Wolbachia and Cytoplasmic Incompatibility in the CaliforniaCulex pipiensMosquito Species Complex: Parameter Estimates and Infection Dynamics in Natural Populations

Genetics ◽  
2003 ◽  
Vol 165 (4) ◽  
pp. 2029-2038 ◽  
Author(s):  
Jason L Rasgon ◽  
Thomas W Scott
Keyword(s):  
Species Complex ◽  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Wolbachia Infection ◽  
Field Conditions ◽  
Parameter Estimates ◽  
Infection Prevalence ◽  
Infection Frequency ◽  
Specific Pcr ◽  
Vector Borne

AbstractBefore maternally inherited bacterial symbionts like Wolbachia, which cause cytoplasmic incompatibility (CI; reduced hatch rate) when infected males mate with uninfected females, can be used in a program to control vector-borne diseases it is essential to understand their dynamics of infection in natural arthropod vector populations. Our study had four goals: (1) quantify the number of Wolbachia strains circulating in the California Culex pipiens species complex, (2) investigate Wolbachia infection frequencies and distribution in natural California populations, (3) estimate the parameters that govern Wolbachia spread among Cx. pipiens under laboratory and field conditions, and (4) use these values to estimate equilibrium levels and compare predicted infection prevalence levels to those observed in nature. Strain-specific PCR, wsp gene sequencing, and crossing experiments indicated that a single Wolbachia strain infects Californian Cx. pipiens. Infection frequency was near or at fixation in all populations sampled for 2 years along a >1000-km north-south transect. The combined statewide infection frequency was 99.4%. Incompatible crosses were 100% sterile under laboratory and field conditions. Sterility decreased negligibly with male age in the laboratory. Infection had no significant effect on female fecundity under laboratory or field conditions. Vertical transmission was >99% in the laboratory and ∼98.6% in the field. Using field data, models predicted that Wolbachia will spread to fixation if infection exceeds an unstable equilibrium point above 1.4%. Our estimates accurately predicted infection frequencies in natural populations. If certain technical hurdles can be overcome, our data indicate that Wolbachia can invade vector populations as part of an applied transgenic strategy for vector-borne disease reduction.

scholarly journals Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations.

Genetics ◽  
1995 ◽  
Vol 140 (4) ◽  
pp. 1319-1338 ◽  
Author(s):  
M Turelli ◽  
A A Hoffmann
Keyword(s):  
South America ◽  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Wolbachia Infection ◽  
Drosophila Simulans ◽  
Parameter Estimates ◽  
Maternal Transmission ◽  
Egg Hatch ◽  
Pcr Assays ◽  
Parameter Values

Abstract In Drosophila simulans, cytoplasmically transmitted Wolbachia microbes cause reduced egg hatch when infected males mate with uninfected females. A Wolbachia infection and an associated mtDNA variant have spread northward through California since 1986. PCR assays show that Wolbachia infection is prevalent throughout the continental US and Central and South America, but some lines from Florida and Ecuador that are PCR-positive for Wolbachia do not cause incompatibility. We estimate from natural populations infection frequencies and the transmission and incompatibility parameter values that affect the spread of the infection. On average, infected females from nature produce 3-4% uninfected ova. Infected females with relatively low fidelity of maternal transmission show partial incompatibility with very young infected laboratory males. Nevertheless, crosses between infected flies in nature produce egg-hatch rates indistinguishable from those produced by crosses between uninfected individuals. Incompatible crosses in nature produce hatch rates 30-70% as high as those from compatible crosses. Wild-caught infected and uninfected females are equally fecund in the laboratory. Incompatibility decreases with male age, and age-specific incompatibility levels suggest that males mating in nature may often be 2 or 3 weeks old. Our parameter estimates accurately predict the frequency of Wolbachia infection in California populations.

Population Dynamics of the Wolbachia Infection Causing Cytoplasmic Incompatibility in Drosophila melanogaster

Genetics ◽  
1998 ◽  
Vol 148 (1) ◽  
pp. 221-231 ◽  
Author(s):  
Ary A Hoffmann ◽  
Miriam Hercus ◽  
Hayat Dagher
Keyword(s):  
Population Dynamics ◽  
Drosophila Melanogaster ◽  
Cytoplasmic Incompatibility ◽  
Larval Density ◽  
Natural Populations ◽  
Wolbachia Infection ◽  
Field Conditions ◽  
Exact Nature ◽  
Infection Status ◽  
Factors Influencing

Abstract Field populations of Drosophila melanogaster are often infected with Wolbachia, a vertically transmitted microorganism. Under laboratory conditions the infection causes partial incompatibility in crosses between infected males and uninfected females. Here we examine factors influencing the distribution of the infection in natural populations. We show that the level of incompatibility under field conditions was much weaker than in the laboratory. The infection was not transmitted with complete fidelity under field conditions, while field males did not transmit the infection to uninfected females and Wolbachia did not influence sperm competition. There was no association between field fitness as measured by fluctuating asymmetry and the infection status of adults. Infected field females were smaller than uninfecteds in some collections from a subtropical location, but not in other collections from the same location. Laboratory cage studies showed that the infection did not change in frequency when populations were maintained at a low larval density, but it decreased in frequency at a high larval density. Monitoring of infection frequencies in natural populations indicated stable frequencies in some populations but marked fluctuations in others. Simple models suggest that the infection probably provides a fitness benefit for the host in order to persist in populations. The exact nature of this benefit remains elusive.

scholarly journals Artificial Triple Wolbachia Infection in Aedes albopictus Yields a New Pattern of Unidirectional Cytoplasmic Incompatibility

2010 ◽  
Vol 76 (17) ◽  
pp. 5887-5891 ◽  
Author(s):  
Yuqing Fu ◽  
Laurent Gavotte ◽  
David R. Mercer ◽  
Stephen L. Dobson
Keyword(s):  
Aedes Albopictus ◽  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Wolbachia Infection ◽  
Host Population ◽  
Invasive Pest ◽  
Gene Drive ◽  
Population Replacement ◽  
Asian Tiger ◽  
Spread Of Infection

ABSTRACT Obligately intracellular Wolbachia bacteria infect numerous invertebrates and often manipulate host reproduction to facilitate the spread of infection. An example of reproductive manipulation is Wolbachia-induced cytoplasmic incompatibility (CI), which occurs commonly in insects. This CI has been the focus both of basic scientific studies of naturally occurring invasion events and of applied investigations on the use of Wolbachia as a vehicle to drive desired genotypes into insect populations (“gene drive” or “population replacement” strategies). The latter application requires an ability to generate artificial infections that cause a pattern of unidirectional incompatibility with the targeted host population. A suggested target of population replacement strategies is the mosquito Aedes albopictus (Asian tiger mosquito), an important invasive pest and disease vector. Aedes albopictus individuals are naturally “superinfected” with two Wolbachia types: wAlbA and wAlbB. Thus, generating a strain that is unidirectionally incompatible with field populations requires the introduction of an additional infection into the preexisting superinfection. Although prior reports demonstrate an ability to transfer Wolbachia infections to A. albopictus artificially, including both intra- and interspecific Wolbachia transfers, previous efforts have not generated a strain capable of invading natural populations. Here we describe the generation of a stable triple infection by introducing Wolbachia wRi from Drosophila simulans into a naturally superinfected A. albopictus strain. The triple-infected strain displays a pattern of unidirectional incompatibility with the naturally infected strain. This unidirectional CI, combined with a high fidelity of maternal inheritance and low fecundity effects, suggests that the artificial cytotype could serve as an appropriate vehicle for gene drive.

scholarly journals Mutualistic Wolbachia Infection in Aedes albopictus: Accelerating Cytoplasmic Drive

Genetics ◽  
2002 ◽  
Vol 160 (3) ◽  
pp. 1087-1094
Author(s):  
Stephen L Dobson ◽  
Eric J Marsland ◽  
Wanchai Rattanadechakul
Keyword(s):  
Aedes Albopictus ◽  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Wolbachia Infection ◽  
Host Population ◽  
Population Replacement ◽  
Infection Dynamics ◽  
Model Predictions ◽  
Wolbachia Infection Dynamics ◽  
Hatching Rates

Abstract Maternally inherited rickettsial symbionts of the genus Wolbachia occur commonly in arthropods, often behaving as reproductive parasites by manipulating host reproduction to enhance the vertical transmission of infections. One manipulation is cytoplasmic incompatibility (CI), which causes a significant reduction in brood hatch and promotes the spread of the maternally inherited Wolbachia infection into the host population (i.e., cytoplasmic drive). Here, we have examined a Wolbachia superinfection in the mosquito Aedes albopictus and found the infection to be associated with both cytoplasmic incompatibility and increased host fecundity. Relative to uninfected females, infected females live longer, produce more eggs, and have higher hatching rates in compatible crosses. A model describing Wolbachia infection dynamics predicts that increased fecundity will accelerate cytoplasmic drive rates. To test this hypothesis, we used population cages to examine the rate at which Wolbachia invades an uninfected Ae. albopictus population. The observed cytoplasmic drive rates were consistent with model predictions for a CI-inducing Wolbachia infection that increases host fecundity. We discuss the relevance of these results to both the evolution of Wolbachia symbioses and proposed applied strategies for the use of Wolbachia infections to drive desired transgenes through natural populations (i.e., population replacement strategies).

Offsetting Effects of Wolbachia Infection and Heat Shock on Sperm Production inDrosophila simulans: Analyses of Fecundity, Fertility and Accessory Gland Proteins

Genetics ◽  
2000 ◽  
Vol 155 (1) ◽  
pp. 167-178 ◽  
Author(s):  
Rhonda R Snook ◽  
Sophia Y Cleland ◽  
Mariana F Wolfner ◽  
Timothy L Karr
Keyword(s):  
Heat Shock ◽  
Natural Populations ◽  
Adult Life ◽  
Reproductive Factors ◽  
Male Gamete ◽  
Wolbachia Infection ◽  
Accessory Gland ◽  
Sperm Production ◽  
Accessory Gland Proteins ◽  
Mating Conditions

AbstractInfection in Drosophila simulans with the endocellular symbiont Wolbachia pipientis results in egg lethality caused by failure to properly initiate diploid development (cytoplasmic incompatibility, CI). The relationship between Wolbachia infection and reproductive factors influencing male fitness has not been well examined. Here we compare infected and uninfected strains of D. simulans for (1) sperm production, (2) male fertility, and (3) the transfer and processing of two accessory gland proteins, Acp26Aa or Acp36De. Infected males produced significantly fewer sperm cysts than uninfected males over the first 10 days of adult life, and infected males, under varied mating conditions, had lower fertility compared to uninfected males. This fertility effect was due to neither differences between infected and uninfected males in the transfer and subsequent processing of accessory gland proteins by females nor to the presence of Wolbachia in mature sperm. We found that heat shock, which is known to decrease CI expression, increases sperm production to a greater extent in infected compared to uninfected males, suggesting a possible link between sperm production and heat shock. Given these results, the roles Wolbachia and heat shock play in mediating male gamete production may be important parameters for understanding the dynamics of infection in natural populations.

scholarly journals On the mod resc Model and the Evolution of Wolbachia Compatibility Types

Genetics ◽  
2001 ◽  
Vol 159 (4) ◽  
pp. 1415-1422 ◽  
Author(s):  
Sylvain Charlat ◽  
Claire Calmet ◽  
Hervé Merçot
Keyword(s):  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Evolutionary Process ◽  
Embryonic Mortality ◽  
Step Process ◽  
Zygote Development ◽  
Specific Manner

Abstract Cytoplasmic incompatibility (CI) is induced by the endocellular bacterium Wolbachia. It results in an embryonic mortality occurring when infected males mate with uninfected females. The mechanism involved is currently unknown, but the mod resc model allows interpretation of all observations made so far. It postulates the existence of two bacterial functions: modification (mod) and rescue (resc). The mod function acts in the males' germline, before Wolbachia are shed from maturing sperm. If sperm is affected by mod, zygote development will fail unless resc is expressed in the egg. Interestingly, CI is also observed in crosses between infected males and infected females when the two partners bear different Wolbachia strains, demonstrating that mod and resc interact in a specific manner: Two Wolbachia strains are compatible with each other only if they harbor the same compatibility type. Here we focus on the evolutionary process involved in the emergence of new compatibility types from ancestral ones. We argue that new compatibility types are likely to evolve under a wider range of conditions than previously thought, through a two-step process. First, new mod variants can arise by mutation and spread by drift. This is possible because mod is expressed in males and Wolbachia is transmitted by females. Second, once such a mod variant achieves a certain frequency, it can create the conditions for the deterministic invasion of a new resc variant, allowing the invasion of a new mod resc pair. Furthermore, we show that a stable polymorphism might be maintained in natural populations, allowing the long-term existence of “suicidal” Wolbachia strains.

Molecular Evidence of Wolbachia Infection in Natural Populations of Tropical Odonates

2003 ◽  
Vol 47 (4) ◽  
pp. 314-318 ◽  
Author(s):  
Apisit Thipaksorn ◽  
Wanwisa Jamnongluk ◽  
Pattamaporn Kittayapong
Keyword(s):  
Natural Populations ◽  
Wolbachia Infection ◽  
Molecular Evidence

scholarly journals Contrasting Patterns of Virus Protection and Functional Incompatibility Genes in Two ConspecificWolbachiaStrains fromDrosophila pandora

2018 ◽  
Vol 85 (5) ◽  
Author(s):  
Angelique K. Asselin ◽  
Simon Villegas-Ospina ◽  
Ary A. Hoffmann ◽  
Jeremy C. Brownlie ◽  
Karyn N. Johnson
Keyword(s):  
Disease Transmission ◽  
Cytoplasmic Incompatibility ◽  
Natural Populations ◽  
Differential Protection ◽  
Content Type ◽  
Infection Dynamics ◽  
Modification Factor ◽  
Control Disease ◽  
Multiple Strains ◽  
High Degree

ABSTRACTWolbachiainfections can present different phenotypes in hosts, including different forms of reproductive manipulation and antiviral protection, which may influence infection dynamics within host populations. In populations ofDrosophila pandoratwo distinctWolbachiastrains coexist, each manipulating host reproduction: strainwPanCI causes cytoplasmic incompatibility (CI), whereas strainwPanMK causes male killing (MK). CI occurs when aWolbachia-infected male mates with a female not infected with a compatible type ofWolbachia, leading to nonviable offspring.wPanMK can rescuewPanCI-induced CI but is unable to induce CI. The antiviral protection phenotypes provided by thewPanCI andwPanMK infections were characterized; the strains showed differential protection phenotypes, whereby cricket paralysis virus (CrPV)-induced mortality was delayed in flies infected withwPanMK but enhanced in flies infected withwPanCI compared to their respectiveWolbachia-cured counterparts. Homologs of thecifAandcifBgenes involved in CI identified inwPanMK andwPanCI showed a high degree of conservation; however, the CifB protein inwPanMK is truncated and is likely nonfunctional. The presence of a likely functional CifA inwPanMK andwPanMK’s ability to rescuewPanCI-induced CI are consistent with the recent confirmation of CifA’s involvement in CI rescue, and the absence of a functional CifB protein further supports its involvement as a CI modification factor. Taken together, these findings indicate thatwPanCI andwPanMK have different relationships with their hosts in terms of their protective and CI phenotypes. It is therefore likely that different factors influence the prevalence and dynamics of these coinfections in naturalDrosophila pandorahosts.IMPORTANCEWolbachiastrains are common endosymbionts in insects, with multiple strains often coexisting in the same species. The coexistence of multiple strains is poorly understood but may rely onWolbachiaorganisms having diverse phenotypic effects on their hosts. AsWolbachiais increasingly being developed as a tool to control disease transmission and suppress pest populations, it is important to understand the ways in which multipleWolbachiastrains persist in natural populations and how these might then be manipulated. We have therefore investigated viral protection and the molecular basis of cytoplasmic incompatibility in two coexistingWolbachiastrains with contrasting effects on host reproduction.

scholarly journals Variance additivity of genetic populational parameter estimates obtained through bootstrapping

2003 ◽  
Vol 60 (1) ◽  
pp. 97-103 ◽  
Author(s):  
Luciana Aparecida Carlini-Garcia ◽  
Roland Vencovsky ◽  
Alexandre Siqueira Guedes Coelho
Keyword(s):  
Bootstrap Method ◽  
Natural Populations ◽  
Molecular Data ◽  
Fixation Index ◽  
Parameter Estimates ◽  
Genetic Population ◽  
Relative Contribution ◽  
Population Structure Analysis ◽  
Resampling Procedure ◽  
Variance Estimates

Studying the genetic structure of natural populations is very important for conservation and use of the genetic variability available in nature. This research is related to genetic population structure analysis using real and simulated molecular data. To obtain variance estimates of pertinent parameters, the bootstrap resampling procedure was applied over different sampling units, namely: individuals within populations (I), populations (P), and individuals and populations simultaneously (I, P). The considered parameters were: the total fixation index (F or F IT), the fixation index within populations (f or F IS) and the divergence among populations or intrapopulation coancestry (theta or F ST). The aim of this research was to verify if the variance estimates of <IMG SRC="/img/fbpe/sa/v60n1/14549x09.gif">, <IMG SRC="/img/fbpe/sa/v60n1/14549x10.gif">and <IMG SRC="/img/fbpe/sa/v60n1/14549x11.gif">, found through the resampling over individuals and populations simultaneously (I, P), correspond to the sum of the respective variance estimates obtained from separated resampling over individuals and populations (I+P). This equivalence was verified in all cases, showing that the total variance estimate of <IMG SRC="/img/fbpe/sa/v60n1/14549x09.gif">, <IMG SRC="/img/fbpe/sa/v60n1/14549x10.gif">and <IMG SRC="/img/fbpe/sa/v60n1/14549x11.gif">can be obtained summing up the variances estimated for each source of variation separately. Results also showed that this facilitates the use of the bootstrap method on data with hierarchical structure and opens the possibility of obtaining the relative contribution of each source of variation to the total variation of estimated parameters.

scholarly journals Causation without correlation: parasite-mediated frequency-dependent selection and infection prevalence

2021 ◽  
Author(s):  
Curtis M Lively ◽  
Julie Xu ◽  
Frida Ben-Ami
Keyword(s):  
Genetic Diversity ◽  
Natural Populations ◽  
Infection Prevalence ◽  
Strong Positive Correlation ◽  
Frequency Dependent ◽  
Frequency Dependent Selection ◽  
Host Diversity ◽  
Host Genetic ◽  
Host Parasite

Parasite-mediated selection is thought to maintain host genetic diversity for resistance. We might thus expect to find a strong positive correlation between host genetic diversity and infection prevalence across natural populations. Here we used computer simulations to examine host-parasite coevolution in 20 simi-isolated clonal populations across a broad range of values for both parasite virulence and parasite fecundity. We found that the correlation between host genetic diversity and infection prevalence can be significantly positive for intermediate values of parasite virulence and fecundity. But the correlation can also be weak and statistically non-significant, even when parasite-mediated frequency-dependent selection is the sole force maintaining host diversity. Hence correlational analyses of field populations, while useful, might underestimate the role of parasites in maintaining host diversity.

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