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

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.

Mosquitoes of the Maculipennis complex in Northern Italy

“…messeae s.l. sequences, as previously reported (Lilja et al , 2020; Naumenko et al ., 2020), in three sites of An. atroparvus and one site in An.…”

“…messeae s.l., where all sequences showed the same pattern with A in position 362 and C in position 382, the two positions considered diagnostic for the identification of An. daciae (Lilja et al , 2020; Naumenko et al , 2020).…”

“…Other species in the complex were described in the Palearctic region based on cytogenetic (e.g. polytene chromosome inversions) (Artemov et al , 2018; Andreeva et al , 2007; Naumenko et al , 2020) and barcoding approaches (Nicolescu et al , 2004; Gordeev et al , 2005; Djadid et al , 2007): Anopheles beklemishevi, Stegnii & Kabanova, 1976, Anopheles martinius, Shingarev, 1926, Anopheles artemievi, Gordeyev, Zvantsov, Goryacheva, Shaikevich & Yezhov, 2005, Anopheles persiensis, Linton, Sedaghat & Harbach, 2003, Anopheles daciae, Linton, Nicolescu & Harbach, 2004, although the validity of some of these taxa is still debated. For instance, the species An.…”

Analysis of Anopheles messeae s.l. intron gene polymorphism associated with imidacloprid resistance

“…messeae and An. daciae seems to be incomplete and these species are very close (Naumenko et al 2020). Therefore, it is expected that the level of insecticide resistance is similar for these species and it is not surprising that differences between An.…”

“…messeae Falleroni 1926 and An. daciae Linton, Nicolescu & Harbach 2004, which have incomplete reproductive isolation (Naumenko et al 2020) but also have a number of ecological differences in preferred habitats and their relation to human environments (Danabalan et al 2013, Lühken et al 2016, Vaulin et al 2018). Different degrees of association with anthropogenic landscapes suggests that An.…”