Limits...
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.

Show MeSH

Related in: MedlinePlus

Chromosome arm-specific differences in rates of accumulation of disrupted gene blocks. X axis shows rates of accumulation of disrupted blocks per region length per unit length, z = (λj(diff) γj(diff))/L. Y axis shows a density of p(z/D); p--density, D--data.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3094232&req=5

Figure 7: Chromosome arm-specific differences in rates of accumulation of disrupted gene blocks. X axis shows rates of accumulation of disrupted blocks per region length per unit length, z = (λj(diff) γj(diff))/L. Y axis shows a density of p(z/D); p--density, D--data.

Mentions: The difference between these sets of rates (λj(diff) =λj(c+d) - λj(c) and γj(diff) = γj(c+d) - γj(c)) models the rates governing the disrupted blocks, which were then used to compare the levels of block disruption between groups. We report these rate parameters in conjunction with the combined summary (λj(diff) γj(diff))/Lj, where Lj is the total length of arm j. This combined summary has the interpretation of blocks per region length per total length (See Methods for further explanation). For both fitted processes, posterior summaries are displayed in Table 3. We demonstrated that the rate of accumulation of conserved and conserved+disrupted blocks was mildly higher for arms 2R and 3L. However, the lengths of the blocks were dramatically smaller on 2R than those found on other arms. For inferences of disrupted blocks, we considered the difference of these parameter pairings λj(diff) = λj(c)- λj(c+d) and (γj-1)(diff) = (γj(c))-1 -(γj(c+d))-1. Strong overlap with zero, in each of the above parameter differences, indicated a negligible disruption rate. On the other hand, highly negative values indicated that the rates for the disrupted blocks were less than those for the conserved blocks. Conversely, large values suggested higher rates for the disrupted blocks. The analysis revealed that the 2R arm has the highest rate of accumulation of disrupted blocks per unit length, λj(diff), with a probability equal to 0.905 (Figure 7, Table 3). The effects for the other arms were less pronounced. Moreover, the 3R arm of An. gambiae and the homologous arms of the other species had the lowest λj(diff) value with a probability of 0.5, and all identified gene blocks in this arm were preserved among An. gambiae, An. funestus, and An. stephensi. The data suggest that this chromosomal arm possesses evolutionary conserved breakpoint clusters and has low tolerance to generating new breakpoints.


Arm-specific dynamics of chromosome evolution in malaria mosquitoes.

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

Chromosome arm-specific differences in rates of accumulation of disrupted gene blocks. X axis shows rates of accumulation of disrupted blocks per region length per unit length, z = (λj(diff) γj(diff))/L. Y axis shows a density of p(z/D); p--density, D--data.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 7: Chromosome arm-specific differences in rates of accumulation of disrupted gene blocks. X axis shows rates of accumulation of disrupted blocks per region length per unit length, z = (λj(diff) γj(diff))/L. Y axis shows a density of p(z/D); p--density, D--data.
Mentions: The difference between these sets of rates (λj(diff) =λj(c+d) - λj(c) and γj(diff) = γj(c+d) - γj(c)) models the rates governing the disrupted blocks, which were then used to compare the levels of block disruption between groups. We report these rate parameters in conjunction with the combined summary (λj(diff) γj(diff))/Lj, where Lj is the total length of arm j. This combined summary has the interpretation of blocks per region length per total length (See Methods for further explanation). For both fitted processes, posterior summaries are displayed in Table 3. We demonstrated that the rate of accumulation of conserved and conserved+disrupted blocks was mildly higher for arms 2R and 3L. However, the lengths of the blocks were dramatically smaller on 2R than those found on other arms. For inferences of disrupted blocks, we considered the difference of these parameter pairings λj(diff) = λj(c)- λj(c+d) and (γj-1)(diff) = (γj(c))-1 -(γj(c+d))-1. Strong overlap with zero, in each of the above parameter differences, indicated a negligible disruption rate. On the other hand, highly negative values indicated that the rates for the disrupted blocks were less than those for the conserved blocks. Conversely, large values suggested higher rates for the disrupted blocks. The analysis revealed that the 2R arm has the highest rate of accumulation of disrupted blocks per unit length, λj(diff), with a probability equal to 0.905 (Figure 7, Table 3). The effects for the other arms were less pronounced. Moreover, the 3R arm of An. gambiae and the homologous arms of the other species had the lowest λj(diff) value with a probability of 0.5, and all identified gene blocks in this arm were preserved among An. gambiae, An. funestus, and An. stephensi. The data suggest that this chromosomal arm possesses evolutionary conserved breakpoint clusters and has low tolerance to generating new breakpoints.

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