Structural Variation of the X Chromosome Heterochromatin in the Anopheles gambiae Complex

Abstract

Heterochromatin is identified as a potential factor driving diversification of species. To understand the magnitude of heterochromatin variation within the Anopheles gambiae complex of malaria mosquitoes, we analyzed metaphase chromosomes in An. arabiensis, An. coluzzii, An. gambiae, An. merus, and An. quadriannulatus. Using fluorescence in situ hybridization (FISH) with ribosomal DNA (rDNA), a highly repetitive fraction of DNA, and heterochromatic Bacterial Artificial Chromosome (BAC) clones, we established the correspondence of pericentric heterochromatin between the metaphase and polytene X chromosomes of An. gambiae. We then developed chromosome idiograms and demonstrated that the X chromosomes exhibit qualitative differences in their pattern of heterochromatic bands and position of satellite DNA (satDNA) repeats among the sibling species with postzygotic isolation, An. arabiensis, An. merus, An. quadriannulatus, and An. coluzzii or An. gambiae. The identified differences in the size and structure of the X chromosome heterochromatin point to a possible role of repetitive DNA in speciation of mosquitoes. We found that An. coluzzii and An. gambiae, incipient species with prezygotic isolation, share variations in the relative positions of the satDNA repeats and the proximal heterochromatin band on the X chromosomes. This previously unknown genetic polymorphism in malaria mosquitoes may be caused by a differential amplification of DNA repeats or an inversion in the sex chromosome heterochromatin.

Anopheles gambiae Genome Conservation as a Resource for Rational Gene Drive Target Site Selection

“…This discrepancy is in agreement with a number of works that describe centromeric sequences as highly variable in size and composition [31,32]. Overall, a lower average sequence identity (67%) was observed for the X chromosome, reflecting the expectation that genetic divergence tends to be higher on sex chromosomes [33,34] and confirming the previously shown diversity of this chromosome within the species of the complex [24,[35][36][37][38]. This conservation pattern across the more distantly related species, albeit at a lower level (4.8%), is consistent with longer evolutionary distances that separate them [24].…”

Chromosome-level genome assemblies of the malaria vectors Anopheles coluzzii and Anopheles arabiensis

“…This result indicates that the AaraD3 and AcolMOP1 chromosomes are more complete than the AgamP4 chromosomes. We also analyzed the presence of the Ag53C tandem repeat and its junction with the Tsessebe III transposable element, which are known to be located in the pericentromeric regions of the autosomes [ 78 , 83 ]. The A. coluzzii assembly contains the highest number (646) of these repeats and the A. arabiensis assembly contains a comparable number of the repeats to AgamP4, while the AcolN1 assembly contains just 41 repeat copies (Table 5 ).…”

“…However, they may also represent novel rearrangements segregating between A. gambiae and A. coluzzii . We recently described a new type of shared cytogenetic polymorphism in the incipient species, A. gambiae and A. coluzzii —an inversion of the satellite DNA location in relation to the proximal gene-free X chromosome band [ 83 ]. The findings suggest that structural variations can be common in the sex chromosome heterochromatin of mosquitoes.…”

Chromosome-level genome assemblies of the malaria vectors Anopheles coluzzii and Anopheles arabiensis

“…This result indicates that the AaraD3 and AcolMOP1 chromosomal scaffolds are more complete than the AgamP4 scaffolds. We also analyzed the presence of the Ag53C tandem repeat and its junction with the Tsessebe III transposable element, which are known to be located in the pericentromeric regions of the autosomes [89, 94]. The An.…”

“…gambiae and An. coluzzii —an inversion of the satDNA location in relation to the proximal gene-free X chromosome band [83]. The findings suggest that structural variations can be common in the sex-chromosome heterochromatin of mosquitoes.…”