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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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Ecological niche overlap along the discriminant factor. Ecological niche overlap between An. gambiae M and S forms (A), M and An. arabiensis (B) and S and An. arabiensis (C). Left, frequency plot along the discriminant factor showing niche breadth and overlap; Right, schematic representation of the discriminant function showing the contribution of the different eco-geographical variables (EGVs, see Methods) to the discriminant factor.
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Figure 4: Ecological niche overlap along the discriminant factor. Ecological niche overlap between An. gambiae M and S forms (A), M and An. arabiensis (B) and S and An. arabiensis (C). Left, frequency plot along the discriminant factor showing niche breadth and overlap; Right, schematic representation of the discriminant function showing the contribution of the different eco-geographical variables (EGVs, see Methods) to the discriminant factor.

Mentions: Results of the discriminant analysis of the ecological niche of species pairs are shown in Figure 4 and Table 1. In all pair comparisons, the discriminant axis did not segregate the two species under scrutiny. However, the discriminant functions indicate for which eco-geographical variables the species differed the most (Figure 4). Arid conditions (e.g., higher sunlight exposure, higher temperatures, higher levels of evapotranspiration) in an open environment favoured the S form and An. arabiensis over the M form. On the other hand, a higher frequency of forest, higher water vapour pressure and higher rainfall correlated with the occurrence of the M form. Niche differentiation between the S form and An. arabiensis was mainly due to the ability of the S form to colonize forested areas in South Cameroon, while the suitability of arid environments was more pronounced for An. arabiensis. Niche breadth indices indicated that the habitat niche of the S form is substantially larger than that of the M form and An. arabiensis (Table 1). The Lloyd's asymmetric ecological niche overlap indices of the S form over the niche of the M form and An. arabiensis were 13.7 and 18.1, respectively, whereas the reciprocal overlap was only 3.3 with the M form, and 10.5 with An. arabiensis. These findings indicate that the habitat width of An. gambiae S largely encompassed the habitat width of the M form, while the overlap with the M form occurred only in a limited fraction of the S range in Cameroon. Interspecific overlap was more pronounced between An. arabiensis and the S form, whereas An. arabiensis and the M form occurred in opposite geographical areas of Cameroon, resulting in very limited overlap between their respective ecological niches (Table 1).


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)

Ecological niche overlap along the discriminant factor. Ecological niche overlap between An. gambiae M and S forms (A), M and An. arabiensis (B) and S and An. arabiensis (C). Left, frequency plot along the discriminant factor showing niche breadth and overlap; Right, schematic representation of the discriminant function showing the contribution of the different eco-geographical variables (EGVs, see Methods) to the discriminant factor.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Ecological niche overlap along the discriminant factor. Ecological niche overlap between An. gambiae M and S forms (A), M and An. arabiensis (B) and S and An. arabiensis (C). Left, frequency plot along the discriminant factor showing niche breadth and overlap; Right, schematic representation of the discriminant function showing the contribution of the different eco-geographical variables (EGVs, see Methods) to the discriminant factor.
Mentions: Results of the discriminant analysis of the ecological niche of species pairs are shown in Figure 4 and Table 1. In all pair comparisons, the discriminant axis did not segregate the two species under scrutiny. However, the discriminant functions indicate for which eco-geographical variables the species differed the most (Figure 4). Arid conditions (e.g., higher sunlight exposure, higher temperatures, higher levels of evapotranspiration) in an open environment favoured the S form and An. arabiensis over the M form. On the other hand, a higher frequency of forest, higher water vapour pressure and higher rainfall correlated with the occurrence of the M form. Niche differentiation between the S form and An. arabiensis was mainly due to the ability of the S form to colonize forested areas in South Cameroon, while the suitability of arid environments was more pronounced for An. arabiensis. Niche breadth indices indicated that the habitat niche of the S form is substantially larger than that of the M form and An. arabiensis (Table 1). The Lloyd's asymmetric ecological niche overlap indices of the S form over the niche of the M form and An. arabiensis were 13.7 and 18.1, respectively, whereas the reciprocal overlap was only 3.3 with the M form, and 10.5 with An. arabiensis. These findings indicate that the habitat width of An. gambiae S largely encompassed the habitat width of the M form, while the overlap with the M form occurred only in a limited fraction of the S range in Cameroon. Interspecific overlap was more pronounced between An. arabiensis and the S form, whereas An. arabiensis and the M form occurred in opposite geographical areas of Cameroon, resulting in very limited overlap between their respective ecological niches (Table 1).

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