Biology subjects

Turelli, M.

Publications and source records attributed to Turelli, M..

6 recordsLinked to original sources

bioRxiv2026

Calibrating and documenting host-switching and evolution of incompatibility loci for two closely related Wolbachia clades

Maternally inherited Wolbachia alphaproteobacteria are the most common arthropod endosymbionts. Often Wolbachia spread to high frequencies through cytoplasmic incompatibility, in which cif loci act through sperm to kill embryos lacking Wolbachia. Closely related Wolbachia with diverse cif loci often associate with anciently diverged hosts, but the timescale of associations remains uncertain. We produce new calibrations based on filarial nematodes with vertically inherited Wolbachia that codiverge with their hosts. Applying these calibrations to Wolbachia variants closely related to pathogen-blocking wMel from Drosophila melanogaster, we demonstrate that over a timescale of 1-2 million years, a core set of single-copy Wolbachia loci evolve largely through bifurcation rather than by gene exchange with distant Wolbachia. Dating bifurcating core genomes, we show that "wMel-like" Wolbachia diverged 2.1x105-2.4x106 years inhabit dipteran and hymenopteran hosts diverged more than 108 years. Previous published analysis of variants related to wRi from D. simulans, the first Wolbachia found in a drosophilid, concluded that "wRi-like" Wolbachia spread among different Drosophila in tens of thousands of years. However, our new calibrations suggest these estimates from a mutation-based calibration underestimated wRi-like spread by about a factor of seven. In addition, cif exchanges between wMel-like and wRi-like Wolbachia genomes have occurred over [~]104-106 years. Comparing intact cif loci found in various Wolbachia, we find function-preserving selection in their evolution. We discuss these results in light of theoretical predictions concerning selection on cytoplasmic incompatibility phenotypes within and among host lineages. The wMel variants analyzed may offer new options for Wolbachia-based biocontrol efforts. Article SummaryMaternally transmitted Wolbachia endosymbionts associate with many arthropods. Closely related Wolbachia are known to occupy anciently diverged hosts, but the timescale of associations remains uncertain. Using genomic data from obligate Wolbachia codiverging with filarial nematodes, we calibrate Wolbachia molecular evolution. wMel-like variants that diverged about 104-106 years ago occur in hosts that diverged more than 108 years ago. Incompatibility loci move even more rapidly among these Wolbachia genomes. As these variants diverge, selection occurred on loci involved in both inducing and protecting against cytoplasmic incompatibility. These results elucidate Wolbachia host-range and genome dynamics and provide potential material for applications.

microbiology↗

bioRxiv2023

Rapid turnover of pathogen-blocking Wolbachia and their incompatibility loci

About half of all insect species carry maternally inherited Wolbachia alphaproteobacteria, making Wolbachia the most common endosymbionts known in nature. Often Wolbachia spread to high frequencies within populations due to cytoplasmic incompatibility (CI), a Wolbachia-induced sperm modification caused by prophage-associated genes (cifs) that kill embryos without Wolbachia. Several Wolbachia variants also block viruses, including wMel from Drosophila melanogaster when transinfected into the mosquito Aedes aegypti. CI enables the establishment and stable maintenance of pathogen-blocking wMel in natural Ae. aegypti populations. These transinfections are reducing dengue disease incidence on multiple continents. While it has long been known that closely related Wolbachia occupy distantly related hosts, the timing of Wolbachia host switching and molecular evolution has not been widely quantified. We provide a new, conservative calibration for Wolbachia chronograms based on examples of co-divergence of Wolbachia and their insect hosts. Synthesizing publicly available and new genomic data, we use our calibration to demonstrate that wMel-like variants separated by only about 370,000 years have naturally colonized holometabolous dipteran and hymenopteran insects that diverged approximately 350 million years ago. Data from Wolbachia variants closely related to those currently dominant in D. melanogaster and D. simulans illustrate that cifs are rapidly acquired and lost among Wolbachia genomes, on a time scale of 104-105 years. This turnover occurs with and without the Wovirus prophages that contain them, with closely related cifs found in distantly related phages and distantly related cifs found in closely related phages. We present evidence for purifying selection on CI rescue function and on particular Cif protein domains. Our results quantify the tempo and mode of rapid host switching and horizontal gene transfer that underlie the spread and diversity of Wolbachia sampled from diverse host species. The wMel variants we highlight from hosts in different climates may offer new options for broadening Wolbachia-based biocontrol of diseases and pests.

evolutionary biology↗

bioRxiv2019

Introgressive and horizontal acquisition of Wolbachia by hybridizing Drosophila yakuba-clade hosts and horizontal transfer of phage loci between distantly related Wolbachia

Maternally transmitted Wolbachia infect about half of insect species, yet the predominant mode(s) of Wolbachia acquisition remains uncertain. Species-specific associations could be old, with Wolbachia and hosts co-diversifying (i.e., cladogenic acquisition), or relatively young and acquired by horizontal transfer or introgression. The three Drosophila yakuba-clade hosts ((D. santomea, D. yakuba), D. teissieri) diverged about three million years ago and currently hybridize on Bioko and Sao Tome, west African islands. Each species is polymorphic for nearly identical Wolbachia that cause weak cytoplasmic incompatibility (CI)-reduced egg hatch when uninfected females mate with infected males. D. yakuba-clade Wolbachia are closely related to wMel, globally polymorphic in D. melanogaster. We use draft Wolbachia and mitochondrial genomes to demonstrate that D. yakuba-clade Wolbachia and mitochondrial phylogenies tend to follow host nuclear phylogenies; however, roughly half of D. santomea individuals, sampled both inside and outside of the Sao Tome hybrid zone, have introgressed D. yakuba mitochondria. Both mitochondria and Wolbachia possess far more recent common ancestors than the bulk of the host nuclear genomes, precluding cladogenic Wolbachia acquisition. General concordance of Wolbachia and mitochondrial phylogenies suggests that horizontal transmission is rare, but varying relative rates of molecular divergence complicate time-based statistical tests. Loci that cause CI in wMel are disrupted in D. yakuba-clade Wolbachia; however, a second set of loci predicted to cause CI are located in the same WO prophage region. These alternative CI loci seem to have been acquired horizontally from distantly related Wolbachia, with transfer mediated by flanking Wolbachia-specific ISWpi1 transposons.

evolutionary biology↗

bioRxiv2018

Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively low Wolbachia frequencies in Drosophila mauritiana

Maternally transmitted Wolbachia bacteria infect about half of all insect species. Many Wolbachia cause cytoplasmic incompatibility (CI), reduced egg hatch when uninfected females mate with infected males. CI produces a frequency-dependent fitness advantage that leads to high equilibrium Wolbachia frequencies but does not aid Wolbachia spread from low frequencies. The fitness advantages that produce initial Wolbachia spread and maintain non-CI Wolbachia remain elusive. Wolbachia variant wMau that infects Drosophila mauritiana does not cause CI, despite being very closely related to the CI-causing Wolbachia wNo in D. simulans (0.068% sequence divergence over 682,494 bp), suggesting that CI was recently lost. Using draft Wolbachia genomes, we identify a deletion in a WO phage gene that may disrupt CI. We find no evidence that wMau increases host fecundity. We report intermediate and apparently stable wMau infection frequencies on the Indian Ocean island of Mauritius, consistent with no CI and no appreciable positive effect on fecundity. Our data indicate that wMau frequencies reflect a balance between unknown, weak positive effects on fitness and imperfect maternal transmission. Phylogenomic analyses suggest that Supergroup B Wolbachia, including wMau, diverged from Supergroup A Wolbachia, including wMel from D. melanogaster, 6-46 million years ago, later than previously estimated.

evolutionary biology↗

bioRxiv2017

Genome Comparisons Indicate Recent Transfer Of wRi-Like Wolbachia Between Sister Species Drosophila suzukii And D. subpulchrella

Wolbachia endosymbionts may be acquired by horizontal transfer, by introgression through hybridization between closely related species, or by cladogenic retention during speciation. All three modes of acquisition have been demonstrated, but their relative frequency is largely unknown. Drosophila suzukii and its sister species D. subpulchrella harbor Wolbachia, denoted wSuz and wSpc, very closely related to wRi, identified in California populations of D. simulans. However, these variants differ in their induced phenotypes: wRi causes significant cytoplasmic incompatibility (CI) in D. simulans, but CI has not been detected in D. suzukii or D. subpulchrella. Our draft genomes of wSuz and wSpc contain full-length copies of 703 of the 734 single-copy genes found in wRi. Over these coding sequences, wSuz and wSpc differ by only 0.004% (i.e., 28 of 704,883 bp); they are sisters relative to wRi, from which each differs by 0.014-0.015%. Using published data from D. melanogaster, Nasonia wasps and Nomada bees to calibrate relative rates of Wolbachia versus host nuclear divergence, we conclude that wSuz and wSpc are too similar - by at least a factor of 100 - to be plausible candidates for cladogenic transmission. These three wRi-like Wolbachia, which differ in CI phenotype in their native hosts, have different numbers of orthologs of genes postulated to contribute to CI; and the CI loci differ at several nucleotides that may account for the CI difference. We discuss the general problem of distinguishing alternative modes of Wolbachia acquisition, focusing on the difficulties posed by limited knowledge of variation in absolute and relative rates of molecular evolution for host nuclear genomes, mitochondria and Wolbachia.

evolutionary biology↗

bioRxiv2016

Deploying dengue-suppressing Wolbachia: robust models predict slow but effective spatial spread in Aedes aegypti

A novel strategy for controlling the spread of arboviral diseases such as dengue, Zika and chikungunya is to transform mosquito populations with virus-suppressing Wolbaehia. In general, Wolbachia transinfected into mosquitoes induce fitness costs through lower viability or fecundity. These maternally inherited bacteria also produce a frequency-dependent advantage for infected females by inducing cytoplasmic incompatibility (CI), which kills the embryos produced by uninfected females mated to infected males. These competing effects, a frequency-dependent advantage and frequency-independent costs, produce bistable Wolbachia frequency dynamics. Above a threshold frequency, denoted p, CI drives fitness-decreasing Wolbachia transinfections through local populations; but below p, infection frequencies tend to decline to zero. If p is not too high, CI also drives spatial spread once infections become established over sufficiently large areas. We illustrate how simple models provide testable predictions concerning the spatial and temporal dynamics of Wolbachia introductions, focusing on rate of spatial spread, the shape of spreading waves, and the conditions for initiating spread from local introductions. First, we consider the robustness of diffusion-based predictions to incorporating two important features of wMel-Aedes aegypti biology that may be inconsistent with the diffusion approximations, namely fast local dynamics induced by complete CI (i.e., all embryos produced from incompatible crosses die) and long-tailed, non-Gaussian dispersal. With complete CI, our numerical analyses show that long-tailed dispersal changes wave-width predictions only slightly; but it can significantly reduce wave speed relative to the diffusion prediction; it also allows smaller local introductions to initiate spatial spread. Second, we use approximations for[p] and dispersal distances to predict the outcome of 2013 releases of wMel-infected Aedes aegypti in Cairns, Australia, Third, we describe new data from Aedes aegypti populations near Cairns, Australia that demonstrate long-distance dispersal and provide an approximate lower bound on p for wMel in northeastern Australia. Finally, we apply our analyses to produce operational guidelines for efficient transformation of vector populations over large areas. We demonstrate that even very slow spatial spread, on the order of 10-20 m/month (as predicted), can produce area-wide population transformation within a few years following initial releases covering about 20-30% of the target area.

zoology↗