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

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          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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          Most cited references89

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          Chromosome inversions, local adaptation and speciation.

          We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.
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            On the relationship between niche and distribution

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              Evaluating the ability of habitat suitability models to predict species presences

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                Author and article information

                Journal
                BMC Ecol
                BMC Ecology
                BioMed Central
                1472-6785
                2009
                21 May 2009
                : 9
                : 17
                Affiliations
                [1 ]Laboratoire de Lutte contre les Insectes Nuisibles (LIN), Institut de Recherche pour le Développement (IRD), UR016, 911 Av. Agropolis, 34394 Cedex 5, Montpellier, France
                [2 ]Laboratoire de Recherche sur le Paludisme, Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale (OCEAC), B.P. 288, Yaoundé, Cameroon
                [3 ]Sezione di Parassitologia, Dipartimento di Scienze di Sanità Pubblica, Università di Roma "La Sapienza", P.le Aldo Moro 5, 00185, Rome, Italy
                [4 ]Institut National de Cartographie (INC), Département de Recherches Géographiques, B.P. 157, Yaoundé, Cameroun
                [5 ]Institut de Recherche pour le Développement (IRD), US140, BP 165, Cayenne, Guyane française
                [6 ]Eck Institute for Global Health, Department of Biological Sciences, 317 Galvin Life Sciences Bldg., University of Notre Dame, Notre Dame, IN 46556-0369, USA
                [7 ]Institut de Recherche en Sciences de la Santé – Direction Régionale de l'Ouest (IRSS-DRO), B.P. 545, Bobo-Dioulasso, Burkina Faso
                [8 ]IRD/IRSS-DRO, BP 545, Bobo-Dioulasso, Burkina Faso
                Article
                1472-6785-9-17
                10.1186/1472-6785-9-17
                2698860
                19460146
                8f3c60d1-7d31-4da6-80b4-9efc7d1995f0
                Copyright © 2009 Simard et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 October 2008
                : 21 May 2009
                Categories
                Research Article

                Ecology
                Ecology

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