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Open Access Highly Accessed Research article

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

Frédéric Simard128*, Diego Ayala1, Guy Colince Kamdem12, Marco Pombi3, Joachim Etouna4, Kenji Ose5, Jean-Marie Fotsing5, Didier Fontenille1, Nora J Besansky6 and Carlo Costantini17

Author 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

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BMC Ecology 2009, 9:17  doi:10.1186/1472-6785-9-17

Published: 21 May 2009

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.