Combining phylogeography and climate models to track the diversification and spread of Phlebotomus simici
Language English Country Great Britain, England Media electronic
Document type Journal Article
PubMed
40128321
PubMed Central
PMC11933271
DOI
10.1038/s41598-025-94601-1
PII: 10.1038/s41598-025-94601-1
Knihovny.cz E-resources
- Keywords
- Adlerius, COI, Central Europe, Divergence time, Phylogeography,
- MeSH
- Phylogeny * MeSH
- Phylogeography * MeSH
- Insect Vectors genetics classification MeSH
- Phlebotomus * classification genetics MeSH
- Climate MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Europe MeSH
Phlebotomine sand flies (Diptera: Psychodidae: Phlebotominae) are the principal vectors of Leishmania spp. (Kinetoplastida: Trypanosomatidae) worldwide. The subgenus Adlerius is taxonomically challenging and currently comprises about 20 species with a wide geographic distribution from eastern Asia to southeastern Europe. Some species are confirmed or suspected vectors of Leishmania donovani/infantum, L. major, and L. tropica, and are thus of high medical and veterinary relevance. A single record of Phlebotomus (Adlerius) simici in Austria from 2018 marks its sporadic northernmost and westernmost occurrence, with the origin of its appearance remaining unclear. To better understand Adlerius diversification and particularly post-glacial spread of Ph. simici to northern parts of Europe, we combined phylogenetic analyses with climatic suitability modelling. Divergence time estimates well supported the currently observed geographic distribution of the studied species and revealed several taxonomic challenges in the subgenus. We clearly delineated three distinct genetic and geographic Ph. simici lineages and phylogeographically assessed diversification that were well supported by climatic models. This study provides a comprehensive phylogenetic analysis of the subgenus Adlerius, enhancing our understanding of the diversification in relation to changing climate of this understudied group, and we present new insights into the post-glacial spread of Ph. simici, a suspected vector of L. infantum.
Department of Parasitology Faculty of Science Charles University Prague Czech Republic
Faculty of Agriculture and Veterinary University of Prishtina Prishtina Kosovo
Institute of Biology University of Graz Graz Austria
Laboratory of Entomology Ministry of Health Jerusalem Israel
Sustainability Solutions Research Lab University of Pannonia Veszprém Hungary
See more in PubMed
Cecílio, P., Cordeiro-da-Silva, A. & Oliveira, F. Sand flies: Basic information on the vectors of leishmaniasis and their interactions with Leishmania parasites. Commun. Biol.5, 305 (2022). PubMed PMC
Jia, L. Y. & Min, Z. L. Chinese phlebotomine sandflies of subgenus Adlerius NITZULESCU, 1931, (Diptera: Psychodidae) and the identity of Phlebotomus sichuanensis LENG & Yin, 1983, Part I—Taxonomical study and geographical distribution. Parasite8, 3–9 (2001). PubMed
Jacobson, R. L. Leishmaniasis in an era of conflict in the Middle East. Vector-Borne Zoon. Dis.11, 247–258 (2011). PubMed
Kasap, O. E., Linton, Y.-M., Karakus, M., Ozbel, Y. & Alten, B. Revision of the species composition and distribution of Turkish sand flies using DNA barcodes. Parasit. Vectors12, 410 (2019). PubMed PMC
Dvorak, V. et al. Sand flies (Diptera: Psychodidae) in eight Balkan countries: Historical review and region-wide entomological survey. Parasit. Vectors13, 573 (2020). PubMed PMC
Zhang, L., Ma, Y. & Xu, J. Genetic differentiation between sandfly populations of Phlebotomus chinensis and Phlebotomus sichuanensis (Diptera: Psychodidae) in China inferred by microsatellites. Parasit. Vectors6, 115 (2013). PubMed PMC
Perrotey, S., Benabdennbi, I., Haddad, N., Pesson, B. & Léger, N. Electrophoretic and morphological differentiation between two sympatric species of Adlerius: Phlebotomus brevis and Phlebotomus simici (Diptera: Psychodidae). J. Med. Entomol.37, 289–294 (2009). PubMed
Artemiev, M. M. A revision of sandflies of the subgenus Adlerius (Diptera, Phlebotominae, Phlebotomus). Zool. Zhurnal59, 1177–1192 (1980).
Dvořák, V. et al. Sand fly fauna of Crete and the description of Phlebotomus (Adlerius) creticus n. sp. (Diptera: Psychodidae). Parasit. Vectors13, 1–17 (2020). PubMed PMC
Kniha, E. et al. Phlebotomus (Adlerius) simici NITZULESCU, 1931: First record in Austria and phylogenetic relationship with other Adlerius species. Parasit. Vectors14, 20 (2021). PubMed PMC
Șuleșco, T. et al. Phlebotomine sand fly survey in the Republic of Moldova: Species composition, distribution and host preferences. Parasit. Vectors14, 371 (2021). PubMed PMC
Pareyn, M. et al. An integrative approach to identify sand fly vectors of leishmaniasis in Ethiopia by morphological and molecular techniques. Parasit. Vectors13, 580 (2020). PubMed PMC
Guan, L.-R., Zhou, Z.-B., Jin, C.-F., Fu, Q. & Chai, J.-J. Phlebotomine sand flies (Diptera: Psychodidae) transmitting visceral leishmaniasis and their geographical distribution in China: A review. Infect. Dis. Poverty5, 15 (2016). PubMed PMC
Svobodová, M., Volf, P. & Votýpka, J. Experimental transmission of Leishmania tropica to hyraxes (Procavia capensis) by the bite of Phlebotomus arabicus. Microbes Infect.8, 1691–1694 (2006). PubMed
Sádlová, J., Hajmová, M. & Volf, P. Phlebotomus (Adlerius) halepensis vector competence for Leishmania major and Le. tropica. Med. Vet. Entomol.17, 244–250 (2003). PubMed
Chaskopoulou, A., Giantsis, I. A., Demir, S. & Bon, M. C. Species composition, activity patterns and blood meal analysis of sand fly populations (Diptera: Psychodidae) in the metropolitan region of Thessaloniki, an endemic focus of canine leishmaniasis. Acta Trop.158, 170–176 (2016). PubMed
Giorgobiani, E. et al. Incrimination of Phlebotomus kandelakii and Phlebotomus balcanicus as vectors of Leishmania infantum in Tbilisi, Georgia. PLoS Negl. Trop. Dis.6 (2012). PubMed PMC
Kniha, E. et al. Reconstructing the post-glacial spread of the sand fly Phlebotomus mascittii Grassi, 1908 (Diptera: Psychodidae) in Europe. Commun. Biol.6, 1244 (2023). PubMed PMC
Cruaud, A., Lehrter, V., Genson, G., Rasplus, J.-Y. & Depaquit, J. Evolution, systematics and historical biogeography of sand flies of the subgenus Paraphlebotomus (Diptera, Psychodidae, Phlebotomus) inferred using restriction-site associated DNA markers. PLoS Negl. Trop. Dis.15, e0009479 (2021). PubMed PMC
Pavlou, C. et al. A molecular phylogeny and phylogeography of Greek Aegean Island sand flies of the genus Phlebotomus (Diptera: Psychodidae). Arthropod Syst. Phylogeny80, 137–154 (2022).
Alten, B. Speciation and dispersion hypotheses of phlebotomine sandflies of the subgenus Paraphlebotomus (Diptera: Psychodidae): The case in Turkey. Hacettepe J. Biol. Chem.38, 229–246 (2010).
Trájer, A. J. Investigation of the possible role of the Central Paratethys as a migration route and speciation area of the ancestors of Mediterranean Larroussius, Paraphlebotomus and Phlebotomus species. Palaeobiodiversity Palaeoenvironments103, 165–192 (2023).
Trájer, A. J. Palaeoclimatic models - predicted changes in the potential Neogene distribution patterns of Phlebotomus similis and Phlebotomus sergenti (Insecta: Diptera: Psychodidae). Palaeobiodiversity Palaeoenvironments102, 149–172 (2022).
Esseghir, S. & Ready, P. D. Speciation of Phlebotomus sandflies of the subgenus Larroussius coincided with the late Miocene-Pliocene aridification of the Mediterranean subregion. Biol. J. Linn. Soc.70, 189–219 (2000).
Garcia-Castellanos, D. et al. Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature462, 778–781 (2009). PubMed
Trájer, A. J., Sebestyén, V. & Padisák, J. The impacts of the Messinian Salinity Crisis on the biogeography of three Mediterranean sandfly (Diptera: Psychodidae) species. Geobios65, 51–66 (2021).
Trájer, A. J., Hammer, T. & Padisák, J. Reflection of the Neogene-Quaternary phylogeography in the recent distribution limiting climatic factors of eight Mediterranean Phlebotomus species (Diptera: Psychodidae). J. Nat. Hist.52, 1763–1784 (2018).
Brower, A. V. Z. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci.91, 6491–6495 (1994). PubMed PMC
Farrell, B. D. Evolutionary assembly of the milkweed fauna: Cytochrome oxidase I and the age of tetraopes beetles. Mol. Phylogenet. Evol.18, 467–478 (2001). PubMed
Quek, S.-P., Davies, S. J., Itino, T. & Pierce, N. E. Codiversification in an ant-plant mutualism: Stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution.58, 554–570 (2004). PubMed
Trájer, A. J. Characterization of the palaeoenvironmental conditions in the Pannonian Basin during the last 34 mys related to the formation of haematitic and kaolinitic sedimentary rocks. Int. J. Earth Sci.112, 1361–1387 (2023).
Sanjoba, C., Omachi, S., Sato, K. & Matsumoto, Y. Additional distribution record of Sergentomyia (Neophlebotomus) squamirostris (Newstead) (Diptera: Psychodidae) from Tokyo, Japan. Med. Entomol. Zool.68, 45–48 (2017).
Trájer, A. J., Walochnik, J. & Kniha, E. The possible region of the Late Miocene split of the sandfly subgenus Transphlebotomus Artemiev and the early late Neogene to late Quaternary dispersal of the ancestor of Phlebotomus mascittii Grassi. Palaeobiodiversity Palaeoenvironments10.1007/s12549-022-00570-y (2023).
Kasap, O. E. et al. Phylogeography of the subgenus Transphlebotomus Artemiev with description of two new species, Phlebotomus anatolicus n. sp. and Phlebotomus killicki n. sp. Infect. Genet. Evol.34, 467–479 (2015). PubMed
Usarov, G. X. et al. Phlebotomine sand fly (Diptera: Phlebotominae) diversity in the foci of cutaneous leishmaniasis in the Surxondaryo Region of Uzbekistan: 50 years on. Parasitol. Res.123, 170 (2024). PubMed PMC
Akhoundi, M., Parvizi, P., Baghaei, A. & Depaquit, J. The subgenus Adlerius Nitzulescu (Diptera, Psychodidae, Phlebotomus) in Iran. Acta Trop.122, 7–15 (2012). PubMed
Dergacheva, T. I. & Strelkova, M. V. Epidemiological role of sandflies Phlebotomus smirnovi Perfiliev, 1941 and P. longiductus Parrot, 1928 in visceral leishmaniasis foci in the Kazakh SSR. Trans. R. Soc. Trop. Med. Hyg.79, 34–36 (1985). PubMed
Ježek, J., Chvojka, P., Manko, P. & Oboňa, J. Faunistic and bibliographical inventory of moth flies from Ukraine (Diptera, Psychodidae). Zookeys693, 109–128 (2017). PubMed PMC
Trájer, A. J. & Sebestyén, V. The changing distribution of Leishmania infantum Nicolle, 1908 and its Mediterranean sandfly vectors in the last 140 kys. Sci. Rep.9, 11820 (2019). PubMed PMC
Trájer, A. J. Paradox negative effects of the mid-pliocene warming on the climatic suitability of six Mediterranean sandfly species in Europe. Biosis: Biol. Syst.1, 141–156 (2020).
Trájer, A. J. Age and environmental conditions for the formation of the Pannonian mega-yardang system. Int. J. Earth Sci.113, 875–901 (2024).
Trájer, A. J. Checklist, distribution maps, bibliography of the Hungarian Phlebotomus (Diptera: Psychodidae) fauna complementing with the climate profile of the recent sandfly distribution areas in Hungary. Folia Faun. Slov.22, 7–12 (2017).
Orshan, L. et al. Distribution and dispersal of Phlebotomus papatasi (Diptera: Psychodidae) in a zoonotic cutaneous leishmaniasis focus, the Northern Negev, Israel. PLoS Negl. Trop. Dis.10, e0004819 (2016). PubMed PMC
Vaselek, S. et al. A survey of sand flies (Diptera, Phlebotominae) along recurrent transit routes in Serbia. Acta Trop.197, 105063 (2019). PubMed
Studentsky, L. et al. Leishmania donovani transmission cycle associated with human infection, Phlebotomus alexandri sand flies, and hare blood meals, Israel. Emerg. Infect. Dis.29, 945–955 (2023). PubMed PMC
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics23, 2947–2948 (2007). PubMed
Nicholas, K. B. Genedoc: A tool for editing and annotating multiple sequence alignments. http://www.pscedu/biomed/genedoc. (1997).
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol.32, 268–274 (2015). PubMed PMC
Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol.61, 539–542 (2012). PubMed PMC
Zhang, D. et al. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol. Ecol. Resour.20, 348–355 (2020). PubMed
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods14, 587–589 (2017). PubMed PMC
Kuhner, M. K. Coalescent genealogy samplers: Windows into population history. Trends Ecol. Evol.24, 86–93 (2009). PubMed PMC
Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst. Biol.67, 901–904 (2018). PubMed PMC
Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol.15, e1006650 (2019). PubMed PMC
Villesen, P. FaBox: An online toolbox for FASTA sequences. Mol. Ecol. Notes7, 965–968 (2007).
Depaquit, J., Grandadam, M., Fouque, F., Andry, P. & Peyrefitte, C. Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: A review. Eurosurveillance15, 19507 (2010). PubMed
Esseghir, S., Ready, P. D., Killick-Kendrick, R. & Ben-Ismail, R. Mitochondrial haplotypes and phylogeography of Phlebotomus vectors of Leishmania major. Insect Mol. Biol.6, 211–225 (1997). PubMed
López‐López, A., Abdul Aziz, A. & Galián, J. Molecular phylogeny and divergence time estimation of Cosmodela (Coleoptera: Carabidae: Cicindelinae) tiger beetle species from Southeast Asia. Zool. Scr.44, 437–445 (2015).
Librado, P. & Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics25, 1451–1452 (2009). PubMed
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol.35, 1547–1549 (2018). PubMed PMC
Templeton, A. R., Crandall, K. A. & Sing, C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics132, 619–633 (1992). PubMed PMC
Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol.6, 1110–1116 (2015).
Excoffier, L., Laval, G. & Schneider, S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinform. Online1, 47–50 (2007). PubMed PMC
Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol.4, 1–5 (2018). PubMed PMC
Chevenet, F., Fargette, D., Bastide, P., Vitré, T. & Guindon, S. EvoLaps 2: Advanced phylogeographic visualization. Virus Evol.10 (2024). PubMed PMC
Xhekaj, B. et al. A cross-sectional study on phlebotomine sand flies in relation to disease transmission in the Republic of Kosovo. Med. Vet. Entomol.38, 573–585 (2024). PubMed
Boutsini, S. et al. Phlebotomine sandflies and factors associated with their abundance in the leishmaniasis endemic area of Attiki, Greece. Parasitol. Res.117, 107–113 (2018). PubMed
Aransay, A. M., Scoulica, E. & Tselentis, Y. Detection and identification of Leishmania DNA within naturally infected sand flies by seminested PCR on minicircle kinetoplastic DNA. Appl. Environ. Microbiol.66, 1933–1938 (2000). PubMed PMC
Xanthopoulou, K. et al. Distribution of sandflies (Diptera, Psychodidae) in two Ionian Islands and Northern Greece. Vector-Borne Zoon. Dis.11, 1591–1594 (2011). PubMed
Fotakis, E. A., Giantsis, I. A., Demir, S., Vontas, J. G. & Chaskopoulou, A. Detection of pyrethroid resistance mutations in the major Leishmaniasis vector Phlebotomus papatasi. J. Med. Entomol.55, 1225–1230 (2018). PubMed
Tsirigotakis, N. et al. Phlebotomine sand flies (Diptera: Psychodidae) in the Greek Aegean Islands: Ecological approaches. Parasit. Vectors11, 1–14 (2018). PubMed PMC
Karanis, P. et al. Sandfly (Diptera: Psychodidae) distributiοn in Northern Greece. Entomol. Hell.13, 13 (2017).
Svobodova, M. et al. Distinct transmission cycles of Leishmania tropica in 2 Adjacent Foci, Northern Israel. Emerg. Infect. Dis.12, 1860–1868 (2006). PubMed PMC
Vaselek, S. et al. Sandfly surveillance and investigation of Leishmania spp. DNA in sandflies in Kosovo. Med. Vet. Entomol.34, 394–401 (2020). PubMed
Yaman, M. & Özbel, Y. The sandflies (Diptera: Psychodidae) in the Turkish province of Hatay: Some possible vectors of the parasites causing human cutaneous leishmaniasis. Ann. Trop. Med. Parasitol.98, 741–750 (2004). PubMed
Kavur, H., Arikan, H. & Ozbel, Y. Phlebotomus halepensis (Diptera: Psychodidae) vectorial capacity in Afyon and Nigde Province, Turkey. J. Med. Entomol.55, 317–322 (2018). PubMed
Omondi, Z. N., Demir, S. & Arserim, S. K. Entomological survey of the sand fly fauna of Kayseri Province: Focus on visceral and cutaneous leishmaniasis in Central Anatolia, Turkey. Turkiye parazitolojii Derg.44, 158–163 (2020). PubMed
Ergunay, K. et al. Molecular evidence indicates that Phlebotomus major sensu lato (Diptera: Psychodidae) is the vector species of the recently-identified sandfly fever sicilian virus variant: Sandfly fever Turkey virus. Vector-Borne Zoon. Dis.12, 690–698 (2012). PubMed
Léger, N., Pesson, B. & Madulo-Leblond, G. Les phlébotomes de Grèce. Bull. Soc. Pathol. Exot.79, 386–397 (1986). PubMed
Léger, N. & Pesson, B. Sur la taxonomie et al répartition géographique de Phlebotomus (Adlerius) chinensis s. l. et de P. (Larroussius) major s.l. (Psychodidae-Diptera). Bull. Soc. Pathol. Exot.80, 252–260 (1987). PubMed
Leger, N. et al. Les phlébotomes de Crète. Biol. Gall.20, 135–143 (1993).
Depaquit, J., Ferte, H. & Leger, N. Les phlebotomes (Diptera - Psychodidae) de lìle de Rhodes (Grece). Bull. la Société Française Parasitol.14, 28–38 (1996).
Wint, G. R. W. et al. VectorNet: Collaborative mapping of arthropod disease vectors in Europe and surrounding areas since 2010. Eurosurveillance28 (2023). PubMed PMC
QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org (2019).
Beck, H. E. et al. Present and future Köppen–Geiger climate classification maps at 1-km resolution. Sci. Data5, 180214 (2018). PubMed PMC
MacFerrin, M. et al. ETOPO 2022: An updated NOAA global relief model. AGUFM2021, NH25B-0560 (2021).
Bruch, A. A., Uhl, D. & Mosbrugger, V. Miocene climate in Europe—Patterns and evolution. Palaeogeogr. Palaeoclimatol. Palaeoecol.253, 1–7 (2007).
Mosbrugger, V. & Utescher, T. The coexistence approach—a method for quantitative reconstructions of tertiary terrestrial palaeoclimate data using plant fossils. Palaeogeogr. Palaeoclimatol. Palaeoecol.134, 61–86 (1997).
Trájer, A. J. The correspondence between the physiological cold tolerance and the distribution border of Mediterranean sandflies in Southeast Europe. J. Vector Borne Dis.61, 376–388 (2024). PubMed
Karger, D. N. et al. CHELSA-TraCE21k v1.0. Downscaled transient temperature and precipitation data since the last glacial maximum. Clim. Past Discuss., 1–27 (2021).
le Roux, R., Henrico, S., Bezuidenhout, J. & Henrico, I. Inverse distance weighting as an alternative interpolation method to create radiometric maps of natural radionuclide concentrations using QGIS. Proc. ICA5, 1–7 (2023).
Boussaa, S., Guernaoui, S., Pesson, B. & Boumezzough, A. Seasonal fluctuations of phlebotomine sand fly populations (Diptera: Psychodidae) in the urban area of Marrakech, Morocco. Acta Trop.95, 86–91 (2005). PubMed
Thornthwaite, C. W. An approach toward a rational classification of climate. Geogr. Rev.38, 55 (1948).
Nayakarathna, N. M. N. G., Ganehiarachchi, G. A. S. M., Rajapakse, R. P. V. J. & Jayanetti, S. R. Influence of humidity and temperature variation of natural breeding sites on abundance of Leishmaniasis vector Phlebotomus argentipes population in Anuradhapura District. In Proceedings of the International Research Symposium on Pure and Applied Sciences 12 (Faculty of Science, University of Kelaniya, 2016).
Kemp, D. Global Environmental Issues (Routledge, 2002). 10.4324/9780203425305
Hijmans, R. J. & Graham, C. H. The ability of climate envelope models to predict the effect of climate change on species distributions. Glob. Change Biol.12, 2272–2281 (2006).
Whitesitt, J. E. Boolean Algebra and Its Applications (Courier Corporation, 2010).
Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics123, 585–595 (1989). PubMed PMC
Fu, Y.-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics147, 915–925 (1997). PubMed PMC