Examination of the interior of sand fly (Diptera: Psychodidae) abdomen reveals novel cuticular structures involved in pheromone release: Discovering the manifold

. 2021 Dec ; 15 (12) : e0009733. [epub] 20211221

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34932549

Grantová podpora
Wellcome Trust - United Kingdom

The males of many species of New World Phlebotomines produce volatile terpenoid chemicals, shown in Lutzomyia longipalpis s.l. to be sex/aggregation pheromones. Pheromone is produced by secretory cells which surround a cuticular reservoir which collects the pheromone and passes it through a cuticular duct to the surface of the insect. The pheromone then passes through specialised cuticular structures on the abdominal surface prior to evaporation. The shape and distribution of the specialised structures are highly diverse and differ according to species. In this study we used SEM to examine the interior cuticular pheromone collection and transport structures of 3 members of the Lu. longipalpis s.l. species complex and Migonemyia migonei. We found a new structure which we have called the manifold which appears to be a substantial extension of the interior tergal cuticle connected in-line with the cuticular duct and reservoir. The manifold of the Campo Grande member of the complex is longer and wider than the Jacobina member whereas the manifold of the Sobral member was shorter than both other members of the complex. Overall, the secretory apparatus of the Sobral member was smaller than the other two. The manifold of M. migonei was very different to those found in Lu. longipalpis s.l. and was positioned in a pit-like structure within the tergal cuticle. The secretory reservoir was connected by a short duct to the manifold. Differences in the size and shape of the manifold may be related to the chemical structure of the pheromone and may have taxonomic value. Examination of the interior cuticle by SEM may help to locate the secretory apparatus of vector species where pheromonal activity has been inferred from behavioural studies but the external secretory structures or pheromones have not yet been found.

Zobrazit více v PubMed

Deane MP, Deane LdM. Infecção experimental do Phlebotomus longipalpis em raposa (Lycalopex vetulus) naturalmente parasitada pela Leishmania donovani. Hospital. 1954;46:651–3. PubMed

Deane LM. Leishmaniose visceral no Brasil: estudos sobre reservatórios e transmissores realizados no estado do Ceará. Rio de Janeiro; Serviço Nacional de Educação Sanitária. 1956:162.

Lainson R, Rangel EF. Lutzomyia longipalpis and the eco-epidemiology of American visceral leishmaniasis, with particular reference to Brazil: a review. Mem Inst Oswaldo Cruz. 2005;100(8):17. doi: 10.1590/s0074-02762005000800001 PubMed DOI

Rangel EF, Vilela ML. Lutzomyia longipalpis (Diptera, Psychodidae, Phlebotominae) and urbanization of visceral leishmaniasis in Brazil. Cad Saude Publica. 2008;24(12):2948–52. Epub 2008/12/17. doi: 10.1590/s0102-311x2008001200025 . PubMed DOI

Casanova C, Colla-Jacques FE, Hamilton JG, Brazil RP, Shaw JJ. Distribution of Lutzomyia longipalpis chemotype populations in Sao Paulo state, Brazil. PLoS neglected tropical diseases. 2015;9(3):e0003620. Epub 2015/03/18. doi: 10.1371/journal.pntd.0003620 ; PubMed Central PMCID: PMC4363371. PubMed DOI PMC

de Carvalho MR, Valença HF, da Silva FJ, de Pita-Pereira D, de Araújo Pereira T, Britto C, et al.. Natural Leishmania infantum infection in Migonemyia migonei (França, 1920) (Diptera:Psychodidae:Phlebotominae) the putative vector of visceral leishmaniasis in Pernambuco State, Brazil. Acta Tropica. 2010;116(1):108–10. doi: 10.1016/j.actatropica.2010.03.009 PubMed DOI

Rangel EF, Lainson R. Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence. Mem Inst Oswaldo Cruz. 2009;104:937–54. doi: 10.1590/s0074-02762009000700001 PubMed DOI

Guimarães VCFV, Pruzinova K, Sadlova J, Volfova V, Myskova J, Filho SPB, et al.. Lutzomyia migonei is a permissive vector competent for Leishmania infantum. Parasit Vectors. 2016;9(1):159. doi: 10.1186/s13071-016-1444-2 PubMed DOI PMC

de Queiroz RG, Vasconcelos Ide A, Vasconcelos AW, Pessoa FA, de Sousa RN, David JR. Cutaneous leishmaniasis in Ceara state in northeastern Brazil: incrimination of Lutzomyia whitmani (Diptera: Psychodidae) as a vector of Leishmania braziliensis in Baturite municipality. Am J Trop Med Hyg. 1994;50(6):693–8. Epub 1994/06/01. doi: 10.4269/ajtmh.1994.50.693 . PubMed DOI

de Pita-Pereira D, Alves CR, Souza MB, Brazil RP, Bertho AL, de Figueiredo Barbosa A, et al.. Identification of naturally infected Lutzomyia intermedia and Lutzomyia migonei with Leishmania (Viannia) braziliensis in Rio de Janeiro (Brazil) revealed by a PCR multiplex non-isotopic hybridisation assay. Trans R Soc Trop Med Hyg. 2005;99(12):905–13. Epub 2005/09/07. doi: 10.1016/j.trstmh.2005.06.019 . PubMed DOI

Morton IE, Ward RD. Laboratory response of female Lutzomyia longipalpis sandflies to a host and male pheromone source over distance. Med Vet Entomol. 1989;3:4. doi: 10.1111/j.1365-2915.1989.tb00218.x PubMed DOI

Nigam Y, Ward RD. The effect of male sandfly pheromone and host factors as attractants for female Lutzomyia longipalpis (Diptera: Psychodidae). Physiol Entomol. 1991;16(3):305–12. doi: 10.1111/j.1365-3032.1991.tb00569.x DOI

Ward RD, Hamilton JG, Dougherty M, Falcao AL. Pheromones in Old and New World sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol. 1991;85(6):667–8. Epub 1991/12/01. doi: 10.1080/00034983.1991.11812624 . PubMed DOI

Jones TM, Hamilton JGC. A role for pheromones in mate choice in a lekking sandfly. Anim Behav. 1998;56(4):891–8. Epub 1998/12/16. doi: 10.1006/anbe.1998.0857 . PubMed DOI

Morrison AC, Ferro C, Pardo R, Torres M, Wilson ML, Tesh RB. Nocturnal activity patterns of Lutzomyia longipalpis (Diptera, Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. J Med Entomol. 1995;32(5):605–17. doi: 10.1093/jmedent/32.5.605 WOS:A1995RT60800007. PubMed DOI

Spiegel CN, Dias DB, Araki AS, Hamilton JG, Brazil RP, Jones TM. The Lutzomyia longipalpis complex: a brief natural history of aggregation-sex pheromone communication. Parasit Vectors. 2016;9(1):580. Epub 2016/11/16. doi: 10.1186/s13071-016-1866-x ; PubMed Central PMCID: PMC5109651. PubMed DOI PMC

Kelly DW, Dye C. Pheromones, kairomones and the aggregation dynamics of the sandfly Lutzomyia longipalpis. Anim Behav. 1997;53:721–31. doi: 10.1006/anbe.1996.0309 WOS:A1997WW45300005. DOI

Bray DP, Hamilton JGC. Host odor synergizes attraction of virgin female Lutzomyia longipalpis (Diptera: Psychodidae). J Med Entomol. 2007;44(5):779–87. doi: 10.1603/0022-2585(2007)44[779:hosaov]2.0.co;2 PubMed DOI

Ward RD, Hamilton JGC, Dougherty M, Falcao AL, Feliciangeli MD, Perez JE, et al.. Pheromone disseminating structures in tergites of male phlebotomines (Diptera: Psychodidae). Bull Entomol Res. 1993;83(3):437–45. Epub 2009/07/10. doi: 10.1017/S0007485300029357 DOI

Bray DP, Bandi KK, Brazil RP, Oliveira AG, Hamilton JG. Synthetic sex pheromone attracts the leishmaniasis vector Lutzomyia longipalpis (Diptera: Psychodidae) to traps in the field. J Med Entomol. 2009;46(3):428–34. Epub 2009/06/06. doi: 10.1603/033.046.0303 ; PubMed Central PMCID: PMC3197723. PubMed DOI PMC

Bray DP, Carter V, Alves GB, Brazil RP, Bandi KK, Hamilton JG. Synthetic sex pheromone in a long-lasting lure attracts the visceral leishmaniasis vector, Lutzomyia longipalpis, for up to 12 weeks in Brazil. PLoS neglected tropical diseases. 2014;8(3):e2723. Epub 2014/03/22. doi: 10.1371/journal.pntd.0002723 ; PubMed Central PMCID: PMC3961206. PubMed DOI PMC

Courtenay O, Dilger E, Calvo-Bado LA, Kravar-Garde L, Carter V, Bell MJ, et al.. Sand fly synthetic sex-aggregation pheromone co-located with insecticide reduces the incidence of infection in the canine reservoir of visceral leishmaniasis: A stratified cluster randomised trial. PLoS neglected tropical diseases. 2019;13(10):e0007767. doi: 10.1371/journal.pntd.0007767 PubMed DOI PMC

Foster SP, Dugdale JS. A comparison of morphological and sex pheromone differences in some New Zealand Tortricinae moths. Biochem Syst Ecol. 1988;16(2):227–32. 10.1016/0305-1978(88)90102-0. DOI

Hamilton JG, Maingon RD, Alexander B, Ward RD, Brazil RP. Analysis of the sex pheromone extract of individual male Lutzomyia longipalpis sandflies from six regions in Brazil. Med Vet Entomol. 2005;19(4):480–8. Epub 2005/12/13. doi: 10.1111/j.1365-2915.2005.00594.x . PubMed DOI

Souza NA, Brazil RP, Araki AS. The current status of the Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae) species complex. Mem Inst Oswaldo Cruz. 2017;112(3):161–74. Epub 2017/02/23. doi: 10.1590/0074-02760160463 ; PubMed Central PMCID: PMC5319373. PubMed DOI PMC

Vigoder FM, Araki AS, Carvalho AB, Brazil RP, Ritchie MG. Dinner and a show: The role of male copulatory courtship song and female blood-feeding in the reproductive success of Lutzomyia longipalpis from Lapinha, Brazil. Infect Genet Evol. 2020;85:104470. doi: 10.1016/j.meegid.2020.104470 PubMed DOI

Boufana B. The tergal pheromone gland and antennal sensilla of the sandfly Lutzomyia longipalpis [PhD]: University of Liverpool; 1990.

Lane RP, Ward RD. The morphology and possible function of abdominal patches in males of two forms of the leishmaniasis vector Lutzomyia longipalpis (Diptera: Phlebotominae). Cahiers ORSTOM Serie Entomologie Medicale et Parasitologie. 1984;22:5.

Spiegel CN, Brazil RP, Soares MJ. Ultrastructure of male sex pheromone glands in abdominal tergites of five Lutzomyia sandfly species (Diptera: Psychodidae). Arthropod Struct Dev. 2002;30(3):219–27. doi: 10.1016/s1467-8039(01)00033-0 PubMed DOI

Hamilton JG, Brazil RP, Maingon R. A fourth chemotype of Lutzomyia longipalpis (Diptera: Psychodidae) from Jaibas, Minas Gerais State, Brazil. J Med Entomol. 2004;41(6):1021–6. Epub 2004/12/21. doi: 10.1603/0022-2585-41.6.1021 . PubMed DOI

Palframan MJ, Bandi KK, Hamilton JGC, Pattenden G. Sobralene, a new sex-aggregation pheromone and likely shunt metabolite of the taxadiene synthase cascade, produced by a member of the sand fly Lutzomyia longipalpis species complex. Tetrahedron Lett. 2018;59(20):1921–3. Epub 2018/05/22. doi: 10.1016/j.tetlet.2018.03.088 ; PubMed Central PMCID: PMC5937913. PubMed DOI PMC

Hickner PV, Timoshevskaya N, Nowling RJ, Labbé F, Nguyen AD, McDowell MA, et al.. Molecular signatures of sexual communication in the phlebotomine sand flies. PLoS neglected tropical diseases. 2021;14(12):e0008967. doi: 10.1371/journal.pntd.0008967 PubMed DOI PMC

Serrano AK, Rojas JC, Cruz-López LC, Malo EA, Mikery OF, Castillo A. Presence of Putative Male-Produced Sex Pheromone in Lutzomyia cruciata (Diptera: Psychodidae), Vector of Leishmania mexicana. J Med Entomol. 2016;53(6):1261–7. doi: 10.1093/jme/tjw118 PubMed DOI

Hamilton JGC, Brazil RP, Morgan ED, Alexander B. Chemical analysis of oxygenated homosesquiterpenes: a putative sex pheromone from Lutzomyia lichyi (Diptera: Psychodidae). Bull Entomol Res. 1999;89(2):139–45. Epub 2007/03/09. doi: 10.1017/S000748539900022X DOI

Hamilton JG, Brazil RP, Campbell-Lendrum D, Davies CR, Kelly DW, Pessoa FA, et al.. Distribution of putative male sex pheromones among Lutzomyia sandflies (Diptera: Psychodidae). Ann Trop Med Parasitol. 2002;96(1):83–92. Epub 2002/05/07. doi: 10.1179/000349802125000547 . PubMed DOI

Ward RD, Morton IE, Lancaster V, Smith P, Swift A. Bioassays as an indicator of pheromone communication in Lutzomyia longipalpis (Diptera: Psychodidae). New York: Plenum Press; 1989. 1 p.

Costa PL. Aspectos biológicos, morfológicos e genéticos de diferentes populações de Lutzomyia migonei (França, 1920) do Brasil. [PhD]. Recife: Fundação Oswaldo Cruz; 2016.

Noirot C, Quennedey A. Fine Structure of Insect Epidermal Glands. Ann Rev Entomol. 1974;19(1):61–80. doi: 10.1146/annurev.en.19.010174.000425 DOI

Mangabeira Filho O. Sobre a sistemática e biologia dos Phlebotomus do Ceará. Rev Bras Malariol. 1969;21:1–25. PubMed

Volf P, Volfova V. Establishment and maintenance of sand fly colonies. J Vect Ecol. 2011;36(s1):S1–S9. doi: 10.1111/j.1948-7134.2011.00106.x PubMed DOI

Clarke JFG. The preparation of slides of the genitalia of Lepidoptera. Bull Brooklyn Entomol Soc. 1941;36:149–61.

Lane RP, de Souza Bernardes D. Histology and ultrastructure of pheromone secreting glands in males of the phlebotomine sandfly Lutzomyia longipalpis. Ann Trop Med Parasitol. 1990;84(1):53–61. Epub 1990/02/01. doi: 10.1080/00034983.1990.11812433 . PubMed DOI

Spiegel CN, Batista-Pereira LG, Bretas JAC, Eiras AE, Hooper AM, Peixoto AA, et al.. Pheromone Gland Development and Pheromone Production in Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). J Med Entomol. 2011;48(3):489–95. doi: 10.1603/me10133 PubMed DOI

Noirot C, Quennedey A. Glands, gland cells, glandular units: some comments on terminology and classification. Ann Soc Entomol Fr. 1991;27:6.

Percy JE. Development and ultrastructure of cells of the sex pheromone gland in the white-marked tussock moth, Orgyia leucostigma (J. E. Smith) (Lepidoptera: Lymantriidae). Int J Insect Morphol Embryol. 1975;4(6):567–79. 10.1016/0020-7322(75)90032-X. DOI

Percy J. Development and ultrastructure of sex-pheromone gland cells in females of the cabbage looper moth, Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae). Can J Zool. 1979;57(1):16. doi: 10.1139/z79-021 DOI

Lensky Y, Cassier P, Finkel A, Delorme-Joulie C, Levinsohn M. The fine structure of the tarsal glands of the honeybee Apis mellifera L. (Hymenoptera). Cell Tissue Res. 1985;240(1):153–8. doi: 10.1007/BF00217569 DOI

Nardi JB, Dowd PF, Bartelt RJ. Fine structure of cells specialized for secretion of aggregation pheromone in a nitidulid beetle Carpophilus freemani (coleoptera: Nitidulidae). Tissue Cell. 1996;28(1):43–52. Epub 1996/02/01. doi: 10.1016/s0040-8166(96)80043-7 . PubMed DOI

Pierre D, Biémont J-C, Pouzat J, Lextrait P, Thibeaudeau C. Location and ultrastructure of sex pheromone glands in female Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae). Int J Insect Morphol Embryol. 1996;25(4):391–404. 10.1016/S0020-7322(96)00014-1. DOI

Raina AK, Wergin WP, Murphy CA, Erbe EF. Structural organization of the sex pheromone gland in Helicoverpa zea in relation to pheromone production and release. Arthropod Struct Dev. 2000;29(4):343–53. Epub 2007/12/20. . PubMed

Melnitsky SI, Deev RV. The fine structure of sternal pheromone glands in the two caddisfly species from the Rhyacophilidae and Limnephilidae families (Insecta: Trichoptera). Russ Entomol J. 2009;18:10.

Sreng L. Cockroach tergal glands producing female sex attractant pheromones and male aphrodisiacs in particular in the subfamily Blaberinae (Blattaria: Blaberidae). Eur J Entomol. 2006;103:817–29. doi: 10.14411/eje.2006.112 DOI

Kellner RLL, Dettner K. Comparative morphology of abdominal glands in Paederinae (Coleoptera: Staphylinidae). Int J Insect Morphol Embryol. 1992;21(2):117–35. 10.1016/0020-7322(92)90011-B. DOI

Gonzalez MA, Bandi KK, Bell MJ, Brazil RP, Dilger E, Guerrero A, et al.. A temporal comparison of sex-aggregation pheromone gland content and dynamics of release in three members of the Lutzomyia longipalpis (Diptera: Psychodidae) species complex. PLoS neglected tropical diseases. 2017;11(12):e0006071. Epub 2017/12/02. doi: 10.1371/journal.pntd.0006071 ; PubMed Central PMCID: PMC5745125. PubMed DOI PMC

Hoshino K, Nakaba S, Inoue H, Iwabuchi K. Structure and development of male pheromone gland of longicorn beetles and its phylogenetic relationships within the tribe Clytini. J Exp Zool B Mol Dev Evol. 2015;324(1):68–76. Epub 2014/12/17. doi: 10.1002/jez.b.22606 . PubMed DOI

Agus HH. Chapter 4—Terpene toxicity and oxidative stress. In: Patel VB, Preedy VR, editors. Toxicology: Academic Press; 2021. p. 33–42.

Jarvis EK, Rutledge LC. Laboratory observations on mating and leklike aggregations in Lutzomyia longipalpis (Diptera: Psychodidae). J Med Entomol. 1992;29(2):171–7. Epub 1992/03/01. doi: 10.1093/jmedent/29.2.171 . PubMed DOI

Soares RPP, Turco SJ. Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae): a review. An Acad Bras Cienc. 2003;75:301–30. doi: 10.1590/s0001-37652003000300005 PubMed DOI

Terry LI, Dyreson E. Behavior of Frankliniella occidentalis (Thysanoptera: Thripidae) within Aggregations, and Morphometric Correlates of Fighting. Ann Entomol Soc Am. 1996;89(4):589–602. doi: 10.1093/aesa/89.4.589 DOI

Hamilton JG, Hall DR, Kirk WD. Identification of a male-produced aggregation pheromone in the western flower thrips Frankliniella occidentalis. J Chem Ecol. 2005;31(6):1369–79. Epub 2005/10/14. doi: 10.1007/s10886-005-1351-z . PubMed DOI

Enriquez JJS, Sena G, Cataldi M, Silveira LHMd, Braz D, Barroso RC, et al.. The Methodology to produce Rhodnius prolixus head structures made by 3D printing using Synchrotron Radiation Microtomography. J Instrum. 2021;16(2):P02014–P. doi: 10.1088/1748-0221/16/02/p02014 DOI

Chelbi I, Zhioua E, Hamilton JG. Behavioral evidence for the presence of a sex pheromone in male Phlebotomus papatasi scopoli (Diptera: Psychodidae). J Med Entomol. 2011;48(3):518–25. Epub 2011/06/15. doi: 10.1603/me10132 . PubMed DOI

Kumar V, Krishnakumari B, Kesari S, Kumari K, Kumar R, Ranjan A, et al.. Preliminary Observations on the Female Behavior of the Indian Sandfly Vector, Phlebotomus argentipes (Diptera: Psychodidae). Ann Entomol Soc Am. 2012;105(2):201–5. doi: 10.1603/an11089 DOI

Yaman K. Semiochemical mediated oviposition and mating in Phlebotomus argentipes (Diptera: Psychodidae) sand flies: Keele University; 2016.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...