Genomic composition and evolution of Aedes aegyptichromosomes revealed by the analysis of physically mapped supercontigs
© Timoshevskiy et al.; licensee BioMed Central Ltd. 2014
Received: 28 March 2014
Accepted: 1 April 2014
Published: 14 April 2014
An initial comparative genomic study of the malaria vector Anopheles gambiae and the yellow fever mosquito Aedes aegypti revealed striking differences in the genome assembly size and in the abundance of transposable elements between the two species. However, the chromosome arms homology between An. gambiae and Ae. aegypti, as well as the distribution of genes and repetitive elements in chromosomes of Ae. aegypti, remained largely unexplored because of the lack of a detailed physical genome map for the yellow fever mosquito.
Using a molecular landmark-guided fluorescent in situ hybridization approach, we mapped 624 Mb of the Ae. aegypti genome to mitotic chromosomes. We used this map to analyze the distribution of genes, tandem repeats and transposable elements along the chromosomes and to explore the patterns of chromosome homology and rearrangements between Ae. aegypti and An. gambiae. The study demonstrated that the q arm of the sex-determining chromosome 1 had the lowest gene content and the highest density of minisatellites. A comparative genomic analysis with An. gambiae determined that the previously proposed whole-arm synteny is not fully preserved; a number of pericentric inversions have occurred between the two species. The sex-determining chromosome 1 had a higher rate of genome rearrangements than observed in autosomes 2 and 3 of Ae. aegypti.
The study developed a physical map of 45% of the Ae. aegypti genome and provided new insights into genomic composition and evolution of Ae. aegypti chromosomes. Our data suggest that minisatellites rather than transposable elements played a major role in rapid evolution of chromosome 1 in the Aedes lineage. The research tools and information generated by this study contribute to a more complete understanding of the genome organization and evolution in mosquitoes.
KeywordsPhysical mapping Mosquito Genome Chromosome
The genome of the major vector of arboviruses Aedes aegypti was the second published mosquito genome after the genome of the malaria vector Anopheles gambiae. The size of Ae. aegypti genome - 1,376 mega base pairs (Mb) - is the largest among other mosquito genomes sequenced so far. It is five times bigger than the 264 Mb genome of An. gambiae. The most striking difference between these two mosquito genomes is in the abundance of transposable elements (TEs). TEs cover approximately 50% of the Ae. aegypti genome versus 16% in the malaria mosquito genome . There are also differences in the karyotype structure between the two species. The mitotic chromosome complement of Ae. aegypti consists of three pairs of metacentric chromosomes . The smallest, largest and intermediate chromosomes are numbered as 1, 2 and 3, respectively . There are no sex chromosomes in Ae. aegypti; sex determination alleles have been linked to the smallest homomorphic autosome 1 . By contrast, An. gambiae has two submetacentric autosomes and clearly distinguishable sex chromosomes: an acrocentric, half-heterochromatic X and a completely heterochromatic Y . The An. gambiae genome is subdivided into two compartments - gene-rich euchromatin and gene-poor pericentromeric and intercalary heterochromatin . TEs and satellites have been found to be the most abundant in the heterochromatic regions. Unlike in An. gambiae, TEs in the Ae. aegypti genome predominantly infiltrated introns of most of the protein-coding genes . Although C-banding studies located heterochromatin in centromeres of all chromosomes and in the intercalary region on the q arm of the homomorphic sex-determining chromosome 1 of Ae. aegypti[9–11], molecular characteristics of the heterochromatic regions in this species remain unclear.
The availability of genome sequences for mosquitoes provides an opportunity to study the molecular structures of their chromosomes and the patterns of chromosome evolution. To facilitate this investigation, physical chromosome-based maps for various species of mosquitoes have been developed [12–15]. The most detailed polytene chromosome-based physical map was constructed for the malaria vector An. gambiae[2, 15, 16]. This map includes 2,000 bacterial artificial chromosome (BAC) clone markers and anchors 88% of the genome to the chromosomes. Lower resolution physical maps were also created for An. funestus and An. stephensi. Only about 31% of the Ae. aegypti genome was originally assigned to the chromosomes without specifying order and orientation  based on previous genetic mapping data [17, 18]. A recent genetic mapping effort assigned 60% of the genome to 62 chromosome positions . Although the physical maps of the mosquitoes are incomplete, they provide important insights into chromosomal evolution. A comparative study between An. gambiae and two other malaria mosquitoes, An. funestus and An. stephensi, demonstrated that chromosome arms have different rates of evolution associated with arm-specific genomic features [20, 21]. The highest rate of evolution was detected in the sex chromosome X in association with an abundance of TEs and tandem repeats. A comparative cytogenomic study between Aedes and Anopheles shed light on the pattern of chromosomal evolution in mosquito lineages that diverged about 145 to 200 million years ago  and provided some clues about the evolution of homomorphic and heteromorphic sex chromosomes . Coarse-scale chromosome comparison between Ae. aegypti and An. gambiae detected whole chromosome arm translocations between chromosomes 2 and 3 as well as the conserved gene orthology between the homomorphic sex-determining chromosome 1 of Ae. aegypti and both the X chromosome and autosome 2R arm of An. gambiae[1, 23]. However, a fine-scale analysis of the chromosomal rearrangements in association with the genomic landscape has not been performed. The major limitation for this analysis is a lack of sufficient information about the position of genomic supercontigs on chromosomes of Ae. aegypti.
Physical mapping on polytene chromosomes of Ae. aegypti is difficult due to the low levels of polyteny, which result in poor quality chromosome preparations [24–26]. Furthermore, fluorescent in situ hybridization (FISH) experiments are complicated by the abundance of repetitive elements, which requires using unlabeled repetitive DNA fractions to block unspecific hybridization. The first physical map for Ae. aegypti was developed by FISH of 37 markers on mitotic chromosomes from the ATC-10 cell line . This map was later integrated with the genetic linkage map  by direct placement of 27 DNA probes containing previously mapped genetic markers to chromosomes . The map was distance-based, meaning that positions of the markers were determined by direct measurements of their locations on the chromosomes from the p terminus (FLpter). Recently, we introduced a band-based approach for the physical mapping of the Ae. aegypti genome to mitotic chromosomes [14, 29]. Instead of previously used cell lines, which usually accumulate chromosome rearrangements [27, 30], our method utilizes chromosomes from imaginal discs of fourth instar larvae. The positions of the probes are determined based on idiograms - schematic representations of the chromosome banding patterns. Idiograms have been constructed for chromosomes at early metaphase stained by YOYO-1 iodide. The three chromosomes of Ae. aegypti are subdivided into 23 regions and 94 subdivisions. Using FISH, 100 BAC clones were assigned to the specific bands on idiograms. These BAC clones contained previously mapped genetic markers as determined by PCR . All BAC clones were additionally ordered within each band by multicolor FISH . In addition to 100 genetic markers and 183 Mb of genomic sequences, a marker linked with sex determination  and 12 quantitative trait loci (QTL) associated with pathogen transmission [32–36] were also anchored to the chromosomes. However, the available physical map covered only 13.3% of the genome, and it required further improvement.
In this study, we constructed a more detailed physical map of the Ae. aegypti genome. Together with our previous mapping , a total of 624 Mb equal to approximately 45% of the Ae. aegypti genome were assigned to chromosome bands on idiograms. Our study revealed differences among chromosome arms in the composition of genomic features, such as genes, tandem repeats and TEs. We demonstrated that the sex-determining chromosome 1 has a significantly higher coverage of minisatellites than observed with chromosomes 2 and 3. We also investigated chromosome rearrangements between Ae. aegypti and An. gambiae. Our data demonstrated that previously proposed whole-arm synteny [1, 23] is not fully preserved; a number of pericentric inversions have occurred between culicines and anophelines. Mapping 1:1 orthologs and microsynteny blocks common to Ae. aegypti and An. gambiae suggests a higher rate of gene reshuffling in the sex-determining chromosome of Ae. aegypti compared with chromosomes 2 and 3. Further development of a high-resolution physical map of the Ae. aegypti genome will lead to a significant improvement in the genome assembly and will guide future efforts to study genome organization and chromosome evolution in mosquitoes.
A physical map of the Ae. aegyptigenome
Results of a physical mapping of the Ae. aegypti genome
Number of BAC clone
FISH results suitable for mapping
Assigned to chromosome 1
Assigned to chromosome 2
Assigned to chromosome 3
Mapped portion of the genome
624 Mb (45%)
Our physical mapping detected 29 cases of potential misassembly of genomic supercontigs. In these cases, two or more BAC clones identified in the same supercontig hybridized to very different chromosomal locations. Of these, 12 supercontigs (1.2, 1.30, 1.54, 1.74, 1.80, 1.91, 1.99, 1.154, 1.243, 1.286, 1.288 and 1.302) contained only two BAC clones hybridized to the different chromosome bands, and we indicated their positions on the chromosomes as unknown (Additional file 1: Table S1). Supercontigs 1.11, 1.12, 1.20, 1.31 and 1.48, which contained more than two mapped BAC clones, were assigned to the chromosomes based on the majorities of FISH results. The other 12 supercontigs (1.1, 1.3, 1.7, 1.25, 1.44, 1.50, 1.76, 1.98, 1.148, 1.206, 1.209 and 1.328) were previously assigned to chromosomes , and we also kept them on the map because their chromosome positions have been confirmed by genetic mapping . These supercontigs are indicated in bold on the chromosome map (Figure 2). In 84 of 119 cases (73%), when we mapped two or more BAC clones from the same supercontig to the chromosomes, the mapping results were consistent with the genome data, indicating a proper assembly of these supercontigs.
Genomic composition of Ae. aegyptichromosomes
The overall coverage of TEs was almost equal among chromosomes: 51.9% on chromosome 1, 51.8% on chromosome 2 and 53.0% on chromosome 3 (P = 0.25) (Figure 3). The analysis of various types of TEs revealed differences in classes distributed among the chromosomes (Figure 3C). For example, chromosome 1 had a lower density of Class II, DNA-mediated transposons (747.2 per Mb) than chromosomes 2 (819.1 per Mb, P <10−7) and 3 (805.1 per Mb, P = 1.3×10−4). All chromosomes differed in the abundance (coverage and counts) of miniature inverted-repeat TEs (MITEs). This class of short, 500 bp-long TEs belongs to DNA-mediated TEs. MITEs were most abundant in chromosome 2 (13.5%, 484.3 per Mb) as compared with chromosomes 1 (P <10−4) and 3 (P = 1.3×10−2). Chromosome 3 had a higher coverage of Class I, RNA-mediated TEs than chromosome 2 (26.5% versus 28.1%, P = 2×10−2). Interestingly, the overall densities of TEs were slightly lower in sex-determining chromosome 1 (1,540 per Mb) than in chromosomes 2 (1,634 per Mb; P = 2.2×10−5) and 3 (1,630 per Mb; P = 2.73×10−4). This fact can be explained by the differences in sizes between different classes of TEs and preferable location of the TEs in gene introns that makes them abundant in the gene-rich environment on Ae. aegypti chromosomes 2 and 3.
Chromosome rearrangements between Ae. aegypti and An. gambiae
Orthologs and microsynteny blocks in the Ae. aegypti and An. gambiae genome maps
Chromosome arms (Aa/Ag)
Orthologs in synteny blocks
Percent in blocks
Availability of previously constructed physical maps for An. gambiae[2, 15, 16] and the newly developed physical map for Ae. aegypti allows comparison of the genomic composition of the chromosomes in two species of mosquitoes. Cytogenetic studies conducted in the past demonstrated striking differences in chromosome organization between the two mosquitoes. Despite the fact that both mosquitoes have chromosome number 2n equal to six, the length of the chromosomes and the karyotype structure are different . The average length of the X chromosome and two autosomes together in malaria mosquitoes is equal to about 11 μm . Malaria mosquitoes have clearly distinguishable heteromorphic sex chromosomes X and Y. These two chromosomes contain large amounts of heterochromatin. Almost half of the X chromosome is represented by heterochromatic blocks . The Y chromosome is almost entirely heterochromatic. Autosomes 2 and 3 also contain large heterochromatic blocks around the centromeres. The analysis of the polytene chromosomes found three regions of intercalary heterochromatin in arms 2L, 3R and 3L in addition to pericentromeric heterochromatin . Chromosomes of Ae. aegypti are approximately 2.3 times longer than chromosomes of An. gambiae. The average lengths of the chromosomes at metaphase are equal to 7.15 μm for chromosome 1, 9.46 μm for chromosome 2 and 8.36 μm for chromosome 3 . Sex in Ae. aegypti is determined by a locus on the smallest homomorphic autosome 1 . The position of heterochromatin in Ae. aegypti chromosomes was demonstrated using a Giemsa C-banding technique [10, 40]. C-bands were originally found in pericentromeric regions of female sex-determining chromosome 1 and autosomes 2 and 3. An additional intercalary C-band was found in the female sex-determining chromosome 1. Male sex-determining chromosome 1 demonstrated no heterochromatin in two original reports. However, the presence of heterochromatin in the pericentromeric region of the male-determining chromosome has been demonstrated by a silver-staining technique . Comparative studies of different strains of Ae. aegypti[11, 40] and natural populations in Brazil  demonstrated polymorphism in the presence/absence and sizes of intercalary band in both male- and female-determining chromosomes 1. An additional polymorphic intercalary C-band was also found in chromosome 3 in a Brazilian population of Ae. aegypti.
The 2R arm of An. gambiae has the highest gene densities and the lowest coverage of tandem repeats and densities of TEs . Interestingly, chromosome arm 1q, which is homologous to the 2R arm of An. gambiae, has by contrast the lowest gene densities and the highest coverage of tandem repeats in Ae. aegypti (Figure 7). However, the q arm of chromosome 1 cannot be considered entirely heterochromatic as was previously suggested . Even with approximately 45% of the genome placement to the chromosomes, we found that at least 594 (8%) of genes were located in this arm. The heterochromatic nature of this particular arm can be explained by the presence of the ribosomal DNA locus and the sex determination locus that can directly stimulate accumulation of the repetitive DNA. Formation of the heterochromatin around the ribosomal locus prolongs lifespan by silencing transcription of the ribosomal genes in Drosophila. Another study conducted on Drosophila showed that heterochromatin controls male viability by regulating genes in the sex determination pathway . Thus, our data suggest that a high coverage of satellites rather than TEs could be the major characteristic of the heterochromatin in Ae. aegypti. We also argue that the genomic composition of the sex-determining chromosome 1 in Ae. aegypti is influenced by the presence of the sex-determining locus and ribosomal genes.
Our analysis of the chromosome rearrangements revealed that the pattern of chromosome evolution between An. gambiae and Ae. aegypti was more complex than previously suggested . In addition to the known exchange of genomic material between chromosome X and a part of the 2R arm of An. gambiae in chromosome 1 of Ae. aegypti, a number of pericentric inversions have reshuffled the genetic materials between chromosome arms 1p and 1q (Figure 7B). Similar patterns of pericentric inversions were also found in autosomes 2 and 3 as an addition to the previously determined whole-arm translocation . Our study has also shown that gene order within chromosome arms of Ae. aegypti was poorly conserved, because of multiple paracentric inversion. Similar types of chromosome rearrangements have been determined in Drosophila. For example, the metacentric X chromosomes in D. willistoni, D. pseudoobscura and D. persimilis were generated by a fusion of the X and autosomal 3L arm of D. melanogaster. Additional pericentric inversions were detected in D. erecta, D. yakuba, D. pseudoobscura and D. persimilis compared with the chromosome pattern of D. melanogaster. Similarly to the heteromorphic sex chromosomes in Anopheles and Drosophila, homomorphic sex-determining chromosomes 1 in Ae. aegypti demonstrated the highest rate of the rearrangements among the chromosomes. However, unlike in Drosophila and Anopheles, chromosome 1 in Ae. aegypti was not enriched with TEs, which can be associated with inversion formation [47–50]. Instead, we demonstrated a high coverage of minisatellites suggesting that tandem repeats might play a special role in chromosome evolution of Aedes mosquitoes. Indeed, simple repeats can be involved in DNA breaks and chromosome rearrangements by the formation of hairpin and cruciform structures . Thus, despite the morphological and molecular differences between homomorphic sex-determining chromosomes in Aedes and heteromorphic sex chromosomes in Anopheles, they both display the rapid rate of gene order evolution.
This study developed a physical map comprising 45% of the yellow fever mosquito genome by assigning 624 Mb of 294 genomic supercontigs to chromosome bands. This map guided the analyses of the genes, satellites and TE landscapes in the Ae. aegypti genome and provided important insights into chromosome evolution in mosquitoes. Lower gene densities and higher satellite DNA content were detected in pericentromeric regions and region 1q22 in the homomorphic sex-determining chromosome 1, which also contains the ribosomal DNA locus. These regions can be defined as heterochromatic in Ae. aegypti chromosomes. In contrast to satellites, genes and TEs were more abundant in chromosomes 2 and 3, and also in euchromatic areas of the chromosomes. A comparative genomic analysis with An. gambiae demonstrated that the whole-arm synteny was not fully preserved. Multiple pericentric inversions substantially reshuffled the genetic material of the 1p and 1q arms. Despite this reshuffling, the homologies between 1p and X chromosome, as well as between 1q and 2R arm of An. gambiae, are evident. The homomorphic sex-determining chromosome 1 demonstrated the highest rate of the chromosome rearrangements. We believe that additional physical mapping is still needed to improve the current fragmented genome assembly of Ae. aegypti. Assignment and orientation of the supercontig assemblies of the Ae. aegypti genome to the chromosomes will facilitate more advanced studies of the genome organization and chromosome evolution in mosquitoes.
This study was performed with the Liverpool IB-12 strain of Ae. aegypti, which originated from the Liverpool strain following several rounds of inbreeding and was previously used for the genome sequencing project of Ae. aegypti. The Liverpool strain has also been utilized for genetic-linkage and QTL mapping studies [17, 34, 35].
Fluorescent in situhybridization
Slides of mitotic chromosomes were prepared from imaginal discs of fourth instar larvae following published protocols [14, 29, 39]. Samples of BAC clone DNA were prepared by Clemson University Genomics Institute in 96-well plates. FISH was performed as previously described [14, 39]. A two-color version of FISH was used for localizing BAC positions on mitotic chromosomes. BAC DNA for hybridization was labeled with Cy3- or Cy5-dUTP (GE Healthcare UK Ltd., Amersham, UK) by nick translation. Chromosomes were stained with YOYO-1 iodide (Invitrogen Corporation, Grand Island, NY, USA). Slides were analyzed using a Zeiss LSM 510 Laser Scanning Microscope (Carl Zeiss Microimaging, Inc., Thornwood, NY, USA) at 600× magnification.
Genomic features analysis
For analysis of the genetic element distribution on the chromosomes, we used the sequence data from Vector Base  regarding each supercontig. Gene density was calculated based on the number of protein-coding genes belonging to the individual supercontigs per Mb using the BioMart tool of Vector Base . Repetitive DNA content was analyzed using Tandem Repeat Finder with basic parameters . Tandem repeats were defined by motif sizes from 2 to 6, from 7 to 99, and from 100 or more as microsatellites, minisatellites and satellites, respectively. Analysis of TEs was performed using Repeat Masker (version 3.2.9)  at the default settings using the Ae. aegypti TEs in TEfam database  as the custom repeat library. Repeat Masker output was then used to count the frequency of occurrence and the base occupied by each TE in each supercontig.
Chromosome synteny and ortholog mapping
A collection of 5,265 previously identified orthologs in Ae. aegypti and An. gambiae was downloaded from OrthoDB . This collection was used to test for chromosome synteny between the two species. Among these 2,335 orthologs were located in correctly assembled supercontigs  within the physical map of Ae. aegypti. Chromosome synteny was then tested for in each subregion: each Ae. aegypti subregion was identified with the An. gambiae chromosomes sharing the greatest number of orthologs. Physical maps of 1:1 orthologs (at subregion resolution) were constructed using the physical map of Ae. aegypti and the genome map of An. gambiae. Microsynteny blocks, defined here as the sharing of nine or more orthologs between subregions of Ae. aegypti and An. gambiae, were also mapped.
bacterial artificial chromosome
fluorescent in situ hybridization
mega base pairs
miniature inverted-repeat transposable elements
polymerase chain reaction
quantitative trait loci
This research was funded by grant R21 AI088035 (to MVS) from NIH/NIAID. Authors thank William C. Black for the productive discussion of the manuscript, Joanne Cunningham for the technical help and Melissa Wade for editing the manuscript.
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