A standard photomap of ovarian nurse cell chromosomes and inversion polymorphism in  Anopheles beklemishevi

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Abstract

Background

Anopheles beklemishevi is a member of the Maculipennis group of malaria mosquitoes that has the most northern distribution among other members of the group. Although a cytogenetic map for the larval salivary gland chromosomes of this species has been developed, a high-quality standard cytogenetic photomap that enables genomics and population genetics studies of this mosquito at the adult stage is still lacking.

Methods

In this study, a cytogenetic map for the polytene chromosomes of An. beklemishevi from ovarian nurse cells was developed using high-resolution digital imaging from field collected mosquitoes. PCR-amplified DNA probes for fluorescence in situ hybridization (FISH) were designed based on the genome of An. atroparvus. The DNA probe obtained by microdissection procedures from the breakpoint region was labelled in a DOP-PCR reaction. Population analysis was performed on 371 specimens collected in 18 locations.

Results

We report the development of a high-quality standard photomap for the polytene chromosomes from ovarian nurse cells of An. beklemishevi. To confirm the suitability of the map for physical mapping, several PCR-amplified probes were mapped to the chromosomes of An. beklemishevi using FISH. In addition, we identified and mapped DNA probes to flanking regions of the breakpoints of two inversions on chromosome X of this species. Inversion polymorphism was determined in 13 geographically distant populations of An. beklemishevi. Four polymorphic inversions were detected. The positions of common chromosomal inversions were indicated on the map.

Conclusions

The study constructed a standard photomap for ovarian nurse cell chromosomes of An. beklemishevi and tested its suitability for physical genome mapping and population studies. Cytogenetic analysis determined inversion polymorphism in natural populations of An. beklemishevi related to this species’ adaptation.

Electronic supplementary material

The online version of this article (10.1186/s13071-018-2657-3) contains supplementary material, which is available to authorized users.

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Most cited references 17

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The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships.

R. Harbach (2004)

The internal classification of genus Anopheles is updated to reflect taxonomic actions published since the classification was last reviewed in 1994. Both formal and informal taxa are included. The classification is intended to aid researchers and students who are interested in analysing species relationships, making group comparisons and testing phylogenetic hypotheses. The genus includes 444 formally named and 40 provisionally designated extant species divided between six subgenera: Anopheles, Cellia, Kerteszia, Lophopodomyia, Nyssorhynchus and Stethomyia. Subgenera Anopheles, Cellia and Nyssorhynchus are subdivided hierarchically into nested informal groups of morphologically similar species that are believed to represent monophyletic lineages based on morphological similarity. Changes to the classification include additional species, eliminated species and changes to the hierarchical organization and composition of supraspecific groups, some as a result of molecular studies.

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A standard cytogenetic photomap for the mosquito Anopheles stephensi (Diptera: Culicidae): application for physical mapping.

Igor V. Sharakhov, Maria Sharakhova, Mark S. McAlister … (2006)

To facilitate physical genome mapping, we have developed a new cytogenetic photomap for Anopheles stephensi (Liston) (Diptera: Culicidae), an important malaria vector in Asia. The high-resolution images of the ovarian polytene chromosomes have been straightened and divided by numbered divisions and lettered subdivisions. The exact chromosomal locations of eight DNA probes have been determined by fluorescent in situ hybridization. Using the DNA sequences, we have established correspondence between chromosomal arms among An. stephensi, Anopheles gambiae (Patton), and Anopheles funestus (Giles). The results support previous cytogenetic observations of arm translocations taking place during diversification of the species. To make the cytogenetic map useful for population genetics studies, we have indicated the chromosomal positions for the breakpoints of 19 polymorphic inversions.

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Linear and spatial organization of polytene chromosomes of the African malaria mosquito Anopheles funestus.

Chang G. Yan, Maria Sharakhova, Lizette Koekemoer … (2001)

Anopheles funestus Giles is one of the major malaria vectors in Africa, but little is known about its genetics. Lack of a cytogenetic map characterized by regions has hindered the progress of genetic research with this important species. This study developed a cytogenetic map of An. funestus using ovarian nurse cell polytene chromosomes. We demonstrate an important application with the cytogenetic map for characterizing various chromosomal inversions for specimens collected from coastal Kenya. The linear and spatial organization of An. funestus polytene chromosomes was compared with the best-studied malaria mosquito, An. gambiae Giles. Comparisons of chromosome morphology between the two species have revealed that the most extensive chromosomal rearrangement occurs in pericentromeric heterochromatin of autosomes. Differences in pericentromeric heterochromatin types correlate with nuclear organization differences between An. funestus and An. gambiae. Attachments of chromosomes to the nuclear envelope strongly depend on the presence of diffusive beta-heterochromatin. Thus, An. funestus and An. gambiae exhibit species-specific characteristics in chromosome-linear and -spatial organizations.

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Author and article information

Contributors

Gleb N. Artemov: g-artemov@mail.ru

Mikhail I. Gordeev: gordeev_mikhail@mail.ru

Alina A. Kokhanenko: g-artemov@mail.ru

Anton V. Moskaev: av.moskaev@mgou.ru

Alena I. Velichevskaya: alena.velichevskaya@gmail.com

Vladimir N. Stegniy: stegniy@res.tsu.ru

Igor V. Sharakhov: igor@vt.edu

Maria V. Sharakhova: msharakh@vt.edu

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 27 March 2018

Publication date PMC-release: 27 March 2018

Publication date Collection: 2018

Volume: 11

Electronic Location Identifier: 211

Affiliations

[1 ]ISNI 0000 0001 1088 3909, GRID grid.77602.34, Laboratory of Ecology, Genetics and Environmental Protection, , Tomsk State University, ; Tomsk, Russia

[2 ]ISNI 0000000092721542, GRID grid.18763.3b, Department of General Biology and Ecology, , Moscow Regional State University, ; Moscow, Russia

[3 ]Virginia Tech, Department of Entomology, Fralin Life Science Institute, Blacksburg, VA USA

Article

Publisher ID: 2657

DOI: 10.1186/s13071-018-2657-3

PMC ID: 5870207

SO-VID: bc8165f0-bcc1-4dab-8b46-6c00bb3ca61d

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 19 September 2017

Date accepted : 17 January 2018

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100006769, Russian Science Foundation;

Award ID: 15-14-20011

Award Recipient : Igor V. Sharakhov

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: anopheles,mosquito,cytogenetic map,inversion polymorphism,physical mapping

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: anopheles, mosquito, cytogenetic map, inversion polymorphism, physical mapping

A standard photomap of ovarian nurse cell chromosomes and inversion polymorphism in Anopheles beklemishevi

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Abstract

Background

Methods

Results

Conclusions

Electronic supplementary material

Related collections

Vector Biology

Most cited references 17

The classification of genus Anopheles (Diptera: Culicidae): a working hypothesis of phylogenetic relationships.

A standard cytogenetic photomap for the mosquito Anopheles stephensi (Diptera: Culicidae): application for physical mapping.

Linear and spatial organization of polytene chromosomes of the African malaria mosquito Anopheles funestus.

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