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Am. J. Trop. Med. Hyg., 79(2), 2008, pp. 218-229
Copyright © 2008 by The American Society of Tropical Medicine and Hygiene

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Aedes aegypti in Senegal: Genetic Diversity and Genetic Structure of Domestic and Sylvatic Populations

Karine Huber, Yamar Ba, Ibrahima Dia, Christian Mathiot, Amadou A. Sall, AND Mawlouth Diallo*
Institut Pasteur de Dakar, Dakar, Senegal


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Aedes aegypti is the main vector of dengue viruses. The epidemiology of dengue fever remains poorly understood in Senegal. A sylvatic transmission seems to predominate. However, despite the sylvatic circulation of the dengue virus and the presence of vectors in urban areas, only sporadic cases have been reported. Ae. aegypti is a polytypic species. In Senegal, a purely sylvatic form is found in the forest gallery areas and a domestic form is found in the villages in savannah and sahelian areas and in urban areas. Using allozymes, we analyzed the genetic diversity and the genetic structure of Ae. aegypti populations differing in their ecological characteristics. Populations from Senegal were significantly structured but with a low level of genetic differentiation. Ae. aegypti from the "domestic" populations show a decreased genetic diversity and a lower genetic differentiation compared with "sylvatic" populations. These findings suggest that environmental conditions, ecological factors, and human activities may impact the genetic structure of Ae. aegypti populations in Senegal.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Dengue fever (DF) and dengue hemorrhagic fever (DHF) are tropical and sub-tropical, mosquito-borne diseases resulting from infection with one of the four antigenically distinct serotypes of dengue viruses (DENV) in the family Flaviviridae. DF/DHF is the most important arboviral disease of humans occurring in tropical countries of the world, where > 2.5 billion people are at risk of infection.1 It is estimated that between 50 and 100 million new dengue infections occur annually,2 and the average fatality rate for DHF ranges from 5% to 40%.3

The epidemiology of dengue fever is not well understood in West Africa. As in Asia, a sylvatic transmission cycle has been shown in this region.4,5 However, unlike Southeast Asia where inter-human transmission is most commonly detected, in West Africa, the sylvatic transmission seems to be predominant. In Senegal, although DENV-1, -2, and -4 (never DENV-3) have been isolated incidentally from humans, only DENV-2 was repeatedly isolated from mosquitoes and humans and once from a monkey, mostly from the sylvatic focus in Kedougou area.6,7 However, despite sylvatic manifestations and the presence of mosquito vectors in urban areas, only sporadic cases have been reported during or after these sylvatic viral amplifications, and DENV isolations from Aedes aegypti are rare.8,9

It was shown experimentally that the susceptibility and capacity of Ae. aegypti to transmit DENV are variable and depend on geographical origin of natural populations.10 A difference in the sensitivity to infection has also been observed among Ae. aegypti females from the same progeny.11 In fact, Ae. aegypti, the main mosquito vector of DENV, is a polytypic species that includes two main forms differing in their morphology, ecology, ethology, and genetics12,13: 1) Ae. aegypti aegypti, a light-colored form that breeds in domestic or peri-domestic environments and occurs in the New World, Asia, and in the coastal areas of East Africa, and 2) Ae. aegypti formosus, a dark form that breeds in tree holes and sometimes in rock holes, and is mainly found in sub-Saharan Africa. Only Ae. aegypti aegypti is associated with dengue epidemics in the Americas and Asia.

The lack of data on genetic variation of Ae. aegypti populations from West Africa limits conclusions about whether both forms exist there, although certain authors described the absence of Ae. aegypti aegypti in this part of the continent.14 In Burkina Faso, the domestic/peridomestic nature of the aquatic breeding stages permitted the differentiation of two distinct morphological forms: a wild dark form and a clear domestic form.15

In Senegal, morphologic and ethologic variations were observed between Ae. aegypti populations, related to their geographical localization and type of habitat. A sylvatic form is found in the gallery forests near Kedougou (southern Senegal). This form is more abundant in the forest gallery than in the villages, has zoophilic tendencies, and uses tree holes as breeding sites. A domestic form is present in savannah villages, sahelian areas, and in urban areas. This later form is similar ecologically to Ae. aegypti aegypti. It colonizes artificial water containers, water storage containers (i.e., clay jars, metallic barrels), as well as abandoned containers (i.e., cans, plastic bottles, worn tires) and is highly anthropophilic. Morphologically, both forms found in Senegal are characterized by a dark color, the "domestic" form is slightly paler and always has pale scales present on the first abdominal tergite, whereas the sylvatic form does not (M. Diallo, unpublished data). In Senegal, data on the genetic status of the Ae. aegypti populations are scarce. Studies including populations from Senegal date back to 25 years ago and therefore need to be revised because of profound environment changes that may have affected Ae. aegypti populations there.

In this study, we analyzed the genetic diversity and structure of Ae. aegypti populations collected in five distinct areas of Senegal differing in their ecological characteristics: 1) sylvatic populations from the gallery forest area of Kedougou and 2) domestic populations from the savannah areas of Koungheul, Kaffrine, and Diourbel and the sahelian area of Barkedji (Figure 1Go).


Figure 1
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  		FIGURE 1. Map of Senegal showing the locations of Ae. aegypti samples collected from November 2002 to January 2003.

 

MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Mosquito samples. Twenty-five mosquito samples were collected from November 2002 to January 2003 (Table 1Go) in five distinct areas of Senegal (Figure 1Go) differing in ecological characteristics: five samples were from the gallery forest area of Kedougou where a sylvatic cycle of dengue virus transmission takes place, from the savannah areas of Koungheul (seven samples), Kaffrine (three samples), and Diourbel (five samples), and five from the sahelian area of Barkedji. Natural (tree holes) and peridomestic and domestic artificial breeding sites (water storage containers) were studied. Samples collected include eggs, larvae, and pupae, which were reared to the adult stage in an insectarium. Adults were stored at –80°C until analysis for isoenzyme polymorphisms. A total of 1,086 mosquitoes were analyzed with an average of 43.4 mosquitoes per collection site.


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TABLE 1.
Location of Ae. aegypti samples collected in Senegal from November 2002 to January 2003
 
Isoenzyme polymorphism. Individual mosquitoes were homogenized in 25 µL distilled water. The homogenate was centrifuged (15,000g, 3 minutes at +4°C), and the supernatant was subjected to starch gel electrophoresis in Tris-maleate-EDTA (TME), pH 7.4, buffer. Ten isoenzymes loci were studied: phosphoglucoisomerase (PGI), glutamate-oxaloacetate transaminase (GOT1 and GOT2), glycerol-phosphate dehydrogenase (GPD), hexokinases (HK1, HK2, and HK3), malate dehydrogenase (MDH), malic enzyme (ME), and phosphoglucomutase (PGM). These techniques are described in detail by Paupy and others.16 A strain developed from an isofemale lineage of Ae. aegypti "Paea" (Tahiti, French Polynesia) was used as a mobility control. For field-collected samples, alleles were numbered according to their mobility and compared with the most common allele obtained at each locus in the control strain.

Genetic analysis. POPGENE (v. 1.31)17 was use to calculate allele frequencies, observed (HO) and expected (HE) heterozygosity, and effective number of alleles.

FSTAT (v. 2.9.3.2)18 was used for testing the significance of differences in average values of HE among the groups of populations (10,000 permutations, one-sided test or two-sided test of the null hypothesis of no difference).

Analysis of molecular variance (AMOVA)19 was performed using ARLEQUIN (v. 3.0).20 Four different grouping factors were tested: geography (location of samples), vegetation type, the subspecies, and type of breeding site. Total genetic variance was partitioned into the following hierarchical levels for each analysis: among groups, among populations within groups, and within populations. For each computation, {Phi} statistics were calculated and tested for significance using 1,000 permutations.

Deviation from Hardy-Weinberg proportions, genotypic linkage disequilibrium, and genetic differentiation was tested using GENEPOP (v. 3.3) software.21 Fis and Fst were estimated as described by Weir and Cockerham.22 Heterozygote deficits were tested using an exact test procedure.23 Global disequilibrium between pairs of loci was tested for each sample. Genotypic differentiation was tested by calculating the P value of an Fst estimate. The overall significance of multiple tests was estimated using the Fisher combined probability test. Isolation by distance was assessed by determining the significance of the correlation between Fst estimates and geographical distances.24,25 The significance level of each test was adjusted, based on the number of tests run, according to the sequential method of Bonferroni.26 Kruskal-Wallis tests were performed for mean comparisons using R software (version 2.0.1).27 A genetic distance matrix based on pairwise Fst’s calculated with ARLEQUIN (v. 3.0)20 was used to construct a tree among all collections using the neighbor-joining method in the NEIGHBOR procedure in PHYLIP (v. 3.6b).28


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Genetic diversity. All 10 isozyme loci analyzed were polymorphic, displaying a total of 39 alleles (Table 2Go, the raw data is available on request). All the populations from the savannah areas (Koungheul, Kaffrine, and Diourbel) and from the sahelian area of Barkedji harbored relatively few alleles (17–21; mean number of alleles per locus, 1.3–2.1). The largest number of alleles (27) was observed in the forest gallery area of Kedougou (KED4). The other populations of this area harbored at least 20 alleles (mean number of alleles per locus, 2.0–2.7).


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TABLE 2.
Fis and deviations from Hardy-Weinberg proportions observed at 10 izoenzyme loci in 25 Ae. aegypti samples collected in Senegal 2002–2003
 
To highlight populations with unusual allelic compositions, the presence of "private" alleles (occurring in a single population) were identified. There were four such private alleles: four were present in populations from Kedougou [KED4 (HK2 and PGI), KED2 (MDH), and KED3 (MDH)] and one in the savannah population KOU3 (MDH) from the Koungheul area. Some alleles were also specific to a region; one allele from ME was only present in populations from the Kedougou area, and one allele from PGI and one from PGM were present only in populations from the Barkedji area.

The population with the richest allelic composition (KED4, 27 alleles) had, when we excluded the 10 alleles that were automatically present because there were 10 loci, 58.6% [(27 – 10)/(39 – 10)] of the allelic diversity. All the populations from the Kedougou area combined yielded 89.7% of the total allelic diversity detected in this study.

When samples were grouped according to geographical location, expected heterozygosity was significantly higher (P = 0.019) for the populations from the Kedougou area (HE = 0.189) than for those from the other areas (HE= 0.160). Among expected heterozygosity of these four other areas (Barkedji [HE = 0.158], Diourbel [HE = 0.171], Koungheul [HE = 0.162], Kaffrine [HE = 0.154]), no significant difference was detected (P = 0.85).

AMOVA analysis. AMOVA results (Table 3Go) did not indicate any genetic structure associated with geographical location, ecological characteristics of the sampling area, the subspecies, or the type of breeding site. For all types of groupings, most of the genetic variation was found within populations (~90%) and among populations within groups (~5.5%) with significant P values (< 0.00001). Genetic variation among groups is higher (3.56%) when samples are grouped according to subspecies than when they are grouped by geographical location (1.93%), vegetation type (2.64%), or type of breeding site (2.36%).


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TABLE 3.
AMOVA of Ae. aegypti population from Senegal using four different grouping factors
 
Hardy-Weinberg equilibrium. Of 124 tests run, only two significant deviations from Hardy-Weinberg equilibrium were detected after application of Bonferroni procedures: GOT1/KED5 (Fis = +0.668) and GPD/KED2 (Fis = +1) (Table 2Go). Hardy-Weinberg equilibrium was also tested assuming that the alternative hypothesis, H1, was heterozygote deficit (H0: random mating). All deviations detected were caused by a heterozygote deficit. When considering global tests (i.e., all loci for each sample), two samples showed significant heterozygote deficit, KED4 and KED5, and one showed a heterozygote excess (BAR3). When samples were grouped according to their collection origin, significant heterozygote deficits were observed for the samples from Kedougou and Koungheul.

Genetic differentiation. The overall Fst value for all 25 samples was highly significant (Fst = +0.078, P < 10–6; Table 4Go). When samples were pooled according to collection origin, those collected in Barkedji (Fst = +0.046, P < 10–6), Diourbel (Fst = +0.055, P < 10–6), Kaffrine (Fst = +0.043, P < 10–6), and Kedougou (Fst = +0.046, P < 10–6) were 2- to 10-fold less differentiated than those collected in the Koungheul area (Fst = +0.109, P < 10–6).


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TABLE 4.
Population differentiation of Ae. aegypti in Senegal, 2002–2003, as shown by isoenzyme polymorphism analysis
 
When estimating differentiation between pairs of samples, {theta}ij (Fst) ranged from –0.010 to 0.2454 (0.077 ± 0.049; Table 5Go): from –0.010 to 0.2314 for the "Savannah-sahelian" (S) group (0.076 ± 0.050) and from 0.0101 to 0.1456 for the "Forest" (F) group (0.050 ± 0.042). For heterologous combinations, {theta}ij (Fst) ranged from 0.0041 to 0.2454 (0.082 ± 0.049). Of 300 combinations, 9 showed non-significant differentiation, among which 8 were S combinations (4.2% in the S group) and 1 was a heterologous combination (1% in the heterologous group). Thus, genetic differentiation of S combinations seemed to be lower than other combinations. The mean {theta}ij-S, {theta}ij-TF, and {theta}ij-Heterologous were similar (P = 0.07).


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TABLE 5.
{theta}ij (Fst) estimates computed using allozyme variations for all pair of samples according to the ecological characteristics of the sampling areas
 
In the neighbour joining dendrogram (Figure 2Go), allozyme data did not cluster in populations according to their geographical location.


Figure 2
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  		FIGURE 2. Neighbor-joining tree based on pairwise Fst' distances between collections.

 
When estimating genetic divergence according to geographic distance, the relation (Fst/[1 – Fst] = a + b[Ln distance]) was not significant when considering all samples (P = 0.10). The correlation was not significant among samples from the Barkedji (P = 0.32), Diourbel (P = 0.61), Kaffrine (P = 0.67), and Kedougou (P = 0.09) areas, whereas it was significant among samples from the Koungheul area (P = 0.03; Figure 3Go).


Figure 3
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  		FIGURE 3. Regression analysis of pairwise Fst/(1 – Fst) regressed on pairwise ln (geographic distances) between collections.

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our objectives were to analyze the genetic significances of the morphologic and behavioral differences observed among Ae. aegypti populations from Senegal. The results obtained showed that the overall Fst value (+0.078) is low, whereas it is significant. This result is consistent with other studies taking place in West Africa.14,29,30 In Nigeria, Ae. aegypti from rural and urban areas are genetically similar.31 As in Senegal, many of these populations are dark in color but show white spotting on the first abdominal tergite, a characteristic of the domestic Ae. aegypti aegypti studied by Petersen32 in East Africa.

The "domestic" populations showed a decreased genetic diversity compared with "sylvatic" populations from Kedougou. In fact, we observed that the "domestic" populations had a significantly lower expected heterozygosity than the "sylvatic" ones. Domestic populations may have come from populations exhibiting higher population diversity. In that case, relatively small numbers of individuals involved in each colonization event, and an initial slow growth rate of the founding populations could have created a genetic bottleneck that further reduced variation in the "domestic" populations. Because Ae. aegypti has a short flight range (~10–400 m) during its entire lifetime,33–35 only passive migrations through the accidental transportation of eggs, larvae, or adults of mosquitoes or the adaptation of sylvatic populations in a changing environment could explain the establishment of this domestic form. Indeed, it is probable that the domestic populations evolved from sylvatic ones through an adaptation after deforestation for cultivation, urbanization, and desertification that have greatly reduced the natural sylvatic habitat. During these events, few founding individuals were probably involved, leading to genetic bottlenecks that support this hypothesis.

Although Ae. aegypti populations from Senegal are significantly structured, a low genetic differentiation was observed for the domestic populations. This level of differentiation is similar to the one observed for Asian domestic Ae. aegypti in Cambodia36 and Vietnam.37 In these countries, it has been shown that the population structure is shaped by human activities, especially by water storage practices. In Senegal, in the villages where the "domestic" samples were collected, piped water supplies are generally not available, leading to water storage in clay jars or metallic barrels within houses. Dwelling in the villages are organized in residential compounds, which comprise one or more households, together with some members of the extended family. Some domestic animals also live inside the compound. Thus, host–vector contacts with this endophagic, endophilic mosquito are quite frequent. It has been proposed that dispersal is driven by the search for oviposition sites.35,38 The accumulation of breeding sites (for females to lay eggs) at the vicinity of houses and the presence of human beings (for females to feed on) could enhance Ae. aegypti movements and genetic exchange and reduce the genetic differentiation explaining the moderate level of differentiation observed in the "domestic" samples.

In the Kedougou region, the samples analyzed were collected in the forest gallery area and belong to the "sylvatic" zoophilic form. The larvae inhabit natural breeding sites such as tree holes that are subjected to seasonal rainfall (in contrast to water storage containers that are available throughout the year). The search for oviposition sites and for blood meals depends on numerous factors such as the amount of rainfall, the availability of tree species tending to generate tree holes, and the presence of wild vertebrate hosts. The complexity of these factors may explain the higher level of differentiation observed. Moreover seasonal fluctuations in mosquito populations may also explain the higher differentiation observed, because it has been shown that the dynamics and genetic structure of Ae. aegypti populations changes according to the seasons.39 This study was undertaken during the dry season when all natural breeding sites were dry. Samples were collected by scraping tree holes with spoons to collect Aedes eggs, known to be resistant to desiccation, and flooded in the laboratory for hatching. These eggs could have represented an accumulation laid by several populations during different years and throughout the year according to the flooding of the breeding sites.

The departure from Hardy-Weinberg equilibrium observed in two populations from the Kedougou area was always associated with heterozygote deficiencies. This could be because of factors such as null alleles, inbreeding, or a Wahlund effect. The occurrence of null alleles in allozymes is very rare.40,41 The fact to have sampled several offsprings from the same female that has laid its eggs in the same breeding site or in breeding sites of different nature—phenomenon already known in Ae. aegypti35—can be a cause of inbreeding. To avoid such a phenomenon, we tested for the same geographical area, some individuals belonging to various breeding sites and various localities (Fadiga and PK 10). Furthermore, inbreeding could be excluded as an explanation because deficits would be expected in all loci. Therefore, the Wahlund effect is the most plausible explanation of the heterozygote deficiency in Kedougou. Such a phenomenon may be explained by the sampling method we used, which was egg collections in tree holes as mentioned above.

In our study, the geographical distance between populations was not a good indicator of the genetic distance between populations. Various extrinsic forces could disrupt genetic isolation by distance as has been shown in northeastern Mexico42: arid environment that cause populations to undergo genetic bottlenecks or human transportations of eggs or larvae that could cause geographically distant populations to become genetically similar, thus reducing genetic isolation by distance.

The findings of this study allowed us to put forward two hypotheses. The first one is that the domestic Ae. aegypti populations may have a sylvatic origin. The genetic relatedness, showing a clear persistence of gene flow between sylvatic and domestic populations, supports this hypothesis.

The domestication process could have been associated with a series of morphologic, behavioral, and demographic changes as previously reported for different populations in Burkina Faso14 and in other arthropods like Triatomids.43,44 This evolution could be associated with three key factors: 1) exploitation of human blood as a food source (anthropophagy), 2) adaptation to the human host environment (i.e., artificial containers as breeding sites), and 3) progressive reliance on human activities as a means for dispersal by passive transport. This process involves specialization and simplification reflected in genetics and phenotypic characteristics.44 Genetic simplification during domestication may occur through founder effects followed by intraspecific competition. In addition, when a newly founded population becomes isolated from its sylvatic focus, a further loss of genetic variability can be expected.43 These findings implicate environmental conditions, ecological factors, and human activities as factors shaping the genetic structure of Ae. aegypti populations in Senegal.

The second hypothesis is that the "domestic" form could be a recent hybrid between the North African domestic Ae. a. aegypti and the sylvan West African Ae. a. formosus as suggested by Tabachnick.30 He supposed that domesticity was not sufficiently established to maintain a distinct sympatric population. This hypothesis could explain the low level of genetic differentiation observed in Senegal and that this form has a dark color as the formosus form but harbors white spotting on the first abdominal tergite and shows a preference for human hosts. However, the absence of Ae. aegypti aegypti populations remains questionable because of the lack of reliable methods to distinguish the subspecies. The morphologic keys based on color are not sufficiently accurate to distinguish Ae. aegypti aegypti from Ae. aegypti formosus or to identify intermediate forms. Additional studies, with microsatellite markers, that provide often a more sensitive measure of divergence than isoenzyme markers will help to distinguish populations that may have recently diverged.45,46 Moreover, studying their ecology, morphology, and vector competence, as well as the development of more reliable taxonomic tools, is needed to better characterize these mosquito populations and should help elucidate the epidemiology of dengue in Senegal.

Received November 12, 2007. Accepted for publication April 3, 2008.

Acknowledgments: The authors thank Mamoudou Diallo, Ignace Rakotoarivony, Pedro Rodriguez Menendez, Mouhamadou Lamine Soumare, and Amadou Thiaw for technical assistance and help during field investigations and Dr. Scott C. Weaver, Director for Tropical and Emerging Infectious Diseases, UTMB Center for Biodefense and Emerging Infectious Diseases, Departments of Pathology, Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, for improving the manuscript with helpful suggestions.

Financial support: This work received financial support from the UNICEF/UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Disease (TDR): A00398.

* Address correspondence to Mawlouth Diallo, Institut Pasteur, 36 Avenue Pasteur, BP 220, Dakar, Senegal. E-mail: diallo{at}pasteur.sn Back

Authors’ addresses: Karine Huber, UPR Contrôle des Maladies Animales Exotiques et Emergentes, Campus International de Baillarguet, TA A-15/G, 34398 Montpellier cedex 5, France, Tel: 33-4-67-59-37-24, Fax: 33-4-67-59-37-98, E-mail: karine.huber{at}cirad.fr. Yamar Ba, Ibrahima Dia, Amadou A. Sall, and Mawlouth Diallo, Institut Pasteur, 36 Avenue Pasteur, BP 220 Dakar, Senegal. Christian Mathiot, WHO Office in Lyon, 58 Avenue Debourg, 69007 Lyon, France.

Reprint requests: Karine Huber, UPR Contrôle des Maladies Animales Exotiques et Emergentes, Campus International de Baillarguet, TA A-15/G, 34398 Montpellier cedex 5, France, E-mail: karine.huber{at}cirad.fr.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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