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

Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing JM, Fontenille D, Besansky NJ, Costantini C - BMC Ecol. (2009)

Bottom Line: Population structure analysis identified three chromosomal clusters, each containing a mixture of M and S specimens.Rather, they are involved in ecological specialization to a similar extent in both genetic backgrounds, and most probably predated lineage splitting between molecular forms.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire de Lutte contre les Insectes Nuisibles, Institut de Recherche pour le Développement, UR016, 911 Av. Agropolis, Cedex 5, Montpellier, France. frederic.simard@ird.fr

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

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Habitat suitability maps of An. gambiae complex mosquitoes in Cameroon. Habitat suitability (HS) maps showing presence points (black dots) that were used for the ENFA for members of the An. gambiae complex in Cameroon. Habitat quality is classified in four classes of decreasing suitability: optimal (red), suitable (orange), marginal (yellow) and unsuitable (white). A: An. gambiae S form. HS map based on N = 328 presence points showing optimal (4.0% of the total study area), suitable (12.3%), marginal (25.3%) and unsuitable (58.4%) habitat. B: An. gambiae M form. HS map based on N = 80 presence points showing optimal (2.3% of the total study area), suitable (18.3%), marginal (34.7%) and unsuitable (44.7%) habitat. C: An. arabiensis. HS map based on N = 189 presence points showing optimal (5.6% of the total study area), suitable (22.0%), marginal (3.6%) and unsuitable (68.8%) habitat.
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Figure 3: Habitat suitability maps of An. gambiae complex mosquitoes in Cameroon. Habitat suitability (HS) maps showing presence points (black dots) that were used for the ENFA for members of the An. gambiae complex in Cameroon. Habitat quality is classified in four classes of decreasing suitability: optimal (red), suitable (orange), marginal (yellow) and unsuitable (white). A: An. gambiae S form. HS map based on N = 328 presence points showing optimal (4.0% of the total study area), suitable (12.3%), marginal (25.3%) and unsuitable (58.4%) habitat. B: An. gambiae M form. HS map based on N = 80 presence points showing optimal (2.3% of the total study area), suitable (18.3%), marginal (34.7%) and unsuitable (44.7%) habitat. C: An. arabiensis. HS map based on N = 189 presence points showing optimal (5.6% of the total study area), suitable (22.0%), marginal (3.6%) and unsuitable (68.8%) habitat.

Mentions: Applying MacArthurs' broken-stick rule, ten factors, explaining 93.5% of the overall information, were retained to calculate the habitat suitability of the S form (Additional file 1). As shown in Figure 3A, a core of favourable habitat for this taxon is found in the dry savanna of North Cameroon, encompassing the large region where cotton is produced in this country. Habitat suitability decreases when moving northwards, in the most arid area around Lake Chad, and southwards, toward more humid environments. Patches of favourable habitat however, are also found in areas where the vegetation cover is highly degraded by human activities, such as the hilly landscapes at the fringe of the Adamaoua and Western Highlands, and the densely populated area around Yaoundé. The humid Atlantic Coast, as well as the remote regions of the deep evergreen rainforest of the Congo basin in the East or the uninhabited natural game reserves in the North-central part of the country, appear unsuitable for this mosquito.


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

Simard F, Ayala D, Kamdem GC, Pombi M, Etouna J, Ose K, Fotsing JM, Fontenille D, Besansky NJ, Costantini C - BMC Ecol. (2009)

Habitat suitability maps of An. gambiae complex mosquitoes in Cameroon. Habitat suitability (HS) maps showing presence points (black dots) that were used for the ENFA for members of the An. gambiae complex in Cameroon. Habitat quality is classified in four classes of decreasing suitability: optimal (red), suitable (orange), marginal (yellow) and unsuitable (white). A: An. gambiae S form. HS map based on N = 328 presence points showing optimal (4.0% of the total study area), suitable (12.3%), marginal (25.3%) and unsuitable (58.4%) habitat. B: An. gambiae M form. HS map based on N = 80 presence points showing optimal (2.3% of the total study area), suitable (18.3%), marginal (34.7%) and unsuitable (44.7%) habitat. C: An. arabiensis. HS map based on N = 189 presence points showing optimal (5.6% of the total study area), suitable (22.0%), marginal (3.6%) and unsuitable (68.8%) habitat.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2698860&req=5

Figure 3: Habitat suitability maps of An. gambiae complex mosquitoes in Cameroon. Habitat suitability (HS) maps showing presence points (black dots) that were used for the ENFA for members of the An. gambiae complex in Cameroon. Habitat quality is classified in four classes of decreasing suitability: optimal (red), suitable (orange), marginal (yellow) and unsuitable (white). A: An. gambiae S form. HS map based on N = 328 presence points showing optimal (4.0% of the total study area), suitable (12.3%), marginal (25.3%) and unsuitable (58.4%) habitat. B: An. gambiae M form. HS map based on N = 80 presence points showing optimal (2.3% of the total study area), suitable (18.3%), marginal (34.7%) and unsuitable (44.7%) habitat. C: An. arabiensis. HS map based on N = 189 presence points showing optimal (5.6% of the total study area), suitable (22.0%), marginal (3.6%) and unsuitable (68.8%) habitat.
Mentions: Applying MacArthurs' broken-stick rule, ten factors, explaining 93.5% of the overall information, were retained to calculate the habitat suitability of the S form (Additional file 1). As shown in Figure 3A, a core of favourable habitat for this taxon is found in the dry savanna of North Cameroon, encompassing the large region where cotton is produced in this country. Habitat suitability decreases when moving northwards, in the most arid area around Lake Chad, and southwards, toward more humid environments. Patches of favourable habitat however, are also found in areas where the vegetation cover is highly degraded by human activities, such as the hilly landscapes at the fringe of the Adamaoua and Western Highlands, and the densely populated area around Yaoundé. The humid Atlantic Coast, as well as the remote regions of the deep evergreen rainforest of the Congo basin in the East or the uninhabited natural game reserves in the North-central part of the country, appear unsuitable for this mosquito.

Bottom Line: Population structure analysis identified three chromosomal clusters, each containing a mixture of M and S specimens.Rather, they are involved in ecological specialization to a similar extent in both genetic backgrounds, and most probably predated lineage splitting between molecular forms.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire de Lutte contre les Insectes Nuisibles, Institut de Recherche pour le Développement, UR016, 911 Av. Agropolis, Cedex 5, Montpellier, France. frederic.simard@ird.fr

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

Show MeSH
Related in: MedlinePlus