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McMahon, D. P.

Publications and source records attributed to McMahon, D. P..

8 recordsLinked to original sources

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↗

Horizontal transfer of an antimicrobial peptide across insects

Antimicrobial peptides (AMPs) are key defence molecules of the innate immune system of plants and animals. Understanding the evolutionary origins of AMPs can help to explain how immune systems acquire novelty and vary in their defensive capabilities. However, AMPs evolve rapidly, and so the origins of similar AMPs across organisms is often unclear. Furthermore, false negatives due to low search sensitivity are common and can hinder confident annotations about true absences. Due to these difficulties, understanding whether similar AMP genes found in diverse organisms represent ancestral molecules or evolutionary novelties has been challenging. In this report, we present evidence of horizontal gene transfer (HGT) of the antifungal peptide gene Drosomycin across insects. We show that in Diptera, the presence of Drosomycin is restricted to the Melanogaster group and additionally the distant relative Drosophila busckii. We go on to recover Drosomycin genes in cockroaches (Blattodea), mantises (Mantodea), one katydid (Orthoptera), various beetles (Coleoptera), and a recently acquired pseudogenized Drosomycin locus in Liposcelis booklice (Psocodea), but no other insects. Explaining this diversity through shared ancestry requires at least 50 independent loss events, or just seven HGT events. Previous studies have suggested that similar AMPs found across divergent species reflect conservation from a common ancestor, or due to their small size, that they arose via convergent evolution resulting from pathogen-imposed selection. Our findings suggest horizontal gene transfer can be responsible for the presence of some AMP genes found scattered across the tree of life. By presenting a mechanism through which immune systems can acquire novelty, our study also suggests a possible explanation for certain lineage-specific competencies for defence against infectious disease. While loss of AMP genes is common in certain lineages, here we suggest gain of AMPs can occur just as suddenly.

evolutionary biology↗

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↗

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↗

Co-incubation of dsRNA reduces proportion of viable spores of Ascosphaera apis, a honey bee fungal pathogen

There are viral, fungal, bacterial and trypanosomal pathogens that negatively impact the individual and superorganismal health of the western honey bee. One fungal pathogen, Ascosphaera apis, affects larvae and causes the disease chalkbrood. A previous genome analysis of As. apis revealed that its genome encodes for RNA interference genes, similar to other fungi and eukaryotes. Here, we examined whether As. apis-targeting double-stranded RNA species could disrupt the germination of As. apis. We observed that when spores were co-incubated with As. apis-targeting dsRNA, fewer spores were activated for germination, suggesting an uptake of exogenous genetic material at the very onset of germination and consequent damage to essential transcripts needed for germination. Overall, these results indicate that the causative agent of chalkbrood disease, As. apis, can be successfully targeted using an RNAi-based strategy.

microbiology↗

When to care and when to kill: termites shape their collective response based on stage of infection

Termites defend their colonies from disease using an array of social behaviours, including allogrooming, cannibalism, and burial. We tested how groups of eastern subterranean termites (Reticulitermes flavipes) deploy these behaviours when presented with a nestmate at different stages of infection with the entomopathogenic fungus Metarhizium anisopliae. As expected, the termites groomed pathogen-exposed individuals significantly more than mock-treated controls; however, grooming levels were significantly higher after spore germination than before. Cannibalism became prevalent only after exposed termites became visibly ill, and burial was rarely observed. These results demonstrate that termites employ different strategies depending on the stage of infection that they encounter. Grooming intensity is linked not only to pathogen presence, but also to germination status, and, given the temporal correlation between cannibalism and visible signs of illness, the host may play a role in triggering its own sacrifice.

animal behavior and cognition↗