rates along the species tree and showed that TE activity is positively correlated with termite diversification during the last [~]150 million years of evolution, providing evidence for a link between TE activity and diversification over a macroevolutionary timescale.

evolutionary biology↗

Deciphering the evolution of sex determination across the termite tree of life using high-quality genome assemblies

Most termites exhibit a unique sex-determining system, featuring multiple X and Y chromosomes that fuse into large complexes during male meiosis. The evolutionary origins of such complexes remain largely unknown. Using the genomes of 45 termites and two cockroaches, we investigated the evolution of sex determination systems in an entire insect lineage. We found that termite sex chromosomes are largely undifferentiated, likely reflecting extensive ongoing recombination. Evolving from the X0 system of cockroaches, most early-diverging termites exhibit a Y chromosome bearing the sex-determining gene doublesex, whereas doublesex is autosomal in most other termites. In contrast, other species exhibit multiple sex chromosomes that have undergone frequent turnover, except for Termitidae, which harbor conserved sex chromosomes. Our findings reveal important reworkings of the ancestral transformer-doublesex pathway in termites and suggest a potential role of doublesex in the formation of meiotic chromosomal complexes and caste differentiation.

evolutionary biology↗

Convergent genetic rewiring of the brain underlies termite sociality

How genomes encode major transitions in social evolution is unclear. We use 29 near-chromosome-quality genomes across a spectrum of social complexity to explore the genomic basis of termite sociality. We show that shifts in selection and gene family evolution preceded the emergence of sociality, pointing to subtler genetic causes of this major evolutionary transition (MET). In comparisons of convergent societal forms, we find that a subset of Odorant Receptors (ORs) underwent parallel expansions in independent advanced termite societies displaying true worker phenotypes. The identified OR genes play caste-differentiated roles in termite but not nearest roach brains and are especially elaborated in true workers. Together with evidence of co-opted nutritional signaling and behavioral genes at different levels of social complexity, our study illuminates the rewiring of the molecular machinery underlying this MET.

genomics↗

Genomic Insights into the Evolution of Parental Care in Weevils

Parental care, a key step in the evolution of sociality, has evolved multiple times in insects, yet the molecular mechanisms underlying its emergence remain poorly understood. Weevils (Curculionidae) exhibit diverse parental care behaviours, from nest building to egg and larval attendance, making them an ideal system to investigate genomic changes associated with subsociality. We analysed 13 high-quality weevil genomes, encompassing independent origins of egg and larval attendance, to test two predictions: (1) the sheltering hypothesis, where parental care relaxes selection on traits critical for independent larval survival, and (2) the regulatory hypothesis, where behavioural shifts are driven by changes in transcriptional regulation. Gene family evolution analyses revealed significantly more convergent contractions, particularly in genes linked to transcriptional regulation and enzymatic activity, on branches where larval attendance evolved, consistent with functional gene loss under relaxed selection. Selection analyses identified over 400 genes under relaxed selection, especially those associated with transcriptional regulation and neural plasticity, further supporting hypothesis 1. In contrast, positive selection and intensified selection were rare but enriched for genes regulating gene expression, consistent with hypothesis 2. Together, these results suggest that parental care in weevils drives both simplification of larval traits through relaxed selection and convergent gene loss, and innovation in caregiving behaviours via adaptive changes in gene regulation. Significance statementParental care is a pivotal evolutionary innovation, yet its genetic basis in insects remains underexplored. By comparing genomes from weevil species with and without care behaviours, we reveal two key processes shaping the emergence of subsociality: relaxation of selection on genes linked to larval independence and adaptive evolution in genes regulating gene expression. This combination likely reflects reduced demands on protected larvae alongside fine-tuning of parental behaviours. Our findings highlight how simple social systems can evolve through both loss and innovation, offering a comparative framework for understanding social evolution across insects.

evolutionary biology↗

Cryptocercus genomes expand knowledge of adaptations to xylophagy and termite sociality

Subsociality and wood-eating or xylophagy are understood as key drivers in the evolution of eusociality in Blattodea (cockroaches and termites), two features observed in the cockroach genus Cryptocercus, the sister group of all termites. We present and analyse two new high-quality genomes from this genus, C. punctulatus from North America and C. meridianus from Southeast Asia, to explore the evolutionary transitions to xylophagy and subsociality within Blattodea. Our analyses reveal evidence of relaxed selection in both Cryptocercus and termites, indicating that a reduction in effective population size may have occurred in their subsocial ancestors. These findings challenge the expected positive correlation between dN/dS ratios and social complexity, as Cryptocercus exhibits elevated dN/dS values that may exceed those of eusocial termites. Additionally, we identify positive selection on mitochondrial ribosomal proteins and components of the NADH dehydrogenase complex, suggesting significant evolutionary changes in energy production. Future studies incorporating additional genomic data from diverse blattodean species are essential to elucidate the molecular mechanisms driving transitions to xylophagy and eusociality.

evolutionary biology↗

Convergent Evolutionary Traces of Genomic Innovations and Depletions in Socially Parasitic Ants

Parasitism, a common strategy across life, often involves genomic reduction. Socially parasitic "slavemaking" ants provide an excellent model to study the evolution of this lifestyle. Here, we compared the genomes of four closely related, independently evolved parasite-host pairs and their outgroups to identify convergent patterns. While genome size and gene numbers remain relatively stable, parasites show increased positive and relaxed selection, more putative de novo genes which have recently emerged from previously non-coding regions, and a significant loss of chemical receptors, particularly those associated with the evolution of sociality. Hosts, however, retain many duplicated genes. Gene co-expression networks associated with nest-defence in hosts are rather conserved, while the network structure of raiding parasites is much more variable and reflects the independent evolutionary origin of social parasitism. Our findings suggest that while hosts primarily rely on existing molecular mechanisms for defence, parasite genome evolution is characterised by extensive, convergent gene loss, innovation, and network rewiring.

evolutionary biology↗

Investigating the mechanisms of antibody binding to alpha-synuclein for the treatment of Parkinson's Disease

Parkinsons Disease (PD) is an idiopathic neurodegenerative disorder with the second-highest prevalence rate behind Alzheimers Disease. The pathophysiological hallmarks of PD are both degeneration of dopaminergic neurons in the substantia nigra pars compacta and the inclusion of misfolded alpha-synuclein (-syn) aggregates known as Lewy bodies. Despite decades of research for potential PD treatments, none have been developed, and developing new therapeutic agents is a time-consuming and expensive process. Computational methods can be used to investigate the properties of drug candidates currently undergoing clinical trials to determine their theoretical efficiency at targeting -syn. Monoclonal antibodies (mAbs) are biological drugs with high specificity, and Prasinezumab (PRX002) is a mAb currently in Phase II, which targets the C-terminus (AA 118-126) of -syn. We utilized BioLuminate and PyMol for structure prediction and preparation of the fragment antigen-binding (Fab) region of PRX002 and 34 different conformations of -syn. Protein-protein docking simulations were performed using PIPER, and 3 of the docking poses were selected based on the best fit. Molecular dynamics simulations were conducted on the docked protein structures for 1000 ns, and hydrogen bonds, electrostatic, and hydrophobic interactions were analyzed using MDAnalysis to determine which residues were interacting and how often. Hydrogen bonds were shown to form frequently between the HCDR2 region of PRX002 and -syn. Free energy was calculated to determine binding affinity. The predicted binding affinity shows a strong antibody-antigen attraction between PRX002 and -syn. RMSD was calculated to determine the conformational change of these regions throughout the simulation. The mAbs developability was determined using computational screening methods. Our results demonstrate the efficiency and developability of this therapeutic agent.

biophysics↗

Major changes in domain arrangements are associated with the evolution of termite castes

Domains as functional protein units and their rearrangements along the phylogeny can shed light on the functional changes of proteomes associated with the evolution of complex traits like eusociality. This complex trait is associated with sterile soldiers and workers, and long-lived, highly fecund reproductives. Unlike in Hymenotpera (ants, bees, and wasps), the evolution of eusociality within Blattodea, where termites evolved from within cockroaches, was accompanied by a reduction in proteome size, raising the question of whether functional novelty was achieved with existing rather than novel proteins. To address this, we investigated the role of domain rearrangements during the evolution of termite eusociality. Analysing domain rearrangements in the proteomes of three solitary cockroaches and five eusocial termites, we inferred more than 5000 rearrangements over the phylogeny of Blattodea. The 90 novel domain arrangements that emerged at the origin of termites were enriched for several functions related to longevity, such as protein homeostasis, DNA repair, mitochondrial activity, and nutrient sensing. Many domain rearrangements were related to changes in developmental pathways, important for the emergence of novel castes. Along with the elaboration of social complexity, including permanently sterile workers and larger, foraging colonies, we found 110 further domain arrangements with functions related to protein glycosylation and ion transport. We found an enrichment of caste-biased expression and splicing within rearranged genes, highlighting their importance for the evolution of castes. Furthermore, we found increased levels of DNA methylation among rearranged compared to non-rearranged genes suggesting fundamental differences in their regulation. Our findings indicate an importance of domain rearrangements in the generation of functional novelty necessary for termite eusociality to evolve.

evolutionary biology↗

Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite.

The reproductive castes of eusocial insects are often characterised by extreme lifespans and reproductive output, indicating an absence of the fecundity/longevity trade-off. The role of DNA methylation in the regulation of caste- and age-specific gene expression in eusocial insects is controversial. While some studies find a clear link to caste formation in honeybees and ants, others find no correlation when replication is increased across independent colonies. Although recent studies have identified transcription patterns involved in the maintenance of high reproduction throughout the long lives of queens, the role of DNA methylation in the regulation of these genes is unknown. We carried out a comparative analysis of DNA methylation in the regulation of caste-specific transcription and its importance for the regulation of fertility and longevity in queens of the higher termite, Macrotermes natalensis. We found evidence for significant, well-regulated changes in DNA methylation in mature compared to young queens, especially in several genes related to ageing and fecundity in mature queens. We also found a strong link between methylation and caste-specific alternative splicing. This study reveals a complex regulatory role of fat body DNA methylation both in the division of labour in termites, and during the reproductive maturation of queens.

evolutionary biology↗

Live-bearing cockroach genome reveals convergent evolutionary mechanisms linked to viviparity in insects and beyond

Insects provide an unparalleled opportunity to link genomic changes with the rise of novel phenotypes, given tremendous variation in the numerous and complex adaptations displayed across the group. Among these numerous and complex adaptations, live-birth has arisen repeatedly and independently in insects and across the tree of life, suggesting this is one of the most common types of convergent evolution among animals. We sequenced the genome and transcriptome of the Pacific beetle-mimic cockroach, the only truly viviparous cockroach, and performed comparative analyses including two other viviparous insect lineages, the tsetse and aphids, to unravel the genomic basis underlying the transition to viviparity in insects. We identified pathways experiencing adaptive evolution, common in all viviparous insects surveyed, involved in uro-genital remodeling, maternal control of embryo development, tracheal system, and heart development. Our findings suggest the essential role of those pathways for the development of placenta-like structure enabling embryo development and nutrition. Viviparous transition seems also to be accompanied by the duplication of genes involved in eggshell formation. Our findings from the viviparous cockroach and tsetse reveal that genes involved in uterine remodeling are up-regulated and immune genes are down-regulated during the course of pregnancy. These changes may facilitate structural changes to accommodate developing young and protect them from the mothers immune system. Our results denote a convergent evolution of live-bearing in insects and suggest similar adaptive mechanisms occurred in vertebrates, targeting pathways involved in eggshell formation, uro-genital remodeling, enhanced tracheal and heart development, and reduced immunity.

genomics↗

Extreme longevity of highly fecund termite queens achieved by mitochondrial and insulin upregulation without harmful lipid signatures or accumulation

Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. To investigate the molecular mechanisms underlying their long lifespan, we carried out transcriptomics, lipidomics and metabolomics in Macrotermes natalensis on sterile short-lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. Reproductives share gene expression differences from workers in agreement with a reduction of several aging-related processes, involving upregulation of DNA damage repair and mitochondrial functions. Anti-oxidant gene expression is downregulated, while peroxidability of membranes in queens decreases. Against expectations, we observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp9. This pattern does not lead to deleterious fat storage in physogastric queens, while simple sugars dominate in their hemolymph and large amounts of resources are allocated towards oogenesis. Our findings support the notion that all processes causing aging need to be addressed simultaneously in order to prevent it.

molecular biology↗

Gene co-expression network reveals highly conserved, well-regulated anti-ageing mechanisms in old ant queens.

Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called selection shadow, due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analysed a gene co-expression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several anti-ageing mechanisms such as maintenance of proteostasis, transcriptional regulation and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared to young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens possibly facilitated by strong selection at old age and well-regulated anti-ageing mechanisms. Significance StatementUnderstanding the exceptional longevity of ant queens and how they defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory and molecular biology of ageing. In this study we offer several clues as to how this occurs on a molecular level in C. obscurior queens. Specifically, we believe a reduction in the selection shadow due to low extrinsic mortality, has allowed the evolution of well-regulated anti-ageing mechanisms. Consequently, we suggest several promising starting points for future research into the poorly understood phenomenon of extreme longevity in ant queens. Making progress in this field will not only allow us to better understand longevity and fertility in social insects but may also offer interesting research strategies for human ageing.

evolutionary biology↗

Hemimetabolous genomes reveal molecular basis of termite eusociality

Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the first, 2GB genome of a cockroach, Blattella germanica, and the 1.3GB genome of the drywood termite, Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.

evolutionary biology↗