Open Access Research article

Chromosomal plasticity and evolutionary potential in the malaria vector Anopheles gambiae sensu stricto: insights from three decades of rare paracentric inversions

Marco Pombi12*, Beniamino Caputo12, Frederic Simard3, Maria A Di Deco12, Mario Coluzzi1, Alessandra della Torre12, Carlo Costantini4, Nora J Besansky5* and Vincenzo Petrarca26

Author Affiliations

1 Sezione di Parassitologia, Dipartimento di Scienze di Sanità Pubblica, Università di Roma "Sapienza", P.le Aldo Moro 5, 00185 Roma, Italy

2 Istituto Pasteur – Fondazione Cenci Bolognetti, P.le Aldo Moro 5, 00185 Roma, Italy

3 Institut de Recherche pour le Développement, Unité de Recherche 016, and Institut de Recherche en Sciences de la Santé, BP 545 Bobo Dioulasso, Burkina Faso

4 Institut de Recherche pour le Développement, Unité de Recherche 016, and Organisation de Coordination pour la lutte contre les Endémies en Afrique Centrale, BP 288 Yaoundé, Cameroon

5 Eck Family Center for Global Health and Infectious Diseases, Dept. of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA

6 Dipartimento di Genetica e Biologia Molecolare, Università di Roma "Sapienza", P.le Aldo Moro 5, 00185 Roma, Italy

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BMC Evolutionary Biology 2008, 8:309  doi:10.1186/1471-2148-8-309

Published: 10 November 2008

Abstract

Background

In the Anopheles gambiae complex, paracentric chromosomal inversions are non-randomly distributed along the complement: 18/31 (58%) of common polymorphic inversions are on chromosome arm 2R, which represents only ~30% of the complement. Moreover, in An. gambiae sensu stricto, 6/7 common polymorphic inversions occur on 2R. Most of these inversions are considered markers of ecological adaptation that increase the fitness of the carriers of alternative karyotypes in contrasting habitats. However, little is known about the evolutionary forces responsible for their origin and subsequent establishment in field populations.

Results

Here, we present data on 82 previously undescribed rare chromosomal inversions (RCIs) recorded during extensive field sampling in 16 African countries over a 30 year period, which may shed light on the dynamics of chromosomal plasticity in An. gambiae. We analyzed breakpoint distribution, length, and geographic distribution of RCIs, and compared these measures to those of the common inversions. We found that RCIs, like common inversions, are disproportionately clustered on 2R, which may indicate that this arm is especially prone to breakages. However, contrasting patterns were observed between the geographic distribution of common inversions and RCIs. RCIs were equally frequent across biomes and on both sides of the Great Rift Valley (GRV), whereas common inversions predominated in arid ecological settings and west of the GRV. Moreover, the distribution of RCI lengths followed a random pattern while common inversions were significantly less frequent at shorter lengths.

Conclusion

Because 17/82 (21%) RCIs were found repeatedly at very low frequencies – at the same sampling location in different years and/or in different sampling locations – we suggest that RCIs are subject mainly to drift under unperturbed ecological conditions. Nevertheless, RCIs may represent an important reservoir of genetic variation for An. gambiae in response to environmental changes, further testifying to the considerable evolutionary potential hidden within this pan-African malaria vector.