Dataset Information

Dissecting functional components of reproductive isolation among closely related sympatric species of the Anopheles gambiae complex.

ABSTRACT: Explaining how and why reproductive isolation evolves and determining which forms of reproductive isolation have the largest impact on the process of population divergence are major goals in the study of speciation. By studying recent adaptive radiations in incompletely isolated taxa, it is possible to identify barriers involved at early divergence before other confounding barriers emerge after speciation is complete. Sibling species of the Anopheles gambiae complex offer opportunities to provide insights into speciation mechanisms. Here, we studied patterns of reproductive isolation among three taxa, Anopheles coluzzii, An. gambiae s.s. and Anopheles arabiensis, to compare its strength at different spatial scales, to dissect the relative contribution of pre- versus postmating isolation, and to infer the involvement of ecological divergence on hybridization. Because F1 hybrids are viable, fertile and not uncommon, understanding the dynamics of hybridization in this trio of major malaria vectors has important implications for how adaptations arise and spread across the group, and in planning studies of the safety and efficacy of gene drive as a means of malaria control. We first performed a systematic review and meta-analysis of published surveys reporting on hybrid prevalence, showing strong reproductive isolation at a continental scale despite geographically restricted exceptions. Second, we exploited our own extensive field data sets collected at a regional scale in two contrasting environmental settings, to assess: (i) levels of premating isolation; (ii) spatio/temporal and frequency-dependent dynamics of hybridization, (iii) relationship between reproductive isolation and ecological divergence and (iv) hybrid viability penalty. Results are in accordance with ecological speciation theory predicting a positive association between the strength of reproductive isolation and degree of ecological divergence, and indicate that postmating isolation does contribute to reproductive isolation among these species. Specifically, only postmating isolation was positively associated with ecological divergence, whereas premating isolation was correlated with phylogenetic distance.

SUBMITTER: Pombi M

PROVIDER: S-EPMC5680640 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Dissecting functional components of reproductive isolation among closely related sympatric species of the <i>Anopheles gambiae</i> complex.

Pombi Marco M Kengne Pierre P Gimonneau Geoffrey G Tene-Fossog Billy B Ayala Diego D Kamdem Colince C Santolamazza Federica F Guelbeogo Wamdaogo Moussa WM Sagnon N'Falé N Petrarca Vincenzo V Fontenille Didier D Besansky Nora J NJ Antonio-Nkondjio Christophe C Dabiré Roch Kounbobr RK Della Torre Alessandra A Simard Frédéric F Costantini Carlo C

Evolutionary applications 20171005 10

Explaining how and why reproductive isolation evolves and determining which forms of reproductive isolation have the largest impact on the process of population divergence are major goals in the study of speciation. By studying recent adaptive radiations in incompletely isolated taxa, it is possible to identify barriers involved at early divergence before other confounding barriers emerge after speciation is complete. Sibling species of the <i>Anopheles gambiae</i> complex offer opportunities to ...[more]

PMID: 29151864

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Project description:BACKGROUND:Accurate Anopheles species identification is key for effective malaria vector control. Identification primarily depends on morphological analysis of field samples as well as molecular species-specific identifications. During an intra-laboratory assessment (proficiency testing) of the Anopheles funestus group multiplex PCR assay, it was noted that Anopheles arabiensis can be misidentified as Anopheles leesoni, a zoophilic member of the An. funestus group. The aim of this project was, therefore, to ascertain whether other members of the Anopheles gambiae complex can also be misidentified as An. leesoni when using the standard An. funestus multiplex PCR. METHODS:The An. funestus multiplex PCR was used to amplify DNA from An. gambiae complex specimens. These included specimens from the laboratory colonies and field samples from the Democratic Republic of Congo. Amplified DNA from these specimens, using the universal (UV) and An. leesoni species-specific primers (LEES), were sequence analysed. Additionally, An. leesoni DNA was processed through the diagnostic An. gambiae multiplex PCR to determine if this species can be misidentified as a member of the An. gambiae complex. RESULTS:Laboratory-colonized as well as field-collected samples of An. arabiensis, An. gambiae, Anopheles merus, Anopheles quadriannulatus, Anopheles coluzzii as well as Anopheles moucheti produced an amplicon of similar size to that of An. leesoni when using an An. funestus multiplex PCR. Sequence analysis confirmed that the UV and LEES primers amplify a segment of the ITS2 region of members of the An. gambiae complex and An. moucheti. The reverse was not true, i.e. the An. gambiae multiplex PCR does not amplify DNA from An. leesoni. CONCLUSION:This investigation shows that An. arabiensis, An. gambiae, An. merus, An. quadriannulatus, An. coluzzii and An. moucheti can be misidentified as An. leesoni when using An. funestus multiplex PCR. This shows the importance of identifying specimens using standard morphological dichotomous keys as far as possible prior to the use of appropriate PCR-based identification methods. Should there be doubt concerning field-collected specimens molecularly identified as An. leesoni, the An. gambiae multiplex PCR and sequencing of the internal transcribed spacer 2 (ITS2) can be used to eliminate false identifications.

Project description:The Anopheles gambiae species complex includes at least seven morphologically indistinguishable species, one of which, Anopheles gambiae sensu stricto, is the primary mosquito vector responsible for the transmission of malaria across sub-Saharan Africa. Sympatric ecological diversification of An. gambiae s.s. is in progress within this complex, leading to the emergence of at least two incipient species (the M and S molecular forms now recognized as good species and named An. coluzzii and An. gambiae respectively) that show heterogeneous levels of divergence in most parts of Africa. However, this process seems to have broken down in coastal areas of West Africa at the extreme edge of the distribution. We undertook a longitudinal study to describe An. gambiae s.s. populations collected from two inland transects with different ecological characteristics in south-eastern Senegal. Analysis of samples collected from 20 sites across these two transects showed the M and S molecular forms coexisted at almost all sampled sites. Overall, similar hybridization rates (2.16% and 1.86%) were recorded in the two transects; sites with relatively high frequencies of M/S hybrids (up to 7%) were clustered toward the north-western part of both transects, often near urban settings. Estimated inbreeding indices for this putative speciation event varied spatially (range: 0.52-1), with hybridization rates being generally lower than expected under panmictic conditions. Such observations suggest substantial reproductive isolation between the M and S molecular forms, and further support the ongoing process of speciation in these inland areas. According to a recent reclassification of the An. gambiae complex, the M and S molecular forms from this zone correspond to An. coluzzii and An. gambiae, respectively. There is considerable evidence that these molecular forms differ in their behavioural and ecological characteristics. Detailed study of these characteristics will allow the development and implementation of better insect control strategies for combating malaria.

Dataset Information

Dissecting functional components of reproductive isolation among closely related sympatric species of the Anopheles gambiae complex.

Publications

Dissecting functional components of reproductive isolation among closely related sympatric species of the <i>Anopheles gambiae</i> complex.

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