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Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation.

ABSTRACT: Speciation among members of the Anopheles gambiae complex is thought to be promoted by disruptive selection and ecological divergence acting on sets of adaptation genes protected from recombination by polymorphic paracentric chromosomal inversions. However, shared chromosomal polymorphisms between the M and S molecular forms of An. gambiae and insufficient information about their relationship with ecological divergence challenge this view. We used Geographic Information Systems, Ecological Niche Factor Analysis, and Bayesian multilocus genetic clustering to explore the nature and extent of ecological and chromosomal differentiation of M and S across all the biogeographic domains of Cameroon in Central Africa, in order to understand the role of chromosomal arrangements in ecological specialisation within and among molecular forms.Species distribution modelling with presence-only data revealed differences in the ecological niche of both molecular forms and the sibling species, An. arabiensis. The fundamental environmental envelope of the two molecular forms, however, overlapped to a large extent in the rainforest, where they occurred in sympatry. The S form had the greatest niche breadth of all three taxa, whereas An. arabiensis and the M form had the smallest niche overlap. Correspondence analysis of M and S karyotypes confirmed that molecular forms shared similar combinations of chromosomal inversion arrangements in response to the eco-climatic gradient defining the main biogeographic domains occurring across Cameroon. Savanna karyotypes of M and S, however, segregated along the smaller-scale environmental gradient defined by the second ordination axis. Population structure analysis identified three chromosomal clusters, each containing a mixture of M and S specimens. In both M and S, alternative karyotypes were segregating in contrasted environments, in agreement with a strong ecological adaptive value of chromosomal inversions.Our data suggest that inversions on the second chromosome of An. gambiae are not causal to the evolution of reproductive isolation between the M and S forms. Rather, they are involved in ecological specialization to a similar extent in both genetic backgrounds, and most probably predated lineage splitting between molecular forms. However, because chromosome-2 inversions promote ecological divergence, resulting in spatial and/or temporal isolation between ecotypes, they might favour mutations in other ecologically significant genes to accumulate in unlinked chromosomal regions. When such mutations occur in portions of the genome where recombination is suppressed, such as the pericentromeric regions known as speciation islands in An. gambiae, they would contribute further to the development of reproductive isolation.

SUBMITTER: Simard F

PROVIDER: S-EPMC2698860 | biostudies-other | 2009 May

REPOSITORIES: biostudies-other

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Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation.

Simard Frédéric F Ayala Diego D Kamdem Guy Colince GC Pombi Marco M Etouna Joachim J Ose Kenji K Fotsing Jean-Marie JM Fontenille Didier D Besansky Nora J NJ Costantini Carlo C

BMC ecology 20090521

<h4>Background</h4>Speciation among members of the Anopheles gambiae complex is thought to be promoted by disruptive selection and ecological divergence acting on sets of adaptation genes protected from recombination by polymorphic paracentric chromosomal inversions. However, shared chromosomal polymorphisms between the M and S molecular forms of An. gambiae and insufficient information about their relationship with ecological divergence challenge this view. We used Geographic Information System ...[more]

PMID: 19460146

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Project description:BackgroundSINEs (Short INterspersed Elements) are homoplasy-free and co-dominant genetic markers which are considered to represent useful tools for population genetic studies, and could help clarifying the speciation processes ongoing within the major malaria vector in Africa, Anopheles gambiae s.s. Here, we report the results of the analysis of the insertion polymorphism of a nearly 200 bp-long SINE (SINE200) within genome areas of high differentiation (i.e. "speciation islands") of M and S A. gambiae molecular forms.MethodsA SINE-PCR approach was carried out on thirteen SINE200 insertions in M and S females collected along the whole range of distribution of A. gambiae s.s. in sub-Saharan Africa. Ten specimens each for Anopheles arabiensis, Anopheles melas, Anopheles quadriannulatus A and 15 M/S hybrids from laboratory crosses were also analysed.ResultsEight loci were successfully amplified and were found to be specific for A. gambiae s.s.: 5 on 2L chromosome and one on X chromosome resulted monomorphic, while two loci positioned respectively on 2R (i.e. S200 2R12D) and X (i.e. S200 X6.1) chromosomes were found to be polymorphic. S200 2R12D was homozygote for the insertion in most S-form samples, while intermediate levels of polymorphism were shown in M-form, resulting in an overall high degree of genetic differentiation between molecular forms (Fst = 0.46 p < 0.001) and within M-form (Fst = 0.46 p < 0.001). The insertion of S200 X6.1 was found to be fixed in all M- and absent in all S-specimens. This led to develop a novel easy-to-use PCR approach to straightforwardly identify A. gambiae molecular forms. This novel approach allows to overcome the constraints associated with markers on the rDNA region commonly used for M and S identification. In fact, it is based on a single copy and irreversible SINE200 insertion and, thus, is not subjected to peculiar evolutionary patterns affecting rDNA markers, e.g. incomplete homogenization of the arrays through concerted evolution and/or mixtures of M and S IGS-sequences among the arrays of single chromatids.ConclusionThe approach utilized allowed to develop new easy-to-use co-dominant markers for the analysis of genetic differentiation between M and S-forms and opens new perspectives in the study of the speciation process ongoing within A. gambiae.

Project description:The African malaria mosquito, Anopheles gambiae sensu stricto (A. gambiae), provides a unique opportunity to study the evolution of reproductive isolation because it is divided into two sympatric, partially isolated subtaxa known as M form and S form. With the annotated genome of this species now available, high-throughput techniques can be applied to locate and characterize the genomic regions contributing to reproductive isolation. In order to quantify patterns of differentiation within A. gambiae, we hybridized population samples of genomic DNA from each form to Affymetrix GeneChip microarrays. We found that three regions, together encompassing less than 2.8 Mb, are the only locations where the M and S forms are significantly differentiated. Two of these regions are adjacent to centromeres, on Chromosomes 2L and X, and contain 50 and 12 predicted genes, respectively. Sequenced loci in these regions contain fixed differences between forms and no shared polymorphisms, while no fixed differences were found at nearby control loci. The third region, on Chromosome 2R, contains only five predicted genes; fixed differences in this region were also verified by direct sequencing. These "speciation islands" remain differentiated despite considerable gene flow, and are therefore expected to contain the genes responsible for reproductive isolation. Much effort has recently been applied to locating the genes and genetic changes responsible for reproductive isolation between species. Though much can be inferred about speciation by studying taxa that have diverged for millions of years, studying differentiation between taxa that are in the early stages of isolation will lead to a clearer view of the number and size of regions involved in the genetics of speciation. Despite appreciable levels of gene flow between the M and S forms of A. gambiae, we were able to isolate three small regions of differentiation where genes responsible for ecological and behavioral isolation are likely to be located. We expect reproductive isolation to be due to changes at a small number of loci, as these regions together contain only 67 predicted genes. Concentrating future mapping experiments on these regions should reveal the genes responsible for reproductive isolation between forms.

Project description:BackgroundOngoing lineage splitting within the African malaria mosquito Anopheles gambiae is compatible with ecological speciation, the evolution of reproductive isolation by divergent natural selection acting on two populations exploiting alternative resources. Divergence between two molecular forms (M and S) identified by fixed differences in rDNA, and characterized by marked, although incomplete, reproductive isolation is occurring in West and Central Africa. To elucidate the role that ecology and geography play in speciation, we carried out a countrywide analysis of An. gambiae M and S habitat requirements, and that of their chromosomal variants, across Burkina Faso.ResultsMaps of relative abundance by geostatistical interpolators produced a distinct pattern of distribution: the M-form dominated in the northernmost arid zones, the S-form in the more humid southern regions. Maps of habitat suitability, quantified by Ecological Niche Factor Analysis based on 15 eco-geographical variables revealed less contrast among forms. M was peculiar as it occurred proportionally more in habitat of marginal quality. Measures of ecological niche breadth and overlap confirmed the mismatch between the fundamental and realized patterns of habitat occupation: forms segregated more than expected from the extent of divergence of their environmental envelope--a signature of niche expansion. Classification of chromosomal arm 2R karyotypes by multilocus genetic clustering identified two clusters loosely corresponding to molecular forms, with 'mismatches' representing admixed individuals due to shared ancestral polymorphism and/or residual hybridization. In multivariate ordination space, these karyotypes plotted in habitat of more marginal quality compared to non-admixed, 'typical', karyotypes. The distribution of 'typical' karyotypes along the main eco-climatic gradient followed a consistent pattern within and between forms, indicating an adaptive role of inversions at this geographical scale.ConclusionEcological segregation between M and S is consistent with niche expansion into marginal habitats by chromosomal inversion variants during early lineage divergence; presumably, this process is promoted by inter-karyotype competition in the higher-quality core habitat. We propose that the appearance of favourable allelic combinations in other regions of suppressed recombination (e.g. pericentromeric portions defining speciation islands in An. gambiae) fosters development of reproductive isolation to protect linkage between separate chromosomal regions.

Project description:The geographic and temporal distribution of M and S molecular forms of the major Afrotropical malaria vector species Anopheles gambiae s.s. at the western extreme of their range of distribution has never been investigated in detail.Collections of indoor-resting An. gambiae s.l. females were carried out along a ca. 400 km west to east transect following the River Gambia from the western coastal region of The Gambia to south-eastern Senegal during 2005 end of rainy season/early dry season and the 2006 rainy season. Specimens were identified to species and molecular forms by PCR-RFLP and the origin of blood-meal of fed females was determined by ELISA test.Over 4,000 An. gambiae s.l. adult females were collected and identified, 1,041 and 3,038 in 2005 and 2006, respectively. M-form was mainly found in sympatry with Anopheles melas and S-form in the western part of the transect, and with Anopheles arabiensis in the central part. S-form was found to prevail in rural Sudan-Guinean savannah areas of Eastern Senegal, in sympatry with An. arabiensis. Anopheles melas and An. arabiensis relative frequencies were generally lower in the rainy season samples, when An. gambiae s.s. was prevailing. No large seasonal fluctuations were observed for M and S-forms. In areas where both M and S were recorded, the frequency of hybrids between them ranged from to 0.6% to 7%.The observed pattern of taxa distribution supports the hypothesis of a better adaptation of M-form to areas characterized by water-retaining alluvial deposits along the Gambia River, characterized by marshy vegetation, mangrove woods and rice cultivations. In contrast, the S-form seems to be better adapted to free-draining soil, covered with open woodland savannah or farmland, rich in temporary larval breeding sites characterizing mainly the eastern part of the transect, where the environmental impact of the Gambia River is much less profound and agricultural activities are mainly rain-dependent. Very interestingly, the observed frequency of hybridization between the molecular forms along the whole transect was much higher than has been reported so far for other areas.The results support a bionomic divergence between the M and S-forms, and suggest that the western extreme of An. gambiae s.s. geographical distribution may represent an area of higher-than-expected hybridization between the two molecular forms.

Project description:The need for evidence-based data, to inform policy decisions on malaria vector control interventions in Nigeria, necessitated the establishment of mosquito surveillance sites in a few States in Nigeria. In order to make evidence-based-decisions, predictive studies using available data becomes imperative. We therefore predict the distribution of the major members of the Anopheles gambiae s.l. in Nigeria. Immature stages of Anopheles were collected from 72 study locations which span throughout the year 2020 resulted in the identification of over 60,000 Anopheline mosquitoes. Of these, 716 breeding sites were identified with the presence of one or more vector species from the An. gambiae complex and were subsequently used for modelling the potential geographical distribution of these important malaria vectors. Maximum Entropy (MaxEnt) distribution modeling was used to predict their potentially suitable vector habitats across Nigeria. A total of 23 environmental variables (19 bioclimatic and four topographic) were used in the model resulting in maps of the potential geographical distribution of three dominant vector species under current climatic conditions. Members of the An. gambiae complex dominated the collections (98%) with Anopheles stephensi, Anopheles coustani, Anopheles funestus, Anopheles moucheti, Anopheles nilli also present. An almost equal distribution of the two efficient vectors of malaria, An. gambiae and Anopheles coluzzii, were observed across the 12 states included in the survey. Anopheles gambiae and Anopheles coluzzii had almost equal, well distributed habitat suitability patterns with the latter having a slight range expansion. However, the central part of Nigeria (Abuja) and some highly elevated areas (Jos) in the savannah appear not suitable for the proliferation of these species. The most suitable habitat for Anopheles arabiensis was mainly in the South-west and North-east. The results of this study provide a baseline allowing decision makers to monitor the distribution of these species and establish a management plan for future national mosquito surveillance and control programs in Nigeria.

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Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation.

Publications

Ecological niche partitioning between Anopheles gambiae molecular forms in Cameroon: the ecological side of speciation.

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