Arm-specific dynamics of chromosome evolution in malaria mosquitoes

Abstract

BackgroundThe 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.ResultsTo 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.ConclusionsOur 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.

Ecological Genomics ofAnopheles gambiaeAlong a Latitudinal Cline: A Population-Resequencing Approach

“…gambiae complex, but also in other major malaria vectors in the same Anopheles subgenus (Cellia), similar nonuniform distributions of fixed and polymorphic inversions are observed (Kitzmiller 1977;Xia et al 2010;Sharakhova et al 2011). The enrichment of polymorphic inversions on chromosome 2 in An.…”

“…gambiae is observed on the homologous chromosome arms in Anopheles stephensi (2R, 3L) and An. funestus (2R, 3R) (Xia et al 2010;Sharakhova et al 2011). Even more remarkable, at least some of the independently derived inversions on 2R nonrandomly share common genes between species (this is not true of 2L and its homologs).…”

2D and 3D Chromosome Painting in Malaria Mosquitoes

“…Aneuploidy, polyploidy, and chromosomal rearrangements such as translocations, inversions, deletions, and ring chromosomes have been detected in different mosquito cell lines 53,54 . Classical cytogenetic observations 55 and physical mapping 56 have demonstrated the occurrence of whole-arm chromosomal translocations in the evolution of malaria mosquitoes. Therefore, microdissected material can be used in conjunction with FISH experiments to compare homology of chromosomal regions between species.…”

Abbreviations and acronyms

“…Recently, a band-based approach was used to perform a physical mapping of the Ae. aegypti genome to its mitotic chromosomes (Sharakhova et al, 2011;Timoshevskiy et al, 2013). The mitotic chromosome complement of Ae.…”

“…A physical map for Ae. aegypti corresponding to 13.3% of the genome was developed using FISH markers on mitotic chromosomes (Severson et al, 1993), genetic linked map (RFLP cDNA-based map) (Brown et al, 1995(Brown et al, , 2001Sharakhova et al, 2011), and QTL (Severson et al, 1994(Severson et al, , 1995Bosio, Fulton and Salasek, 2000;Gomez-Machorro, Bennett and Muñoz, 2004;Zhong et al, 2006). More recently, a more detailed physical map of the mosquito was constructed and a total of 624 Mb covered approximately 45% of the Ae.…”