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Population genetics of two key mosquito vectors of Rift Valley Fever virus reveals new insights into the changing disease outbreak patterns in Kenya.

Tchouassi DP, Bastos AD, Sole CL, Diallo M, Lutomiah J, Mutisya J, Mulwa F, Borgemeister C, Sang R, Torto B - PLoS Negl Trop Dis (2014)

Bottom Line: Our data strongly suggest that unlike Ae. mcintoshi, Ae. ochraceus appears to be a relatively recent, single 'introduction' into Kenya.These results, together with increasing isolations from this vector, indicate that Ae. ochraceus will likely be of greater epidemiological importance in future RVF outbreaks in Kenya.Furthermore, the overall vector complexity calls into question the feasibility of mosquito population control approaches reliant on genetic modification.

View Article: PubMed Central - PubMed

Affiliation: International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya; Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa.

ABSTRACT
Rift Valley fever (RVF) outbreaks in Kenya have increased in frequency and range to include northeastern Kenya where viruses are increasingly being isolated from known (Aedes mcintoshi) and newly-associated (Ae. ochraceus) vectors. The factors contributing to these changing outbreak patterns are unclear and the population genetic structure of key vectors and/or specific virus-vector associations, in particular, are under-studied. By conducting mitochondrial and nuclear DNA analyses on >220 Kenyan specimens of Ae. mcintoshi and Ae. ochraceus, we uncovered high levels of vector complexity which may partly explain the disease outbreak pattern. Results indicate that Ae. mcintoshi consists of a species complex with one of the member species being unique to the newly-established RVF outbreak-prone northeastern region of Kenya, whereas Ae. ochraceus is a homogeneous population that appears to be undergoing expansion. Characterization of specimens from a RVF-prone site in Senegal, where Ae. ochraceus is a primary vector, revealed direct genetic links between the two Ae. ochraceus populations from both countries. Our data strongly suggest that unlike Ae. mcintoshi, Ae. ochraceus appears to be a relatively recent, single 'introduction' into Kenya. These results, together with increasing isolations from this vector, indicate that Ae. ochraceus will likely be of greater epidemiological importance in future RVF outbreaks in Kenya. Furthermore, the overall vector complexity calls into question the feasibility of mosquito population control approaches reliant on genetic modification.

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Related in: MedlinePlus

Map of Kenya showing location of study sites and geographical distribution of putative species within what is called Ae. mcintoshi in Kenya, delineated on the basis of the COI barcoding region.The broad sampling areas are color-coded as follows: red (clade II; green (clade I); blue (clade IV).
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pntd-0003364-g001: Map of Kenya showing location of study sites and geographical distribution of putative species within what is called Ae. mcintoshi in Kenya, delineated on the basis of the COI barcoding region.The broad sampling areas are color-coded as follows: red (clade II; green (clade I); blue (clade IV).

Mentions: Despite intensified research efforts, several gaps remain in our understanding of the roles of Ae. mcintoshi and Ae. ochraceus in the maintenance and transmission of RVFV in Kenya. First, the taxonomic status of Ae. mcintoshi, included in subgenus Neomelaniconion, comprising RVFV vector and non-vector species, remains contentious [10], [15]. Separation of adult females among members of this group are based upon phenotypic characters such as color of the scales of the vertex, scutum and subspiracular scales including degree of development of the pleural scale patches [16]. Unfortunately, these characters overlap, are environmentally labile, and therefore not phylogenetically informative. Consequently, accurate identification of adult females encountered in surveillance traps is challenging, as underscored by the earlier misidentification of this species as Aedes lineatopennis[17]. Second, Ae. ochraceus, previously considered of epidemiological importance in West Africa alone [13], [14], became associated with RVF in Kenya and East Africa [10] during the 2006/2007 outbreak. Even though Ae. ochraceus had previously been reported from Kenya [18], there was no direct evidence for its involvement in the epidemiology of RVF despite numerous studies investigating the role of vectors in RVFV transmission dynamics [9], [19], [20]. Whether this vector played a role in the most severe outbreaks in Kenya (1997/1998) is also unknown. However, its confirmed role as a primary vector in the 2006/7 outbreaks signals a change in its epidemiological significance. An understanding of the genetic structure of Ae. ochraceus is therefore crucial as it can help reveal vector species distributions that may in turn influence its vectorial capacity. Third, the role of genetics of key vectors in the maintenance and spread of RVFV is perhaps the least appreciated factor despite evident variation in disease outbreak patterns. Epidemiological diversity of RVF activity in Kenya has been observed based on levels of animal and human exposure and outbreak patterns of the disease in defined ecological areas such as Northeastern, Central (Ruiru), Rift Valley (Marigat and Naivasha) areas of Kenya [5] (Fig. 1). Variation in RVFV patterns as a result of fine-scale local environmental differences have also been suggested, as has genetic diversity within and between populations of vectors that might be due to micro-geographic variation in habitat types [21]–[23]. However, the extent to which the observed temporal and spatial differences in RVFV epidemiologic patterns and spread hinge on vector genetic variation is unclear. Moreover, the genetics of mosquito species is known to influence important traits such as vector competence, which in turn affect the potential for transmission, spread and establishment of arboviruses [24]–[26].


Population genetics of two key mosquito vectors of Rift Valley Fever virus reveals new insights into the changing disease outbreak patterns in Kenya.

Tchouassi DP, Bastos AD, Sole CL, Diallo M, Lutomiah J, Mutisya J, Mulwa F, Borgemeister C, Sang R, Torto B - PLoS Negl Trop Dis (2014)

Map of Kenya showing location of study sites and geographical distribution of putative species within what is called Ae. mcintoshi in Kenya, delineated on the basis of the COI barcoding region.The broad sampling areas are color-coded as follows: red (clade II; green (clade I); blue (clade IV).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4256213&req=5

pntd-0003364-g001: Map of Kenya showing location of study sites and geographical distribution of putative species within what is called Ae. mcintoshi in Kenya, delineated on the basis of the COI barcoding region.The broad sampling areas are color-coded as follows: red (clade II; green (clade I); blue (clade IV).
Mentions: Despite intensified research efforts, several gaps remain in our understanding of the roles of Ae. mcintoshi and Ae. ochraceus in the maintenance and transmission of RVFV in Kenya. First, the taxonomic status of Ae. mcintoshi, included in subgenus Neomelaniconion, comprising RVFV vector and non-vector species, remains contentious [10], [15]. Separation of adult females among members of this group are based upon phenotypic characters such as color of the scales of the vertex, scutum and subspiracular scales including degree of development of the pleural scale patches [16]. Unfortunately, these characters overlap, are environmentally labile, and therefore not phylogenetically informative. Consequently, accurate identification of adult females encountered in surveillance traps is challenging, as underscored by the earlier misidentification of this species as Aedes lineatopennis[17]. Second, Ae. ochraceus, previously considered of epidemiological importance in West Africa alone [13], [14], became associated with RVF in Kenya and East Africa [10] during the 2006/2007 outbreak. Even though Ae. ochraceus had previously been reported from Kenya [18], there was no direct evidence for its involvement in the epidemiology of RVF despite numerous studies investigating the role of vectors in RVFV transmission dynamics [9], [19], [20]. Whether this vector played a role in the most severe outbreaks in Kenya (1997/1998) is also unknown. However, its confirmed role as a primary vector in the 2006/7 outbreaks signals a change in its epidemiological significance. An understanding of the genetic structure of Ae. ochraceus is therefore crucial as it can help reveal vector species distributions that may in turn influence its vectorial capacity. Third, the role of genetics of key vectors in the maintenance and spread of RVFV is perhaps the least appreciated factor despite evident variation in disease outbreak patterns. Epidemiological diversity of RVF activity in Kenya has been observed based on levels of animal and human exposure and outbreak patterns of the disease in defined ecological areas such as Northeastern, Central (Ruiru), Rift Valley (Marigat and Naivasha) areas of Kenya [5] (Fig. 1). Variation in RVFV patterns as a result of fine-scale local environmental differences have also been suggested, as has genetic diversity within and between populations of vectors that might be due to micro-geographic variation in habitat types [21]–[23]. However, the extent to which the observed temporal and spatial differences in RVFV epidemiologic patterns and spread hinge on vector genetic variation is unclear. Moreover, the genetics of mosquito species is known to influence important traits such as vector competence, which in turn affect the potential for transmission, spread and establishment of arboviruses [24]–[26].

Bottom Line: Our data strongly suggest that unlike Ae. mcintoshi, Ae. ochraceus appears to be a relatively recent, single 'introduction' into Kenya.These results, together with increasing isolations from this vector, indicate that Ae. ochraceus will likely be of greater epidemiological importance in future RVF outbreaks in Kenya.Furthermore, the overall vector complexity calls into question the feasibility of mosquito population control approaches reliant on genetic modification.

View Article: PubMed Central - PubMed

Affiliation: International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya; Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa.

ABSTRACT
Rift Valley fever (RVF) outbreaks in Kenya have increased in frequency and range to include northeastern Kenya where viruses are increasingly being isolated from known (Aedes mcintoshi) and newly-associated (Ae. ochraceus) vectors. The factors contributing to these changing outbreak patterns are unclear and the population genetic structure of key vectors and/or specific virus-vector associations, in particular, are under-studied. By conducting mitochondrial and nuclear DNA analyses on >220 Kenyan specimens of Ae. mcintoshi and Ae. ochraceus, we uncovered high levels of vector complexity which may partly explain the disease outbreak pattern. Results indicate that Ae. mcintoshi consists of a species complex with one of the member species being unique to the newly-established RVF outbreak-prone northeastern region of Kenya, whereas Ae. ochraceus is a homogeneous population that appears to be undergoing expansion. Characterization of specimens from a RVF-prone site in Senegal, where Ae. ochraceus is a primary vector, revealed direct genetic links between the two Ae. ochraceus populations from both countries. Our data strongly suggest that unlike Ae. mcintoshi, Ae. ochraceus appears to be a relatively recent, single 'introduction' into Kenya. These results, together with increasing isolations from this vector, indicate that Ae. ochraceus will likely be of greater epidemiological importance in future RVF outbreaks in Kenya. Furthermore, the overall vector complexity calls into question the feasibility of mosquito population control approaches reliant on genetic modification.

Show MeSH
Related in: MedlinePlus