Vol. 36, Supplement 1
Journal of Vector Ecology
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Should sand fly taxonomy predict vectorial and ecological traits?
Paul D. Ready
Department of Entomology, Natural History Museum, Cromwell Road, London SW7 5BD, U.K.
ABSTRACT: 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 cocladogenesis 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. Journal of Vector Ecology 36 (Supplement 1):
S17-S22. 2011.
Keyword Index: Phlebotominae, sand flies, taxonomy, species concepts, vectorial traits, ecological traits, leishmaniasis.
INTRODUCTION
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 (WangSattler et al. 2007), sufficient for insecticide resistance genes
(Weill et al. 2000, Munhenga et al. 2008) to pass between the
Journal of Vector Ecology March 2011
S18
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
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.
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
Le. (Le.)
infantum
Le. (Vi.)
braziliensis
Neotropics
(equatorial,
semi-arid)
Brazil
(equatorial,
sub-humid)
Zoonotic visceral
leishmaniasis
Zoonotic cutaneous
leishmaniasis
Montoya-Lerma
et al. (2003), Lanzaro
(2010)
Killick-Kendrick (1990),
Young and Duncan
(1994), Testa et al.
(2002)
Lutzomyia (Lutzomyia) longipalpis (Lutz & Neiva)
L. evansi (Nuñez-Tovar) in Verrucarum group
L. (Psychodopygus) carrerai (Barretto)
L. (Psychodopygus) wellcomei (Fraiha et al.)
L. (Nyssomyia) intermedia (Lutz & Neiva)
L. (Nyssomyia) whitmani (Antunes & Coutinho)
L. townsendi (Ortiz) complex in Verrucarum group
Killick-Kendrick (1990),
Gallego et al. (2001)
P. (Larroussius) ariasi Tonnoir
P. (Larroussius) perniciosus Newstead
P. (Larroussius) species
Le. (Le.)
infantum
Mediterranean
(semi-arid,
sub-humid)
Zoonotic visceral
leishmaniasis
Killick-Kendrick (1990),
Svobodová et al. (2006)
Le. (Le.)
tropica
Asia,
Mediterranean
(semi-arid)
Anthroponotic
cutaneous
leishmaniasis
P. (Paraphlebotomus) sergenti Parrot
P. (Adlerius) arabicus Theodor
Killick-Kendrick (1990),
Parvizi et al. (2010)
P. (Phlebotomus) papatasi
P. (Phlebotomus) salehi Mesghali
P. (Paraphlebotomus) caucasicus Marzinowsky
P. (Paraphlebotomus) mongolensis Sinton
Le. (Le.)
major
Asia
(arid, semi-arid)
Zoonotic cutaneous
leishmaniasis
Vector incrimination
reviews
Killick-Kendrick (1990)
Vectors
Phlebotomus (Phlebotomus) papatasi (Scopoli)
P. (Phlebotomus) duboscqi Neveu-Lemaire
Africa
(arid, semi-arid)
Zoonotic cutaneous
leishmaniasis
Parasite
Leishmania
(Le.) major
Region
Leishmaniasis
Table 1. Additional details of vector taxonomy and incrimination for the case studies of leishmaniasis transmission cycles, illustrating the imperfect “evolutionary fit” or cocladogenesis of vectors and parasites.
Vol. 36, Supplement 1
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P. (Larroussius) and L. (Lutzomyia) but also L. evansi of
the neotropical Verrucarum subgeneric group (MontoyaLerma 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 (CampbellLendrum 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
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 nonspecialists 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 wellsupported phylogeny of the genera and subgeneric groups of
the subfamily Phlebotominae will probably require a supermatrix 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
I thank my many colleagues in the cited references.
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