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

Pombi M, Caputo B, Simard F, Di Deco MA, Coluzzi M, della Torre A, Costantini C, Besansky NJ, Petrarca V - BMC Evol. Biol. (2008)

Bottom Line: 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.Moreover, the distribution of RCI lengths followed a random pattern while common inversions were significantly less frequent at shorter lengths.

View Article: PubMed Central - HTML - PubMed

Affiliation: Sezione di Parassitologia, Dipartimento di Scienze di Sanità Pubblica, Università di Roma Sapienza, P. Aldo Moro 5, 00185 Roma, Italy. marco.pombi@uniroma1.it

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 approximately 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.

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Length distribution of rare chromosomal inversions for chromosome arm 2R of Anopheles gambiae sensu stricto. Distribution expected from the random breakage model (solid line), plotted along with the observed distribution of relative tract lengths (circles).
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Figure 2: Length distribution of rare chromosomal inversions for chromosome arm 2R of Anopheles gambiae sensu stricto. Distribution expected from the random breakage model (solid line), plotted along with the observed distribution of relative tract lengths (circles).

Mentions: If chromosomal segments break at random, the distribution of observed inversion tract lengths should follow a random pattern. We tested this hypothesis on chromosome arm 2R, where most (67/82) RCIs and most (6/7) common inversions are observed. Given 67 inversions, we simulated their length distribution if they were generated under a random breakage model [22], and compared this to the observed length distribution of RCIs (Fig. 2). The observed distribution departed significantly from that expected under a model of random breakage (Kolmogorov-Smirnov one-sample test, P < 0.01) due to a deficit of shorter lengths. Although this result broadly agrees with emerging evidence against the random breakage model [25-30], it should be treated with caution as the sample of RCIs is biased to an unknown extent toward larger inversion tracts: small inversions are difficult or impossible to observe microscopically, particularly when fixed. In fact, Ranz et al. [31] mapping by in situ hybridization 33 DNA clones containing protein-coding genes in Drosophila repleta and D. buzzatii, showed extensive reorganization via paracentric inversions, including short ones that had gone undetected with the classical polytene chromosome analysis.


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

Pombi M, Caputo B, Simard F, Di Deco MA, Coluzzi M, della Torre A, Costantini C, Besansky NJ, Petrarca V - BMC Evol. Biol. (2008)

Length distribution of rare chromosomal inversions for chromosome arm 2R of Anopheles gambiae sensu stricto. Distribution expected from the random breakage model (solid line), plotted along with the observed distribution of relative tract lengths (circles).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2654565&req=5

Figure 2: Length distribution of rare chromosomal inversions for chromosome arm 2R of Anopheles gambiae sensu stricto. Distribution expected from the random breakage model (solid line), plotted along with the observed distribution of relative tract lengths (circles).
Mentions: If chromosomal segments break at random, the distribution of observed inversion tract lengths should follow a random pattern. We tested this hypothesis on chromosome arm 2R, where most (67/82) RCIs and most (6/7) common inversions are observed. Given 67 inversions, we simulated their length distribution if they were generated under a random breakage model [22], and compared this to the observed length distribution of RCIs (Fig. 2). The observed distribution departed significantly from that expected under a model of random breakage (Kolmogorov-Smirnov one-sample test, P < 0.01) due to a deficit of shorter lengths. Although this result broadly agrees with emerging evidence against the random breakage model [25-30], it should be treated with caution as the sample of RCIs is biased to an unknown extent toward larger inversion tracts: small inversions are difficult or impossible to observe microscopically, particularly when fixed. In fact, Ranz et al. [31] mapping by in situ hybridization 33 DNA clones containing protein-coding genes in Drosophila repleta and D. buzzatii, showed extensive reorganization via paracentric inversions, including short ones that had gone undetected with the classical polytene chromosome analysis.

Bottom Line: 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.Moreover, the distribution of RCI lengths followed a random pattern while common inversions were significantly less frequent at shorter lengths.

View Article: PubMed Central - HTML - PubMed

Affiliation: Sezione di Parassitologia, Dipartimento di Scienze di Sanità Pubblica, Università di Roma Sapienza, P. Aldo Moro 5, 00185 Roma, Italy. marco.pombi@uniroma1.it

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 approximately 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.

Show MeSH
Related in: MedlinePlus