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, 11 (2)

Chromosome and Genome Divergence Between the Cryptic Eurasian Malaria Vector-Species Anopheles messeae and Anopheles daciae

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Chromosome and Genome Divergence Between the Cryptic Eurasian Malaria Vector-Species Anopheles messeae and Anopheles daciae

Anastasia N Naumenko et al. Genes (Basel).

Abstract

Chromosomal inversions are important drivers of genome evolution. The Eurasian malaria vector Anopheles messeae has five polymorphic inversions. A cryptic species, An. daciae, has been discriminated from An. messeae based on five fixed nucleotide substitutions in the internal transcribed spacer 2 (ITS2) of ribosomal DNA. However, the inversion polymorphism in An. daciae and the genome divergence between these species remain unexplored. In this study, we sequenced the ITS2 region and analyzed the inversion frequencies of 289 Anopheles larvae specimens collected from three locations in the Moscow region. Five individual genomes for each of the two species were sequenced. We determined that An. messeae and An. daciae differ from each other by the frequency of polymorphic inversions. Inversion X1 was fixed in An. messeae but polymorphic in An. daciae populations. The genome sequence comparison demonstrated genome-wide divergence between the species, especially pronounced on the inversion-rich X chromosome (mean Fst = 0.331). The frequency of polymorphic autosomal inversions was higher in An. messeae than in An. daciae. We conclude that the X chromosome inversions play an important role in the genomic differentiation between the species. Our study determined that An. messeae and An. daciae are closely related species with incomplete reproductive isolation.

Keywords: genome; internal transcribed spacer 2; malaria mosquitoes; polymorphic inversions.

Conflict of interest statement

Authors declare no competing interests.

Figures

Figure 1
Figure 1
Location of the Moscow region in Eurasia (A) and collection sites of mosquito larvae (B). The ratios of An. messeae, An. daciae, their hybrids, An. maculipennis, and An. beklemishevi are shown as pie charts for each population. The charts show different proportions of the species in three compared populations. The map was developed using OpenStreetMap data [59].
Figure 2
Figure 2
Examples of ITS2 sequence chromatograms for An. messeae (A), An. daciae (B), and their hybrid (C). Dash lines indicate positions of SNPs that distinguish the two species. Chromatograms indicate the presence of double picks in position 150 of An. messeae and in positions 211, 215, and 217 of An. daciae. The specimen with double picks in position 150, 211, 215, 217, 412, and 432 was identified as a hybrid between An. messeae and An. daciae.
Figure 3
Figure 3
Mosquito breeding sites in Novoskosino (A), Noginsk (B), and Yegoryevsk (C). Ponds in Novokosino and Noginsk are preferred by An. messeae and represent typical for Anopheles sunny larval breeding sites with open water and abundant vegetation. The water reservoir in Yegorevsk, preferred by An. daciae, is shaded and characterized by high water saprobity.
Figure 4
Figure 4
Inversions in polytene chromosomes of An. messeae and An. daciae. The specimens in the Moscow region are characterized by the presence of 4 highly polymorphic inversions X1, 2R1, 3R1, and 3L1, and 2 rare endemic inversions X4 and 2R4. A rare karyotype X44, 2R01, 3R01, and 3L00 in An. messeae is shown on panel A. Another rare inversion heterozygote, 2R04, in An. daciae is shown on panel B. Inversion heterozygotes X01 in An. daciae and X14 in An. messeae are indicated on panels C and D, respectively. CC stands for chromocenter.
Figure 5
Figure 5
Inversion frequencies in An. messeae and An. daciae from the Novokosino, Noginsk, and Yegoryevsk populations. Frequencies of inversions: X0, X1, and X4 (A); 2R1 and 2R4 (B); 3R1 (C); and 3L1 (D) are shown by charts. Proportions of standard, inverted, and heterozygote arrangements are shown by different colors. Chromosome X is almost monomorphic in An. messeae but is highly polymorphic in An. daciae in the three Moscow populations. Although all autosomal inversions are present in both species, polymorphism is higher in An. messeae than in An. daciae. Rare inversions, X4 and 2R4, were found in low frequencies in An. messeae and An. daciae, respectively.
Figure 6
Figure 6
Interpopulation PCA plot based on the frequencies of the autosomal chromosomal inversions in three populations of An. messeae and An. daciae. Species are indicated by different colors. PCA analysis separates An. messeae and An. daciae along the PC1.
Figure 7
Figure 7
Level of genetic differentiation (Fst) between An. messeae (n = 5) and An. daciae (n = 5) along the chromosomal arms. Each dot represents a 5 kb window. The y-axis represents Fst values and the x-axis represents the genomic coordinates (Mbp). The X chromosome demonstrates the highest Fst values while the autosomal arms have a low overall level of differentiation, which is elevated in the centromeric regions. T and C stands for telomeres and centromeres, respectively.
Figure 8
Figure 8
Principal Component Analysis (A) and ADMIXTURE (B) plots based on the autosomal SNVs of the whole genomes of An. messeae and An. daciae. Species are shown by different colors. PCA (A) reliably differentiates two species by the PC1. Each bar (B) represents the proportion of ancestral species in a given individual. Two admixed individuals (shown in bold) were identified.

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