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RNA virus populations are composed of highly diverse individuals that form a cloud of related sequences commonly referred to as a ‘quasispecies’1–3. This diversity arises as a consequence of low-fidelity genome replication4,5. By contrast, DNA Virus populations contain more uniform individuals with similar fitness6.
Genome diversity is often correlated with increased Fitness in RNA viruses, while DNA viruses are thought to require more faithful genome replication. During DNA replication, erroneously incorporated bases are removed by a 3′-5′ exonuclease, a highly conserved enzymatic function of replicative DNA but not RNA polymerases. This proofreading process enhances replication fidelity and ensures the genome integrity of DNA organisms, including large DNA viruses7. Here, we show that a herpesvirus can tolerate impaired exonucleolytic proofreading, resulting in DNA virus populations, which, as in RNA viruses8, are composed of highly diverse genotypes of variable individual fitness. This indicates that herpesvirus mutant diversity may compensate for individual Fitness loss. Notably, in vivo infection with diverse virus populations results in a marked increase in virulence compared to genetically homogenous parental virus. While we cannot exclude that the increase in virulence is caused by selection of and/or interactions between individual genotypes, our findings are consistent with quasispecies dynamics. Our results contrast with traditional views of DNA virus replication and evolution, and indicate that a substantial increase in population diversity can lead to higher virulence.
Termitidae comprises 80% of all termite species that play dominant decomposer roles in Tropical cosystems. Two major events during Termite evolution were the loss of cellulolytic gut protozoans in the ancestor of Termitidae and the subsequent gain in the termitid subfamily Macrotermitinae of fungal symbionts cultivated externally in ‘‘combs’’ constructed within the nest. How these symbiotic transitions occurred remains unresolved. Phylogenetic analyses of mitochondrial data previously suggested that Macrotermitinae is the earliest branching termitid lineage, followed soon after by Sphaerotermitinae, which cultivates bacterial symbionts on combs inside its nests. This has led to the hypothesis that comb building was an important evolutionary step in the loss of gut protozoa in ancestral termitids. We sequenced genomes and transcriptomes of 55 termite species and reconstructed phylogenetic trees from up to 4,065 orthologous genes of 68 species. We found strong support for a novel sister-group relationship between the bacterial comb-building Sphaerotermitinae and fungus comb-building Macrotermitinae.
This key finding indicates that comb building is a derived trait within Termitidae and that the creation of a comb-like ‘‘external rumen’’ involving bacteria or fungi may not have driven the loss of protozoa from ancestral termitids, as previously hypothesized.
Instead, associations with gut prokaryotic symbionts, combined with dietary shifts from wood to other plant-based substrates, may have played a more important role in this symbiotic transition. Our phylogenetic tree provides a platform for future studies of comparative termite evolution and the evolution of symbiosis in this taxon.
The importance of soldiers to termite Society defence has long been recognized, but the contribution of soldiers to other societal functions, such as colony immunity, is less well understood.
We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behaviour, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection.
We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of Proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
Virulence determines the impact a pathogen has on the fitness of its host, yet current understanding of the evolutionary origins and causes of virulence of many pathogens is surprisingly incomplete. Here, we explore the evolution of Marek’s disease virus (MDV), a herpesvirus commonly afflicting chickens and rarely other avian species. The history of MDV in the 20th century represents an important case study in the evolution of virulence. The severity of MDV infection in chickens has been rising steadily since the adoption of intensive farming techniques and vaccination programs in the 1950s and 1970s, respectively. It has remained uncertain, however, which of these factors is causally more responsible for the observed increase in virulence of circulating viruses. We conducted a phylogenomic study to understand the evolution of MDV in the context of dramatic changes to poultry farming and disease control. Our analysis reveals evidence of geographical structuring of MDV strains, with reconstructions supporting the emergence of virulent viruses independently in North America and Eurasia. Of note, the emergence of virulent viruses appears to coincide approximately with the introduction of comprehensive vaccination on both continents. The time-dated phylogeny also indicated that MDV has a mean evolutionary rate of ~1.6 × 10−5 substitutions per site per year. An examination of gene-linked mutations did not identify a strong association between mutational variation and virulence phenotypes, indicating that MDV may evolve readily and rapidly under strong selective pressures and that multiple genotypic pathways may underlie virulence adaptation in MDV.
Effective immunity is essential for maintaining insect society integrity but the mechanisms that connect immunity at the level of the individual to the level of society are poorly understood. Here, we begin to resolve this issue by addressing the interaction between individual immunity and caste identity in the termite Neotermes castaneus. We characterize the transcriptomic responses of different castes to a general immune challenge by sequencing mRNAs from false workers, soldiers and reproductive following injection with a cocktail of heat-killed pathogens. We found many more genes to be differentially regulated in reproductives (1420 and 398 genes down- and upregulated respectively) than soldiers (90 and 108 genes) or false workers (135 and 71 genes). We go on to conduct a quantitative analysis of the specific changes to immune regulation across the castes following pathogen exposure, before discussing the implications of these findings for our understanding of the evolution of immunity in eusocial termites.
Differentiation of immune response with castes in termites by de novo transcriptome sequencing
(2017)
Eusociality is one major evolutionary transitions, during which the division of labor is considered as the hallmark feature. This character of evolution, also interpreted as task specialization, is associated with multiple morphological, physiological and behavioral adaptations required for brood care, foraging, and defense. With these adaptations which ultimately cause the formation of castes in insect sociality (mostly in termites, ants, some bees and wasps), while whether immune system is related to eusociality in termites is rare understood. We hypothesis that immune system in termite sociality had also differentiation along with the formation of castes. We address this issue by exploring the immune responses of different castes with de novo transcriptome sequencing. After injection with cocktail of heat-killed pathogens (Pseudomonas entomophila, Bacillus thuringiensis, Saccharomyces cerevisiae), the mRNAs from false workers, soldiers and reproductive of Neotermes canstaneus were sequenced. We found much more genes are regulated (1420 genes downregulated and 398 genes upregulated) in reproductives compared to soldiers (90 genes downregulated and 108 genes upregulated) and false workers (135 genes downregulated and 71 genes upregulated). In these upregulated genes, reproductives had 54 same genes as soldiers, while only 7 same genes as workers which almost is same number between soldiers and workers. In the downregulated genes, reproductives shared 50 and 41 same genes as soldiers
and workers, respectively. Besides, soldiers and workers had 29 same downregulated genes. From these findings, it is indicated that the immune system differentiates with division of labor during eusociality in termites.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
The first sterile caste to evolve in termites was the soldier. While the importance of soldiers to termite society defense has long been recognized, the contribution of soldiers to other societal functions, such as colony immunity, is less well understood. We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behavior, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection. We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
The first sterile caste to evolve in termites was the soldier. While the importance of soldiers to termite society defense has long been recognized, the contribution of soldiers to other societal functions, such as colony immunity, is less well understood. We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behavior, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection. We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
It is thought that the primary function of soldier castes in insect societies is to protect colonies against macroscale predators and parasites. By comparison, little attention has been paid to the role of soldiers against pathogenic microorganisms. This is a significant gap in knowledge because in non-hymenopteran societies, such as the eusocial termites, the first-evolved, and arguably most important sterile caste, is the soldier.
Here, we investigate whether soldiers of the wood-eating termite, Mastotermes darwiniensis, play a significant role in social immunity. Firstly, we show that uninfected soldiers improve the survival of worker nestmates exposed to a lethal dose of a fungal pathogen, despite the fact that soldiers (unlike workers) cannot allogroom. Hazard ratios of pathogen-exposed workers decreased from 6.616 in infected groups to 4.376 and 2.786 in infected groups containing uninfected workers and soldiers, respectively. To explore the basis of soldier protection, we applied soldier-derived oral secretions to infected worker cuticle, resulting in significantly improved worker survival. Soldiers that contacted infected workers were also more active and produced secretions with significantly greater mass variance than soldiers exposed to uninfected workers.
Significantly, we show that secretions produced by soldiers inhibit the growth of a broad range of microorganisms, including gram-negative and gram-positive bacteria, in addition to fungi. Our findings demonstrate that soldiers can contribute powerful antimicrobial factors to external immune defenses, effectively complementing behaviour-based protective activities provided by workers.