Descriptive and Geometric Morphometry of the Wings of Phlebotomus sergenti Populations in Central Morocco
Abstract
Background: Phlebotomus sergenti, the proven vector of Leishmania tropica, the causative agent of anthroponotic cutaneous leishmaniasis, is widely distributed in Morocco. Previous works using molecular markers (Internal Transcribed Spacer 2 rDNA and Cytochrome B mtDNA) hypothesized the existence of multiple closely related populations of sand fly species (cryptic species) that would exhibit distinct vectorial capacities. This work studies morphotypic diversity using traditional and geometric morphometry analyses carried out on Ph. sergenti's wings from central Morocco, where active L. tropica transmission occurs for 30 years.
Methods: Descriptive characteristics (size and shape) of the right wings were measured in Ph. sergenti’s specimens collected from fourteen stations in central Morocco. Both traditional and geometric morphometry methods were used to analyse geographic variations in Ph. sergenti wing’s size and shape.
Results: These analyses support the existence of distinct Ph. sergenti populations, enlightening significant phenotypic variations of Ph. sergenti’s wings, regarding their size and shape, depending on geographic origin. In addition, traditional and geometric morphometric analyses of the wing’s length, centroid size, β, ɵ, and γ distances allowed clear discrimination of Ph. sergenti sub-populations.
Conclusion: These data pinpoint the adaptative ability of Ph. sergenti to local environmental conditions. Additional studies are now required to further shed light on the genetic structure of Ph. sergenti populations in Morocco.
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2. Depaquit J, Grandadam M, Fouque F, An-dry PE, Peyrefitte C (2010) Arthro¬pod-borne viruses transmitted by phlebotom-ine sandflies in Europe: a re¬view. Euro Surveill. 15(10): 19507.
3. Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D (2016) A historical overview of the clas-sification, evolution, and dispersion of Leishmania parasites and Sandflies. PLOS Negl Trop Dis. 10: 1–40.
4. Faraj C, Himmi O (2019) Liste actualisée des Phlebotominae (Diptera: Psychodi-dae) du Maroc. Bull Soc Pathol Exot. 112: 296–301.
5. Galati EAB, Galvis-Ovallos F, Lawyer P, Léger N, Depaquit J (2017) An illustrat-ed guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psychodidae). Parasite. 24: 1–35.
6. Florin DA, Davies SJ, Olsen C, Lawyer P, Lipnick R, Schultz G, Rowton E, Wilker¬son R, Keep L (2011) Morpho-metric and molecular analyses of the sand fly species Lutzomyia shannoni (Diptera: Psychodidae: Phlebotominae) collected from seven different geograph-ical areas in the southeastern United States. J Med Entomol. 48: 154–166.
7. Al-Zahrani MA, Peters W, Evans DA, Chin C, Smith V, Lane RP (1988) Phleboto-mus sergenti a vector of Leish¬mania tropica in Saudi Arabia. Trans R Soc Trop Med Hyg. 82: 416.
8. Guilvard E, Rioux JA, Gallego M, Pratlong F, Mahjour J, Martinez-Ortega E, De-reure J, Saddiki A, Martini A (1991) Leishmania tropica au Maroc III-Rôle de Phlebotomus sergenti. A propos de 89 isolats. Ann Parasitol Hum Comp. 66: 96–99.
9. Oshaghi MA, Rasolian M, Shirzadi MR, Mohtarami F, Doosti S (2010) First re-port on isolation of Leishmania tropica from sandflies of a classical urban Cuta-neous leishmaniasis focus in southern Iran. Exp Parasitol. 126(4): 445–450.
10. Depaquit J, Ferté H, Léger N (2000) Ré-vision du sous-genre Paraphlebotomus (Phlebotomus-Phlebotominae-Psychodi-dae-Diptera). Approches morphologique et moléculaire. Ann Pharm Fr. 58: 333–340.
11. Depaquit J, Ferté H, Léger N, Lefranc F, Alves-Pires C, Hanafi H, Maroli M, Mo-rillas-Marques F, Rioux JA, Svobodova M, Volf P (2002) ITS2 sequences hete-rogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodi-dae): possible consequences in their abi-lity to transmit Leishmania tropica. Int J Parasitol. 32: 1123–1131.
12. Yahia H, Ready PD, Hamdani A, Testa JM, Guessous-Idrissi N (2004) Regional genetic differentiation of Phlebotomus sergenti in three Moroccan foci of cuta-neous leishmaniasis caused by Leishma-nia tropica. Parasite. 11: 189–199.
13. Barón S, Martín-Sánchez J, Gállego M, Morales-Yuste M, Boussaa S, Morillas-Márquez F (2008) Intraspecific variabil-ity (rDNA ITS and mtDNA Cyt b) of Phlebotomus sergenti in Spain and Mo-rocco. Acta Trop. 107: 259–267.
14. Moin-Vaziri V, Depaquit J, Yaghoobi-Er-shadi MR, Oshaghi MA, De-rakhshandeh-Peykar P, Ferté H, Kalten-bach M, Bargues MD, Léger N, Nadim A (2007) Intraspecific variation within Phlebotomus sergenti Parrot (1917) (Diptera: Psy¬chodidae) based on mtDNA sequences in Islamic Republic of Iran. Acta Trop. 102(1): 29–37.
15. Moin-Vaziri V, Oshaghi MA, Yaghoobi-Er¬shadi MR, Derakhshandeh-Peykar P, Abai MR, Mohtarami F, Zahraei-Rameza¬ni AR, Nadim A (2016) ITS2-rDNA Sequence Variation of Phlebotomus sergenti s.l. (Dip: Psy-chodidae) Populations in Iran. J Arthro-pod Borne Dis. 10(4): 462–473.
16. Rioux JA, Rispail P, Lanotte G, Lepart J (1984) Relations Phlébotomes-biocli¬mats en écologie des leishma¬nioses. Corol-laires épidémiologiques. L’exemple du Maroc. Bull Soc Pathol Exot. 31: 549–557.
17. Guernaoui S, Boumezzough A (2009) Hab¬i¬tat preferences of phlebotomine sandflies (Diptera: Psychodidae) in Southwest¬ern Mo¬rocco. J Med Entomol. 46: 1187–1194.
18. Guernaoui S, Boumezzough A, Pesson B, Pichon G (2005) Entomological investi-gations in Chichaoua: An emerging epi-demic focus of cutaneous leishmaniasis in Morocco. J Med Entomol. 42: 697–670.
19. Dujardin JP (2008) Morphometrics ap¬plied to medical entomology. In¬fect Genet Evol. 8: 875–890.
20. Lane R, Ready P (1985) Multivariate dis-crimination between Lutzomyia well-comei, a vector of mucocutaneous leishmaniasis, and Lu. complexus (Dip-tera: Psycho¬di¬dae). Ann Trop Med Para-sitol. 79: 469–472.
21. Prudhomme J, Gunay F, Rahola N, Ouanai¬mi F, Guernaoui S, Boumez-zough A, Bañuls AL, Sereno D, Alten B (2012) Wing size and shape variation of Phleboto¬mus papatasi (Diptera: Psy-chodidae) pop¬ulations from the south and north slopes of the Atlas Mountains in Morocco. J Vector Ecol. 37: 137–147.
22. Oguz G, Kasap OE, Alten B (2017) Wing morphology variations in a natural pop-ulation of Phlebotomus tobbi Adler and Theodor 1930. J Vector Ecol. 42: 223–232.
23. Prudhomme J, Cassan C, Hide M, Toty C, Rahola N, Vergnes B, Dujardin JP, Al-ten B, Sereno D, Bañuls AL (2016) Ecol¬ogy and morphological variations in wings of Phlebotomus ariasi (Diptera: Psycho¬didae) in the region of Roquedur (Gard, France): a geometric morphomet-rics approach. Parasit Vectors. 9: 578.
24. Dvorak V, Aytekin AM, Alten B, Skarupova S, Votypka J, Volf P. (2006) A comparison of the intraspecific varia-bility of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae). J Vector Ecol. 31(2): 229–238.
25. Aytekin AM, Alten B, Caglar SS, Ozbel Y, Kaynas S, Simsek FM, Kasap OE, Belen A (2007) Phenotypic variation among local populations of phlebotom-ine sand flies (Diptera: Psychodidae) in southern Turkey. J Vector Ecol. 32(2): 226–234.
26. Abou-Elaaz FZ, Outourakht A, Bouhout S, Himmi O, Guernaoui S (2019) Thirty years of cutaneous leishmaniasis in Tad-la-Azilal focus, Morocco. Parasite Epi-demiol Control. 4: e00091.
27. Marty P, Le Fichoux Y, Pratlong F, Ri¬oux JA, Rostain G, Lacour JP (1989) Cuta-neous leishmaniasis due to Leish¬mania tropica in a young Moroccan child ob-served in Nice, France. Trans R Soc Trop Med Hyg. 83: 510.
28. Haut-Commissariat au Plan (2017) Mo-nographie régionale Béni Mellal-Khé-nifra. Direction régionale Béni Mel¬lal-Khénifra, Morocco.
29. Ministry of Public Health Morocco (1997) Lutte contre les leishmanioses. Direction de l’épidémiologie et de lutte contre les maladies, Rabat, Morocco.
30. Belen A, Alten B, Aytekin AM (2004) Al-titudinal variation in morphometric and molecular characteristics of Phlebotomus papatasi populations. J Med Entomol. 18: 431–460.
31. Jenoptik Optical Systems GmbH (2020) User Manual for JENOPTIK GRYPHAX ® software. Goeschwitzer Strasse 25 07745 Jena, Germany, p. 198.
32. Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the optimal super-imposition of landmarks. Syst Zo¬ol. 39: 40–59.
33. Klingenberg CP (2011) MorphoJ: an in-tegrated software package for geometric morphometrics. Mol Ecol Resour. 11: 353–357.
34. Stat Soft France (2005) STATISTICA (Logiciel d’analyse des données), ver-sion 7.1. Available at: www. Statsoft. Fr.
35. Ward Jr JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 58: 236–244.
36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics soft-ware package for education and data analysis. Palaeontol Electron. 4: 1–9.
37. Gower JC (1975) Generalized Procrustes Analysis. Psychometrika. 40: 33–51.
38. Jacobson LR (2003) Leishmania tropica (Kinetoplastida: Trypanosomatidae) – a perplexing parasite. Folia Parasitol. 50: 241–250.
39. Dvorak V, Aytekin AM, Alten B, Skarupova S, Votypka J, Volf P (2006) A comparison of the intraspecific varia-bility of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae). J Vector Ecol. 31: 229–238.
40. Guernaoui S, Hamarsheh O, Garcia, D, Fontenille D, Sereno D (2020) Popula-tion Genetics of Phlebotomus papatasi from Endemic and Nonendemic Areas for Zoonotic Cutaneous Leishmaniasis in Morocco, as Revealed by Cyto¬chrome Oxidase Gene Subunit I Se¬quencing. Mi¬croorganisms. 8(7): 1010.
41. Guernaoui S, Boumezzough A, Laamrani A (2006) Altitudinal structuring of phlebotomine sandflies (Diptera: Psy-chodidae) in the High-Atlas Mountains, Morocco. Acta Trop. 97: 346–351.
2. Depaquit J, Grandadam M, Fouque F, An-dry PE, Peyrefitte C (2010) Arthro¬pod-borne viruses transmitted by phlebotom-ine sandflies in Europe: a re¬view. Euro Surveill. 15(10): 19507.
3. Akhoundi M, Kuhls K, Cannet A, Votýpka J, Marty P, Delaunay P, Sereno D (2016) A historical overview of the clas-sification, evolution, and dispersion of Leishmania parasites and Sandflies. PLOS Negl Trop Dis. 10: 1–40.
4. Faraj C, Himmi O (2019) Liste actualisée des Phlebotominae (Diptera: Psychodi-dae) du Maroc. Bull Soc Pathol Exot. 112: 296–301.
5. Galati EAB, Galvis-Ovallos F, Lawyer P, Léger N, Depaquit J (2017) An illustrat-ed guide for characters and terminology used in descriptions of Phlebotominae (Diptera, Psychodidae). Parasite. 24: 1–35.
6. Florin DA, Davies SJ, Olsen C, Lawyer P, Lipnick R, Schultz G, Rowton E, Wilker¬son R, Keep L (2011) Morpho-metric and molecular analyses of the sand fly species Lutzomyia shannoni (Diptera: Psychodidae: Phlebotominae) collected from seven different geograph-ical areas in the southeastern United States. J Med Entomol. 48: 154–166.
7. Al-Zahrani MA, Peters W, Evans DA, Chin C, Smith V, Lane RP (1988) Phleboto-mus sergenti a vector of Leish¬mania tropica in Saudi Arabia. Trans R Soc Trop Med Hyg. 82: 416.
8. Guilvard E, Rioux JA, Gallego M, Pratlong F, Mahjour J, Martinez-Ortega E, De-reure J, Saddiki A, Martini A (1991) Leishmania tropica au Maroc III-Rôle de Phlebotomus sergenti. A propos de 89 isolats. Ann Parasitol Hum Comp. 66: 96–99.
9. Oshaghi MA, Rasolian M, Shirzadi MR, Mohtarami F, Doosti S (2010) First re-port on isolation of Leishmania tropica from sandflies of a classical urban Cuta-neous leishmaniasis focus in southern Iran. Exp Parasitol. 126(4): 445–450.
10. Depaquit J, Ferté H, Léger N (2000) Ré-vision du sous-genre Paraphlebotomus (Phlebotomus-Phlebotominae-Psychodi-dae-Diptera). Approches morphologique et moléculaire. Ann Pharm Fr. 58: 333–340.
11. Depaquit J, Ferté H, Léger N, Lefranc F, Alves-Pires C, Hanafi H, Maroli M, Mo-rillas-Marques F, Rioux JA, Svobodova M, Volf P (2002) ITS2 sequences hete-rogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodi-dae): possible consequences in their abi-lity to transmit Leishmania tropica. Int J Parasitol. 32: 1123–1131.
12. Yahia H, Ready PD, Hamdani A, Testa JM, Guessous-Idrissi N (2004) Regional genetic differentiation of Phlebotomus sergenti in three Moroccan foci of cuta-neous leishmaniasis caused by Leishma-nia tropica. Parasite. 11: 189–199.
13. Barón S, Martín-Sánchez J, Gállego M, Morales-Yuste M, Boussaa S, Morillas-Márquez F (2008) Intraspecific variabil-ity (rDNA ITS and mtDNA Cyt b) of Phlebotomus sergenti in Spain and Mo-rocco. Acta Trop. 107: 259–267.
14. Moin-Vaziri V, Depaquit J, Yaghoobi-Er-shadi MR, Oshaghi MA, De-rakhshandeh-Peykar P, Ferté H, Kalten-bach M, Bargues MD, Léger N, Nadim A (2007) Intraspecific variation within Phlebotomus sergenti Parrot (1917) (Diptera: Psy¬chodidae) based on mtDNA sequences in Islamic Republic of Iran. Acta Trop. 102(1): 29–37.
15. Moin-Vaziri V, Oshaghi MA, Yaghoobi-Er¬shadi MR, Derakhshandeh-Peykar P, Abai MR, Mohtarami F, Zahraei-Rameza¬ni AR, Nadim A (2016) ITS2-rDNA Sequence Variation of Phlebotomus sergenti s.l. (Dip: Psy-chodidae) Populations in Iran. J Arthro-pod Borne Dis. 10(4): 462–473.
16. Rioux JA, Rispail P, Lanotte G, Lepart J (1984) Relations Phlébotomes-biocli¬mats en écologie des leishma¬nioses. Corol-laires épidémiologiques. L’exemple du Maroc. Bull Soc Pathol Exot. 31: 549–557.
17. Guernaoui S, Boumezzough A (2009) Hab¬i¬tat preferences of phlebotomine sandflies (Diptera: Psychodidae) in Southwest¬ern Mo¬rocco. J Med Entomol. 46: 1187–1194.
18. Guernaoui S, Boumezzough A, Pesson B, Pichon G (2005) Entomological investi-gations in Chichaoua: An emerging epi-demic focus of cutaneous leishmaniasis in Morocco. J Med Entomol. 42: 697–670.
19. Dujardin JP (2008) Morphometrics ap¬plied to medical entomology. In¬fect Genet Evol. 8: 875–890.
20. Lane R, Ready P (1985) Multivariate dis-crimination between Lutzomyia well-comei, a vector of mucocutaneous leishmaniasis, and Lu. complexus (Dip-tera: Psycho¬di¬dae). Ann Trop Med Para-sitol. 79: 469–472.
21. Prudhomme J, Gunay F, Rahola N, Ouanai¬mi F, Guernaoui S, Boumez-zough A, Bañuls AL, Sereno D, Alten B (2012) Wing size and shape variation of Phleboto¬mus papatasi (Diptera: Psy-chodidae) pop¬ulations from the south and north slopes of the Atlas Mountains in Morocco. J Vector Ecol. 37: 137–147.
22. Oguz G, Kasap OE, Alten B (2017) Wing morphology variations in a natural pop-ulation of Phlebotomus tobbi Adler and Theodor 1930. J Vector Ecol. 42: 223–232.
23. Prudhomme J, Cassan C, Hide M, Toty C, Rahola N, Vergnes B, Dujardin JP, Al-ten B, Sereno D, Bañuls AL (2016) Ecol¬ogy and morphological variations in wings of Phlebotomus ariasi (Diptera: Psycho¬didae) in the region of Roquedur (Gard, France): a geometric morphomet-rics approach. Parasit Vectors. 9: 578.
24. Dvorak V, Aytekin AM, Alten B, Skarupova S, Votypka J, Volf P. (2006) A comparison of the intraspecific varia-bility of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae). J Vector Ecol. 31(2): 229–238.
25. Aytekin AM, Alten B, Caglar SS, Ozbel Y, Kaynas S, Simsek FM, Kasap OE, Belen A (2007) Phenotypic variation among local populations of phlebotom-ine sand flies (Diptera: Psychodidae) in southern Turkey. J Vector Ecol. 32(2): 226–234.
26. Abou-Elaaz FZ, Outourakht A, Bouhout S, Himmi O, Guernaoui S (2019) Thirty years of cutaneous leishmaniasis in Tad-la-Azilal focus, Morocco. Parasite Epi-demiol Control. 4: e00091.
27. Marty P, Le Fichoux Y, Pratlong F, Ri¬oux JA, Rostain G, Lacour JP (1989) Cuta-neous leishmaniasis due to Leish¬mania tropica in a young Moroccan child ob-served in Nice, France. Trans R Soc Trop Med Hyg. 83: 510.
28. Haut-Commissariat au Plan (2017) Mo-nographie régionale Béni Mellal-Khé-nifra. Direction régionale Béni Mel¬lal-Khénifra, Morocco.
29. Ministry of Public Health Morocco (1997) Lutte contre les leishmanioses. Direction de l’épidémiologie et de lutte contre les maladies, Rabat, Morocco.
30. Belen A, Alten B, Aytekin AM (2004) Al-titudinal variation in morphometric and molecular characteristics of Phlebotomus papatasi populations. J Med Entomol. 18: 431–460.
31. Jenoptik Optical Systems GmbH (2020) User Manual for JENOPTIK GRYPHAX ® software. Goeschwitzer Strasse 25 07745 Jena, Germany, p. 198.
32. Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for the optimal super-imposition of landmarks. Syst Zo¬ol. 39: 40–59.
33. Klingenberg CP (2011) MorphoJ: an in-tegrated software package for geometric morphometrics. Mol Ecol Resour. 11: 353–357.
34. Stat Soft France (2005) STATISTICA (Logiciel d’analyse des données), ver-sion 7.1. Available at: www. Statsoft. Fr.
35. Ward Jr JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc. 58: 236–244.
36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics soft-ware package for education and data analysis. Palaeontol Electron. 4: 1–9.
37. Gower JC (1975) Generalized Procrustes Analysis. Psychometrika. 40: 33–51.
38. Jacobson LR (2003) Leishmania tropica (Kinetoplastida: Trypanosomatidae) – a perplexing parasite. Folia Parasitol. 50: 241–250.
39. Dvorak V, Aytekin AM, Alten B, Skarupova S, Votypka J, Volf P (2006) A comparison of the intraspecific varia-bility of Phlebotomus sergenti Parrot, 1917 (Diptera: Psychodidae). J Vector Ecol. 31: 229–238.
40. Guernaoui S, Hamarsheh O, Garcia, D, Fontenille D, Sereno D (2020) Popula-tion Genetics of Phlebotomus papatasi from Endemic and Nonendemic Areas for Zoonotic Cutaneous Leishmaniasis in Morocco, as Revealed by Cyto¬chrome Oxidase Gene Subunit I Se¬quencing. Mi¬croorganisms. 8(7): 1010.
41. Guernaoui S, Boumezzough A, Laamrani A (2006) Altitudinal structuring of phlebotomine sandflies (Diptera: Psy-chodidae) in the High-Atlas Mountains, Morocco. Acta Trop. 97: 346–351.
| Files | ||
| Issue | Vol 17 No 1 (2023) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v17i1.13200 | |
| Keywords | ||
| Phlebotomus sergenti; Wing traditional morphometry; Wing geometric morphom¬ery; Morocco | ||
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How to Cite
1.
Abou-Elaaz F-Z, Sereno D, Himmi O, Ghamizi M, Guernaoui S. Descriptive and Geometric Morphometry of the Wings of Phlebotomus sergenti Populations in Central Morocco. J Arthropod Borne Dis. 2023;17(1):36–50.
