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 Biology Ecology Section Faculty of Science VERG Laboratories Hacettepe University Ankara Turkey

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

Institute of Specific Prophylaxis and Tropical Medicine Center for Pathophysiology Infectiology and Immunology Medical University of Vienna Vienna Austria

Laboratory of Entomology Ministry of Health Jerusalem Israel

Sustainability Solutions Research Lab University of Pannonia Veszprém Hungary

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Cecílio, P., Cordeiro-da-Silva, A. & Oliveira, F. Sand flies: Basic information on the vectors of leishmaniasis and their interactions with PubMed PMC

Jia, L. Y. & Min, Z. L. Chinese phlebotomine sandflies of subgenus PubMed

Jacobson, R. L. Leishmaniasis in an era of conflict in the Middle East. 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. PubMed PMC

Dvorak, V. et al. Sand flies (Diptera: Psychodidae) in eight Balkan countries: Historical review and region-wide entomological survey. PubMed PMC

Zhang, L., Ma, Y. & Xu, J. Genetic differentiation between sandfly populations of PubMed PMC

Perrotey, S., Benabdennbi, I., Haddad, N., Pesson, B. & Léger, N. Electrophoretic and morphological differentiation between two sympatric species of PubMed

Artemiev, M. M. A revision of sandflies of the subgenus

Dvořák, V. PubMed PMC

Kniha, E. et al. PubMed PMC

Șuleșco, T. et al. Phlebotomine sand fly survey in the Republic of Moldova: Species composition, distribution and host preferences. PubMed PMC

Pareyn, M. et al. An integrative approach to identify sand fly vectors of leishmaniasis in Ethiopia by morphological and molecular techniques. 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. PubMed PMC

Svobodová, M., Volf, P. & Votýpka, J. Experimental transmission of PubMed

Sádlová, J., Hajmová, M. & Volf, P. 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. PubMed

Giorgobiani, E. PubMed PMC

Kniha, E. et al. Reconstructing the post-glacial spread of the sand fly PubMed PMC

Cruaud, A., Lehrter, V., Genson, G., Rasplus, J.-Y. & Depaquit, J. Evolution, systematics and historical biogeography of sand flies of the subgenus PubMed PMC

Pavlou, C. et al. A molecular phylogeny and phylogeography of Greek Aegean Island sand flies of the genus

Alten, B. Speciation and dispersion hypotheses of phlebotomine sandflies of the subgenus

Trájer, A. J. Investigation of the possible role of the Central Paratethys as a migration route and speciation area of the ancestors of Mediterranean

Trájer, A. J. Palaeoclimatic models - predicted changes in the potential Neogene distribution patterns of

Esseghir, S. & Ready, P. D. Speciation of

Garcia-Castellanos, D. et al. Catastrophic flood of the Mediterranean after the Messinian salinity crisis. 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.

Trájer, A. J., Hammer, T. & Padisák, J. Reflection of the Neogene-Quaternary phylogeography in the recent distribution limiting climatic factors of eight Mediterranean

Brower, A. V. Z. Rapid morphological radiation and convergence among races of the butterfly PubMed PMC

Farrell, B. D. Evolutionary assembly of the milkweed fauna: Cytochrome oxidase I and the age of tetraopes beetles. 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 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.

Sanjoba, C., Omachi, S., Sato, K. & Matsumoto, Y. Additional distribution record of

Trájer, A. J., Walochnik, J. & Kniha, E. The possible region of the Late Miocene split of the sandfly subgenus DOI

Kasap, O. E. 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. PubMed PMC

Akhoundi, M., Parvizi, P., Baghaei, A. & Depaquit, J. The subgenus PubMed

Dergacheva, T. I. & Strelkova, M. V. Epidemiological role of sandflies PubMed

Ježek, J., Chvojka, P., Manko, P. & Oboňa, J. Faunistic and bibliographical inventory of moth flies from Ukraine (Diptera, Psychodidae). PubMed PMC

Trájer, A. J. & Sebestyén, V. The changing distribution of PubMed PMC

Trájer, A. J. Paradox negative effects of the mid-pliocene warming on the climatic suitability of six Mediterranean sandfly species in Europe.

Trájer, A. J. Age and environmental conditions for the formation of the Pannonian mega-yardang system.

Trájer, A. J. Checklist, distribution maps, bibliography of the Hungarian

Orshan, L. et al. Distribution and dispersal of PubMed PMC

Vaselek, S. et al. A survey of sand flies (Diptera, Phlebotominae) along recurrent transit routes in Serbia. PubMed

Studentsky, L. et al. PubMed PMC

Larkin, M. A. 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. PubMed PMC

Ronquist, F. PubMed PMC

Zhang, D. et al. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. PubMed

Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: Fast model selection for accurate phylogenetic estimates. PubMed PMC

Kuhner, M. K. Coalescent genealogy samplers: Windows into population history. PubMed PMC

Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using tracer 1.7. PubMed PMC

Bouckaert, R. PubMed PMC

Villesen, P. FaBox: An online toolbox for FASTA sequences.

Depaquit, J., Grandadam, M., Fouque, F., Andry, P. & Peyrefitte, C. Arthropod-borne viruses transmitted by Phlebotomine sandflies in Europe: A review. PubMed

Esseghir, S., Ready, P. D., Killick-Kendrick, R. & Ben-Ismail, R. Mitochondrial haplotypes and phylogeography of PubMed

López‐López, A., Abdul Aziz, A. & Galián, J. Molecular phylogeny and divergence time estimation of

Librado, P. & Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. PubMed

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. 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. PubMed PMC

Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction.

Excoffier, L., Laval, G. & Schneider, S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. PubMed PMC

Suchard, M. A. PubMed PMC

Chevenet, F., Fargette, D., Bastide, P., Vitré, T. & Guindon, S. EvoLaps 2: Advanced phylogeographic visualization. PubMed PMC

Xhekaj, B. et al. A cross-sectional study on phlebotomine sand flies in relation to disease transmission in the Republic of Kosovo. PubMed

Boutsini, S. et al. Phlebotomine sandflies and factors associated with their abundance in the leishmaniasis endemic area of Attiki, Greece. PubMed

Aransay, A. M., Scoulica, E. & Tselentis, Y. Detection and identification of PubMed PMC

Xanthopoulou, K. et al. Distribution of sandflies (Diptera, Psychodidae) in two Ionian Islands and Northern Greece. PubMed

Fotakis, E. A., Giantsis, I. A., Demir, S., Vontas, J. G. & Chaskopoulou, A. Detection of pyrethroid resistance mutations in the major Leishmaniasis vector PubMed

Tsirigotakis, N. et al. Phlebotomine sand flies (Diptera: Psychodidae) in the Greek Aegean Islands: Ecological approaches. PubMed PMC

Karanis, P. et al. Sandfly (Diptera: Psychodidae) distributiοn in Northern Greece.

Svobodova, M. et al. Distinct transmission cycles of PubMed PMC

Vaselek, S. 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. PubMed

Kavur, H., Arikan, H. & Ozbel, Y. 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. PubMed

Ergunay, K. et al. Molecular evidence indicates that PubMed

Léger, N., Pesson, B. & Madulo-Leblond, G. Les phlébotomes de Grèce. 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). PubMed

Leger, N. et al. Les phlébotomes de Crète.

Depaquit, J., Ferte, H. & Leger, N. Les phlebotomes (Diptera - Psychodidae) de lìle de Rhodes (Grece).

Wint, G. R. W. 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. PubMed PMC

MacFerrin, M.

Bruch, A. A., Uhl, D. & Mosbrugger, V. Miocene climate in Europe—Patterns and evolution.

Mosbrugger, V. & Utescher, T. The coexistence approach—a method for quantitative reconstructions of tertiary terrestrial palaeoclimate data using plant fossils.

Trájer, A. J. The correspondence between the physiological cold tolerance and the distribution border of Mediterranean sandflies in Southeast Europe. PubMed

Karger, D. N.

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.

Boussaa, S., Guernaoui, S., Pesson, B. & Boumezzough, A. Seasonal fluctuations of phlebotomine sand fly populations (Diptera: Psychodidae) in the urban area of Marrakech, Morocco. PubMed

Thornthwaite, C. W. An approach toward a rational classification of climate.

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

Kemp, D.

Hijmans, R. J. & Graham, C. H. The ability of climate envelope models to predict the effect of climate change on species distributions.

Whitesitt, J. E.

Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. PubMed PMC

Fu, Y.-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. PubMed PMC

The knowns and unknowns of phlebotomine sand flies (Diptera: Psychodidae) in selected countries of Central Europe