scholarly journals Wolbachia infection in wild mosquitoes (Diptera: Culicidae): implications for transmission modes and host-endosymbiont associations in Singapore

2020 ◽  
Vol 13 (1) ◽  
Author(s):  
Huicong Ding ◽  
Huiqing Yeo ◽  
Nalini Puniamoorthy

Abstract Background Wolbachia are intracellular bacterial endosymbionts found in most insect lineages. In mosquitoes, the influence of these endosymbionts on host reproduction and arboviral transmission has spurred numerous studies aimed at using Wolbachia infection as a vector control technique. However, there are several knowledge gaps in the literature and little is known about natural Wolbachia infection across species, their transmission modes, or associations between various Wolbachia lineages and their hosts. This study aims to address these gaps by exploring mosquito-Wolbachia associations and their evolutionary implications. Methods We conducted tissue-specific polymerase chain reaction screening for Wolbachia infection in the leg, gut and reproductive tissues of wild mosquitoes from Singapore using the Wolbachia surface protein gene (wsp) molecular marker. Mosquito-Wolbachia associations were explored using three methods—tanglegram, distance-based, and event-based methods—and by inferred instances of vertical transmission and host shifts. Results Adult mosquitoes (271 specimens) representing 14 genera and 40 species were screened for Wolbachia. Overall, 21 species (51.2%) were found positive for Wolbachia, including five in the genus Aedes and five in the genus Culex. To our knowledge, Wolbachia infections have not been previously reported in seven of these 21 species: Aedes nr. fumidus, Aedes annandalei, Uranotaenia obscura, Uranotaenia trilineata, Verrallina butleri, Verrallina sp. and Zeugnomyia gracilis. Wolbachia were predominantly detected in the reproductive tissues, which is an indication of vertical transmission. However, Wolbachia infection rates varied widely within a mosquito host species. There was no clear signal of cophylogeny between the mosquito hosts and the 12 putative Wolbachia strains observed in this study. Host shift events were also observed. Conclusions Our results suggest that the mosquito-Wolbachia relationship is complex and that combinations of transmission modes and multiple evolutionary events likely explain the observed distribution of Wolbachia diversity across mosquito hosts. These findings have implications for a better understanding of the diversity and ecology of Wolbachia and for their utility as biocontrol agents.

2020 ◽  
Author(s):  
Huicong Ding ◽  
Huiqing Yeo ◽  
Nalini Puniamoorthy

Abstract Background: Wolbachia is an intracellular bacterial endosymbiont found in most insect lineages. In mosquitoes, the endosymbiont’s influence on host reproduction and arboviral transmission has spurred numerous studies aimed at using Wolbachia-infection as a vector control technique. However, there are several knowledge gaps in the literature and little is known about natural Wolbachia infection across species, transmission modes as well as the associations between various Wolbachia lineages and their hosts. This study aims to address these by exploring mosquito-Wolbachia associations and their evolutionary implications.Methods: We conducted tissue-specific PCR screening for Wolbachia infection in the leg, gut and reproductive tissues of wild mosquitoes from Singapore using the Wolbachia surface protein (wsp) molecular marker. Mosquito-Wolbachia associations were explored using three methods – a tanglegram, distance-based, and event-based method, and inferred instances of vertical transmission and host shifts.Results: Adult mosquitoes (271 specimens) representing 14 genera and 40 species were screened for Wolbachia. Overall, 21 species (51.2%) were found positive for Wolbachia, including Aedes (5 species) and Culex (5 species). Seven out of the 21 infected species were not previously reported: Aedes nr. fumidus, Aedes annandaelei, Uranotaenia obscura, Uranotaenia trilineata, Verrallina butleri, Verrallina sp., and Zeugnomyia gracilis. Wolbachia was predominantly detected in the reproductive tissues, an indication of vertical transmission. Despite this, Wolbachia infection rates vary widely within a mosquito host species. There is no clear signal of co-phylogeny between the mosquito hosts and the twelve putative Wolbachia strains observed in this study. Host shift events were also observed.Conclusions: Our results suggest that the mosquito-Wolbachia relationship is complex and that a combination of transmission modes and multiple evolutionary events likely explain the distribution of Wolbachia diversity observed across mosquito hosts. This has implications towards understanding Wolbachia’s diversity, ecology, and utility as a biocontrol method.


2020 ◽  
Author(s):  
Huicong Ding ◽  
Huiqing Yeo ◽  
Nalini Puniamoorthy

Abstract Background: Wolbachia is an intracellular bacterial endosymbiont found in most insect lineages. In mosquitoes, the endosymbiont’s influence on host reproduction and arboviral transmission has spurred numerous studies aimed at using Wolbachia-infection as a vector control technique. However, there are several knowledge gaps in the literature and little is known about natural Wolbachia infection across species, transmission modes as well as the associations between various Wolbachia lineages and their hosts. This study aims to address them by exploring mosquito-Wolbachia associations and their evolutionary implications.Methods: We conducted tissue-specific PCR screening for Wolbachia infection in the leg, gut and reproductive tissues of wild mosquitoes from Singapore using the Wolbachia surface protein (wsp) molecular marker. Mosquito-Wolbachia associations were explored using three methods – a tanglegram, distance-based, and event-based method, and inferred instances of vertical transmission and host shifts. Results: Adult mosquitoes (271 specimens) representing 14 genera and 40 species were screened for Wolbachia. Overall, 21 species (51.2%) were found positive for Wolbachia, including Aedes (5 species) and Culex (5 species). Seven out of the 21 infected species were not previously reported: Aedes nr. fumidus, Aedes annandaelei, Uranotaenia obscura, Uranotaenia trilineata, Verrallina butleri, Verrallina sp., and Zeugnomyia gracilis. Wolbachia was predominantly detected in the reproductive tissues, an indication of vertical transmission. Despite this, Wolbachia infection rates vary widely within a mosquito host species. There is no clear signal of co-phylogeny between the mosquito hosts and the twelve putative Wolbachia strains observed in this study. Host shift events were also observed. Conclusions: Our results suggest that the mosquito-Wolbachia relationship is complex and that combinations of transmission modes and multiple evolutionary events likely explain the distribution of Wolbachia diversity observed across mosquito hosts. This has implications towards understanding Wolbachia’s diversity, ecology, and utility as a biocontrol method.


2020 ◽  
Author(s):  
Huicong Ding ◽  
Huiqing Yeo ◽  
Nalini Puniamoorthy

Abstract Background: Wolbachia is an intracellular bacterial endosymbiont found in most insect lineages. In mosquitoes, the endosymbiont’s influence on host reproduction and arboviral transmission has spurred numerous studies aimed at using Wolbachia-infection as a vector control technique. However, there exist several gaps in the literature regarding the natural Wolbachia infection across species, modes of transmission as well as the associations between various Wolbachia lineages and their hosts. This study aims to address these by exploring mosquito-Wolbachia associations and their evolutionary implications.Methods: We conducted tissue-specific PCR screening of Wolbachia infection in wild mosquitoes from Singapore using the wsp molecular marker. Tissues examined include leg, gut, and reproductive tissues. We also explored mosquito-Wolbachia associations using three methods – a tanglegram, distance-based, and event-based method, and inferred instances of vertical transmission and host shifts. Results: We screened 271 adult mosquitoes (41 species and 14 genera) for Wolbachia and found that 43.9% of all individuals harboured Wolbachia. Eight out of the 21 infected species were not previously reported. We detected Wolbachia infections predominantly in the reproductive tissues, a strong indication of vertical transmission. Despite this, Wolbachia infection rates vary widely within a mosquito host species. There was no clear signal of co-phylogeny between the mosquito hosts and the twelve putative Wolbachia strains observed in our study. Host shift events were also observed. Conclusions: Our results suggest that the mosquito-Wolbachia relationship is complex and that a combination of transmission modes and multiple evolutionary events likely explain the distribution of Wolbachia diversity observed across mosquito hosts. This has implications towards understanding Wolbachia’s diversity, ecology, and utility as a biocontrol method.


2021 ◽  
Author(s):  
Joanne S. Griffin ◽  
Michael Gerth ◽  
Gregory D. D. Hurst

AbstractHeritable symbionts represent important components of host biology, both as antagonistic reproductive parasites and as beneficial protective partners. An important component of heritable microbes’ biology is their ability to establish in new host species, a process equivalent to a host shift for an infectiously transmitted parasite or pathogen. For a host shift to occur, the symbiont must be compatible with the host: it must not cause excess pathology, must have good vertical transmission, and possess a drive phenotype that enables spread. Classically, compatibility has been considered a declining function of genetic distance between novel and ancestral host species. Here we investigate the evolutionary lability of compatibility to heritable microbes by comparing the capacity for a symbiont to establish in two novel host species equally related to the ancestral host. Compatibility of the protective Spiroplasma from D. hydei with D. simulans and D. melanogaster was tested. The Spiroplasma had contrasting compatibility in these two host species. The transinfection showed pathology and low vertical transmission in D. melanogaster but was asymptomatic and transmitted with high efficiency in D. simulans. These results were not affected by the presence/absence of Wolbachia in either of the two species. The pattern of protection was not congruent with that for pathology/transmission, with protection being weaker in the D. simulans, the host in which Spiroplasma was asymptomatic and transmitted well. Further work indicated pathological interactions occurred in D. sechellia and D. yakuba, indicating that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasises first the rapidity with which host-symbiont compatibility evolves despite compatibility itself not being subject to direct selection, and second the independence of the different components of compatibility (pathology, transmission, protection). This requirement to fit three different independently evolving aspects of compatibility, if commonly observed, is likely to be a major feature limiting the rate of host shifts. Moving forward, the variation between sibling species pairs observed above provides an opportunity to identify the mechanisms behind variable compatibility between closely related host species, which will drive hypotheses as to the evolutionary drivers of compatibility variation.


Genes ◽  
2020 ◽  
Vol 11 (8) ◽  
pp. 852
Author(s):  
Hongli Chen ◽  
Mengwen Zhang ◽  
Mark Hochstrasser

Many species of arthropods carry maternally inherited bacterial endosymbionts that can influence host sexual reproduction to benefit the bacterium. The most well-known of such reproductive parasites is Wolbachia pipientis. Wolbachia are obligate intracellular α-proteobacteria found in nearly half of all arthropod species. This success has been attributed in part to their ability to manipulate host reproduction to favor infected females. Cytoplasmic incompatibility (CI), a phenomenon wherein Wolbachia infection renders males sterile when they mate with uninfected females, but not infected females (the rescue mating), appears to be the most common. CI provides a reproductive advantage to infected females in the presence of a threshold level of infected males. The molecular mechanisms of CI and other reproductive manipulations, such as male killing, parthenogenesis, and feminization, have remained mysterious for many decades. It had been proposed by Werren more than two decades ago that CI is caused by a Wolbachia-mediated sperm modification and that rescue is achieved by a Wolbachia-encoded rescue factor in the infected egg. In the past few years, new research has highlighted a set of syntenic Wolbachia gene pairs encoding CI-inducing factors (Cifs) as the key players for the induction of CI and its rescue. Within each Cif pair, the protein encoded by the upstream gene is denoted A and the downstream gene B. To date, two types of Cifs have been characterized based on the enzymatic activity identified in the B protein of each protein pair; one type encodes a deubiquitylase (thus named CI-inducing deubiquitylase or cid), and a second type encodes a nuclease (named CI-inducing nuclease or cin). The CidA and CinA proteins bind tightly and specifically to their respective CidB and CinB partners. In transgenic Drosophila melanogaster, the expression of either the Cid or Cin protein pair in the male germline induces CI and the expression of the cognate A protein in females is sufficient for rescue. With the identity of the Wolbachia CI induction and rescue factors now known, research in the field has turned to directed studies on the molecular mechanisms of CI, which we review here.


2009 ◽  
Vol 90 (7) ◽  
pp. 1767-1774 ◽  
Author(s):  
Khalid Amari ◽  
Lorenzo Burgos ◽  
Vicente Pallás ◽  
Maria Amelia Sánchez-Pina

The aim of this work was to follow Prunus necrotic ringspot virus (PNRSV) infection in apricot reproductive tissues and transmission of the virus to the next generation. For this, an analysis of viral distribution in apricot reproductive organs was carried out at different developmental stages. PNRSV was detected in reproductive tissues during gametogenesis. The virus was always present in the nucellus and, in some cases, in the embryo sac. Studies within infected seeds at the embryo globular stage revealed that PNRSV infects all parts of the seed, including embryo, endosperm and testa. In the torpedo and bent cotyledon developmental stages, high concentrations of the virus were detected in the testa and endosperm. At seed maturity, PNRSV accumulated slightly more in the embryo than in the cotyledons. In situ hybridization showed the presence of PNRSV RNA in embryos obtained following hand-pollination of virus-free pistils with infected pollen. Interestingly, tissue-printing from fruits obtained from these pistils showed viral RNA in the periphery of the fruits, whereas crosses between infected pistils and infected pollen resulted in a total invasion of the fruits. Taken together, these results shed light on the vertical transmission of PNRSV from gametes to seedlings.


2018 ◽  
Author(s):  
Shelbi L Russell

AbstractSymbiotic associations between bacteria and eukaryotes exhibit a range of transmission strategies. Anecdotal observations suggest that symbionts of terrestrial hosts tend to be strictly vertically inherited through host tissues, whereas symbionts of marine hosts tend towards horizontal transmission. Aside from a few cursory investigations, the rates and distributions of transmission modes have not been investigated in depth across associations, despite the consequences for symbiont and host evolution. To address this empirically and estimate the rate of each mode, I compiled data from the literature and for associations between transmission mode and the environment, transmission route, symbiont function, and taxa involved in the symbiosis. Of the 441 analyzed symbioses, 50.1% were strictly vertically transmitted, 34.0% exhibited some form of mixed mode transmission, and 15.9% were strictly horizontally transmitted. Binning symbioses by their environment revealed a significant skew towards vertical transmission on land and horizontal transmission in aquatic environments, with mixed modes abundant in both. However, host and symbiont taxa were not randomly distributed, which prevented the full separation of these variables. Overall, the data suggest that many symbiotic taxa are capable of horizontal transmission and barriers exist that reduce the rate of these events. Thus, both the environment type and host/symbiont taxa combined influence symbiont transmission mode evolution.One sentence summaryThrough an intensive analysis of the literature on symbiosis transmission modes, estimated rates for each transmission mode were calculated, revealing bias for horizontal transmission in the ocean and vertical transmission on land.


2021 ◽  
Author(s):  
Ehsan Sanaei ◽  
Gregory F Albery ◽  
Yun Kit Yeoh ◽  
Yen-Po Lin ◽  
Lyn G Cook ◽  
...  

AbstractWolbachia are among the most prevalent and widespread endosymbiotic bacteria on earth. Wolbachia’ s success in infecting an enormous number of arthropod species is attributed to two features: the range of phenotypes they induce in their hosts, and their ability to switch to new host species. Whilst much progress has been made in elucidating the phenotypes induced by Wolbachia, our understanding of Wolbachia host shifting is still very limited: we lack answers to even fundamental questions concerning Wolbachia’s routes of transfer and the importance of factors influencing host shifts. Here, we investigate the diversity and host-shift patterns of Wolbachia in scale insects, a group of arthropods with intimate associations with other insects that make them well-suited to studying host shifts. Using Illumina pooled amplicon sequencing of Wolbachia-infected scale insects and their direct associates we determined the identity of all Wolbachia strains, revealing that 32% of samples were multiply infected (with up to five distinct strains per species). We then fitted a Generalised Additive Mixed Model (GAMM) to our data to estimate the influence of factors such as the host phylogeny and the geographic distribution of each species on Wolbachia strain sharing among scale insect species. The model predicts no significant contribution of host geography but strong effects of host phylogeny, with high rates of Wolbachia sharing among closely related species and a sudden drop-off in sharing with increasing phylogenetic distance. We also detected the same Wolbachia strain in scale insects and several intimately associated species (ants, wasps, beetles, and flies). This indicates putative host shifts and potential routes of transfers via these associates and highlights the importance of ecological connectivity in Wolbachia host-shifting.


2008 ◽  
Vol 276 (1655) ◽  
pp. 219-228 ◽  
Author(s):  
Christopher N Balakrishnan ◽  
Kristina M Sefc ◽  
Michael D Sorenson

Behavioural and molecular studies suggest that brood parasitic indigobirds ( Vidua spp.) rapidly diversified through a process of speciation by host shift. However, behavioural imprinting on host song, the key mechanism promoting speciation in this system, may also lead to hybridization and gene flow among established indigobird species when and if female indigobirds parasitize hosts already associated with other indigobird species. It is therefore not clear to what extent the low level of genetic differentiation among indigobird species is due to recent common ancestry versus ongoing gene flow. We tested for reproductive isolation among three indigobird species in Cameroon, one of which comprises two morphologically indistinguishable host races. Mimicry of host songs corresponded with plumage colour in 184 male indigobirds, suggesting that females rarely parasitize the host of another indigobird species. Paternity analyses, however, suggest that imperfect specificity in host and/or mate choice allows for continuing gene flow between recently formed host races of the Cameroon Indigobird Vidua camerunensis ; while 63 pairs of close relatives were associated with the same host, two strongly supported father–son pairs included males mimicking the songs of the two different hosts of V. camerunensis . Thus, complete reproductive isolation is not necessarily an automatic consequence of host shifts, a result that suggests an important role for natural and/or sexual selection in indigobird speciation.


Sign in / Sign up

Export Citation Format

Share Document