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Day, J. P.

Publications and source records attributed to Day, J. P..

11 recordsLinked to original sources

Invasion history of Aedes (Stegomyia) albopictus into Mesoamerica based on mitogenomes and Wolbachia symbionts: Multiple introductions with temperate origins.

The global invasion of the Asian tiger mosquito Aedes albopictus has led to an increase in arboviral disease, including within Mesoamerica. Understanding vector invasion routes is important for public health because it directs biosecurity and identifies sources of adaptive allele spread. Panama is an important hub of global trade with opportunities for Aedes introduction through both maritime and overland routes but dispersal into the Isthmus has not yet been investigated. We therefore sought to investigate the population structure and invasion history of Ae. albopictus into Panama, targeting both its mitogenome and associated Wolbachia. Historical demographic analysis with Bayesian phylogeographic diffusion models and estimates of divergence revealed that Panamanian Ae. albopictus and its associated Wolbachia have a convergent evolutionary history resulting from multiple introductions. Both could be traced to Asian-derived lineages introduced via the Americas, with invasion primarily through the maritime trade of the Panama Canal rather than overland dispersal from neighboring Costa Rica. An investigation of the relative density of Wolbachia in Panama revealed that both the strains wAlbB and wAlbA were at a notably lower density compared to other worldwide locations. This finding has implications for arbovirus transmission and raises important questions about how Wolbachia density is impacted by the environment and impacts on population control. Overall, the Panama Canal is a key route for vector introductions into Mesoamerica.

evolutionary biology↗

Evolutionary genomics of a natural Wolbachia superinfection in the dengue mosquito Aedes albopictus

Aedes albopictus, an invasive mosquito vector of human pathogens, is naturally infected by two strains of the endosymbiotic bacterium Wolbachia, wAlbA and wAlbB. Here, we present a comprehensive genomic analysis of these Wolbachia strains, their associated plasmids, and host mitochondrial DNA (mtDNA). We observed extensive variation in Wolbachia densities--spanning over three orders of magnitude--indicating that infections often exist at extremely low levels and this variation is largely driven by environmental factors. Phylogenetic analyses revealed concordant evolutionary histories among mitochondrial, Wolbachia, and plasmid genomes, with no strong evidence for horizontal or paternal transmission. We estimate that the common ancestor of the superinfection existed [~]6,000--9,000 years ago. Patterns of genetic structure and divergence indicate that the subsequent geographical spread of Wolbachia has mirrored host population history. Comparative rate analyses revealed that wAlbA evolves more slowly than wAlbB, consistent with a reduced mutation rate. Despite the close relationship between wAlbB lineages, gene content in this strain is highly variable, with 184 genes exhibiting presence-absence or copy number variation across strains, including genes involved in inducing cytoplasmic incompatibility. Several of these genes reside in repetitive or prophage regions, indicating that transposable elements appear to drive structural genomic variation in Wolbachia populations. Together, our results highlight extensive natural diversity within Wolbachia populations and provide a foundation for understanding symbiont dynamics in nature and to inform the selection of strains for Wolbachia-based vector control programs.

evolutionary biology↗

MHC-I diversity enables rapid adaptation during viral pandemic in wild rabbit populations

Emerging diseases can have devastating consequences for wild species, with long-term effects depending on the ability of the host to evolve resistance. Here, we show that major histocompatibility complex (MHC) genes provided standing genetic variation that enabled rabbits to mount a rapid evolutionary response to the myxoma virus pandemic that began in the 1950s. Using historical and modern specimens starting in 1865 and spanning the pandemic, we found strong parallel shifts in MHC-I allele frequencies across Australia, Britain and France, alongside population-specific signals. These evolutionary shifts appear to have altered antigen presentation to T cells. Our results provide evidence that MHC-I is under strong selection in natural populations during a pandemic, and that the high polymorphism of MHC may have contributed to the evolutionary rescue of these populations.

evolutionary biology↗

A humoral immune response to parasitoid wasps in Drosophila is regulated by JAK/STAT, NF-κB and GATA

The two arms of innate immunity consist of the cell-mediated cellular defenses and the systemic humoral immune responses. Drosophila humoral immune defenses in the context of antimicrobial immunity, particularly the regulation and activation of antimicrobial peptide secretion from the fat body, have been studied extensively. How Drosophila regulates humoral immunity against another major natural enemy, the parasitoid wasp, is less well-characterized. In this study, we focused on a gene crucial in anti-parasitoid immunity, lectin-24A, which is specifically induced following parasitization. We found that a fluorescent reporter driven by the region upstream of lectin-24A showed localized posterior expression in the larval fat body, the Drosophila tissue mediating humoral immunity. Furthermore, with RNA sequencing of the anterior and posterior fat body sections, we found that components of JAK/STAT, GATA, and Toll pathways were regulated differentially in the anterior-posterior axis of the fat body and/or by infection. Predicted binding motifs for transcription factors in all three of these pathways were identified in the 444bp upstream region of the lectin-24A gene, where scrambling these motifs leads to reduced basal or induced expression of the fluorescent reporter. Investigating each of these pathways, we found that JAK/STAT, the GATA factor Pannier, and the NF-{kappa}B factor dorsal all modulate the expression of lectin-24A. The binding motifs associated with these transcription factors were also enriched in the upstream sequences of parasitism-induced genes in the fat body. Taken together, these results indicate that JAK/STAT, Pannier, and NF-{kappa}B signaling are involved in the regulation of lectin-24A and, more generally, Drosophila humoral anti-parasitoid immunity after infection.

immunology↗

Hunting Drosophila viruses from wild populations: a novel isolation approach and characterisation of viruses

Metagenomic studies have demonstrated that viruses are extremely diverse and abundant in insects, but the difficulty of isolating them means little is known about the biology of these newly discovered viruses. To overcome this challenge in Drosophila, we created a cell line with increased susceptibility to infection and detected novel viruses by the presence of double-stranded RNA. We demonstrate the utility of these tools by isolating La Jolla virus (LJV) and Newfield virus (NFV) from several wild Drosophila populations. These viruses have different potential host ranges, with distinct abilities to replicate in five Drosophila species. Similarly, in some species they cause high mortality and in others they are comparatively benign. In three species, NFV but not LJV caused large declines in female fecundity. This sterilization effect was associated with differences in tissue tropism, as NFV but not LJV was able to infect Drosophila melanogaster ovaries. We saw a similar effect in the invasive pest of fruit crops Drosophila suzukii, where oral infection with NFV caused reductions in the fecundity, suggesting it has potential as a biocontrol agent. In conclusion, a simple protocol allowed us to isolate new viruses and demonstrate that viruses identified by metagenomics have a large effect on the fitness of the model organism D. melanogaster and related species.

evolutionary biology↗

Recognition of non-self is necessary to activate Drosophila's immune response against an insect parasite

Innate immune responses can be activated by pathogen-associated molecular patterns (PAMPs) or danger signals released by damaged tissues. As PAMPs are typically conserved across broad groups of pathogens but absent from the host, it is unclear whether they allow hosts to recognize parasites that are phylogenetically related to themselves, such as parasitoid wasps infecting insects. Parasitoids must penetrate the cuticle of Drosophila larvae to inject their eggs. In line with previous results, we find that the danger signal of wounding triggers the differentiation of specialized immune cells called lamellocytes. However, using oil droplets to mimic infection by a parasitoid wasp egg, we find that the activation of melanization response that kills parasitoids also requires exposure to a parasitoid wasp molecule that acts as a PAMP. The unidentified factor enhances the transcriptional response in hemocytes and induces a specific response in the fat body that includes Tep1, which is essential for efficient melanization. We conclude that a combination of danger signals and PAMPs are required activate Drosophilas immune response against parasitic insects.

immunology↗

Recurrent loss of an immunity gene that protects Drosophila against a major natural parasite

Polymorphisms in immunity genes can have large effects on susceptibility to infection. To understand the origins of this variation, we investigated the genetic basis of resistance to the parasitoid wasp Leptopilina boulardi in Drosophila melanogaster. A cis-regulatory polymorphism in the gene Lectin-24A abolishes expression after infection, strongly reducing survival. Other null mutations have arisen repeatedly in this gene, with additional loss-of-expression and premature stop codons segregating in nature. The frequency of these alleles varies greatly, and in some populations natural selection has driven them near to fixation. We conclude that there is a pleiotropic cost to Lectin-24A expression, and in some populations this outweighs the benefit of resistance, resulting in natural selection causing the repeated loss of this important immune defense. Significance StatementGenetic differences between individuals can have a large effect on susceptibility to infectious disease. We have identified a gene called Lectin-24A that is important in the immune response that protects fruit flies against one of their main natural enemies--parasitic wasps. However, in nature many flies carry mutated copies of this gene that are no longer functional. We found that the high frequency of these loss-of-function mutations can only be explained if they have a selective advantage in some populations. Therefore, we can conclude that this immune defiance is costly, and genetic variation in susceptibility is maintained because in some locations susceptible flies are fitter than resistant flies.

evolutionary biology↗

DrosoPhyla: genomic resources for drosophilid phylogeny and systematics

The vinegar fly Drosophila melanogaster is a pivotal model for invertebrate development, genetics, physiology, neuroscience, and disease. The whole family Drosophilidae, which contains over 4000 species, offers a plethora of cases for comparative and evolutionary studies. Despite a long history of phylogenetic inference, many relationships remain unresolved among the groups and genera in the Drosophilidae. To clarify these relationships, we first developed a set of new genomic markers and assembled a multilocus data set of 17 genes from 704 species of Drosophilidae. We then inferred well-supported group and species trees for this family. Additionally, we were able to determine the phylogenetic position of some previously unplaced species. These results establish a new framework for investigating the evolution of traits in fruit flies, as well as valuable resources for systematics.

evolutionary biology↗

Constitutive activation of cellular immunity underlies the evolution of resistance to infection

Organisms rely on inducible and constitutive immune defences to combat infection. Constitutive immunity enables a rapid response to infection but may carry a cost for uninfected individuals, leading to the prediction that it will be favoured when infection rates are high. When we exposed populations of Drosophila melanogaster to intense parasitism by the parasitoid wasp Leptopilina boulardi, they evolved resistance by developing a more reactive cellular immune response. Using single-cell RNA sequencing, we found that immune-inducible genes had become constitutively upregulated. This was the result of resistant larvae differentiating precursors of specialized immune cells called lamellocytes that were previously only produced after infection. Therefore, populations evolved resistance by genetically hard-wiring an induced immune response to become constitutive.

evolutionary biology↗

Host-pathogen coevolution increases genetic variation in susceptibility to infection

It is common to find considerable genetic variation in susceptibility to infection in natural populations. We have investigated whether natural selection increases this variation by testing whether host populations show more genetic variation in susceptibility to pathogens that they naturally encounter than novel pathogens. In a large cross-infection experiment involving four species of Drosophila and four host-specific viruses, we always found greater genetic variation in susceptibility to viruses that had coevolved with their host. We went on to examine the genetic architecture of resistance in one host species, finding that there are more major-effect genetic variants in coevolved host-parasite interactions. We conclude that selection by pathogens increases genetic variation in host susceptibility, and much of this effect is caused by the occurrence of major-effect resistance polymorphisms within populations.

evolutionary biology↗

Host shifts result in parallel genetic changes when viruses adapt to closely related species

Host shifts, where a pathogen invades and establishes in a new host species, are a major source of emerging infectious diseases. They frequently occur between related host species and often rely on the pathogen evolving adaptations that increase their fitness in the novel host species. To investigate genetic changes in novel hosts, we experimentally evolved replicate lineages of an RNA virus (Drosophila C Virus) in 19 different species of Drosophilidae and deep sequenced the viral genomes. We found a strong pattern of parallel evolution, where viral lineages from the same host were genetically more similar to each other than to lineages from other host species. When we compared viruses that had evolved in different host species, we found that parallel genetic changes were more likely to occur if the two host species were closely related. This suggests that when a virus adapts to one host it might also become better adapted to closely related host species. This may explain in part why host shifts tend to occur between related species, and may mean that when a new pathogen appears in a given species, closely related species may become vulnerable to the new disease.

evolutionary biology↗