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Conner, W. R.

Publications and source records attributed to Conner, W. R..

16 recordsLinked to original sources

Climate predicts wMel Wolbachia frequency variation in Drosophila melanogaster, but genomic variation reflects a recent incomplete cytoplasmic sweep

Maternally transmitted Wolbachia occupy roughly half of terrestrial arthropod species, but the factors maintaining their variable population frequencies are poorly understood. In Drosophila melanogaster, the wMel Wolbachia variant occurs at intermediate and variable frequencies globally. We document rapid wMel frequency shifts up to 0.33 between consecutive weeks in experimental and natural orchards in the eastern United States, with frequencies peaking at intermediate temperatures and declining at thermal extremes. Seven years of seasonal sampling at a Pennsylvania orchard showed wMel frequencies consistently higher in summer than fall, consistent with temperature-dependent maternal transmission. Bayesian models applied to 248 locations across five continents and 42 years of sampling corroborated the previously described wMel frequency cline in eastern Australia but found no latitudinal pattern on any other continent. Precipitation seasonality and driest-quarter precipitation were the strongest global predictors, absorbing the among-continent wMel frequency variation that latitude left unexplained. Wet-season temperature predicted wMel frequency in Australia, where the wettest quarter coincides with summer and peak host reproduction. Analysis of 339 individually sequenced wMel genomes identified 38 wMel SNPs associated with latitude, but these associations did not persist after accounting for cytoplasmic lineage structure, and 35 of the 38 were private to a remnant southwestern European lineage. Our results establish that local climatic conditions shape wMel frequencies globally, plausibly through effects on maternal transmission fidelity that depend on the seasonal alignment of warm temperatures with host reproduction. wMel genomic variation, in contrast, reflects the incomplete replacement of ancestral wMelCS by wMel, rather than local adaptation.

evolutionary biology↗

Temperature-sensitive cytoplasmic incompatibility across divergent Wolbachia partly reflects cifB transcription, not endosymbiont density

Maternally transmitted Wolbachia bacteria are common in insects, with many strains altering host reproduction through cytoplasmic incompatibility (CI). CI kills embryos fertilized by Wolbachia-bearing males unless those embryos also carry Wolbachia, which favors females with Wolbachia and drives the endosymbiont to higher frequencies in host populations. Strong CI now underpins successful applications that rely on maintaining pathogen-blocking Wolbachia transinfections in vector populations to reduce arboviral disease transmission. Temperature modulates CI strength (the proportion of embryos killed), with consequences for Wolbachia prevalence in natural and transinfected populations. Yet the mechanisms regulating temperature-sensitive CI-strength variation are poorly understood. We quantified CI strength across eight divergent Drosophila-associated Wolbachia strains at four temperatures (18{degrees}C-26{degrees}C), while characterizing development time, Wolbachia and Wovirus densities, and transcription of the CI-inducing gene cifB. Four of eight Wolbachia strains exhibited temperature-sensitive CI, three of which induced CI at multiple temperatures. Of these three, two expressed significantly more cifB at the temperature yielding stronger CI, whereas testes Wolbachia density did not predict CI strength. Notably, cifB-transcript levels were consistently decoupled from Wolbachia and Wovirus densities, suggesting that cifB transcription is not regulated solely by symbiont abundance. We also report temperature-sensitive rescue of CI, Wolbachia-associated developmental acceleration, and strain-specific Wovirus-Wolbachia covariance. Our findings reveal temperature as a pervasive modulator of Wolbachia-host interactions at multiple levels and extend evidence that cifB transcription partly predicts variable CI strength across strain identities, male ages, and now temperatures. CI variation unaccounted for by cifB transcription points toward additional regulatory or post-transcriptional mechanisms that we discuss.

molecular biology↗

A centromere but not just a centromere: structure and evolution of a selfish chromosomal supergene in monkeyflowers

Meiotic drivers capitalize on vulnerabilities in eukaryotic meiosis and gametogenesis to gain greater-than-equal transmission to the next generation. In most plants and animals, asymmetric female meiosis is such an arena for selfishness; centromeric variants can bias their chromosomes segregation to the one egg cell with potentially profound effects on individual fitness, population dynamics, and genome structure. However, the mechanisms and consequences of selfish centromere evolution remain obscure, due to both the complexity of centromeric DNA and to a paucity of model systems. Here, we build on representative chromosome-scale assemblies of yellow monkeyflowers (M. guttatus species complex) to compare the structure, gene content, and sequence of three functionally distinct haplotypes at Meiotic Drive Locus on Chromosome 11 (MDL11), whose driving D allele was previously shown to be centromere-containing, costly, and maintained as a balanced polymorphism in wild populations. Relative to both moderately-resistant M. guttatus nondrivers (D-; IM767) and weak (d) M. nasutus, D minimally evolved via two rearrangements (including a hemicentric inversion creating dual arrays of M. guttatus centromeric satellite Cent728 separated by > 200 trapped genes), massive expansions of a novel MDL11-specific subfamily of satellite repeats (Cent728D) that increase D chromosome length by >50%, and the accumulation of >40 extra D-only genes (EDG) from diverse genomic sources in a hemizygous pericentromeric region. Under a strictly centromeric model of selfishness, the recent expansion of Cent728D is a primary candidate for generating centromere drive, either by directly altering the binding of centromeric histone CenH3 or by shifting kinetochore size or position as an epigenetic byproduct of chromosome size. However, elevated divergence in genic presence-absence variants (both in the EDG and elsewhere) and gene sequence across MDL11 strata points to strong candidates for both collusion with the D centromere and for interspecific (D- vs. d) variation in resistance. Overall, our findings support the sequential buildup of this model centromeric driver over time, reveal intriguing parallels with adaptive and gamete-killing supergenes, and provide a strong platform for further dissection of the molecular genetic basis of its dramatic deviations from Mendelian rules.

genetics↗

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↗

Counting cytoplasmic incompatibility factor mRNA using digital droplet PCR

Wolbachia bacteria inhabit over half of all insect species and often spread through host populations via efficient maternal transmission and cytoplasmic incompatibility (CI), killing aposymbiotic embryos when fertilized by symbiotic males. Wolbachias cifB gene triggers CI in males, while cifA, expressed in females, rescues embryos from CI-induced lethality. In some systems, cifA also contributes to CI induction. CI strength--the percentage of embryos that die from CI--is a key determinant of Wolbachias prevalence in host populations, and cifB mRNA levels in testes generally correlate with CI strength. Yet, cifBs rarity can hamper precise quantification, necessitating tissue pooling for reverse transcription quantitative PCR (RT-qPCR) to achieve reliable measurements, obscuring variation at the level of individual insect tissues. Here, we present four RT digital droplet PCR (RT-ddPCR) assays to count rare cifA and cifB mRNA from wMel Wolbachia in Drosophila melanogaster. These assays count cif transcripts alongside a synthetic spike-in RNA or a D. melanogaster housekeeping gene to normalize for technical or biological variation. These assays have a limit of detection of about 1 cifA and 3 cifB copies per reaction. We expect these methods to be useful for mosquito-control programs that use wMel to block the spread of pathogens from Aedes aegypti to humans. Moreover, the oligos were designed with homology to cifA and cifB sequences from at least 33 Wolbachia strains, suggesting utility beyond wMel. These methods will allow researchers to measure cif mRNA levels from individual insect tissues, enabling efforts to pair molecular and phenotypic data at unprecedented resolutions. ImportanceWolbachia, a maternally transmitted bacterium, is found in over half of all insect species. Its ability to induce cytoplasmic incompatibility (CI), which prevents Wolbachia-free eggs from hatching, significantly contributes to its high prevalence in host populations. Public health experts use CI to spread pathogen-blocking Wolbachia through mosquito populations, thereby controlling pathogen spread. CI is often weak, resulting in few egg deaths and consequently slowing Wolbachias spread. We recently discovered that weak CI often correlates with low CI factor B (cifB) mRNA levels. However, our understanding of CI-strength variation remains limited because cifB is transcribed at low levels, making it challenging to measure in individual insects. Here, we report four RT-ddPCR assays to overcome this challenge. These assays offer high sensitivity for rare targets and maintain accuracy and precision across a wide dynamic range. We expect these tools will enhance efforts to understand CI-strength variation in both natural and applied populations.

microbiology↗

Ancient origin of an urban underground mosquito

Understanding how life is adapting to urban environments represents an important challenge in evolutionary biology. Here we investigate a widely cited example of urban adaptation, Culex pipiens form molestus, also known as the London Underground Mosquito. Population genomic analysis of [~]350 contemporary and historical samples counter the popular hypothesis that molestus originated belowground in London less than 200 years ago. Instead, we show that molestus first adapted to human environments aboveground in the Middle East over the course of >1000 years, likely in concert with the rise of agricultural civilizations. Our results highlight the role of early human society in priming taxa for contemporary urban evolution and have important implications for understanding arbovirus transmission.

evolutionary biology↗

Recombination, truncation and horizontal transfer shape the diversity of cytoplasmic incompatibility patterns

Wolbachia are endosymbiotic bacteria inducing various reproductive manipulations of which cytoplasmic incompatibility (CI) is the most common. CI leads to reduced embryo viability in crosses between males carrying Wolbachia and uninfected females or those carrying an incompatible symbiont strain. In the mosquito Culex pipiens, the Wolbachia wPip causes highly complex crossing patterns. This complexity is linked to the amplification and diversification of the CI causal genes, cidA and cidB, with polymorphism located in the CidA-CidB interaction regions. We previously showed correlations between the identity of gene variants and CI patterns. However, these correlations were limited to specific crosses, and it is still unknown whether cid gene polymorphism in males and females Wolbachia can explain and predict the wide range of crossing types observed in C. pipiens. Taking advantage of a new method enabling full-gene acquisition, we sequenced complete cid repertoires from 45 wPip strains collected worldwide. We demonstrated that the extensive diversity of cid genes arises from recombination and horizontal transfers. We uncovered further cidB polymorphism outside the interface regions and strongly correlated with CI patterns. Most importantly, we showed that in every wPip genome, all but one cidB variant are truncated. Truncated cidBs located in palindromes are partially or completely deprived of their deubiquitinase domain, crucial for CI. The identity of the sole full-length cidB variant seems to dictate CI patterns, irrespective of the truncated cidBs present. Truncated CidBs exhibit reduced toxicity and stability in Drosophila cells, which potentially hinders their loading into sperm, essential for CI induction.

evolutionary biology↗

Counting rare Wolbachia endosymbionts using digital droplet PCR

Wolbachia is the most widespread animal-associated intracellular microbe, living within the cells of over half of insect species. Since they can suppress pathogen replication and spread rapidly through insect populations, Wolbachia is at the vanguard of public health initiatives to control mosquito-borne diseases. Wolbachias abilities to block pathogens and spread quickly are closely linked to their abundance in host tissues. The most common method for counting Wolbachia is quantitative polymerase chain reaction (qPCR), yet qPCR can be insufficient to count rare Wolbachia, necessitating tissue pooling and consequently compromising individual-level resolution of Wolbachia dynamics. Digital droplet PCR (ddPCR) offers superior sensitivity, enabling the detection of rare targets and eliminating the need for sample pooling. Here, we report three ddPCR assays to measure total Wolbachia abundance, Wolbachia abundance adjusted for DNA extraction efficiency, and Wolbachia density relative to host genome copies. Using Drosophila melanogaster with wMel Wolbachia as a model, we show these ddPCR assays can reliably detect as few as 7 to 12 Wolbachia gene copies in a 20 L reaction. The designed oligos are homologous to sequences from at least 106 Wolbachia strains across Supergroup A and 53 host species from the Drosophila, Scaptomyza, and Zaprionus genera, suggesting broad utility. These highly sensitive ddPCR assays are expected to significantly advance Wolbachia-host interactions research by enabling the collection of molecular data from individual insect tissues. Their ability to detect rare Wolbachia will be especially valuable in applied and natural field settings where pooling samples could obscure important variation.

microbiology↗

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↗

Hidden endosymbionts: A male-killer concealed by another endosymbiont and a nuclear suppressor

Maternally transmitted endosymbiotic bacteria that cause male killing (MK) have only been described from a few insects, but this may reflect challenges in their detection rather than a rarity of MK. Here we identify MK Wolbachia in populations of Drosophila pseudotakahashii, present at a low frequency (around 4%) in natural populations and previously undetected due to a different fixed Wolbachia strain in this species expressing a different reproductive manipulation, cytoplasmic incompatibility (CI). The MK phenotype was eliminated after tetracycline treatment that removed Wolbachia. Molecular analyses indicated the MK phenotype to be expressed when a second Wolbachia strain was present alongside the CI Wolbachia. A genomic analysis highlighted Wolbachia regions diverged between the strains involving 17 genes and also identified the Wolbachia as representing an outgroup to a clade of Wolbachia infecting melanogaster-group species, including wRi-like and wMel-like strains. Doubly infected males induced CI with uninfected females but not females singly infected with CI-causing Wolbachia. The MK phenotype manifested at the larval stage and was transmitted maternally at a high fidelity but with occasional loss of the MK Wolbachia strain. A rapidly spreading dominant nuclear suppressor genetic element affecting MK was identified through backcrossing and subsequent analysis with ddRAD SNPs of the D. pseudotakahashii genome. These findings highlight the complexity of nuclear and microbial components affecting MK endosymbiont detection and dynamics in populations, and the challenges of making connections between endosymbionts and the host phenotypes affected by them.

evolutionary biology↗

Population structure of Drosophila suzukii and signals of multiple invasions into the continental United States

Drosophila suzukii, or spotted-wing drosophila, is now an established pest in many parts of the world, causing significant damage to numerous fruit crop industries. Native to East Asia, D. suzukii infestations started in the United States a decade ago, occupying a wide range of climates. To better understand invasion ecology of this pest, knowledge of past migration events, population structure, and genetic diversity is needed. To improve on previous studies examining genetic structure of D. suzukii, we sequenced whole genomes of 237 individual flies collected across the continental U.S., as well as several representative sites in Europe, Brazil, and Asia, to identify hundreds of thousands of genetic markers for analysis. We analyzed these markers to detect population structure, to reconstruct migration events, and to estimate genetic diversity and differentiation within and among the continents. We observed strong population structure between West and East Coast populations in the U.S., but no evidence of any population structure North to South, suggesting there is no broad-scale adaptations occurring in response to the large differences in regional weather conditions. We also find evidence of repeated migration events from Asia into North America have provided increased levels of genetic diversity, which does not appear to be the case for Brazil or Europe. This large genomic dataset will spur future research into genomic adaptations underlying D. suzukii pest activity and development of novel control methods for this agricultural pest.

genomics↗

Wolbachia in the spittlebug Prosapia ignipectus: Variable infection frequencies, but no apparent effect on host reproductive isolation

Animals serve as hosts for complex communities of microorganisms, including endosymbionts that live inside their cells. Wolbachia bacteria are perhaps the most common endosymbionts, manipulating host reproduction to propagate. Many Wolbachia cause intense cytoplasmic incompatibility (CI) that promotes their spread to high and relatively stable frequencies. Wolbachia that cause weak or no CI tend to persist at intermediate, often variable, frequencies. Wolbachia could also contribute to host reproductive isolation (RI), although current support for such contributions is limited to a few systems. To test for Wolbachia frequency variation and effects on host RI, we sampled several local Prosapia ignipectus (Fitch)(Hemiptera: Cercopidae) spittlebug populations in the northeastern USA over two years, including closely juxtaposed Maine populations with different monomorphic color forms, "black" and "lined". We discovered a group-B Wolbachia (wPig) infecting P. ignipectus that diverged from group-A Wolbachia--like model wMel and wRi strains in Drosophila--6 to 46 MYA. Populations of the sister species Prosapia bicincta (Say) from Hawaii and Florida are uninfected, suggesting that P. ignipectus acquired wPig after their initial divergence. wPig frequencies were generally high and variable among sites and between years. While phenotyping wPig effects on host reproduction is not currently feasible, the wPig genome contains three divergent sets of CI loci, consistent with high wPig frequencies. Finally, Maine monomorphic black and monomorphic lined populations of P. ignipectus share both wPig and mtDNA haplotypes, implying no apparent effect of wPig on the maintenance of this morphological contact zone. We hypothesize P. ignipectus acquired wPig horizontally as observed for many Drosophila species, and that significant CI and variable transmission produce high but variable wPig frequencies.

evolutionary biology↗

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↗

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↗

Spatial and temporal distribution of genome divergence among California populations of Aedes aegypti.

In the summer of 2013, Aedes aegypti Linnaeus was first detected in three cities in central California (Clovis, Madera and Menlo Park). It has now been detected in multiple locations in central and southern CA as far south as San Diego and Imperial Counties. A number of published reports suggest that CA populations have been established from multiple independent introductions. Here we report the first population genomics analyses of Ae. aegypti based on individual, field collected whole genome sequences. We analyzed 46 Ae. aegypti genomes to establish genetic relationships among populations from sites in California, Florida and South Africa. We identified 3 major genetic clusters within California; one that includes all sample sites in the southern part of the state (South of Tehachapi mountain range) plus the town of Exeter in central California and two additional clusters in central California. A lack of concordance between mitochondrial and nuclear genealogies suggests that the three founding populations were polymorphic for two main mitochondrial haplotypes prior to being introduced to California. One of these has been lost in the Clovis populations, possibly by a founder effect. Genome-wide comparisons indicate extensive differentiation between genetic clusters. Our observations support recent introductions of Ae. aegypti into California from multiple, genetically diverged source populations. Our data reveal signs of hybridization among diverged populations within CA. Genetic markers identified in this study will be of great value in pursuing classical population genetic studies which require larger sample sizes.

genomics↗

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↗