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

Anastasia N Naumenko,Mikhail I Gordeev,Igor V Sharakhov,Elina M Baricheva,Andrey A Yurchenko,Dmitriy A Karagodin,Maria V Sharakhova,Anton V Moskaev,Olga I Martin

doi:10.3390/genes11020165

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.

Highlights

IntroductionChromosomal inversions are essential drivers of genome evolution in diploid organisms [1]
Chromosomal inversions are essential drivers of genome evolution in diploid organisms [1].When a chromosomal inversion occurs, a piece of the chromosome flips 180 degrees and producesGenes 2020, 11, 165; doi:10.3390/genes11020165 www.mdpi.com/journal/genesGenes 2020, 11, 165 a reverse order of the genetic material
Inversion X1 was completely fixed in all three populations of An. messeae, whereas frequencies of the inverted and standard arrangements in An. daciae were almost equal in all populations

Summary

Introduction

Chromosomal inversions are essential drivers of genome evolution in diploid organisms [1]. Genes 2020, 11, 165 a reverse order of the genetic material. As a result, this part of the genome becomes resistant to recombination during meiosis. By capturing different combinations of alleles, inversions have effects on ecological, behavioral, and physiological adaptations of the species to the natural environment [2]. The role of the chromosomal inversions in adaptation and evolution of different Drosophila species has been studied for several decades [3,4,5]. Understanding the population genetics and mechanisms of taxa diversification is extremally important for species that transmit human diseases [15]. An. messeae Falleroni is one of the most geographically widespread [16] and genetically diverse [17]

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