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Keywords:

  • Phlebotominae;
  • sand flies;
  • taxonomy;
  • species concepts;
  • vectorial traits;
  • ecological traits;
  • leishmaniasis

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED

I review species concepts, the taxonomy of phlebotomine sand flies, and some transmission cycles of leishmaniasis in order to illustrate the difficulties of classifying these vectors in a way that will be ideal both for medical parasitologists and sand fly specialists. Choices will have to be made between different classifications, either maintaining a practical one containing few vectorial genera (mostly Phlebotomus for the Old World and Lutzomyia for the Neotropics) or changing the generic names of many vectors so that the classification represents an evolutionary hypothesis. However, sand flies also transmit arboviruses and members of other sand fly genera bite humans, and so vectorial status alone might not provide the criteria for recognizing only a few genera. Vectorial roles are often determined by species-level co-evolution of susceptibility to Leishmania species, with selection being initiated and maintained by ecological contacts. There is only imperfect co-cladogenesis of genus-level groups or subgeneric complexes of sand flies and Leishmania species. Natural hybridization between sand fly species has been recorded in several species complexes, and this highlights the need to focus on gene flow and the distribution of phenotypes of biomedical importance, not on taxa.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED

In this paper I wish to explore what medical parasitologists, including entomologists, should expect from the taxonomy of phlebotomine sand flies (Diptera, Nematocera, Psychodidae, Phlebotominae). The discovery of morphologically similar sibling species of mosquitoes and black flies stimulated the application of cytological (White and Killick-Kendrick 1975), morphometric (Lane and Ready 1985), alloenzyme (Dujardin et al. 1996), and molecular (Ready et al. 1997) techniques for investigating species complexes of sand flies. However, the history of the research on these vectors differs significantly. For example, taxonomic and evolutionary research on the Anopheles gambiae Giles and Simulium damnosum Theobald complexes was prompted by observing phenotypic differences of epidemiological importance, respectively the recognition of varying degrees of zoophily and endophily (Davidson and White 1972, Pennetier et al. 2010) or preferences for forested and savannah ecotopes (Post et al. 2007). In contrast, phenotypic differences have usually been sought between sand fly species only after they have been proposed to be members of a species complex. I suggest that this has led to unrealistic expectations being placed on sand fly taxonomy.

Species concepts

Based on the reviews in Wheeler and Meier (2000), it can be argued that there are three broad categories of species concept: the taxonomic, which is usually based on morphology and therefore often confused with the morphological species concept; the evolutionary (Simpson 1961), which is often applied as the phylogenetic species concept (Cracraft 1983) by using software such as PAUP (Swofford 2002) to discover synapomorphic characters, that is to say those that are shared and derived; and the biological (Mayr 1969), which is based on reproductive isolation. The medical parasitologist should not expect all taxonomic species to be biological species and should realize that it is only the latter that usually provide barriers to gene flow and the sharing of biomedically important phenotypes or traits. Taxonomic species can be valid names, if described correctly using a designated type specimen and following other rules of zoological nomenclature (ICZN 2010), and yet they may not be good biological species or even phylogenetic species. Often, however, taxonomic species are also good phylogenetic species, because an experienced taxonomist tends to search intuitively for synapomorphic morphological characters, rather than a small combination of ancestral characters that might be diagnostic only for local populations.

Are we trying to predict vectorial and ecological traits, or aiming to identify phylogenetic species?

Medical parasitologists should guard against treating every diagnosable local population of a vector as a species. Local populations may be diagnosable by a unique combination of selectively neutral characters, making them a phylogenetic species or subspecies, but they might share all or many traits of biomedical importance because of recent ancestry or periodic interbreeding. Such traits might be shared by two populations that are good phylogenetic or biological species most of the time but occasionally interbreed to produce some inter-specific gene flow. For example, there is a low rate of interbreeding between members of the An. gambiae complex in Africa (Wang-Sattler et al. 2007), sufficient for insecticide resistance genes (Weill et al. 2000, Munhenga et al. 2008) to pass between the species and then spread geographically (Ranson et al. 2009), probably under strong selection pressure.

Insecticide resistance has not been reported as a serious problem for sand flies (WHO 2010), but species boundaries might affect the vectorial competence of regional populations. For example, sand fly morphospecies may be either permissive or specific vectors of the various species of the protozoan Leishmania (Euglenozoa, Kinetoplastida, Trypanosomatidae), which cause leishmaniasis in humans and other mammals (Bates 2007, Volf and Peckova 2007).

Taxonomy of the phlebotomine vectors of leishmaniasis

Agreement on the number of sand fly genera and their relationships awaits a molecular phylogenetic analysis more extensive than that of Aransay et al. (2000). Even then, practical choices will probably have to be made between different classifications, either maintaining a practical one containing few vectorial genera (Lewis et al. 1977, Seccombe et al. 1993) or changing generic names of many vectors so that the classification represents an evolutionary hypothesis (Abonnenc and Léger 1976, Ready et al. 1980, Galati 1995, 2003). Currently, most medical parasitologists place all the vectors of mammalian leishmaniasis in two genera, Phlebotomus for the Old World (OW) and Lutzomyia for the Neotropics (Ready 2008). However, sand flies also transmit arboviruses, including Phlebovirus causing “sand fly fever”, and members of other sand fly genera bite humans (Seccombe et al. 1993, Young and Duncan 1994). Consequently, vectorial status alone might not provide the justification for recognizing only a few genera.

The most widely used generic classification of sand flies (Lewis et al. 1977) provides a practical means of information storage and retrieval, partly because of its stability over the past fifty years. A phylogenetic classification might better represent the evolutionary relationships of sand fly genera and subgenera. However, it would be surprising if it were to predict the vectorial roles of each permissive and specific vector of all strains of Leishmania and arboviruses, because biomedical traits need not “co-evolve” with species even within a genus. This will now be illustrated by relating the vectorial roles and taxonomy of the sand flies involved in some transmission cycles of leishmaniasis.

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED

The following case studies indicate that vectorial roles are often determined by species-level co-evolution of susceptibility to specific parasites, with selection being initiated and maintained by ecological contacts. There is only an imperfect “evolutionary fit” or co-cladogenesis of genus-level groups or subgeneric complexes of sand flies and Leishmania species (Ready 2000). Table 1 gives additional details of vector incrimination and taxonomy.

Table 1.  Additional details of vector taxonomy and incrimination for the case studies of leishmaniasis transmission cycles, illustrating the imperfect “evolutionary fit” or co-cladogenesis of vectors and parasites. Thumbnail image of

Vectors and ecotopes of cutaneous leishmaniasis in Africa and Asia

The proven vectors of Leishmania major Yakimoff & Schokhor, causative agent of OW zoonotic cutaneous leishmaniasis (ZCL), are all in the subgenus Phlebotomus (Phlebotomus) Rondani & Berté, because of the presence of specific midgut receptors, at least in P. (P.) papatasi and P. (P.) duboscqi (Volf and Peckova 2007), as well as close ecological relationships with the gerbil reservoir hosts. However, members of the subgenus Phlebotomus (Paraphlebotomus) Theodor have also been found infected with Le. major in gerbil burrows in Asia, where foci may only be able to persist if the reservoirs are co-infected with Leishmania turanica Strelkova et al. (1990) transmitted by P. (P.) papatasi (review: Parvizi and Ready 2008). Sympatric transmission of Leishmania tropica (Wright), causative agent of anthroponotic cutaneous leishmaniasis (ACL), is believed to involve only P. (Pa.) sergenti (Parvizi et al. 2008). Given such complexities, it is unclear how any re-arrangement of genus-level groups (“splitting” or “lumping”) would improve the biomedical information content of a sand fly classification.

Biomedically, it is more relevant to assess the vectorial roles of each sand fly species, but not always by anticipating separate roles for morphologically similar taxonomic species. In Iran, it is not known whether P. (Pa.) caucasicus and/or P. (Pa.) mongolensis can be naturally infected with Le. major, because the females are morphologically indistinguishable (Moin-Vaziri et al. 2007). However, there is little point in searching for molecular markers for these two species when they are not proven vectors (perhaps being dead-end hosts) and may not be good biological species, as indicated by mitochondrial introgression (Parvizi et al. 2010). It should be remembered that both species are only taxonomic species, separable on minor morphological variation of the male genitalia that may not be linked to any vectorial trait or reproductive isolation.

Vectors and ecotopes of visceral leishmaniasis in the Mediterranean region and the Neotropics

Zoonotic visceral leishmaniasis (ZVL) is caused by Leishmania infantum Nicolle and was probably imported from the Mediterranean region to the Neotropics in the main reservoir host, the domestic dog, starting in the 15th C AD (Lukes et al. 2007). The proven vectors in the Mediterranean region are all in the subgenus Phlebotomus (Larroussius) (Gallego et al. 2001), but there is mitochondrial introgression between some of them (Pesson et al. 2004) and the geographical distributions of the vectors and the parasite's strains are not correlated. The most widespread neotropical vectors are in the Lutzomyia (Lutzomyia) longipalpis species complex. There have been fascinating evolutionary studies of this complex, including the assessment of reproductive barriers and phenotypic differences of biomedical importance between its sibling species (Lanzaro 2010). However, it is not clear that these differences fall within the realms of taxonomy, partly because there is much gene flow between the sympatric sibling species (Maingon et al. 2008). The limits of a taxonomic classification for predicting vectorial roles are highlighted by finding vectors of Le. infantum in three morphologically distinctive taxa, not only the subgenera P. (Larroussius) and L. (Lutzomyia) but also L. evansi of the neotropical Verrucarum subgeneric group (Montoya-Lerma et al. 2003).

Vectors and ecotopes of neotropical ZCL

Lutzomyia evansi is a vector of Le. infantum in Colombia. However, another species complex (L. townsendi) in the Verrucarum subgeneric group contains vectors of Leishmania (Viannia) braziliensis Vianna, causative agent of much ZCL in the Neotropics, and again mitochondrial introgression has been recorded between sibling species (Testa et al. 2002). The same parasite is transmitted in Brazil by species of the subgenera Lutzomyia (Psychodopygus) Mangabeira and Lutzomyia (Nyssomyia) Barretto (Young and Duncan 1994). One of the latter, L. (Ny.) whitmani, appeared to have different behavioral phenotypes in Amazonia (sylvatic, zoophilic) and southern Brazil (peridomestic, anthropophilic). Not surprisingly, mitochondrial DNA indicated that the phylogeography (or regional phylogenetic speciation) of L. whitmani did not match the distribution of its phenotypes, with anthropophily (Campbell-Lendrum et al. 1999) and endophily (Campbell-Lendrum et al. 2000) varying as much within regional mitochondrial lineages as between them, and with populations fixed for the Amazonian mitochondrial lineage being markedly peridomestic in a recently deforested area of southeast Amazonia (Ready et al. 1998). There was even evidence of gene flow between L. whitmani and a distinctive morphospecies in the same subgenus, namely L. (Ny.) intermedia (Marcondes et al. 1997), which is also a vector of Le. braziliensis.

DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED

The evolutionary history of a group of organisms (Avise 2004) can fascinate its specialists, who usually seek to record this history in a phylogeny. This method of relating species, however, is just one way of classifying them, and it does not always produce a perfect solution (Nelson 1978). A long road is being followed to produce a molecular phylogeny of Phlebotominae based on nuclear ribosomal RNA and mitochondrial genes (M.D. Bargues and J. Dépaquit, personal communication), but these loci do not always produce congruent species phylogenies. The case studies set out above illustrate how general phylogenetic relationships are not always correlated with, and therefore need not predict, the distribution of vectorial and ecological traits among genera, species, and geographical populations of sand flies. For this reason, it is not necessary from a biomedical point of view to make frequent changes to sand fly taxonomy, either at the generic or species level. In fact, such changes are likely to make it more difficult for non-specialists to use a sand fly classification for the storage and retrieval of information, which is aided by stability.

This does not deny the importance of phylogenetic analyses of sand flies and their phenotypic traits. In fact, phylogenetic hypothesis testing is essential for stimulating research aimed at understanding the natural distribution of vectorial and ecological traits. The construction of a well-supported phylogeny of the genera and subgeneric groups of the subfamily Phlebotominae will probably require a super-matrix analysis of several nuclear genes, as reported for Drosophilidae (van der Linde et al. 2010). Such an analysis would provide a firmer basis for co-evolutionary studies of vectors and disease agents, as well as resolving whether or not there should be a general acceptance of the higher taxa proposed by Abonnenc and Léger (1976) and Galati (1995, 2003). My personal view is that the recognition of large numbers of genera is unlikely to be practically useful, even if each genus is shown to be unambiguously monophyletic. Recommendations are expected from the next International Symposium on Phlebotomine Sand flies (ISOPS 7), to be held in Antalya, Turkey, in April 2011.

In the biomedical field, sand fly research requires more genetics at the species level. Population genetics can help to assess the threat of the geographical spread of vectors in relation to climate and other environmental change, both past (Mahamdallie et al. 2010) and present (Ready 2008, 2010). More should be known about the inheritance not only of sand fly susceptibility to Leishmania strains (Wu and Tesh 1990) and any sand fly-induced modifications of the parasite's secretory gel that affect infectivity to mammals (Rogers et al. 2009), but also of salivary peptides that can either protect against or exacerbate leishmaniasis (Warburg et al. 1994, Oliveira et al. 2008). It can be helpful to agonize occasionally over the number of siblings in a species complex and whether or not they should be formally described as taxonomic species (Pesson et al. 2004), but only if this gives us timely reminders that species often have fuzzy boundaries and, therefore, no classification is going to serve all users. Natural hybridization between sand fly species has been recorded in several species complexes, and it is widespread in many other groups of organisms (Arnold 1997). This highlights the need for us to focus on gene flow and the distribution of phenotypes of biomedical importance, not on taxa.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED

I thank my many colleagues in the cited references.

REFERENCES CITED

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. RESULTS
  5. DISCUSSION
  6. Acknowledgments
  7. REFERENCES CITED
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