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Miller, W. J.

Publications and source records attributed to Miller, W. J..

7 recordsLinked to original sources

Microbial profiling of native and alien Drosophila in French Guiana reveals candidate taxa potentially affecting invasion dynamics.

Invasive alien species (IAS) represent a major threat to biodiversity, human health, and economy. Yet the role of host-associated microbiomes in invasion processes remains poorly understood in natural systems. Here, we investigated the bacterial and fungal microbiomes of IAS and native Drosophila species collected along an anthropization gradient in French Guiana. Analyses of Drosophila communities revealed that IAS establishment is limited outside coastal habitats. Using bacterial 16S rRNA and fungal ITS metabarcoding of pooled individuals, we assessed microbial diversity, composition, and structure across host species, host category (invasive vs. native), and locality. Bacterial communities associated with IAS harboured reduced alpha diversity and distinct community structure compared to native Drosophila species, and host phylogenetic relatedness and locality also contributed to bacteriome variation. In contrast, fungal communities were mainly structured by locality and host species. We further identified core and exclusive taxa, compared bacteriome composition between native and IAS hosts using global reference datasets, and integrated information from the microbiome literature. This approach led to the identification of 45 bacterial and fungal candidate taxa potentially associated with host adaptation or competitiveness across coastal and rainforest environments. Overall, our results highlight microbiome variation as a potential component of invasion dynamics in Neotropical Drosophila.

ecology↗

Evolutionary persistence of a highly prevalent multicopy mitochondrial-derived nuclear insertion (Mega-NUMT) in Neotropical Drosophila flies

Background: Although strict maternal transmission of mitochondria is a general feature of animals and humans for ensuring homogeneity in mitochondrial DNA (mtDNA) across generations, exceptions were reported in the recent past. For example, some extremely rare but spectacular cases of heteroplasmy and paternal transmission in humans have questioned the universal evolutionary principle. Hence, as an alternative, the Mega-NUMT concept was coined to explain this discovery and was thereafter partly proven to exist. This concept expands on the quite common transfer of mtDNA fragments to the nucleus (NUMTs) by considering the existence of multicopy mitochondrial nuclear insertions. Mega-NUMT reports are currently restricted to a few cases in animals, including humans. However, even in humans, their detailed genomic organization, natural prevalence, and potential biological functions remain unclear. Methodology/Principal Findings: Here, we discovered that up to 60 full-sized mitochondrial genomes are integrated into the nuclear genome of the neotropical fruit fly Drosophila paulistorum using long-read sequencing and confirmed their presence by in situ hybridization. The copies are organized in one cluster on chromosome 3, which we, due to its similarity with the Mega-NUMT concept, designated the Dpau Mega-NUMT. Contrary to the rarity in humans, this Mega-NUMT is found at high prevalence (40%) in both long-term laboratory lines and natural D. paulistorum populations of different semispecies. Additionally, the mitochondrial copies in the Mega-NUMT cluster are phylogenetically separated from the current mitotypes of D. paulistorum. Together, these observations suggest long-term maintenance of the Mega-NUMT in nature. Hence, we propose that the Dpau Mega-NUMT may have been transferred to the nuclear genome before D. paulistorum semispecies radiation and maintained at relatively high prevalence in nature by balancing selection due to yet undetermined functions. Conclusions/Significance: To our knowledge, this is the first verified existence and detailed dissection of a Mega-NUMT outside cats and humans. We show that Mega-NUMTs can be persistent in nature, even at high prevalence, potentially due to balancing selection. Our findings strengthen the importance of high-quality long-read sequencing technologies for deciphering complex repeat-rich genomic regions to deepen our understanding of the dynamics of genome evolution within genomic dark matter.

evolutionary biology↗

A co-speciation dilemma and a lifestyle transition with genomics consequences in Wolbachia of Neotropical Drosophila

BackgroundLong-term persistent symbiotic associations may result in co-speciation and can be inferred if species trees of hosts and symbionts are congruent in topology and divergence times. Co-speciation has been seen to occur relatively frequently in obligate associations, but is less common in parasitic or facultative ones, mainly due to the difference in horizontal transmission rates. The long-term vertical inheritance and close host association of obligate endosymbionts also generally result in smaller genomes than in facultative endosymbionts. Here, we investigate co-speciation and genome reduction using highly similar strains of the endosymbiont Wolbachia infecting Drosophila species from the willistoni and saltans groups, where only one strain, wPau, infecting D. paulistorum, is obligate. ResultsWe sequenced the Wolbachia genomes from five species of the willistoni and saltans groups and constructed phylogenies. Topological congruence was found between these Wolbachia strains and the nuclear DNA of their hosts, except for wPau and D. paulistorum, but full topological congruence was observed between Wolbachia and the host mitochondrial DNA. However, assuming temporal congruence, we estimated extremely low evolutionary rates in Wolbachia of 10-10-10-11 changes/site/year. Additionally, the obligate wPau strain was found to have a larger genome than closely related facultative strains, mainly due to an ongoing expansion of an IS4 element. Furthermore, wPau has lost a large proportion of its prophage WO genes, but the cif genes, known to be involved in the CI phenotype, are intact. Finally, nine of the eleven genes from the prophage WO-associated Undecim cluster are uniquely duplicated. ConclusionsThe congruent topologies between Wolbachia and their willistoni and saltans group hosts indicate co-speciation. However, the high similarity between Wolbachia strains, which results in low mutation rate estimates, challenges this interpretation. Contrary to the expectations of the genome reduction theory, we observed an increase in genome size in the obligate wPau strain, potentially driven by a decreased population size. Finally, the duplication of the Undecim cluster despite a major loss of other prophage-associated genes suggests that the genes in the Undecim cluster are under strong selection and potentially play a role in the obligate association between wPau and their D. paulistorum hosts.

genomics↗

Restriction of Wolbachia bacteria in early embryogenesis of neotropical Drosophila species via ER-mediated autophagy

Wolbachia bacteria are maternally transmitted intracellular microbes that are not only restricted to the reproductive organs but also found in various somatic tissues of their native hosts. The abundance of the endosymbiont in somatic tissues, usually a dead end for vertically transmitted bacteria, causes a multitude of effects on life history traits of their hosts, which are still not well understood. Thus, deciphering the host-symbiont interactions on a cellular level throughout a hosts lifecycle is of great importance to understand their homeostatic nature, persistence and spreading success. Using fluorescent and transmission electron microscopy, we conducted a comprehensive analysis of Wolbachia tropism in somatic and reproductive tissues of six Drosophila species at the intracellular level during host development. Our data uncovered diagnostic patterns of infections to embryonic primordial germ cells and to particular cells of somatic tissues in three different neotropical Drosophila species of the willistoni and saltans groups that have apparently evolved in both independently. We further found that restricted patterns of Wolbachia tropism are already determined in early fly embryogenesis. This is achieved via selective autophagy, and the restriction of infection is preserved through larval hatching and metamorphosis. We further uncovered tight interactions of Wolbachia with membranes of the endoplasmic reticulum, which might play a scaffolding role for autophagosome formation and subsequent elimination of the endosymbiont. Finally, by analyzing D. simulans lines transinfected with non-native Wolbachia, we uncovered that the host genetic background regulates tissue tropism of infection. Our data demonstrate a peculiar and novel mechanism to limit and spatially restrict bacterial infection in somatic tissues during a very early stage of host development.

developmental biology↗

Persistence and invasiveness of high-level heteroplasmy through biparental transmission of a selfish mitochondrion in Drosophila.

Hybridization and the consequent introgression of genomic elements is an important source of genetic diversity for biological lineages. This is particularly evident in young clades in which hybrid incompatibilities are still incomplete and mixing between species is more likely to occur. Drosophila paulistorum, a representative of the Neotropical Drosophila willistoni subgroup, is a classic model of incipient speciation. The species is divided into six semispecies that show varying degrees of pre- and post-mating incompatibility with each other. In the present study, we investigate the mitochondrial evolutionary history of D. paulistorum and the willistoni subgroup. For that, we perform phylogenetic and comparative analyses of the complete mitochondrial genomes and draft nuclear assemblies of 25 Drosophila lines of the willistoni and saltans species groups. Our results show that the mitochondria of D. paulistorum are polyphyletic and form two non-sister clades that we name and {beta}. Identification and analyses of nuclear mitochondrial insertions further reveal that the willistoni subgroup has an -like mitochondrial ancestor and indicate that both the and {beta} mitochondria of D. paulistorum were acquired through introgression from unknown fly lineages of the willistoni subgroup. We also uncover multiple mitochondrial introgressions across D. paulistorum semispecies and generate novel insight into the evolution of the species.

evolutionary biology↗

The Glossina Genome Cluster: Comparative Genomic Analysis of the Vectors of African Trypanosomes

BackgroundTsetse flies (Glossina sp.) are the sole vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood specific diet by both sexes and obligate bacterial symbiosis. This work describes comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans (G.m. morsitans), G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes) and Fusca (G. brevipalpis) which represent different habitats, host preferences and vectorial capacity. ResultsGenomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex linked scaffolds show increased rates of female specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse specific genes are enriched in protease, odorant binding and helicase activities. Lactation associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other characterized insects. Vision associated Rhodopsin genes show conservation of motion detection/tracking functions and significant variance in the Rhodopsin detecting colors in the blue wavelength ranges. ConclusionsExpanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

genomics↗

Wolbachia modifies thermal preference in Drosophila melanogaster

Environmental variation can have profound and direct effects on fitness, fecundity, and host symbiont interactions. Replication rates of microbes within arthropod hosts, for example, are correlated with incubation temperature but less is known about the influence of host-symbiont dynamics on environmental preference. Hence, we conducted thermal preference (Tp) assays and tested if infection status and genetic variation in endosymbiont bacterium Wolbachia affected temperature choice of Drosophila melanogaster. We demonstrate that isogenic flies infected with Wolbachia preferred lower temperatures compared to uninfected Drosophila. Moreover, Tp varied with respect to three investigated Wolbachia variants (wMel, wMelCS and wMelPop). While uninfected individuals preferred 24.4{degrees}C, we found significant shifts of - 1.2{degrees}C in wMel- and -4{degrees}C in flies infected either with wMelCS or wMelPop. We, therefore, postulate that Wolbachia-associated Tp variation within a host species might represent a behavioral accommodation to host-symbiont interactions and trigger behavioral self-medication and bacterial titer regulation by the host.

microbiology↗