Evidence for genetic differentiation at the microgeographic scale in Phlebotomus papatasi populations from Sudan

biomed - Aboud , Alrabba , Elnaiem , Tripet , Khalid , Tripét Frederic

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Cutaneous Leishmaniasis (CL) is endemic in Sudan. It is caused by Leishmania major parasites and transmitted by Phlebotomus papatasi sandflies. Recently, uncommon clinical manifestations of CL have been reported. Moreover, L . donovani parasites that cause Visceral Leishmaniasis (VL) have been isolated from CL lesions of some patients who contracted the disease in Khartoum State, Central Sudan with no history of travelling to VL endemic sites on south-eastern Sudan. Because different clinical manifestations and the parasite behaviour could be related to genetic differentiation, or even sub-structuring within sandfly vector populations, a population genetic study was conducted on P . papatasi populations collected from different localities in Khartoum State known for their uncommon CL cases and characterized by contrasting environmental conditions. Methods A set of seven microsatellite loci was used to investigate the population structure of P . papatasi samples collected from different localities in Khartoum State, Central Sudan. Populations from Kassala State, Eastern Sudan and Egypt were also included in the analyses as outgroups. The level of genetic diversity and genetic differentiation among natural populations of P. papatasi was determined using F ST statistics and Bayesian assignments. Results Genetic analyses revealed significant genetic differentiation ( F ST ) between the Sudanese and the Egyptian populations. Within the Sudanese P. papatasi populations, one population from Gerif West, Khartoum State, exhibited significant genetic differentiation from all other populations including those collected as near as 22 km. Conclusion The significant genetic differentiation of Gerif West P . papatasi population from other Sudanese populations may have important implication for the epidemiology of leishmaniasis in Khartoum State and needs to be further investigated. Primarily, it could be linked to the unique location of Gerif West which is confined by the River Nile and its tributaries that may act as a natural barrier for gene flow between this site and the other rural sites. The observed high migration rates and lack of genetic differentiation among the other P . papatasi populations could be attributed to the continuous human and cattle movement between these localities.

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Phlebotomus papatasi

Sudán

Gene flow

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Publié par	biomed
Publié le	01 janvier 2012
Nombre de lectures	8
Langue	English

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Khalid et al. Parasites & Vectors 2012, 5:249
http://www.parasitesandvectors.com/content/5/1/249
RESEARCH Open Access
Evidence for genetic differentiation at the
microgeographic scale in Phlebotomus papatasi
populations from Sudan
1* 2 3 4 5Noteila M Khalid , Marium A Aboud , Fathi M Alrabba , Dia-Eldin A Elnaiem and Frederic Tripet
Abstract
Background: Cutaneous Leishmaniasis (CL) is endemic in Sudan. It is caused by Leishmania major parasites and
transmitted by Phlebotomus papatasi sandflies. Recently, uncommon clinical manifestations of CL have been
reported. Moreover, L. donovani parasites that cause Visceral Leishmaniasis (VL) have been isolated from CL lesions
of some patients who contracted the disease in Khartoum State, Central Sudan with no history of travelling to VL
endemic sites on south-eastern Sudan. Because different clinical manifestations and the parasite behaviour could be
related to genetic differentiation, or even sub-structuring within sandfly vector populations, a population genetic
study was conducted on P. papatasi populations collected from different localities in Khartoum State known for
their uncommon CL cases and characterized by contrasting environmental conditions.
Methods: A set of seven microsatellite loci was used to investigate the population structure of P. papatasi samples
collected from different localities in Khartoum State, Central Sudan. Populations from Kassala State, Eastern Sudan
and Egypt were also included in the analyses as outgroups. The level of genetic diversity and genetic differentiation
among natural populations of P. papatasi was determined using F statistics and Bayesian assignments.ST
Results: Genetic analyses revealed significant genetic differentiation (F ) between the Sudanese and the EgyptianST
populations. Within the Sudanese P. papatasi populations, one population from Gerif West, Khartoum State,
exhibited significant genetic differentiation from all other populations including those collected as near as 22 km.
Conclusion: The significant genetic differentiation of Gerif West P. papatasi population from other Sudanese
populations may have important implication for the epidemiology of leishmaniasis in Khartoum State and needs to
be further investigated. Primarily, it could be linked to the unique location of Gerif West which is confined by the
River Nile and its tributaries that may act as a natural barrier for gene flow between this site and the other rural
sites. The observed high migration rates and lack of genetic differentiation among the other P. papatasi populations
could be attributed to the continuous human and cattle movement between these localities.
Keywords: Phlebotomus papatasi, Sudan, Gene flow, Genetic differentiation
Background The parasites within the Leishmania donovani complex
Female sandflies of the genus Phlebotomus in the Old usually invade the macrophages of the liver, spleen and
World are vectors of Leishmania parasites, the causative bone marrow causing the severe symptoms of the fatal Vis-
agent of different clinical forms of leishmaniasis [1]. The ceral Leishmaniasis (VL) [3,4]; while the parasites of L.
disease is endemic in 88 countries in five continents with major complex which cause Cutaneous Leishmaniasis (CL)
a total of350 millionpeople atrisk[2]. invade the subcutaneous reticulo-endothelial system and
cause self-healing lesions that leave life-long scars [5,6].
Phlebotomus papatasi (Scopoli, 1786) is the principal
* Correspondence: Noteila@hotmail.com vector of Leishmania major in the Old World [1]. It is a
1
Department of Zoology, Khartoum College of Medical Science, PO Box widely distributed species found in variable habitats and
10995, Khartoum, Sudan
associated with a wide range of vertebrate hosts [7,8].Full list of author information is available at the end of the article
© 2012 Khalid et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.Khalid et al. Parasites & Vectors 2012, 5:249 Page 2 of 13
http://www.parasitesandvectors.com/content/5/1/249
Due to their poor dispersal capacity, populations of of genetic differentiation in P. papatasi populations at
P. papatasi are expected to show some genetic structuring the local scale has not yet been explored using microsat-
along their geographical range as a result of adaptation to ellite markers which, with their higher mutation rates,
local habitats and limited gene flow [9]. Such genetic vari- should be comparatively much more informative than
ability could play an important role in the epidemiology isoenzymes and other sequence loci [19].
and clinical manifestations of leishmaniasis since it affects In Sudan, CL is caused by L. major and transmitted by
the vectorialcapacity ofthe vector [10,11]. P. papatasi [20,21]. Before the 1970s, the disease was
Previous studies focusing on potential population sub- confined to the western parts of the country. Thereafter,
structuringin P. papatasiusedanumberofmolecularmar- major epidemics occurred along the River Nile and the
kers and provided contrasting results. For example, isoen- disease became endemic in many regions of the country
zyme analyses clearly separated Western Mediterranean P. [21]. The usual clinical forms of the disease usually heal
papatasi populations from those from eastern countries spontaneously without the need for medical treatment, a
but, predictably, failed to reveal differences between urban matter which discourages patients from attending the
and rural sandfly populations in Morocco [12]. Mitochon- health centres, and therefore obscures the incidence of
drial DNA sequences coding for cytochrome b (mtDNA cyt the disease [22]. Visceral Leishmaniasis (VL) which is
b) and sequences from the second internal transcribed spa- caused by L. donovani and transmitted by P. orientalis is
cer of the ribosomal DNA (rDNA ITS2) were both used to known to be endemic in eastern and southern parts of
study the population structure of P. papatasi populations Sudan [4,23], with few scattered foci along the White
fromNorthAfricaandthe Mediterraneansub-regioncoun- Nile and Darfur [24]. Recently, uncommon clinical man-
tries [13,14]. The analyses of mtDNA cyt b sequences sug- ifestations of CL that did not heal spontaneously nor
gested some level of genetic differentiation among widely responded to usual drugs have been reported [25].
separated populations and revealed a pattern of isolation- Moreover, L. donovani parasites have been isolated from
by distance between populations from Syria, Egypt, Israel/ CL lesions of some patients who contracted the disease
Palestine and Turkey [13]. The ND4 mtDNA region was in Khartoum State, Central Sudan, with no history of
also used in combination with the rDNA ITS2 to study travelling to VL endemic sites [26]. Recent studies have
the population structure of P. papatasi from 18 coun- demonstrated the possibility of genetic exchanges be-
tries from North Africa, the Mediterranean sub-re- tween different strains and species of the Leishmania
gion, Saudi Arabia and India, but revealed no clear parasites [27-29] which may further complicate the epi-
phylogeographic structure between those populations. demiology of the disease since hybrid parasites may
However, signs of restricted gene flow were found adapt differently to the vector and reservoir hosts [30].
among populations from Iran, Egypt, Syria, Yemen Becausedifferent clinical manifestations and the parasite
and Turkey [14]. behaviour may also be related to genetic differentiation or
Microsatellite markers combined with Bayesian statistic sub-structuring within sandfly vector populations [11,31],
analysis were recently used to study the population struc- we conducted a population genetic study of P. papatasi
ture of Phlebotomus papatasi populations in countries populations in Sudan from broad to local geographical
from the North-African and the Mediterranean sub- scale. This was done using a set of 5 microsatellite mar-
regions. This study confirmed the occurrence of highly kers, especially developed for P. papatasi [32], and given
significant genetic differentiation between some popula- the paucity of such markers, by testing and using add-
tions [15]. However, the geographical scale of the study itional markers developed for P. perniciosus a related phle-
did not allow for detecting possible genetic differentiation botomine species[33].
at the local level, which may be the most relevant for P. papatasi populations were collected from different
explaining the observed patterns of variation in epidemio- localities characterized by the distribution of the atypical
logicallyrelevant traits observed in someregions. CL cases. The level of genetic diversity and genetic dif-
Thus, so far, genetic differentiation among P. papatasi ferentiation among natural populations of P. papatasi
populations could not be demonstrated at the local geo- was determined using F and Bayesian assignments.ST
graphical level, despite evidence suggesting that it may Identifying potential factors leading to genetic differenti-
occur. For example, Schmidt and Schmidt (1963) ation and structuring in P. papatasi populations might
observed marked morphometric variations within the improve our understanding of the epidemiology of the<