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Arm-specific dynamics of chromosome evolution in malaria mosquitoes.

Sharakhova MV, Xia A, Leman SC, Sharakhov IV - BMC Evol. Biol. (2011)

Bottom Line: To gain a better understanding of the arm-specific differences in the rates of genome rearrangements, we compared gene orders and established syntenic relationships among Anopheles gambiae, Anopheles funestus, and Anopheles stephensi.Our results suggest that natural selection favors specific gene combinations within polymorphic inversions when distant species are exposed to similar environmental pressures.Our data support the chromosomal arm specificity in rates of gene order disruption during mosquito evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, Virginia Tech, Blacksburg, VA 24061, USA.

ABSTRACT

Background: The malaria mosquito species of subgenus Cellia have rich inversion polymorphisms that correlate with environmental variables. Polymorphic inversions tend to cluster on the chromosomal arms 2R and 2L but not on X, 3R and 3L in Anopheles gambiae and homologous arms in other species. However, it is unknown whether polymorphic inversions on homologous chromosomal arms of distantly related species from subgenus Cellia nonrandomly share similar sets of genes. It is also unclear if the evolutionary breakage of inversion-poor chromosomal arms is under constraints.

Results: To gain a better understanding of the arm-specific differences in the rates of genome rearrangements, we compared gene orders and established syntenic relationships among Anopheles gambiae, Anopheles funestus, and Anopheles stephensi. We provided evidence that polymorphic inversions on the 2R arms in these three species nonrandomly captured similar sets of genes. This nonrandom distribution of genes was not only a result of preservation of ancestral gene order but also an outcome of extensive reshuffling of gene orders that created new combinations of homologous genes within independently originated polymorphic inversions. The statistical analysis of distribution of conserved gene orders demonstrated that the autosomal arms differ in their tolerance to generating evolutionary breakpoints. The fastest evolving 2R autosomal arm was enriched with gene blocks conserved between only a pair of species. In contrast, all identified syntenic blocks were preserved on the slowly evolving 3R arm of An. gambiae and on the homologous arms of An. funestus and An. stephensi.

Conclusions: Our results suggest that natural selection favors specific gene combinations within polymorphic inversions when distant species are exposed to similar environmental pressures. This knowledge could be useful for the discovery of genes responsible for an association of inversion polymorphisms with phenotypic variations in multiple species. Our data support the chromosomal arm specificity in rates of gene order disruption during mosquito evolution. We conclude that the distribution of breakpoint regions is evolutionary conserved on slowly evolving arms and tends to be lineage-specific on rapidly evolving arms.

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Comparative mapping of chromosomal arms 3L of An. gambiae, 3L of An. funestus, and 2L of An. stephensi. Arrows denote oriented conserved gene orders. The largest block of genes with partly conserved order is highlighted with yellow. Shaded divisions on the An. gambiae chromosomes denote the genomic coordinates in this species. The centromere regions are shown by black circles at the end of the arms.
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Figure 4: Comparative mapping of chromosomal arms 3L of An. gambiae, 3L of An. funestus, and 2L of An. stephensi. Arrows denote oriented conserved gene orders. The largest block of genes with partly conserved order is highlighted with yellow. Shaded divisions on the An. gambiae chromosomes denote the genomic coordinates in this species. The centromere regions are shown by black circles at the end of the arms.

Mentions: To avoid a lineage-specific bias in pair-wise analyses of gene orders, we estimated the chromosomal divergence among the mosquito species. Three-way comparative mapping can be very efficient in determining inversion distances among species. The cDNA and BAC clones physically and in silico mapped to polytene chromosomes of An. funestus, An. stephensi, and An. gambiae [11] were used to identify conserved gene orders among the three species (Additional file 1). The comparison of the physical maps of these species has identified the whole-arm translocations and paracentric inversions and detected no pericentric inversions or partial-arm translocations (Figures 1, 2, 3 and 4). Therefore we were able to determine the arm homology among species [11]. Accordingly, chromosome X (Additional file 2) and arm 2R (Figure 1) are homologous across all three species. The 2L arm of An. gambiae corresponds to the 3R of An. funestus and the 3L of An. stephensi (Figure 2). The 2L arm of An. funestus corresponds to the 3R arms of An. gambiae and An. stephensi (Figure 3). The 2L arm of An. stephensi corresponds to the 3L arms of An. funestus and An. gambiae (Figure 4). We have calculated inversion distances among An. stephensi, An. gambiae, and An. funestus based on locations of 87 common autosomal DNA markers in all three species (Additional file 3). This comparison has been done at the ~2.42-Mb level of resolution using the Multiple Genome Rearrangements (MRG) program (signed option) [25]. The MGR program has estimated 51 fixed inversions between An. stephensi and An. gambiae, 54 fixed inversions between An. stephensi and An. funestus, and 50 fixed inversions between An. gambiae and An. funestus. We also used the Genome Rearrangements In Man and Mouse (GRIMM) program without assuming directionality of the markers (unsigned option) to perform a pair-wise analysis of rearrangements [26]. The GRIMM program calculated 30 fixed inversions between An. stephensi and An. gambiae, 35 fixed inversions between An. stephensi and An. funestus, and 34 fixed inversions between An. gambiae and An. funestus. These data indicate that the three species have approximately equal chromosomal divergence from each other.


Arm-specific dynamics of chromosome evolution in malaria mosquitoes.

Sharakhova MV, Xia A, Leman SC, Sharakhov IV - BMC Evol. Biol. (2011)

Comparative mapping of chromosomal arms 3L of An. gambiae, 3L of An. funestus, and 2L of An. stephensi. Arrows denote oriented conserved gene orders. The largest block of genes with partly conserved order is highlighted with yellow. Shaded divisions on the An. gambiae chromosomes denote the genomic coordinates in this species. The centromere regions are shown by black circles at the end of the arms.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3094232&req=5

Figure 4: Comparative mapping of chromosomal arms 3L of An. gambiae, 3L of An. funestus, and 2L of An. stephensi. Arrows denote oriented conserved gene orders. The largest block of genes with partly conserved order is highlighted with yellow. Shaded divisions on the An. gambiae chromosomes denote the genomic coordinates in this species. The centromere regions are shown by black circles at the end of the arms.
Mentions: To avoid a lineage-specific bias in pair-wise analyses of gene orders, we estimated the chromosomal divergence among the mosquito species. Three-way comparative mapping can be very efficient in determining inversion distances among species. The cDNA and BAC clones physically and in silico mapped to polytene chromosomes of An. funestus, An. stephensi, and An. gambiae [11] were used to identify conserved gene orders among the three species (Additional file 1). The comparison of the physical maps of these species has identified the whole-arm translocations and paracentric inversions and detected no pericentric inversions or partial-arm translocations (Figures 1, 2, 3 and 4). Therefore we were able to determine the arm homology among species [11]. Accordingly, chromosome X (Additional file 2) and arm 2R (Figure 1) are homologous across all three species. The 2L arm of An. gambiae corresponds to the 3R of An. funestus and the 3L of An. stephensi (Figure 2). The 2L arm of An. funestus corresponds to the 3R arms of An. gambiae and An. stephensi (Figure 3). The 2L arm of An. stephensi corresponds to the 3L arms of An. funestus and An. gambiae (Figure 4). We have calculated inversion distances among An. stephensi, An. gambiae, and An. funestus based on locations of 87 common autosomal DNA markers in all three species (Additional file 3). This comparison has been done at the ~2.42-Mb level of resolution using the Multiple Genome Rearrangements (MRG) program (signed option) [25]. The MGR program has estimated 51 fixed inversions between An. stephensi and An. gambiae, 54 fixed inversions between An. stephensi and An. funestus, and 50 fixed inversions between An. gambiae and An. funestus. We also used the Genome Rearrangements In Man and Mouse (GRIMM) program without assuming directionality of the markers (unsigned option) to perform a pair-wise analysis of rearrangements [26]. The GRIMM program calculated 30 fixed inversions between An. stephensi and An. gambiae, 35 fixed inversions between An. stephensi and An. funestus, and 34 fixed inversions between An. gambiae and An. funestus. These data indicate that the three species have approximately equal chromosomal divergence from each other.

Bottom Line: To gain a better understanding of the arm-specific differences in the rates of genome rearrangements, we compared gene orders and established syntenic relationships among Anopheles gambiae, Anopheles funestus, and Anopheles stephensi.Our results suggest that natural selection favors specific gene combinations within polymorphic inversions when distant species are exposed to similar environmental pressures.Our data support the chromosomal arm specificity in rates of gene order disruption during mosquito evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Entomology, Virginia Tech, Blacksburg, VA 24061, USA.

ABSTRACT

Background: The malaria mosquito species of subgenus Cellia have rich inversion polymorphisms that correlate with environmental variables. Polymorphic inversions tend to cluster on the chromosomal arms 2R and 2L but not on X, 3R and 3L in Anopheles gambiae and homologous arms in other species. However, it is unknown whether polymorphic inversions on homologous chromosomal arms of distantly related species from subgenus Cellia nonrandomly share similar sets of genes. It is also unclear if the evolutionary breakage of inversion-poor chromosomal arms is under constraints.

Results: To gain a better understanding of the arm-specific differences in the rates of genome rearrangements, we compared gene orders and established syntenic relationships among Anopheles gambiae, Anopheles funestus, and Anopheles stephensi. We provided evidence that polymorphic inversions on the 2R arms in these three species nonrandomly captured similar sets of genes. This nonrandom distribution of genes was not only a result of preservation of ancestral gene order but also an outcome of extensive reshuffling of gene orders that created new combinations of homologous genes within independently originated polymorphic inversions. The statistical analysis of distribution of conserved gene orders demonstrated that the autosomal arms differ in their tolerance to generating evolutionary breakpoints. The fastest evolving 2R autosomal arm was enriched with gene blocks conserved between only a pair of species. In contrast, all identified syntenic blocks were preserved on the slowly evolving 3R arm of An. gambiae and on the homologous arms of An. funestus and An. stephensi.

Conclusions: Our results suggest that natural selection favors specific gene combinations within polymorphic inversions when distant species are exposed to similar environmental pressures. This knowledge could be useful for the discovery of genes responsible for an association of inversion polymorphisms with phenotypic variations in multiple species. Our data support the chromosomal arm specificity in rates of gene order disruption during mosquito evolution. We conclude that the distribution of breakpoint regions is evolutionary conserved on slowly evolving arms and tends to be lineage-specific on rapidly evolving arms.

Show MeSH
Related in: MedlinePlus