Physical Map** of Two Nested Fixed Inversions in the X Chromosome of the Malaria Mosquito Anopheles messeae

  • Conference paper
  • First Online:
Comparative Genomics (RECOMB-CG 2023)

Abstract

Chromosomal inversions play an important role in genome evolution, speciation and adaptation of organisms to diverse environments. Map** and characterization of inversion breakpoints can be useful for describing mechanisms of rearrangements and identification of genes involved in diversification of species. Mosquito species of the Maculipennis Subgroup include dominant malaria vectors and nonvectors in Eurasia, but breakpoint regions of inversions fixed between species have not been mapped to the genomes. Here, we use the physical genome map** approach to identify breakpoint regions of the X chromosome inversions fixed between Anopheles atroparvus and the most widely spread sibling species An. messeae. We mapped breakpoint regions of two large nested fixed inversions (~13 Mb and ~ 10 Mb in size) using fluorescence in situ hybridization of 53 gene markers with polytene chromosomes of An. messeae. The DNA probes were designed based on gene sequences of the annotated An. atroparvus genome. The two inversions resulted in five syntenic blocks, of which only two syntenic blocks (encompassing at least 179 annotated genes in the An. atroparvus genome) changed their position and orientation in the X chromosome. Analysis of the An. atroparvus genome revealed enrichment of DNA transposons in sequences homologous to three of four breakpoint regions suggesting the presence of “hot spots” for rearrangements in mosquito genomes. Our study demonstrated that the physical genome map** approach can be successfully applied to identification of inversion breakpoint regions in insect species with polytene chromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (France)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 42.79
Price includes VAT (France)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 52.74
Price includes VAT (France)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Availability of Data and Materials

The data and materials used in this study data is archived in a publicly accessible repository (doi.org/https://doi.org/10.5281/zenodo.7749003).

References

  • Amos, B., et al.: VEuPathDB: The eukaryotic pathogen, vector and host bioinformatics resource center. Nucleic Acids Res. 50(D1), D898-911 (2022)

    Article  Google Scholar 

  • Anselmetti, Y., Duchemin, W., Tannier, E., Chauve, C., Bérard, S.: Phylogenetic signal from rearrangements in 18 Anopheles species by joint scaffolding extant and ancestral genomes. BMC Genomics 19(Suppl 2), 96 (2018)

    Article  Google Scholar 

  • Artemov, G.N., Bondarenko, S.M., Naumenko, A.N., Stegniy, V.N., Sharakhova, M.V., Sharakhov, I.V.: Partial-arm translocations in evolution of malaria mosquitoes revealed by high-coverage physical map** of the Anopheles atroparvus genome. BMC Genomics 19(1), 278 (2018)

    Article  Google Scholar 

  • Artemov, G.N., et al.: New cytogenetic photomap and molecular diagnostics for the cryptic species of the malaria mosquitoes and from Eurasia. Insects 12(9) (2021). https://doi.org/10.3390/insects12090835

  • Artemov, G., Stegniy, V., Sharakhova, M., Sharakhov, I.: The development of cytogenetic maps for malaria mosquitoes. Insects 9(3), 121 (2018)

    Article  Google Scholar 

  • Artemov, G.N., et al.: A Standard photomap of ovarian nurse cell chromosomes in the European malaria vector Anopheles atroparvus. Med. Vet. Entomol. 29(3), 230–237 (2015)

    Article  Google Scholar 

  • Ayala, D., Ullastres, A., González, J.: Adaptation through chromosomal inversions in Anopheles. Front. Genet. 5(May), 129 (2014)

    Google Scholar 

  • Ayala, D., Francisco, J., Coluzzi, M.: Chromosome speciation: humans, drosophila, and mosquitoes. Proc. Nat. Acad. Sci. United States America 102(Suppl 1), 6535–6542 (2005)

    Google Scholar 

  • Cáceres, M., Ranz, J.M., Barbadilla, A., Long, M., Ruiz, A.: Generation of a widespread drosophila inversion by a transposable element. Science 285(5426), 415–418 (1999)

    Article  Google Scholar 

  • Charlesworth, B., Coyne, J.A., Barton, N.H.: The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. (1987). https://doi.org/10.1086/284701

    Article  Google Scholar 

  • Cheng, C., Kirkpatrick, M.: Inversions are bigger on the X chromosome. Mol. Ecol. 28(6), 1238–1245 (2019)

    Article  Google Scholar 

  • Connallon, T., Olito, C.: Natural selection and the distribution of chromosomal inversion lengths. Mol. Ecol. 31(13), 3627–3641 (2022)

    Article  Google Scholar 

  • Coulibaly, M.B., et al.: Segmental duplication implicated in the genesis of inversion 2Rj of Anopheles gambiae. PLoS ONE 2(9), e849 (2007)

    Article  Google Scholar 

  • Djadid, N.D., Gholizadeh, S., Tafsiri, E., Romi, R., Gordeev, M., Zakeri, S.: Molecular identification of palearctic members of Anopheles maculipennis in Northern Iran. Malar. J. 6(January), 6 (2007)

    Article  Google Scholar 

  • Flynn, J.M., et al.: RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl. Acad. Sci. U.S.A. 117(17), 9451–9457 (2020)

    Article  Google Scholar 

  • Fontaine, M.C., et al.: Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science (2015). https://doi.org/10.1126/science.1258524

    Article  Google Scholar 

  • Giraldo-Calderón, G.I., et al.: VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Res. 43(Database issue), D707–D713 (2015)

    Google Scholar 

  • Gornostaeva, R.M., Danilov, A.V.: On ranges of the malaria mosquitoes (Diptera: Culicidae: Anopheles) of the maculipennis complex on the territory of Russia. Parazitologiia 36(1), 33–47 (2002)

    Google Scholar 

  • Jetten, T.H., Takken, W.: Anophelism without malaria in Europe: a review of the ecology and distribution of the genus Anopheles. Wageningen Agric. Univ. Papers 94(5), 1–69 (1994)

    Google Scholar 

  • Jiang, X., et al.: Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi. Genome Biol. (2014). https://doi.org/10.1186/s13059-014-0459-2

    Article  Google Scholar 

  • Kamali, M., **a, A., Zhijian, T., Sharakhov, I.V.: A new chromosomal phylogeny supports the repeated origin of vectorial capacity in malaria mosquitoes of the Anopheles gambiae complex. PLoS Pathog. 8(10), e1002960 (2012)

    Article  Google Scholar 

  • Kirkpatrick, M.: How and why chromosome inversions evolve. PLoS Biol. 8(9) (2010). https://doi.org/10.1371/journal.pbio.1000501

  • Kirkpatrick, M., Barton, N.: Chromosome inversions, local adaptation and speciation. Genetics 173(1), 419–434 (2006)

    Article  Google Scholar 

  • Ling, A., Cordaux, R.: Insertion sequence inversions mediated by ectopic recombination between terminal inverted repeats. PLoS ONE 5(12), e15654 (2010)

    Article  Google Scholar 

  • Lobachev, K.S., Rattray, A., Narayanan, V.: Hairpin- and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells. Front. Biosci. (2007). https://doi.org/10.2741/2381

    Article  Google Scholar 

  • Lonnig, W.-E., Saedler, H.: Chromosome rearrangements and transposable elements. Annu. Rev. Genet. 36(June), 389–410 (2002)

    Article  Google Scholar 

  • Lukyanchikova, V., et al.: Anopheles mosquitoes reveal new principles of 3D genome organization in insects. Nat. Commun. 13(1), 1960 (2022)

    Article  Google Scholar 

  • Naumenko, A.N., et al.: Chromosome and genome divergence between the cryptic Eurasian malaria vector-species Anopheles messeae and Anopheles daciae. Genes 11(2) (2020). https://doi.org/10.3390/genes11020165

  • Neafsey, D.E., et al.: Mosquito genomics. highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes. Science 347(6217), 1258522 (2015)

    Article  Google Scholar 

  • Neph, S., et al.: BEDOPS: high-performance genomic feature operations. Bioinformatics 28(14), 1919–1920 (2012)

    Article  Google Scholar 

  • Nicolescu, G., Linton, Y.-M., Vladimirescu, A., Howard, T.M., Harbach, R.E.: Mosquitoes of the Anopheles maculipennis group (Diptera: Culicidae) in Romania, with the discovery and formal recognition of a new species based on molecular and morphological evidence. Bull. Entomol. Res. (2004). https://doi.org/10.1079/ber2004330

    Article  Google Scholar 

  • Ou, S., et al.: Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. Genome Biol. 20(1), 275 (2019)

    Article  Google Scholar 

  • Ranz, J.M., et al.: Principles of genome evolution in the drosophila melanogaster species group. PLoS Biol. (2007). https://doi.org/10.1371/journal.pbio.0050152

    Article  Google Scholar 

  • Schwander, T., Libbrecht, R., Keller, L.: Supergenes and complex phenotypes. Current Biol. CB 24(7), R288–R294 (2014)

    Article  Google Scholar 

  • Sharakhova, M.V., Artemov, G.N., Timoshevskiy, V.A., Sharakhov, I.V.: Physical genome map** using fluorescence in situ hybridization with mosquito chromosomes. Insect Genomics, 177–194 (2019)

    Google Scholar 

  • Sharakhov, I.V., et al.: Breakpoint structure reveals the unique origin of an interspecific chromosomal inversion (2La) in the Anopheles gambiae complex. Proc. Natl. Acad. Sci. U.S.A. 103(16), 6258–6262 (2006)

    Article  Google Scholar 

  • Sharakhov, I.V.: Chromosome phylogenies of malaria mosquitoes. Tsitologiia 55(4), 238–240 (2013)

    Google Scholar 

  • Sinka, M.E., et al.: The dominant Anopheles vectors of human malaria in Africa, Europe and the middle east: occurrence data, distribution maps and bionomic précis. Parasit. Vectors 3(December), 117 (2010)

    Article  Google Scholar 

  • Stegniĭ, V.N., Kabanova, V.M., Novikov, I.: Study of the karyotype of the malaria mosquito. Tsitologiia 18(6), 760–766 (1976)

    Google Scholar 

  • Stegniy, V.N.: Population Genetics and Evolution of Malaria Mosquitoes, p. 137. Tomsk State University Publisher, Tomsk, Russia (1991)

    Google Scholar 

  • Stegniy, V.N.: Genetic adaptation and speciation in sibling species of the Eurasian maculipennis complex. In: Steiner, W.W.M., Tabachnick, W.J., Rai, K.S., Narang, S. (eds.) Recent Developments in the Genetics of lnsect Disease Vectors, pp. 454–464. Stipes, Champaign, 111 (1982)

    Google Scholar 

  • Tesler, G.: GRIMM: genome rearrangements web server. Bioinformatics 18(3), 492–493 (2002)

    Article  MathSciNet  Google Scholar 

  • Thakare, A., et al.: The genome trilogy of Anopheles stephensi, an urban malaria vector, reveals structure of a locus associated with adaptation to environmental heterogeneity. Sci. Rep. 12(1), 3610 (2022)

    Article  Google Scholar 

  • Tubio, J.M.C., et al.: Evolutionary dynamics of the Ty3/gypsy LTR retrotransposons in the genome of Anopheles gambiae. PloS One 6(1), e16328 (2011)

    Google Scholar 

  • Villoutreix, R., Ayala, D., Joron, M., Gompert, Z., Feder, J.L., Nosil, P.: Inversion breakpoints and the evolution of supergenes. Mol. Ecol. 30(12), 2738–2755 (2021)

    Article  Google Scholar 

  • Virtanen, P., et al.: Author correction: SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17(3), 352 (2020)

    Article  Google Scholar 

  • Wicker, T., et al.: A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8(12), 973–982 (2007)

    Article  Google Scholar 

  • **a, A., et al.: Genome landscape and evolutionary plasticity of chromosomes in malaria mosquitoes. PLoS ONE (2010). https://doi.org/10.1371/journal.pone.0010592

    Article  Google Scholar 

  • Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S., Madden, T.L.: Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinf. 13(June), 134 (2012)

    Article  Google Scholar 

  • Yurchenko, A.A., et al.: Phylogenomics revealed migration routes and adaptive radiation timing of holarctic malaria vectors of the maculipennis group (2022). https://doi.org/10.1101/2022.08.10.503503

  • Zhang, C., et al.: Understanding the regulation of overwintering diapause molecular mechanisms in culex pipiens pallens through comparative proteomics. Sci. Rep. 9(1), 1–12 (2019)

    MathSciNet  Google Scholar 

  • Zhang, S., et al.: Anopheles vectors in mainland china while approaching malaria elimination. Trends Parasitol. 33(11), 889–900 (2017)

    Article  Google Scholar 

Download references

Funding

Collection of mosquito samples and map** experiments were supported by the Russian Science Foundation grant № 21-14-00182. Bioinformatics and statistical analyses were supported by the Tomsk State University Development Programme (Priority-2030).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Igor V. Sharakhov .

Editor information

Editors and Affiliations

1 Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 529 kb)

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this paper

Check for updates. Verify currency and authenticity via CrossMark

Cite this paper

Soboleva, E.S., Kirilenko, K.M., Fedorova, V.S., Kokhanenko, A.A., Artemov, G.N., Sharakhov, I.V. (2023). Physical Map** of Two Nested Fixed Inversions in the X Chromosome of the Malaria Mosquito Anopheles messeae. In: Jahn, K., Vinař, T. (eds) Comparative Genomics. RECOMB-CG 2023. Lecture Notes in Computer Science(), vol 13883. Springer, Cham. https://doi.org/10.1007/978-3-031-36911-7_6

Download citation

  • DOI: https://doi.org/10.1007/978-3-031-36911-7_6

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-031-36910-0

  • Online ISBN: 978-3-031-36911-7

  • eBook Packages: Computer ScienceComputer Science (R0)

Publish with us

Policies and ethics

Navigation