Molecular detection of Wolbachia pipientis in natural populations of mosquito vectors of Dirofilaria immitis from continental Portugal: first detection in Culex theileri
Open accessAbstract
Wolbachia pipientis (Rickettsiales: Rickettsiaceae) protects mosquitoes from infections with arboviruses and parasites. However, the effect of its co-infection on vector competence for Dirofilaria immitis (Spirurida: Onchocercidae) in the wild has not been investigated. This study aimed to screen vectors of D. immitis for wPip, to characterize these, and to investigate a possible association between the occurrence of W. pipientis and that of the nematode. The presence of W. pipientis was assessed in the five mosquito potential vectors of D. immitis in Portugal. Polymerase chain reaction (PCR) products were sequenced, and wPip haplotypes were determined by PCR-restricted fragment length polymorphism (RFLP). Results showed that wPip was detected in 61.5% of Culex pipiens (Diptera: Culicidae) pools and 6.3% of Culex theileri pools. wPip 16s rRNA sequences found in Cx. theileri exactly match those from Cx. pipiens, confirming a mosquito origin, rather than a nematode origin, as some specimens were infected with D. immitis. Only wPip haplotype I was found. No association was found between the presence of wPip and D. immitis in mosquitoes and hence a role for this endosymbiont in influencing vectorial competence is yet to be identified. This study contributes to understanding of wPip distribution in mosquito populations and, to the best of the authors' knowledge, is the first report of natural infections by wPip in Cx. theileri.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In Portugal, D. immitis larvae have been identified in new mosquito species Cx. pipiens s.l., Cx. theileri, Ae. caspius, An. maculipennis s.l., and Ae. dentritus s.l. in Coimbra, Santarém, and Setúbal.
“In Portugal, the presence of D. immitis larvae were identified in new species of mosquitoes, such us Cx. pipiens s.l.; Cx. theileri, Ae. caspius, An. maculipennis s.l., and Ae. dentritus s.l. in Coimbra (centre), Santarém, and Setúbal (centre-southern) [145,146].”
From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [146]
There are only three studies that have focused on investigating simultaneous infection with native Wolbachia and Dirofilaria in mosquitoes from natural populations.
“There are only three studies that have focused on investigating simultaneous infection with native Wolbachia and Dirofilaria in mosquitoes from natural populations [22, 23, 51].”
From <i>Dirofilaria</i> and <i>Wolbachia</i> in mosquitoes (Diptera: Culicidae) in central European Russia and on the Black Sea coast (2019) · cites this paper as [22]
Cites
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.22.4673 · Cited by 64,617 · see citing works
MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013) · Molecular biology and evolution · doi:10.1093/molbev/mst197 · Cited by 41,174 · see citing works
Hall, T. A. (1999) · Nucleic Acids Symposium Series · doi:10.14601/phytopathol_mediterr-14998u1.29 · Cited by 38,373 · see citing works
Kimura, M. (1980) · Journal of Molecular Evolution · doi:10.1007/bf01731581 · Cited by 29,778 · see citing works
Wolbachia: master manipulators of invertebrate biology
Werren, J. H., Baldo, L., & Clark, M. E. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1969 · Cited by 2,830 · see citing works
Guo, W. W., Cheng, Y., & Deng, X. (2002) · Plant Cell Reports · doi:10.1007/s00299-001-0399-7 · Cited by 2,227 · see citing works
A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium
Moreira, L. A., Iturbe‐Ormaetxe, I., Jeffery, J. A. L., Lu, G., Pyke, A. T., Hedges, L. M., Rocha, B. C., Hall‐Mendelin, S., Day, A., Riegler, M., et al. (2009) · Cell · doi:10.1016/j.cell.2009.11.042 · Cited by 1,734 · see citing works
Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission
Hoffmann, A. A., Montgomery, B. L., Popovici, J., Iturbe‐Ormaetxe, I., Johnson, P. H., Muzzi, F. C., Greenfield, M., Durkan, M., Leong, Y. S., Dong, Y., et al. (2011) · Nature · doi:10.1038/nature10356 · Cited by 1,586 · see citing works
O’Neill, S. L., Giordano, R., Colbert, A. M. E., Karr, T. L., & Robertson, H. M. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.7.2699 · Cited by 1,099 · see citing works
Immune Activation by Life-Shortening Wolbachia and Reduced Filarial Competence in Mosquitoes
Kambris, Z., Cook, P. E., Phuc, H. K., & Sinkins, S. P. (2009) · Science · doi:10.1126/science.1177531 · Cited by 501 · see citing works
Wolbachia Invades Anopheles stephensi Populations and Induces Refractoriness to Plasmodium Infection
Bian, G., Joshi, D., Dong, Y., Lü, P., Zhou, G., Pan, X., Xu, Y., Dimopoulos, G., & Xi, Z. (2013) · Science · doi:10.1126/science.1236192 · Cited by 477 · see citing works
Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans.
Hoffmann, A. A., Turelli, M., & Harshman, L. G. (1990) · Genetics · doi:10.1093/genetics/126.4.933 · Cited by 457 · see citing works
Wolbachia infections are distributed throughout insect somatic and germ line tissues
Dobson, S. L., Bourtzis, K., Braig, H. R., Jones, B. F., Zhou, W., Rousset, F., & O’Neill, S. L. (1999) · Insect Biochemistry and Molecular Biology · doi:10.1016/s0965-1748(98)00119-2 · Cited by 425 · see citing works
Wolbachia and the biological control of mosquito‐borne disease
Iturbe‐Ormaetxe, I., Walker, T., & Neill, S. L. O. (2011) · EMBO Reports · doi:10.1038/embor.2011.84 · Cited by 419 · see citing works
van den Hurk, A. F., Hall‐Mendelin, S., Pyke, A. T., Frentiu, F. D., McElroy, K. L., Day, A., Higgs, S., & O’Neill, S. L. (2012) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001892 · Cited by 406 · see citing works
A contig assembly program based on sensitive detection of fragment overlaps
Huang, X. (1992) · Genomics · doi:10.1016/s0888-7543(05)80277-0 · Cited by 296 · see citing works
Genome Evolution of Wolbachia Strain wPip from the Culex pipiens Group
Klasson, L., Walker, T., Sebaihia, M., Sanders, M., Quail, M. A., Lord, A., Sanders, S., Earl, J., O’Neill, S. L., Thomson, N. R., et al. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn133 · Cited by 249 · see citing works
Comparison of methods for estimation of individual-level prevalence based on pooled samples
Cowling, D. W., Gardner, I. A., & Johnson, W. O. (1999) · Preventive Veterinary Medicine · doi:10.1016/s0167-5877(98)00131-7 · Cited by 178 · see citing works
Diversification of Wolbachia Endosymbiont in the Culex pipiens Mosquito
Atyame, C. M., Delsuc, F., Pasteur, N., Weill, M., & Duron, O. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr083 · Cited by 158 · see citing works
Ricci, I., Cancrini, G., Gabrielli, S., D'amelio, S., & Favia, G. (2002) · Journal of Medical Entomology · doi:10.1603/0022-2585-39.4.562 · Cited by 126 · see citing works
Natural vectors of dirofilariasis in rural and urban areas of the Tuscan region, central Italy
Cancrini, G., Magi, M., Gabrielli, S., Arispici, M., Tolari, F., Dell’Omodarme, M., & Prati, M. C. (2006) · Journal of Medical Entomology · doi:10.1093/jmedent/43.3.574 · Cited by 105 · see citing works
Duron, O., Lagnel, J., Michel Raymond, A., Bourtzis, K., Fort, P., & Weill, M. (2005) · Molecular Ecology · doi:10.1111/j.1365-294x.2005.02495.x · Cited by 86 · see citing works
Duron, O., Boureux, A., Echaubard, P., Berthomieu, A., Berticat, C., Fort, P., & Weill, M. (2007) · Journal of Bacteriology · doi:10.1128/jb.00142-07 · Cited by 75 · see citing works
Zélé, F., Nicot, A., Duron, O., & Rivero, A. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02519.x · Cited by 74 · see citing works
Population structure of Wolbachia and cytoplasmic introgression in a complex of mosquito species
Dumas, É., Atyame, C. M., Milesi, P., et al. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-181 · Cited by 73 · see citing works
Zug, R., Koehncke, A., & Hammerstein, P. (2012) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2012.02601.x · Cited by 63 · see citing works
First molecular identification of mosquito vectors of Dirofilaria immitis in continental Portugal
Ferreira, C. A. C., de Pinho Mixão, V., Novo, M. T. L. M., Calado, M. M. P., Gonçalves, L. A. P., Belo, S. M. D., & de Almeida, A. P. G. (2015) · Parasites & Vectors · doi:10.1186/s13071-015-0760-2 · Cited by 61 · see citing works
Self-citationAndrews, E. S., Crain, P. R., Fu, Y., et al. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003075 · Cited by 55 · see citing works
Шайкевич, Е. В., Vinogradova, E. B., Bouattour, A., & de Almeida, A. P. G. (2016) · Parasites & Vectors · doi:10.1186/s13071-016-1333-8 · Cited by 54 · see citing works
Self-citationPrevalence of canine heartworm ( <i>Dirofilaria immitis</i> ) disease in dogs of central Portugal
Vieira, A. L., Vieira, M. J., Oliveira, J. M., Simões, A. R., Diez-Baños, P., & Gestal, J. (2014) · Parasite · doi:10.1051/parasite/2014003 · Cited by 53 · see citing works
Aedes vexans and Culex pipiens as the potential vectors of Dirofilaria immitis in Central Turkey
Yildirim, A., Inci, A., Duzlu, O., Biskin, Z., Ica, A., & Sahin, I. (2011) · Veterinary Parasitology · doi:10.1016/j.vetpar.2010.12.023 · Cited by 48 · see citing works
Prevalence and seasonal variations of canine dirofilariosis in Portugal
Alho, A. M., Landum, M., Ferreira, C., Meireles, J., Gonçalves, L., de Carvalho, L. M., & Belo, S. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.08.014 · Cited by 45 · see citing works
Self-citationMany compatible Wolbachia strains coexist within natural populations of Culex pipiens mosquito
Duron, O., Raymond, M., & Weill, M. (2010) · Heredity · doi:10.1038/hdy.2010.146 · Cited by 44 · see citing works
Morchón, R., Bargues, M. D., Latorre, J. M., Melero-Alcíbar, R., Pou-Barreto, C., Mas-Coma, S., & Simón, F. (2007) · Vector-Borne and Zoonotic Diseases · doi:10.1089/vbz.2007.0124 · Cited by 43 · see citing works
Vieira, L., Silvestre-Ferreira, A. C., Fontes-Sousa, A. P., Balreira, A. C., Morchón, R., Carretón, E., Vilhena, H., Simón, F., & Montoya-Alonso, J. A. (2015) · Journal of Helminthology · doi:10.1017/s0022149x14000352 · Cited by 37 · see citing works
Seroreactivity to Dirofilariaantigens in people from different areas of Serbia
Tasić-Otašević, S. A., Gabrielli, S. V., Tasić, A. V., MiladinovićTasić, N. L., Kostić, J. T., Ignjatović, A. M., Popović Dragonjić, L. D., Milošević, Z. G., Arsić-Arsenijević, V. S., & Cancrini, G. A. (2014) · BMC Infectious Diseases · doi:10.1186/1471-2334-14-68 · Cited by 24 · see citing works
Filarial susceptibility and effects of Wolbachia in Aedes pseudoscutellaris mosquitoes
Dutton, T. J., & Sinkins, S. P. (2005) · Medical and Veterinary Entomology · doi:10.1111/j.0269-283x.2005.00557.x · Cited by 22 · see citing works
Wolbachia Infection and Mitochondrial DNA Comparisons among Culex Mosquitoes in South West Iran
Behbahani, A. (2011) · Pakistan Journal of Biological Sciences · doi:10.3923/pjbs.2012.54.57 · Cited by 16 · see citing works
Khrabrova, N. V., Bukhanskaya, E. D., Sibataev, A. K., et al. (2009) · European mosquito bulletin · Cited by 13 · see citing works
Shaikevich, E. V., & Zakharov, I. A. (2014) · Russian Journal of Genetics · doi:10.1134/s1022795414110131 · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
What has happened to heartworm disease in Europe in the last 10 years?
Morchón, R., Montoya-Alonso, J. A., Rodríguez-Escolar, I., & Carretón, E. (2022) · Pathogens · doi:10.3390/pathogens11091042 · Cited by 69 · see citing works
Shaikevich, E., Bogacheva, A., & Ganushkina, L. (2019) · Parasite · doi:10.1051/parasite/2019002 · Cited by 47 · see citing works
Current state of canine heartworm in Portugal
Esteves-Guimarães, J., Matos, J. I., Leal-Sousa, B., Oliveira, P., Lobo, L., Silvestre-Ferreira, A. C., Soares, C. S., Rodríguez-Escolar, I., Carretón, E., Morchón, R., et al. (2024) · Animals · doi:10.3390/ani14091300 · Cited by 11 · see citing works
- Authors
- DE PINHO MIXÃO, V., MENDES, A. M., MAURÍCIO, I. L., CALADO, M. M., NOVO, M. T., BELO, S., & ALMEIDA, A. P. G.
- Affiliations
- Global Health and Tropical Medicine, GHTM, UEI Medical Parasitology, Instituto de Higiene e Medicina Tropical, IHMT Universidade Nova de Lisboa, UNL Lisbon Portugal
- Universidade Politécnica de Lisboa (PT)
- Universidade Nova de Lisboa (PT)
- University of Pretoria (ZA)
- Corresponding author
- ALMEIDA, A. P. G.
- Venue
- Medical and Veterinary Entomology
- Publisher
- Wiley
- Published
- 2016-06-09
- Volume
- 30
- Issue
- 3
- Pages
- 301-309
- ISSN
- 0269-283X (ISSN-L)
- 1365-2915
- OpenAlex
- W2409934405
- Cited by
- 17
- References
- 40
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 4 · 2022: 2 · 2021: 1 · 2020: 3 · 2019: 4
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- Medical and Veterinary Entomology (publishedVersion)
- PubMed (publishedVersion)
- Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT) (submittedVersion, cc-by-nc-nd)
- Funders
- Fundação para a Ciência e Tecnologia (PTDC/SAU-SAP/113523/2009)
- Global Health and Tropical Medicine (UID/Multi/04413/2013)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
- Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
- Keywords
- Wolbachia pipientis, Dirofilaria immitis, Culex theileri, Culex pipiens, mosquito vectors, vector competence, 16S rRNA, endosymbionts, natural infection, Portugal
- MeSH terms
- Mosquito Vectors, Animals, Culex, Dirofilaria immitis, Dirofilariasis, DNA, Bacterial, Haplotypes, Portugal, Polymorphism, Restriction Fragment Length, RNA, Ribosomal, 16S, Polymerase Chain Reaction, Wolbachia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review