Infection, Genetics and Evolution 28 (2014) 744–756

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Molecular systematics applied to Phlebotomine sandflies: Review and perspectives Jérôme Depaquit ⇑ Université de Reims Champagne-Ardenne, ANSES, EA4688 – USC «transmission vectorielle et épidémiosurveillance de maladies parasitaires (VECPAR)», SFR Cap Santé, Faculté de Pharmacie, 51 rue Cognacq-Jay, 51096 Reims, France

a r t i c l e

i n f o

Article history: Received 20 March 2014 Received in revised form 23 October 2014 Accepted 28 October 2014 Available online 31 October 2014 Keywords: Review Phlebotomus Sergentomyia Lutzomyia Molecular systematics DNA barcoding

a b s t r a c t A review of the literature related to the molecular systematics of the Phlebotomine sandflies (Diptera, Psychodidae) is proposed. It shows that molecular systematics is more frequently used to perform evolutionary systematics than to help in the field of alpha taxonomy. On more than 900 living species and subspecies described, 180 (about 20%) have been processed for molecular systematics. The countries of origin where the sandflies processed come from are endemic for leishmaniases and the ratio of species sampled for molecular systematics studies is high for vector groups and low for species not involved in the transmission of leishmaniasis. The main studies focused on intraspecific topics, others on closely related species, and a few compared genera of sandflies. Mitochondrial markers (more than 50% of the markers studied) are preferred to non mitochondrial markers. The use of mtDNA markers alone to explore phylogenetic relationships is considered as dangerous, especially concerning closely related species. Ó 2014 Elsevier B.V. All rights reserved.

1. Introduction DNA markers are interesting characters for Phlebotomine sandflies (Diptera, Psychodidae) systematics, as well as for many other groups of vectors, parasites, animals, plants, fungi, and bacteria. Their first application to the systematics of Phlebotomine sandflies was done by pioneers in the 1990’s (Adamson et al., 1991; Booth et al., 1991; Adamson et al., 1993; Maingon et al., 1993; Zeledon et al., 1993; Booth et al., 1996; Esseghir et al., 1997; Friedrich and Tautz, 1997; Depaquit et al., 1998; Dias et al., 1998). They constitute powerful tools to define populations with evident consequences to characterise vectors and non-vectors, to emphasise cryptic species, to associate males with females in a same species or to propose evolutionary systematics. These molecular approaches tend to supplant the traditional morphological ones in the field of systematics for several reasons. The latter is longer and more difficult to carry out than the former, and this independently of the application (alpha taxonomy or phylogenetical systematics). Nevertheless, it is clear that phylogenetical studies between not closely related species, belonging to many genera, from different continents, require a perfect

⇑ Tel.: +33 326913723. E-mail address: [email protected] http://dx.doi.org/10.1016/j.meegid.2014.10.027 1567-1348/Ó 2014 Elsevier B.V. All rights reserved.

knowledge of the group and can only be considered by some taxonomists who have an important background in the field. Moreover, the expensive cost of molecular techniques has dropped dramatically over the past 15 years. These tools are used routinely in many laboratories and do not require an important background on Phlebotomine sandflies. Lastly, molecular studies are more easily publishable than morphological studies and are appreciated by journal’s editors. However, this facility is only apparent and many pitfalls remain. Three families of molecules were processed for sandflies systematics: - Proteins like isoenzymes (Miles and Ward, 1978; Caillard et al., 1986; Ryan et al., 1986; Perrotti et al., 1991; Pesson et al., 1991; Zhang and Leng, 1991; Lanzaro et al., 1993; Maingon et al., 1993; Zeledon et al., 1993; Dujardin et al., 1996; RemyKristensen et al., 1996; Dujardin et al., 1997; Mukhopadhyay et al., 1998; Munstermann et al., 1998; Benabdennbi et al., 1999; Kassem et al., 1999; Lampo et al., 1999; Arrivillaga et al., 2000; Perrotey et al., 2000; Feliciangeli and Lampo, 2001; Marquez et al., 2001; Mukhopadhyay et al., 2001; Zhang and Leng, 2002; Aransay et al., 2003; Arrivillaga et al., 2003; Torgerson et al., 2003; Belen et al., 2004; Dujardin et al., 2004; Pesson et al., 2004; Meneses et al., 2005; Perrotey et al., 2005; Boussaa et al., 2008a,b; Hernández et al., 2008;

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Arrivillaga and Marrero, 2009; Boussaa et al., 2009) and more recently an analysis of the complete proteome using matrixassisted laser desorption/ionization time of flight mass spectrometry (MALDI-TOF) (Dvorak et al., 2014). - Cuticular hydrocarbons (Ryan et al., 1986; Kamhawi et al., 1987; Phillips et al., 1990a,b; Mahamat and Hassanali, 1998) and chemical molecules involved in the communication between species, like pheromones (Lane et al., 1985; Ward et al., 1991; Zeledon et al., 1993; Dujardin et al., 1997; Mahamat and Hassanali, 1998; Bauzer et al., 2002a,b; Maingon et al., 2003; Hamilton et al., 2005; Watts et al., 2005; Salomon et al., 2010; Vigoder et al., 2010). - DNA sequences focusing on the heart of this work. The use of the adjective molecular does not refer in routine to the use of any molecules for systematics. In fact, in its current application, it is restricted to DNA markers. We follow this convention in this article proposing an analysis of the literature concerning the molecular systematics of Phlebotomine sandflies.

2. Material and methods The key words selected to find references were: molecular, systematics, phylogeny, barcoding, Psychodidae, Phlebotomine, sandfly, sand fly, sandflies, sand flies, Phlebotomus, Lutzomyia, and Sergentomyia. The databases selected were PubMed, (National Center for Biotechnology Information (NCBI), National Library of Medicine, NIH) (http://www.ncbi.nlm.nih.gov/pubmed), Armed Forces Pest Management Board Literature Retrieval System (http://www.afpmb.org/content/literature-retrieval-system), and my personal database. The last search was conducted on August, 22nd 2014. For each publication, the molecular markers selected, the taxa processed, their geographic origin (countries) and the taxonomic goal have been registered. Concerning the latter approach, we divided the goals in alpha taxonomy and evolutionary systematics subdivided in different levels of analysis: intraspecific, interspecific within a genus, and intergeneric. We used the abbreviations for the genera and subgenera of sandflies (Marcondes, 2007).

3. Results The publications included in the present study focus on different goals. Regarding the taxonomy, a few publications focus on alphataxonomy. A first category includes description of new taxa for Science using molecular biology to be sure that males and females belong to the same taxa (Depaquit et al., 2007, 2008a, 2009; Muller et al., 2007; Léger et al., 2012, 2014; Zapata et al., 2012a; Randrianambinintsoa et al., 2013). A second category includes publications describing new species for Science on one gender only and sequences are provided as a tool for a future description of the hitherto unknown gender (Depaquit et al., 2004b; Randrianambinintsoa et al., 2012; Randrianambinintsoa and Depaquit, 2013). Thirdly, in four publications, DNA sequences have been used to associate males and females in existing species (Depaquit et al., 2004a; Khadri et al., 2008; Parvizi et al., 2010b; Zhang et al., 2013). Molecular markers have been sequenced several times to identify species (Mukhopadhyay et al., 2000; Depaquit et al., 2005a; Florin et al., 2010; Manonmani et al., 2010; Parvizi et al., 2010b; Latrofa et al., 2011a,b; Tiwary et al., 2012; Minter et al., 2013) whereas cyt b sequences, associated to isoenzymes revealed a new species not named (Pesson et al., 2004).

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The other publications are related to evolutionary systematics. They focus on different taxonomic levels (Fig. 1). A total of 83 intraspecific studies has been recorded in the literature (Esseghir et al., 1997; Marcondes, 1997; Marcondes et al., 1997; Dias et al., 1998; Aransay et al., 2000, 2003; Di Muccio et al., 2000; Esseghir and Ready, 2000; Mukhopadhyay et al., 2000; Yin et al., 2000; Marquez et al., 2001; Soto et al., 2001; Arrivillaga et al., 2002, 2003; Bauzer et al., 2002a,b; Depaquit et al., 2002, 2004a, 2005b, 2008b, 2013, 2014; Hodgkinson et al., 2002, 2003; Testa et al., 2002; Bottecchia et al., 2004; Margonari et al., 2004; Pesson et al., 2004; Yahia et al., 2004; Elnaiem et al., 2005; Meneses et al., 2005; Perrotey et al., 2005; de Queiroz Balbino et al., 2006; Dvorak et al., 2006, 2011; Mazzoni et al., 2006, 2008; de Souza Rocha et al., 2007; Hamarsheh et al., 2007; Moin-Vaziri et al., 2007a,b; Baron et al., 2008; Bounamous et al., 2008, 2014; Lins et al., 2008, 2012; Araki et al., 2009, 2013; Bejarano et al., 2009; Vivero et al., 2009; Zhang et al., 2009, 2013; Ferroglio et al., 2010; Franco et al., 2010; Khalid et al., 2010, 2012; Mahamdallie et al., 2010; Parvizi et al., 2010a,b; Salomon et al., 2010; Belen et al., 2011; Florin et al., 2011; Kruger et al., 2011; Boudabous et al., 2012; Cohnstaedt et al., 2012; Kumar et al., 2012; Randrianambinintsoa et al., 2012; Scarpassa and Alencar, 2012, 2013; Zapata et al., 2012a,b; Gajapathy et al., 2013; Jafari et al., 2013; Kasap et al., 2013; Minter et al., 2013; Pech-May et al., 2013; Peyrefitte et al., 2013; Santos et al., 2013; Seblova et al., 2013; Yamamoto et al., 2013; Contreras Gutierrez et al., 2014; Valderrama et al., 2014). A total of 55 papers comparing different species or subspecies within a genus has been recorded (Booth et al., 1991, 1994; Adamson et al., 1993; Maingon et al., 1993; Esseghir et al., 1997; Marcondes et al., 1997; Aransay et al., 2000; Depaquit et al., 2000, 2002, 2005b, 2008a,b, 2014; Di Muccio et al., 2000; Esseghir and Ready, 2000; Mukhopadhyay et al., 2000; Soto et al., 2001; Lins et al., 2002; Mazzoni et al., 2002, 2006, 2008; Testa et al., 2002; Torgerson et al., 2003; Beati et al., 2004; Pesson et al., 2004; Moin-Vaziri et al., 2007a; Bounamous et al., 2008, 2014; Perez-Doria et al., 2008a; Absavaran et al., 2009; Kuwahara et al., 2009; Vivero et al., 2009; Azpurua et al., 2010; Franco et al., 2010; Khalid et al., 2010, 2012; Parvizi et al., 2010a,b; Belen et al., 2011; Kruger et al., 2011; Latrofa et al., 2011a,b; Kumar et al., 2012; Randrianambinintsoa et al., 2012, 2013; Jafari et al., 2013; Kasap et al., 2013; Minter et al., 2013; Pech-May et al., 2013; Randrianambinintsoa and Depaquit, 2013; Scarpassa and Alencar, 2013; Yamamoto et al., 2013; Zhang et al., 2013; Contreras Gutierrez et al., 2014). Lastly, a total of 22 publications comparing taxa belonging to different genera has been recorded (Esseghir et al., 1997; Depaquit et al., 1998, 1999; Aransay et al., 2000; Esseghir and Ready, 2000; Lins et al., 2002, 2012; Mazzoni et al., 2002; Torgerson et al., 2003; Vivero et al., 2007, 2009; Terayama et al., 2008; Kuwahara et al., 2009; Azpurua et al., 2010; Kruger et al., 2011; Latrofa et al., 2011b; Kumar et al., 2012; Jafari et al., 2013; Minter et al., 2013; Yamamoto et al., 2013; Bounamous et al., 2014; Contreras Gutierrez et al., 2014). The methods used for DNA sequences analyses are mainly sequences alignment and Neighbor-Joining, maximum parsimony and probabilistic methods like maximum likelihood and Bayesian inferences. Two focuses on the secondary structure of the molecular marker (Vivero et al., 2007, 2009; Perez-Doria et al., 2008b). Some studies used Random Amplified polymorphic DNA (RAPD) (Adamson et al., 1993; Maingon et al., 1993; Dias et al., 1998; Mukhopadhyay et al., 2000; Margonari et al., 2004; Meneses et al., 2005; de Queiroz Balbino et al., 2006; Dvorak et al., 2006, 2011; de Souza Rocha et al., 2007; Seblova et al., 2013), Restriction Fragment Length polymorphism (RFLP) (Terayama et al., 2008; Latrofa et al., 2011a; Tiwary et al., 2012; Minter et al., 2013;

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14 12 10 8

intraspecific

6

interspecific

4

intergeneric

2 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014

0

Fig. 1. Number of publications per year (1991–2013) related to intraspecific, interspecific–intrageneric, and intergeneric taxonomic levels concerning Phlebotomine sandflies.

Bounamous et al., 2014) or the Single Strand Conformation Polymorphism (SSCP) (Hodgkinson et al., 2002). A few studies have been carried out on microsatellites (Maingon et al., 2003; Watts et al., 2005; Zhang et al., 2009, 2013; Mahamdallie et al., 2010; Khalid et al., 2012; Santos et al., 2013) and the majority of studies focuses on the amplification of one or several molecular markers. A lot of publications used the mitochondrial DNA (mtDNA) markers. Cytochrome b (cyt b), complete or not, with or without partial flanking NADH1 and tRNA-ser is the most commonly used (Table 1 and Fig. 2) (Esseghir et al., 1997; Marcondes et al., 1997; Esseghir and Ready, 2000; Hodgkinson et al., 2002, 2003; Testa et al., 2002; Aransay et al., 2003; Torgerson et al., 2003; Pesson et al., 2004; Yahia et al., 2004; Depaquit et al., 2005a, 2007, 2008a, 2013, 2014; Perrotey et al., 2005; Hamarsheh et al., 2007; Moin-Vaziri et al., 2007a,b; Muller et al., 2007; Vivero et al., 2007, 2009; Baron et al., 2008; Bounamous et al., 2008, 2014; Perez-Doria et al., 2008a; Absavaran et al., 2009; Bejarano et al., 2009; Franco et al., 2010; Mahamdallie et al., 2010; Parvizi et al., 2010a,b; Belen et al., 2011; Dvorak et al., 2011; Kruger et al., 2011; Latrofa et al., 2011a,b; Cohnstaedt et al., 2012; Léger et al., 2012, 2014; Randrianambinintsoa et al., 2012, 2013; Zapata et al., 2012a; Gajapathy et al., 2013; Jafari et al., 2013; Kasap et al., 2013; Pech-May et al., 2013; Peyrefitte et al., 2013; Seblova et al., 2013; Yamamoto et al., 2013; Valderrama et al., 2014). Cytochrome C oxidase subunit I (COI) has been used more recently (Arrivillaga et al., 2002, 2003; Depaquit et al., 2009; Azpurua et al., 2010; Florin et al., 2010, 2011; Boudabous et al., 2012; Hoyos et al., 2012; Kumar et al., 2012; Scarpassa and Alencar, 2012, 2013; Gajapathy et al., 2013; Minter et al., 2013; Seblova et al., 2013; Bounamous et al., 2014; Contreras Gutierrez et al., 2014) whereas other genes are less used

Table 1 Molecular marker used for molecular systematics of Phlebotomine sandflies. Cytochrome b COI NADH1 NADH4 12S

50 16 2 5 2

mtDNA

75

18S ITS1 ITS2 28S

8 1 20 4

rDNA

33

Others

29

EF-alpha Period Cacophony Others Total

6 9 6 8 137

137

cytochrome b COI NADH1 NADH4 12S 18S ITS1 ITS2 28S EF-alpha

Fig. 2. Molecular markers used for the molecular systematics of Phlebotomine sandflies.

(Table 1 and Fig. 2): NADH1 (Latrofa et al., 2011a,b), NADH4: (Soto et al., 2001; Depaquit et al., 2004a, 2005b, 2008b; Khadri et al., 2008; Cohnstaedt et al., 2012) and 12S (Arrivillaga et al., 2003; Beati et al., 2004). The ribosomal DNA (rDNA) markers have been commonly used (Table 1 and Fig. 2). The small subunit (SSU, 18S) is used partially or totally (Aransay et al., 2000; Terayama et al., 2008; Azpurua et al., 2010; Ferroglio et al., 2010; Manonmani et al., 2010; Tiwary et al., 2012; Gajapathy et al., 2013; Pech-May et al., 2013), the first internal transcribed spacer (ITS1) has been used one time (Kuwahara et al., 2009). The second ITS (ITS2) has been selected 20 times (Depaquit et al., 2000, 2002, 2004a,b, 2008b, 2013; Di Muccio et al., 2000; Baron et al., 2008; Kuwahara et al., 2009; Florin et al., 2010, 2011; Khalid et al., 2010; Belen et al., 2011; Dvorak et al., 2011; Latrofa et al., 2011a,b; Zapata et al., 2012a; Gajapathy et al., 2013; Randrianambinintsoa and Depaquit, 2013; Zhang et al., 2013). Several markers which are parts of the long subunit (LSU, 28S) have been studied four times (Depaquit et al., 1998, 1999; Beati et al., 2004; Gajapathy et al., 2013). The use of nuclear and non ribosomal markers is frequent. A study coupling 21 multicloci has been proposed for New World sand flies (Araki et al., 2013). Most commonly, these markers are sequenced alone or coupled to one or two others. The most frequent are genes coding for lovesongs: period (Bauzer et al., 2002a,b; Mazzoni et al., 2002, 2006, 2008; Araki et al., 2009; Salomon et al., 2010; Vigoder et al., 2010) and cacophony (Oliveira et al., 2001; Lins et al., 2002; Bottecchia et al., 2004; Mazzoni et al., 2008; Depaquit et al., 2014) of the elongation factor alpha (Esseghir and Ready, 2000; Testa et al., 2002; Absavaran et al., 2009; Mahamdallie et al., 2010; Kasap et al., 2013;

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Valderrama et al., 2014). Other markers have only been used one time each: copulatory courtship songs: (Souza et al., 2004), Reverse transcriptase (Booth et al., 1991), Non-LTR retrotransposons (Booth et al., 1994), para genes: (Lins et al., 2008, 2012), Ca1D (Mazzoni et al., 2008), Rp49 (Mazzoni et al., 2008), maxadilan (Yin et al., 2000) and SP15-Saliva protein (Elnaiem et al., 2005). The countries of origin of the processed sandflies are listed below (Fig. 3). In Europe, processed Phlebotomine sandflies came from the following 13 countries: - Albania (Depaquit et al., 2008b), - Belgium (Depaquit et al., 2005b), - Cyprus: (Esseghir et al., 1997; Aransay et al., 2000; Depaquit et al., 2002, 2005b, 2008b, 2013; Hamarsheh et al., 2007), - France (Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2005b; Esseghir and Ready, 2000; Perrotey et al., 2005; Franco et al., 2010; Mahamdallie et al., 2010; Peyrefitte et al., 2013), - Germany (Depaquit et al., 2005b), - Greece (Booth et al., 1991; Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2002, 2008b, 2013; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Moin-Vaziri et al., 2007a), - Italy (Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2002, 2008b, 2013; Di Muccio et al., 2000; Pesson et al., 2004; Hamarsheh et al., 2007; Ferroglio et al., 2010; Latrofa et al., 2011a,b), - Kosovo (Kruger et al., 2011), - Malta (Booth et al., 1994; Esseghir et al., 1997; Depaquit et al., 2002; Pesson et al., 2004), - Montenegro (Depaquit et al., 2008b), - Portugal (Depaquit et al., 2002; Franco et al., 2010; Mahamdallie et al., 2010), - Spain (Booth et al., 1991, 1994, 1996; Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2002, 2008b; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Pesson et al., 2004; Perrotey et al., 2005; Baron et al., 2008; Franco et al., 2010; Mahamdallie et al., 2010), - Ukraine (Crimea) (Depaquit et al., 2013). In Asia, the sampling included the following 22 countries: - Afghanistan (Esseghir et al., 1997; Kruger et al., 2011; Depaquit et al., 2014), - Azerbaidjan: (Depaquit et al., 2013), - China: (Zhang et al., 2009, 2013), - India (Esseghir et al., 1997; Aransay et al., 2000; Di Muccio et al., 2000; Depaquit et al., 2008b; Manonmani et al., 2010; Kumar et al., 2012; Tiwary et al., 2012),

Asia including Turkey (n=21) Europe (n=13) Africa (n=17) North America (n=1) South America (n=13) Fig. 3. Continents where sandflies have been sampled for molecular taxonomy studies.

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- Iran (Moin-Vaziri et al., 2007a,b; Depaquit et al., 2008b, 2013, 2014; Absavaran et al., 2009; Parvizi et al., 2010a,b; Jafari et al., 2013), - Iraq (Esseghir et al., 1997), - Israel/Palestine (Esseghir et al., 1997; Aransay et al., 2000; Mukhopadhyay et al., 2000; Depaquit et al., 2002, 2005b, 2008b, 2013; Elnaiem et al., 2005; Dvorak et al., 2006, 2011; Hamarsheh et al., 2007; Minter et al., 2013), - Jordan (Elnaiem et al., 2005; Hamarsheh et al., 2007; Minter et al., 2013), - Lebanon (Depaquit et al., 1999, 2000, 2002, 2005b, 2008b; Moin-Vaziri et al., 2007a), - Malaysia (Khadri et al., 2008), - Oman (Depaquit et al., 2000, 2008b, 2014), - Pakistan (Depaquit et al., 1998, 1999, 2000, 2002; Moin-Vaziri et al., 2007a), - the Philippines (Léger et al., 2012, 2014), - Saudi Arabia (Esseghir et al., 1997; Elnaiem et al., 2005; Depaquit et al., 2008b), - Sri Lanka (Gajapathy et al., 2013), - Syria (Booth et al., 1991; Esseghir et al., 1997; Depaquit et al., 2000, 2002, 2008b; Hamarsheh et al., 2007; Moin-Vaziri et al., 2007a; Dvorak et al., 2011), - Thailand (Muller et al., 2007; Depaquit et al., 2009), - Turkmenistan (Depaquit et al., 2000), - Turkey (Depaquit et al., 2002, 2008b; Dvorak et al., 2006, 2011; Hamarsheh et al., 2007; Moin-Vaziri et al., 2007a; Belen et al., 2011; Kasap et al., 2013; Minter et al., 2013), - Uzbekistan (Dvorak et al., 2011; Depaquit et al., 2014), - Yemen (Depaquit et al., 2008b). A total of 17 African countries provided Phlebotomine sandflies for molecular taxonomy: - Algeria (Bounamous et al., 2008, 2014; Depaquit et al., 2008b, 2013, 2014; Franco et al., 2010), - Benin (Depaquit et al., 2014), - Burkina Faso: (Depaquit et al., 2005a, 2008b), - Cameroon (Depaquit et al., 2014), - the Comoros (Randrianambinintsoa et al., 2012), - Egypt (Booth et al., 1991; Esseghir et al., 1997; Depaquit et al., 2000, 2002, 2008b, 2014; Esseghir and Ready, 2000; Elnaiem et al., 2005; Hamarsheh et al., 2007; Khalid et al., 2012; Minter et al., 2013), - Ethiopia (Esseghir et al., 1997; Esseghir and Ready, 2000; Seblova et al., 2013), - the Republic of Guinea (Depaquit et al., 2014), - Kenya (Mukhopadhyay et al., 2000; Esseghir et al., 1997; Depaquit et al., 1998, 2000, 2008b; Esseghir and Ready, 2000), - Madagascar (Depaquit et al., 2004a,b, 2007, 2008a; Randrianambinintsoa et al., 2012, 2013; Randrianambinintsoa and Depaquit, 2013), - Mali (Khalid et al., 2010), - Morocco (Esseghir et al., 1997; Di Muccio et al., 2000; Depaquit et al., 2002; Pesson et al., 2004; Yahia et al., 2004; Hamarsheh et al., 2007; Moin-Vaziri et al., 2007a; Baron et al., 2008; Franco et al., 2010; Mahamdallie et al., 2010), - Namibia (Depaquit et al., 1999), - Senegal (Booth et al., 1991; Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2000, 2008b, 2013, 2014; Lins et al., 2002; Mazzoni et al., 2002), - the Seychelles (Depaquit et al., 2014), - Sudan (Khalid et al., 2010, 2012; Depaquit et al., 2014), - Tunisia (Esseghir et al., 1997; Esseghir and Ready, 2000; Pesson et al., 2004; Hamarsheh et al., 2007; Bounamous et al., 2008; Depaquit et al., 2008b; Boudabous et al., 2012).

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An important number of studies included sandflies from the following latin American countries: - Argentina (Salomon et al., 2010), - Brazil (Booth et al., 1991, 1996; Marcondes et al., 1997; Depaquit et al., 1998, 1999; Dias et al., 1998; Yin et al., 2000; Oliveira et al., 2001; Soto et al., 2001; Arrivillaga et al., 2002, 2003; Bauzer et al., 2002a,b; Hodgkinson et al., 2002, 2003; Lins et al., 2002, 2008, 2012; Mazzoni et al., 2002, 2006, 2008; Maingon et al., 2003; Bottecchia et al., 2004; Margonari et al., 2004; Souza et al., 2004; Meneses et al., 2005; de Queiroz Balbino et al., 2006; de Souza Rocha et al., 2007; Araki et al., 2009, 2013; Vigoder et al., 2010; Scarpassa and Alencar, 2012, 2013; Minter et al., 2013; Santos et al., 2013), - Colombia (Dias et al., 1998; Yin et al., 2000; Soto et al., 2001; Arrivillaga et al., 2002, 2003; Testa et al., 2002; Beati et al., 2004; Vivero et al., 2007, 2009; Perez-Doria et al., 2008a; Bejarano et al., 2009; Hoyos et al., 2012; Contreras Gutierrez et al., 2014), - Costa Rica (Dias et al., 1998; Yin et al., 2000; Arrivillaga et al., 2002, 2003), - Ecuador: (Terayama et al., 2008; Kuwahara et al., 2009; Zapata et al., 2012a,b), - Honduras (Soto et al., 2001; Arrivillaga et al., 2002, 2003), - Guatemala (Soto et al., 2001), - Mexico (Aransay et al., 2000; Pech-May et al., 2013), - Nicaragua: (Arrivillaga et al., 2003), - Panama (Azpurua et al., 2010; Valderrama et al., 2014), - Peru (Beati et al., 2004; Kuwahara et al., 2009; Cohnstaedt et al., 2012; Yamamoto et al., 2013), - Venezuela (Adamson et al., 1993; Maingon et al., 1993; Depaquit et al., 1998; Soto et al., 2001; Arrivillaga et al., 2002, 2003; Torgerson et al., 2003; Watts et al., 2005). In North America, three studies included sandflies from the USA (Florin et al., 2010, 2011; Minter et al., 2013) whereas no study included sandflies from Oceania. The total number of species and subspecies processed for molecular systematics is 177 on a total of 911 living species living actually described (excluding fossil species) according to the main reviews for the Old and New World sandflies respectively (Galati, 2013; Seccombe et al., 1993). This review also includes some new species described from Madagascar and in other countries without being exhaustive (Table 2). In the Old World, many species of the genus Phlebotomus have been sequenced whereas a few Sergentomyia, Grassomyia, Chinius and Idiophlebotomus have been processed. Some confidential genera have not been sequenced yet (Table 2). The analysis of the species processed in the genera Phlebotomus and Sergentomyia has been carried out at a subgeneric level which can probably be considered as of generic level regarding to the American systematics we consider as valid (Galati, 2013). The four species of the subgenus Phlebotomus have been sequenced: Phlebotomus papatasi (Booth et al., 1991, 1994; Esseghir et al., 1997; Aransay et al., 2000; Depaquit et al., 2000, 2005b, 2008b; Di Muccio et al., 2000; Esseghir and Ready, 2000; Mukhopadhyay et al., 2000; Elnaiem et al., 2005; Hamarsheh et al., 2007; Khalid et al., 2010, 2012; Manonmani et al., 2010; Belen et al., 2011; Kruger et al., 2011; Latrofa et al., 2011a,b; Tiwary et al., 2012; Minter et al., 2013), Phlebotomus duboscqi (Booth et al., 1991; Esseghir et al., 1997; Depaquit et al., 1998, 1999, 2000, 2008b; Esseghir and Ready, 2000; Mukhopadhyay et al., 2000; Lins et al., 2002; Mazzoni et al., 2002; Khalid et al., 2010), Phlebotomus bergeroti (Esseghir et al., 1997; Esseghir and Ready, 2000; Depaquit et al., 2008b; Khalid et al., 2010;

Bounamous et al., 2014) and Phlebotomus salehi (Depaquit et al., 2008b). Many species of the subgenus Paraphlebotomus have been processed including the type-species Phlebotomus sergenti (Depaquit et al., 1998, 1999, 2000, 2002; Aransay et al., 2000; Esseghir and Ready, 2000; Yahia et al., 2004; Dvorak et al., 2006, 2011; MoinVaziri et al., 2007a; Bounamous et al., 2008, 2014; Belen et al., 2011; Kruger et al., 2011; Jafari et al., 2013), Phlebotomus alexandri (Aransay et al., 2000; Depaquit et al., 2000; Bounamous et al., 2008, 2014; Kruger et al., 2011), Phlebotomus caucasicus (Moin-Vaziri et al., 2007b; Parvizi et al., 2010b; Kruger et al., 2011; Jafari et al., 2013), Phlebotomus chabaudi (Esseghir and Ready, 2000; Bounamous et al., 2008, 2014), Phlebotomus riouxi (Bounamous et al., 2008, 2014), Phlebotomus mireillae (Depaquit et al., 1998, 2000), Phlebotomus saevus (Depaquit et al., 2000), Phlebotomus jacusieli (Depaquit et al., 2000), Phlebotomus kazeruni (Depaquit et al., 2000), Phlebotomus similis (Depaquit et al., 2000; MoinVaziri et al., 2007a), Phlebotomus andrejevi (Depaquit et al., 2000), and Phlebotomus mongolensis (Depaquit et al., 2000; Parvizi et al., 2010b). Only one species of the subgenus Synphlebotomus has been processed: Phlebotomus ansarii (Jafari et al., 2013). The subgenus Larroussius has been well explored by inclusion of Phlebotomus ariasi (Esseghir et al., 1997; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Franco et al., 2010; Mahamdallie et al., 2010; Bounamous et al., 2014), Phlebotomus betisi (Khadri et al., 2008), Phlebotomus chadlii (Franco et al., 2010; Bounamous et al., 2014), Phlebotomus keshishiani (Kruger et al., 2011), Phlebotomus langeroni (Booth et al., 1991; Esseghir and Ready, 2000), Phlebotomus longicuspis (Di Muccio et al., 2000; Esseghir and Ready, 2000; Pesson et al., 2004; Depaquit et al., 2005a; Boudabous et al., 2012; Bounamous et al., 2014), Phlebotomus major group (Depaquit et al., 1998, 1999; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Absavaran et al., 2009; Parvizi et al., 2010a; Kruger et al., 2011; Latrofa et al., 2011a,b; Kasap et al., 2013), Phlebotomus orientalis (Esseghir and Ready, 2000; Seblova et al., 2013), Phlebotomus perfiliewi s. l. (Booth et al., 1991; Esseghir et al., 1997; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Parvizi et al., 2010a; Kruger et al., 2011; Latrofa et al., 2011a,b; Depaquit et al., 2013; Bounamous et al., 2014), Phlebotomus perniciosus (Booth et al., 1991, 1994; Esseghir et al., 1997; Depaquit et al., 1998, 1999; Aransay et al., 2000, 2003; Di Muccio et al., 2000; Esseghir and Ready, 2000; Pesson et al., 2004; Perrotey et al., 2005; Ferroglio et al., 2010; Latrofa et al., 2011a,b; Boudabous et al., 2012; Peyrefitte et al., 2013; Bounamous et al., 2014), and Phlebotomus tobbi: (Booth et al., 1991, 1994, 1996; Esseghir et al., 1997; Aransay et al., 2000; Di Muccio et al., 2000; Esseghir and Ready, 2000; Absavaran et al., 2009; Parvizi et al., 2010a; Belen et al., 2011). The three members of the subgenus Transphlebotomus have been included in molecular studies: Phlebotomus mascittii (Depaquit et al., 2005b), Phlebotomus economidesi (Depaquit et al., 2005b), and Phlebotomus canaaniticus (Depaquit et al., 1999, 2005b). Six species of the subgenus Adlerius have been studied: Phlebotomus brevis (Depaquit et al., 1999), Phlebotomus chinensis (Zhang et al., 2009, 2013), Phlebotomus halepensis: (Parvizi et al., 2010a), Phlebotomus sichuanensis (Zhang et al., 2013), Phlebotomus simici (Depaquit et al., 1999; Aransay et al., 2000), Phlebotomus turanicus (Kruger et al., 2011) and one unidentified species: Ph. (Adlerius) sp. (Kruger et al., 2011). Regarding the Anaphlebotomus, five malagasy species which are going to be placed in a new subgenus (Depaquit, personal communication) have been studied: Phlebotomus fertei, Phlebotomus

J. Depaquit / Infection, Genetics and Evolution 28 (2014) 744–756 Table 2 Number of species and subspecies sequenced versus existing taxa (excluding fossils). The classification of Galati (2013) is adopted. Processed HERTIGIINI HERTIGIINA Warileya Hertigia IDIOPHLEBOTOMINA Spelaophlebotomus Idiophlebotomus Chinius PHLEBOTOMINI PHLEBOTOMINA Phlebotomus (Phlebotomus) (Paraphlebotomus) (Synphlebotomus) (Larroussius) (Adlerius) (Transphlebotomus) (Euphlebotomus) (Anaphlebotomus) (Abonnencius) (Kasaulius) AUSTRALOPHLEBOTOMINA Australophlebotomus BRUMPTOMYINA Brumptomyia Oligodontomyia SERGENTOMYINA Sergentomyia (Sergentomyia) (Parrotomyia) (Sintonius) (Rondanomyia) and (Neophlebotomus) (Vattieromyia) (Capensomyia) (Demeillonius) ungrouped Grassomyia Spelaeomyia Parvidens Daenemyia Micropygomyia LUTZOMYINA Sciopemyia Lutzomyia Migonemyia Pintomyia Dampfomyia Expapillata Pressatia Trichopygomyia Evandromyia PSYCHODOPYGINA Psathyromyia Viannamyia Martinsmyia Bichromomyia Psychodopygus Nyssomyia Trichophoromyia UNGROUPED Edentomyia Total number of species and subspecies

Existing

Ratio (%)

2 0

8 1

25 0

0 1 1

2 12 4

0 8 25

46 4 12 1 11 7 3 3 5 0 0

101 4 14 9 29 20 3 11 9 1 1

46 100 86 11 38 35 100 27 56 0 0

0

8

0

6 1

26 3

23 33

24 9 4 3 2 4 0 0 4 2 0 0 0 6

273 47 51 30 60 4 10 1 70 7 4 4 5 58

9 19 8 10 3 100 0 0 6 29 0 0 0 10

2 26 2 18 1 0 2 1 6

8 75 6 61 21 2 8 16 40

25 35 33 30 5 0 25 6 15

9 1 0 2 7 10 2

40 4 11 6 40 18 38

23 25 0 33 18 56 5

0 180

1 911

0 20

berentiensis, Phlebotomus fontenillei (Depaquit et al., 2004b), Phlebotomus vaomalalae (Randrianambinintsoa et al., 2013) and Phlebotomus vincenti (Randrianambinintsoa and Depaquit, 2013). In the subgenus Euphlebotomus, three species have been processed: Phlebotomus argentipes (Aransay et al., 2000; Manonmani et al., 2010; Kumar et al., 2012; Tiwary et al., 2012; Gajapathy et al., 2013), Phlebotomus barguesae (Depaquit et al., 2009) and Phlebotomus mascomai (Muller et al., 2007).

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Regarding the two Asiatic genera Chinius and Idiophlebotomus, we recorded the sequencing of two species: Chinius samarensis (Léger et al., 2012) and Idiophlebotomus padillarum (Léger et al., 2014). Regarding the widely distributed genus Sergentomyia, we recorded sequences of nine species belonging to the subgenus Sergentomyia: Sergentomyia antennata (Bounamous et al., 2014), Sergentomyia dentata (Depaquit et al., 1998, 1999; Aransay et al., 2000), Sergentomyia fallax (Bounamous et al., 2014), Sergentomyia mervynnae (Jafari et al., 2013), Sergentomyia minuta (Esseghir et al., 1997; Depaquit et al., 1999; Aransay et al., 2000; Kruger et al., 2011; Latrofa et al., 2011a,b; Bounamous et al., 2014), Sergentomyia murgabiensis (Kruger et al., 2011), Sergentomyia punjabensis (Kumar et al., 2012), Sergentomyia schwetzi (Bounamous et al., 2014) and Sergentomyia sintoni (Jafari et al., 2013). In the subgenus Sintonius, Sergentomyia clydei (Kruger et al., 2011; Bounamous et al., 2014; Depaquit et al., 2014), Sergentomyia christophersi (Bounamous et al., 2014; Depaquit et al., 2014), and Sergentomyia meilloni (Depaquit et al., 1999) have been processed. A total of four taxa belonging to the subgenus Parrotomyia has been sequenced: Sergentomyia babu (Kumar et al., 2012; Tiwary et al., 2012), Sergentomyia babu insularis (Kumar et al., 2012), Sergentomyia grekovi (Kruger et al., 2011) and one unidentified species recorded as Se. (Parrotomyia) sp. (Kruger et al., 2011). Without taking into account the problems of the definitions and limits of the subgenera Rondanomyia and Neophlebotomus (Léger et al., 2005), only two species belonging to the first group have been processed: Sergentomyia goodmani (Randrianambinintsoa et al., 2012) and its subspecies Sergentomyia goodmani comorensis (Randrianambinintsoa et al., 2012). The four species of the subgenus Vattieromyia have been processed: Sergentomyia anka (Depaquit et al., 2008a; Randrianambinintsoa et al., 2012), Se. namo (Depaquit et al., 2008a; Randrianambinintsoa et al., 2012) Sergentomyia pessoni (Randrianambinintsoa et al., 2012), Sergentomyia sclerosiphon (Depaquit et al., 2008a; Randrianambinintsoa et al., 2012) and four ungrouped Sergentomyia: Sergentomyia majungaensis (Depaquit et al., 2007), Sergentomyia vadhanurensis (Kumar et al., 2012), Sergentomyia bailyi (Kumar et al., 2012) and Sergentomyia huberti (Depaquit et al., 2004a). In the genus Grassomyia, only two species has been processed: Grassomyia dreyfussi turkestanica (Kruger et al., 2011) and Grassomyia dreyfussi (Bounamous et al., 2014). Many papers are related to the molecular systematics of New World sandflies. The species processed belong to the genera: - Bichromomyia: Bichromomyia olmeca (Azpurua et al., 2010) and Bichromomyia flaviscutellata (Beati et al., 2004); - Brumptomyia: Brumptomyia beaupertuyi (Torgerson et al., 2003; Contreras Gutierrez et al., 2014), Brumptomyia devenanzii (Torgerson et al., 2003), Brumptomyia galindoi (Azpurua et al., 2010), Brumptomyia guimareasi (Contreras Gutierrez et al., 2014), Brumptomyia hamata (Azpurua et al., 2010; Contreras Gutierrez et al., 2014) and Brumptomyia mesai (Contreras Gutierrez et al., 2014); - Dampfomyia: Dampfomyia vespertilionis (Azpurua et al., 2010); - Evandromyia: Evandromyia cortelezzi (Beati et al., 2004), Evandromyia dubitans (Vivero et al., 2007), Evandromyia evandroi (Lins et al., 2002), Evandromyia lenti (Lins et al., 2002), Evandromyia sallesi (Kuwahara et al., 2009; Mazzoni et al., 2002) and Evandromyia walkeri (Minter et al., 2013; Contreras Gutierrez et al., 2014); - Lutzomyia: Lutzomyia longipalpis (Booth et al., 1991, 1994; Depaquit et al., 1998, 1999; Dias et al., 1998; Aransay et al., 2000; Yin et al., 2000; Oliveira et al., 2001; Soto et al., 2001; Arrivillaga et al., 2002, 2003; Bauzer et al., 2002a,b;

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Hodgkinson et al., 2002, 2003; Lins et al., 2002, 2008, 2012; Mazzoni et al., 2002; Maingon et al., 2003; Torgerson et al., 2003; Bottecchia et al., 2004; Souza et al., 2004; Watts et al., 2005; de Queiroz Balbino et al., 2006; Vivero et al., 2007; Terayama et al., 2008; Araki et al., 2009, 2013; Salomon et al., 2010; Vigoder et al., 2010; Hoyos et al., 2012; Minter et al., 2013; Pech-May et al., 2013; Santos et al., 2013; Contreras Gutierrez et al., 2014), Lutzomyia ayacuchensis (Beati et al., 2004; Terayama et al., 2008; Kuwahara et al., 2009; Yamamoto et al., 2013), Lutzomyia battistini (Beati et al., 2004; Contreras Gutierrez et al., 2014), Lutzomyia bifoliata (Hoyos et al., 2012), Lutzomyia caballeroi (Beati et al., 2004; Yamamoto et al., 2013), Lutzomyia castanea (Beati et al., 2004; Yamamoto et al., 2013), Lutzomyia cruciata (Hoyos et al., 2012; Pech-May et al., 2013), Lutzomyia cruzi: (Watts et al., 2005; Vigoder et al., 2010; Lins et al., 2012), Lutzomyia hartmanni: (Terayama et al., 2008; Kuwahara et al., 2009; Contreras Gutierrez et al., 2014), Lutzomyia gomezi (Soto et al., 2001; Torgerson et al., 2003; Beati et al., 2004; Vivero et al., 2007, 2009; Terayama et al., 2008; Kuwahara et al., 2009; Azpurua et al., 2010; Hoyos et al., 2012; Contreras Gutierrez et al., 2014; Valderrama et al., 2014), Lutzomyia gonzaloi (Beati et al., 2004), Lutzomyia guderiani (Beati et al., 2004), Lutzomyia lichyi (Contreras Gutierrez et al., 2014), Lutzomyia munaypata (Beati et al., 2004; Yamamoto et al., 2013), Lutzomyia noguchii (Beati et al., 2004; Yamamoto et al., 2013), Lutzomyia peruensis (Beati et al., 2004; Yamamoto et al., 2013), Lutzomyia pescei (Beati et al., 2004), Lutzomyia pseudolongipalpis (Torgerson et al., 2003; Watts et al., 2005), Lutzomyia quillabamba (Beati et al., 2004), Lutzomyia renei (Mazzoni et al., 2002), Lutzomyia sanguinaria (Azpurua et al., 2010), Lutzomyia scorzai (Beati et al., 2004; Contreras Gutierrez et al., 2014), Lutzomyia sherlocki (Beati et al., 2004), Lutzomyia tejadai (Beati et al., 2004), Lutzomyia tortura (Kuwahara et al., 2009) and Lu. sp. (Contreras Gutierrez et al., 2014); Micropygomyia: Micropygomyia absonodonta (Torgerson et al., 2003), Micropygomyia cayennensis (Torgerson et al., 2003; Vivero et al., 2007, 2009; Contreras Gutierrez et al., 2014), Micropygomyia dispar (Lins et al., 2002; Mazzoni et al., 2002), Micropygomyia trinidadensis (Torgerson et al., 2003; Vivero et al., 2007, 2009; Azpurua et al., 2010; Contreras Gutierrez et al., 2014), Micropygomyia venezuelensis (Torgerson et al., 2003) and Micropygomyia vexator (Minter et al., 2013); Migonemyia: Migonemyia dubitans (Vivero et al., 2009; Torgerson et al., 2003) and Migonemyia migonei (Depaquit et al., 1998; Lins et al., 2002; Mazzoni et al., 2002; Torgerson et al., 2003; Beati et al., 2004; Kuwahara et al., 2009; Contreras Gutierrez et al., 2014); Nyssomyia: Nyssomyia anduzei (Scarpassa and Alencar, 2012, 2013), Nyssomyia antunesi (Contreras Gutierrez et al., 2014), Nyssomyia hernandezi (Torgerson et al., 2003), Nyssomyia intermedia (Marcondes et al., 1997; Lins et al., 2002; Mazzoni et al., 2002, 2006, 2008; Meneses et al., 2005; de Souza Rocha et al., 2007; Terayama et al., 2008), Nyssomyia neivai (Marcondes et al., 1997; Terayama et al., 2008), Nyssomyia trapidoi (Terayama et al., 2008; Kuwahara et al., 2009; Azpurua et al., 2010; Contreras Gutierrez et al., 2014), Nyssomyia umbratilis (Lins et al., 2002; Mazzoni et al., 2002; Scarpassa and Alencar, 2012, 2013), Nyssomyia whitmani (Marcondes et al., 1997; Lins et al., 2002; Mazzoni et al., 2002, 2006, 2008; Torgerson et al., 2003; Margonari et al., 2004), Nyssomyia yuilli yuilli (Beati et al., 2004; Contreras Gutierrez et al., 2014) and Nyssomyia yuilli (Beati et al., 2004); Oligodontomyia: Oligodontomyia toroensis (Terayama et al., 2008);

- Pintomyia: Pintomyia colombiana (Testa et al., 2002; Contreras Gutierrez et al., 2014), Pintomyia evansi (Testa et al., 2002; Vivero et al., 2007, 2009; Bejarano et al., 2009; Contreras Gutierrez et al., 2014), Pintomyia fisheri (Beati et al., 2004), Pintomyia longiflocosa (Contreras Gutierrez et al., 2014), Pintomyia maranonensis (Beati et al., 2004; Yamamoto et al., 2013), Pintomyia nevesi (Beati et al., 2004; Kuwahara et al., 2009; Yamamoto et al., 2013), Pintomyia nuneztovari (Beati et al., 2004; Terayama et al., 2008; Contreras Gutierrez et al., 2014), Pintomyia ovallesi (Testa et al., 2002; Torgerson et al., 2003; Beati et al., 2004; Azpurua et al., 2010), Pintomyia pia (Perez-Doria et al., 2008a; Contreras Gutierrez et al., 2014), Pintomyia rangeliana (Torgerson et al., 2003; Vivero et al., 2007, 2009), Pintomyia robusta (Beati et al., 2004; Yamamoto et al., 2013), Pintomyia serrana (Beati et al., 2004; Terayama et al., 2008; Kuwahara et al., 2009), Pintomyia spinicrassa (Adamson et al., 1993; Maingon et al., 1993; Contreras Gutierrez et al., 2014), Pintomyia tejadai (Yamamoto et al., 2013), Pintomyia tihuiliensis: (Perez-Doria et al., 2008a), Pintomyia townsendi: (Maingon et al., 1993; Testa et al., 2002; Torgerson et al., 2003), Pintomyia verrucarum (Beati et al., 2004; Terayama et al., 2008; Cohnstaedt et al., 2012; Yamamoto et al., 2013) and Pintomyia youngi: (Adamson et al., 1993; Maingon et al., 1993; Depaquit et al., 1998; Testa et al., 2002; Contreras Gutierrez et al., 2014); - Pressatia: Pressatia camposi (Azpurua et al., 2010) and Pressatia dysponeta (Kuwahara et al., 2009; Azpurua et al., 2010); - Psathyromyia: Psathyromyia abonnenci (Torgerson et al., 2003), Psathyromyia aclydifera (Azpurua et al., 2010), Psathyromyia barrettoi barrettoi (Kuwahara et al., 2009), Psathyromyia barrettoi majuscula (Contreras Gutierrez et al., 2014), Psathyromyia carpenteri (Azpurua et al., 2010; Contreras Gutierrez et al., 2014), Psathyromyia coutinhoi (Contreras Gutierrez et al., 2014), Psathyromyia punctigeniculata (Torgerson et al., 2003), Psathyromyia runoides (Azpurua et al., 2010) and Psathyromyia shannoni (Torgerson et al., 2003; Kuwahara et al., 2009; Florin et al., 2010, 2011; Minter et al., 2013; Contreras Gutierrez et al., 2014); - Psychodopygus: Psychodopygus carrerai thula (Azpurua et al., 2010; Contreras Gutierrez et al., 2014), Psychodopygus corossoniensis (Zapata et al., 2012a), Psychodopygus francoisleponti (Zapata et al., 2012a), Psychodopygus luisleoni (Zapata et al., 2012a), Psychodopygus geniculatus (Beati et al., 2004; Terayama et al., 2008; Zapata et al., 2012a), Psychodopygus guyanensis (Azpurua et al., 2010), and Psychodopygus panamensis (Torgerson et al., 2003; Vivero et al., 2007, 2009; Terayama et al., 2008; Kuwahara et al., 2009; Azpurua et al., 2010; Contreras Gutierrez et al., 2014); - Sciopemyia: Sciopemyia sordellii (Contreras Gutierrez et al., 2014) and Sciopemyia vattierae (Terayama et al., 2008); - Trichophoromyia: Th reburra: (Kuwahara et al., 2009; Contreras Gutierrez et al., 2014) and sp. (Beati et al., 2004); - Trichopygomyia: Trichopygomyia triramula (Azpurua et al., 2010; Contreras Gutierrez et al., 2014); - Viannamyia: Viannamyia tuberculata (Beati et al., 2004); - Warileya: Warileya rotundipennis (Contreras Gutierrez et al., 2014) and Warileya phlebotomanica (Yamamoto et al., 2013). 4. Discussion The taxonomic problems in many groups of insect vectors have been detailed in general by Lane and Crosskey (1995) who distinguished three categories: 1. Minute arthropods that require careful preparation before identification is possible. It applies to Phlebotomine sand flies.

J. Depaquit / Infection, Genetics and Evolution 28 (2014) 744–756

2. Species that can be easily distinguished but only during a single life stage. It applies to Phlebotomine sand flies, not about the life stage (sensu larvae versus imago) but according to the genders taking into account that in many groups, males or females can be indistinguishable. 3. Closely related but reproductively isolated species that are morphologically identical, corresponding to cryptic species. The latter item is easily linkable to the concept of species complexes well known for many Phlebotomine sandflies from the Old World and the New World (Marcondes et al., 1997; Testa et al., 2002; Pesson et al., 2004; Zapata et al., 2012a; Depaquit et al., 2013). For systematicians, species complexes include in fact populations closely related morphologically but remaining identifiable, able to live in sympatry. For geographically segregated populations, the status of subspecies, commonly used in the past (Abonnenc, 1972) has curiously completely disappeared after 1980, the taxa described during the last three decades have been ranked to the specific level. The only exception to our knowledge is in the genus Sergentomyia (Randrianambinintsoa et al., 2012). The species complexes have been well characterized: ‘‘When two populations of a species become reproductively isolated either through geographic separation or as a consequence of the evolution (. . .) isolation mechanisms, they gradually accumulate genetic differences. Given sufficient time, these genetic differences may eventually become manifest as subtle morphological differences. Over an extended time, these may become manifest as distinct morphological differences. However, character differences arising from recent or incipient (ongoing) reproductive isolation are frequently difficult to use in routine identification. Closely related but reproductively isolated species that appear morphologically identical are often referred to as cryptic or sibling species, and a group of cryptic species is referred to as a species complex’’ (Black and Munstermann, 2004). Talking about systematics cannot be considered without first talking about species, which is the basic unit of the systematics. The concept of species is indefinable in general (Lherminier and Solignac, 2005). Concerning Phlebotomine sandflies, this concept is mostly based on two former concepts. The first is the similarity (which may apply between individuals of the same gender but also between males and females with adaptation e.g., genitalias: length of male genital filaments – length of spermathecal ducts). It is true for a majority of species. The second concept is related to the fertility of the specimens. However, it is rarely tested in sandflies taxonomy because of the difficulty to colonize these insects. Moreover, this concept is wrong regarding introgression phenomena demonstrated or strongly suspected and probably largely underestimated in sandflies. Lastly, how could we apply this concept to the probable parthenogenesis of the cave dweller Deanemyia maruaga (Alves et al., 2011)? Ultimately, the feeling of the taxonomist drives the systematics of the group. An important question remains unanswered: should population genetics be regarded as a part of molecular systematics? To our opinion, it cannot. The population genetics is the study of the distribution and changes of allele frequencies in populations of living organisms. A population means any set of individuals of the same species cohabiting in the same geographical area and genetically related to each other. Based on the Hardy–Weinberg equilibrium, considering that frequencies of alleles and genotypes do not vary over generations, population genetics applies the principles of Mendelian genetics at the level of populations of individuals belonging to the same species. Despite the use of common methods (sequencing of DNA markers), population genetics cannot be confused with taxonomy, as molecular as they could be. However, the boundaries between molecular systematics concerning closely related species, the discovery of cryptic species or intraspecific taxa, and population genetics is sometimes difficult to define

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because population genetics also estimates the genetic diversity intra-population, delimits populations and defines the level and the limit of gene flow among subpopulations. By the way, population genetics studies are intraspecific, and need markers having a fast evolution rate and more specimens per each location than in the molecular systematics studies. The goal of the study indicates the method: the study of frequencies of alleles in a population refers to population genetics whereas a molecular approach, mainly conducted on several independent markers to individualize populations in a species or between species, and not to emphasize a gene flow, refers to molecular systematics. The literature related to sandflies molecular systematics shows that a few papers (Fig. 1) focus on alpha taxonomy. In this field, molecular tools are not irreplaceable because many studies have been made exclusively on morphological characters. In the foci of leishmaniases endemicity, the vector species inventory is often well known, and correct identifications are obtained by local epidemiologists who well know the local fauna, without the need of specialized taxonomists. The power of molecular tools to emphasize and understand these complexes of species is obvious. Therefore, not surprisingly, the main studies focus on intraspecific systematics (Fig. 1). Sequencing of variable molecular markers in closely related specimens will provide many informative characters. Phenetic or phylogenetic systematics? Presently, phylogenies are fashionable and also for sand fly specialists do not escape this tendency. The use of softwares is easy and several packages allow different analyses like Neighbor-Joining, maximum parsimony and maximum likelihood. The results are trees but the trees built using Neighbor-Joining are phenograms. They show similarities between taxa and because the characters are not polarized (plesiomorphies versus apomorphies), they cannot be considered as phylogenetic trees. Many confusions generated by the use of concepts and different methods often come from the fact that the topologies of the trees obtained by Neighbor-Joining are often identical to those obtained by parsimony. Nevertheless, the vocabulary used by the authors selecting the Neighbor-Joining must be adapted. A major advantage of the molecular systematics is the opportunity to immediately compare our own sequences with those from Genbank. It is easier to do than to arrange the loan of slides. But, it highlights the need for accurate identification of specimens. Now, the apology of the molecular approaches will inevitably decrease the number of specialists able to correctly identify the sandflies. Those who are still active are in general more than 50 years old and many of them are already retired. What will be this situation after 2030? Everything is done in the scientific community to prefer molecular approaches to morphological ones. An awareness of researchers, editors of scientific journals, and reviewers and publishers is therefore urgently needed to encourage studies carried out on morphological approaches. In the analysis of the publications of molecular systematics related to sandflies, the most studied species are three major proven vectors of leishmaniases Ph. papatasi, P. perniciosus and Lu. longipalpis. Other proven vectors like Ph. sergenti, Ph. tobbi, Ph. major group, Ph. perfiliewi, Ph. duboscqi, Lu gomezi, Mi migonei, Ny. intermedia, Ny. trapidoi, Ny. umbratilis, Ny. whitmani, Ps. panamensis were included in some studies of molecular systematics. Some proven vectors were included only in a few studies like Ph. ariasi, Ph. argentipes, even one like Bi. flaviscutellata or Bi. olmeca. Obviously, the ratio of species sampled for molecular systematics studies is high for vector groups and low for species not involved in the transmission of leishmaniasis or considered as such (Table 2). In the Old World, 46% of species of the genus Phlebotomus resulted in molecular systematics against only 9% of the Sergentomyia. This constitutes an error. In a recent past, species like Se. gemmea,

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Se. dubia, Sa darlingi appeared as suspected vectors of L. siamensis, L. infantum and L. major, respectively (Senghor et al., 2011; Berdjane-Brouk et al., 2012; Kanjanopas et al., 2013) whereas Se. minuta was suspected in the transmission of the virus Toscana (Charrel et al., 2006). Regarding the countries of origin of the sandflies processed in the molecular systematics papers come from, it appears that the countries providing the greatest number of specimens for these studies are endemic for leishmaniases (Alvar et al., 2012): Brazil, Colombia, Venezuela in the New World, Egypt, France, Greece, Iran, Israel/Palestine, Italy, Morocco, Senegal, Spain or Turkey in the Old World. Countries from areas free of leishmaniases provided no or a few specimens, with the exception of Madagascar due to an important program of systematics of sandflies in this country. However, it is a reality that in the field of phylogenetic or phenetic approaches, molecular biology is easier to apply than morphology. In fact, a few morphological studies have been carried out (Galati, 2013,1995; Rispail and Léger, 1998a,b). The morphological approach needs a long and careful implementation which can only be performed by experienced specialists. The main difficulty is the selection of characters corresponding to the hypothesis of primary homology necessary for the development of any matrix. The temptation is to reduce the number of characters. In an assay, six genital characters only, probably subject to homoplasy events, were selected for the cladistic analysis of 32 Old World taxa (Ilango, 2010). 4.1. Perspectives The molecular systematics of the main vectors has been studied for intraspecific variability and also to compare them to closely related species using highly variable markers. In the future, there will be the need to associate at least two independent markers, including at least one non-mitochondrial. The mitochondrial markers are very commonly used for the systematics of Phlebotomine sandflies (Fig. 1), because (i) they are easily amplified and, because (ii) they are haploids, their sequences can be obtained without cloning, (iii) their slow evolutionary rate is of interest for population studies and (iv) their low recombination suggests they have the same history as the taxa. However, mtDNA evolution is not sufficiently neutral to be considered as a marker for genomic history (Ballard and Whitlock, 2004). Moreover, the effects of inherited symbionts in populations, phylogeographic and phylogenetic studies were reviewed. Direct and indirect selection is sufficiently common to make inferences from mtDNA data unreliable (Hurst and Jiggins, 2005). The later authors noted that (i) a single population may be infected with more than one strain or species of parasitic inherited microorganism, (ii) different Populations may show different infection statuses and (iii) inherited micro-organisms could influence the mtDNA sequences of their hosts. The use of mtDNA markers alone to explore phylogenetic relationships between closely related taxa is considered as questionable (Azpurua et al., 2010) or as unsafe and dangerous (Hurst and Jiggins, 2005), especially according to the existence of introgression in Phlebotomine sandflies. Moreover, mitochondrial DNA sequences are not good candidates to molecular clock (Galtier et al., 2009). Safe data well characterizing species will serve as identification tools by sequencing or to apply techniques as RFLP. The latter have to be used to distinguish closely related species and not to distinguish species very easy to identify (Latrofa et al., 2011a; Tiwary et al., 2012; Minter et al., 2013). We regret the lack of a molecular systematics of the whole Phlebotominae in the literature. It will be important to compare the morphological (Galati, 2013, 1995; Rispail and Léger, 1998a,b) and future molecular hypotheses in order to confirm

the position of some taxa like Chinius, Australophlebotomus, Abonnencius, Legeromyia, Daenemyia, Micropygomyia and Edentomyia. This work will also be useful to help the choice of out-groups for the future molecular studies carried out on Phlebotomine sandflies. Lastly, it will be difficult or impossible to replace the traditional morphological identification by molecular systematics because the former is the base for all studies, including the molecular approaches. I believe that integrative taxonomy should be ideal in the future to apply, and especially to the more complex groups of Phlebotomine sandflies. Acknowledgements We thank Nicole Léger for fruitful discussions and Sylvette Gobert for proofreading this manuscript. References Abonnenc, E., 1972. Les phlébotomes de la région éthiopienne (Diptera, Psychodidae). Cah. ORSTOM Sér. Ent. Méd. Parasitol. 55, 239. Absavaran, A., Rassi, Y., Parvizi, P., Oshaghi, M., Abaie, M., Rafizadeh, S., Mohebali, M., Zarea, Z., Javadian, E., 2009. Identification of sand flies of the subgenus Larroussius based on molecular and morphological characters in North Western Iran. Iran J. Arthropod Borne Dis. 3, 22–35. Adamson, R.E., Chance, M.L., Ward, R.D., Feliciangeli, D., Maingon, R.D., 1991. Molecular approaches applied to the analysis of sympatric sandfly populations in endemic areas of western Venezuela. Parassitologia 33 (Suppl.), 45–53. Adamson, R.E., Ward, R.D., Feliciangeli, M.D., Maingon, R., 1993. The application of random amplified polymorphic DNA for sandfly species identification. Med. Vet. Entomol. 7, 203–207. Alvar, J., Velez, I.D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., den Boer, M., 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671. Alves, V.R., Freitas, R.A., Santos, F.L., Barrett, T.V., 2011. Diversity of sandflies (Psychodidae: Phlebotominae) captured in sandstone caves from Central Amazonia, Brazil. Mem. Inst. Oswaldo Cruz 106, 353–359. Araki, A.S., Vigoder, F.M., Bauzer, L.G., Ferreira, G.E., Souza, N.A., Araujo, I.B., Hamilton, J.G., Brazil, R.P., Peixoto, A.A., 2009. Molecular and behavioral differentiation among Brazilian populations of Lutzomyia longipalpis (Diptera: Psychodidae: Phlebotominae). PLoS Negl. Trop. Dis. 3, e365. Araki, A.S., Ferreira, G.E., Mazzoni, C.J., Souza, N.A., Machado, R.C., Bruno, R.V., Peixoto, A.A., 2013. Multilocus analysis of divergence and introgression in sympatric and allopatric sibling species of the Lutzomyia longipalpis complex in Brazil. PLoS Negl. Trop. Dis. 7, e2495. Aransay, A.M., Scoulica, E., Tselentis, Y., Ready, P.D., 2000. Phylogenetic relationships of phlebotomine sandflies inferred from small subunit nuclear ribosomal DNA. Insect Mol. Biol. 9, 157–168. Aransay, A.M., Ready, P.D., Morillas-Marquez, F., 2003. Population differentiation of Phlebotomus perniciosus in Spain following postglacial dispersal. Heredity 90, 316–325. Arrivillaga, J.C., Rangel, Y.N., Oviedo, M., Feliciangeli, M.D., 2000. Correlated morphologic and genetic diversity among Lutzomyia longipalpis (Diptera: Psychodidae) collections in Venezuela. J. Am. Mosq. Control. Assoc. 16, 171– 174. Arrivillaga, J.C., Norris, D.E., Feliciangeli, M.D., Lanzaro, G.C., 2002. Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infect. Genet. Evol. 2, 83–95. Arrivillaga, J., Mutebi, J.P., Pinango, H., Norris, D., Alexander, B., Feliciangeli, M.D., Lanzaro, G.C., 2003. The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. J. Med. Entomol. 40, 615–627. Arrivillaga, J., Marrero, R., 2009. Dos nuevas poblaciones de Lutzomyia pseudolongipalpis Arrivillaga y Feliciangeli (Diptera: Phlebotominae) vector de leishmaniasis visceral en Venezuela. Neotrop. Entomol. 38, 556–559. Azpurua, J., De La Cruz, D., Valderama, A., Windsor, D., 2010. Lutzomyia sand fly diversity and rates of infection by Wolbachia and an exotic Leishmania species on Barro Colorado Island, Panama. PLoS Negl. Trop. Dis. 4, e627. Ballard, J.W., Whitlock, M.C., 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729–744. Baron, S., Martin-Sanchez, J., Gallego, M., Morales-Yuste, M., Boussaa, S., MorillasMarquez, F., 2008. Intraspecific variability (rDNA ITS and mtDNA Cyt b) of Phlebotomus sergenti in Spain and Morocco. Acta Trop. 107, 259–267. Bauzer, L.G., Gesto, J.S., Souza, N.A., Ward, R.D., Hamilton, J.G., Kyriacou, C.P., Peixoto, A.A., 2002a. Molecular divergence in the period gene between two putative sympatric species of the Lutzomyia longipalpis complex. Mol. Biol. Evol. 19, 1624–1627. Bauzer, L.G., Souza, N.A., Ward, R.D., Kyriacou, C.P., Peixoto, A.A., 2002b. The period gene and genetic differentiation between three Brazilian populations of Lutzomyia longipalpis. Insect Mol. Biol. 11, 315–323.

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Molecular systematics applied to Phlebotomine sandflies: review and perspectives.

A review of the literature related to the molecular systematics of the Phlebotomine sandflies (Diptera, Psychodidae) is proposed. It shows that molecu...
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