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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 exploitmultiple ecological niches. Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis.
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. 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.
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.
Virologists. You might know a couple of them, but unless you are a virologist yourself, the probability that you have collaborated with one in the past is low. The community is relatively small, but they pack a heavy punch and are expected to play a leading role in the research into pathogens that lies ahead. You may ask why we think virologists are our future. Suffice it to say that it is not just because they have invented technologies that belong to the space age, including use of viruses as vehicles to shuttle genes into cells[1], organic nanoparticles with specific tools attached to their surfaces to get inside target cells[2], and using genetically modified viruses as therapies to fight against cancer[3]. Did you know that virologists currently only know of about 3,200 viral species but that more than 320,000 mammal-associated viruses[4] are thought to await discovery? Just think about the viruses hidden in the Arctic ice[5] or in the insects and other animals from once cut-off regions in the world, which now face ever-increasing human exposure[6]. But a heroic (as well as an apocalyptic) role for virologists may also be on the horizon, as the adoption of phage therapy may, in the future, be used to control harmful bacteria when antibiotics fail
Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens
(2017)
Background: Organisms typically face infection by diverse pathogens, and hosts are thought to have developed specific responses to each type of pathogen they encounter. The advent of transcriptomics now makes it possible to test this hypothesis and compare host gene expression responses to multiple pathogens at a genome-wide scale. Here, we performed a meta-analysis of multiple published and new transcriptomes using a newly developed bioinformatics approach that filters genes based on their expression profile across datasets. Thereby, we identified common and unique molecular responses of a model host species, the honey bee (Apis mellifera), to its major pathogens and parasites: the Microsporidia Nosema apis and Nosema ceranae, RNA viruses, and the ectoparasitic mite Varroa destructor, which transmits viruses.
Results: We identified a common suite of genes and conserved molecular pathways that respond to all investigated pathogens, a result that suggests a commonality in response mechanisms to diverse pathogens. We found that genes differentially expressed after infection exhibit a higher evolutionary rate than non-differentially expressed genes. Using our new bioinformatics approach, we unveiled additional pathogen-specific responses of honey bees; we found that apoptosis appeared to be an important response following microsporidian infection, while genes from the immune signalling pathways, Toll and Imd, were differentially expressed after Varroa/virus infection. Finally, we applied our bioinformatics approach and generated a gene co-expression network to identify highly connected (hub) genes that may represent important mediators and regulators of anti-pathogen responses.
Conclusions: Our meta-analysis generated a comprehensive overview of the host metabolic and other biological processes that mediate interactions between insects and their pathogens. We identified key host genes and pathways that respond to phylogenetically diverse pathogens, representing an important source for future functional studies as well as offering new routes to identify or generate pathogen resilient honey bee stocks. The statistical and bioinformatics approaches that were developed for this study are broadly applicable to synthesize information across transcriptomic datasets. These approaches will likely have utility in addressing a variety of biological questions.
The bipartite interactions between insect hosts and their bacterial gut microbiota, or their bacterial pathogens, are empirically and theoretically well-explored. However, direct, and indirect tripartite interactions will also likely occur inside a host. These interactions will almost certainly affect the trajectory of pathogen virulence evolution, an area that is currently under researched. The interactions within tripartite associations can be competitive, that is, exploitative-competition, interference-competition or apparent-competition. Competitive interactions will be significantly influenced by non-competitive effects, for example, immunopathology, immunosuppression, and microbiota-mediated tolerance. Considering a combination of these interactions and effects, will enable an increased understanding of the evolution of pathogen virulence. This new perspective allows us to identify several novel research questions, which we hope will be a useful framework for future research.
Bees are considered to be threatened globally, with severe overwinter losses of the most important commercial pollinator, the Western honeybee, a major concern in the Northern Hemisphere. Emerging infectious diseases have risen to prominence due to their temporal correlation with colony losses. Among these is Deformed wing virus (DWV), which has been frequently linked to colony mortality. We now provide evidence of a strong statistical association between overwintering colony decline in the field and the presence of DWV genotype-B (DWV-B), a genetic variant of DWV that has recently been shown to be more virulent than the original DWV genotype-A. We link the prevalence of DWV-B directly to a quantitative measure of overwinter decline (workforce mortality) of honeybee colonies in the field. We demonstrate that increased prevalence of virus infection in individual bees is associated with higher overwinter mortality. We also observed a substantial reduction of infected colonies in the spring, suggesting that virus-infected individuals had died during the winter. Our findings demonstrate that DWV-B, plus possible A/B recombinants exhibiting DWV-B at PCR primer binding sites, may be a major cause of elevated overwinter honeybee loss. Its potential emergence in naïve populations of bees may have far-reaching ecological and economic impacts.
The soil-feeding habit is an evolutionary novelty found in some advanced groups of termites. The study of such groups is important to revealing interesting adaptations to this way-of-life. The genus Verrucositermes is one such example, characterized by peculiar outgrowths on the head capsule, antennae and maxillary palps, which are not found in any other termite. These structures have been hypothesized to be linked to the presence of a new exocrine organ, the rostral gland, whose structure has remained unexplored.
We have thus studied the ultrastructure of the epidermal layer of the head capsule of Verrucositermes tuberosus soldiers.We describe the ultrastructure of the rostral gland, which consists of class 3 secretory cells only. The dominant secretory organelles comprise rough endoplasmic reticulum and Golgi apparatus, which provide secretions delivered to the surface of the head, likely made of peptide-derived components of unclear function. We discuss a possible role of the rostral gland of soldiers as an adaptation to the frequent encounter with soil pathogens during search for new food resources.
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 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 termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.
A broad suite of immune adaptations have evolved in social insects which hold close parallels with the immune systems of multicellular individuals. However, comparatively little is known about the evolutionary origins of immunity in social insects. We tackle this by identifying immune genes from 18 cockroach and termite species, spanning a gradient of social lifestyles. Termites have undergone contractions of major immune gene families during the early origin of the group, particularly in antimicrobial effector and receptor proteins, followed by later re-expansions in some lineages. In a comparative gene expression analysis, we find that reproductive individuals of a termite invest more in innate immune regulation than other castes. When colonies encounter immune-challenged nestmates, gene expression responses are weak in reproductives but this pattern is reversed when colony members are immune-challenged individually, with reproductives eliciting a greater response to treatment than other castes. Finally, responses to immune challenge were more comprehensive in both subsocial and solitary cockroaches compared to termites, indicating a reduced overall ability to respond to infection in termites. Our study indicates that the emergence of termite sociality was associated with the evolution of a tapered yet caste-adapted immune system.