Partial-arm translocations in evolution of malaria mosquitoes revealed by high-coverage physical mapping of the Anopheles atroparvus genome

Abstract

BackgroundMalaria mosquitoes have had a remarkable stability in the number of chromosomes in their karyotype (2n = 6) during 100 million years of evolution. Moreover, autosomal arms were assumed to maintain their integrity even if their associations with each other changed via whole-arm translocations. Here we use high-coverage comparative physical genome mapping of three Anopheles species to test the extent of evolutionary conservation of chromosomal arms in malaria mosquitoes.ResultsIn this study, we developed a physical genome map for Anopheles atroparvus, one of the dominant malaria vectors in Europe. Using fluorescence in situ hybridization (FISH) of DNA probes with the ovarian nurse cell polytene chromosomes and synteny comparison, we anchored 56 genomic scaffolds to the An. atroparvus chromosomes. The obtained physical map represents 89.6% of the An. atroparvus genome. This genome has the second highest mapping coverage among Anophelinae assemblies after An. albimanus, which has 98.2% of the genome assigned to its chromosomes. A comparison of the An. atroparvus, An. albimanus, and An. gambiae genomes identified partial-arm translocations between the autosomal arms that break down the integrity of chromosome elements in evolution affecting the structure of the genetic material in the pericentromeric regions. Unlike An. atroparvus and An. albimanus, all chromosome elements of An. gambiae are fully syntenic with chromosome elements of the putative ancestral Anopheles karyotype. We also detected nonrandom distribution of large conserved synteny blocks and confirmed a higher rate of inversion fixation in the X chromosome compared with autosomes.ConclusionsOur study demonstrates the power of physical mapping for understanding the genome evolution in malaria mosquitoes. The results indicate that syntenic relationships among chromosome elements of Anopheles species have not been fully preserved because of multiple partial-arm translocations.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4663-4) contains supplementary material, which is available to authorized users.

Anophelesmosquitoes revealed new principles of 3D genome organization in insects

“…Multiple misassemblies and several chromosome rearrangements were detected and fixed manually. Available physical maps of the genomes were used to verify these corrections [23][24][25][26][27] . For An.…”

Evolutionary superscaffolding and chromosome anchoring to improve Anopheles genome assemblies

“…the A. funestus and A. stephensi (SDA-500) scaffold counts both dropped by almost 22% and the newly anchored A. arabiensis assembly resulted in an 8.5-fold larger N50 value (Table 1). For the anophelines with chromosome mapping data, the contributions of the synteny-based and/or RNAseq-based adjacencies to the numbers and genomic spans of anchored scaffolds were largest for A. stephensi (SDA-500) and A. funestus, but negligible or low for the recently updated A. albimanus (Artemov et al 2017), A. atroparvus (Artemov et al 2018a), and A. sinensis (Chinese) (Wei et al 2017) assemblies ( Table 2). The two A. stephensi assemblies achieved updated assembly anchoring of 62% and 84% (both improvements of more than 20%) and A. funestus more than doubled to reach 73% anchored and a further 17% with chromosome arm assignments ( Fig.…”

“…Methods for chromosomal mapping of scaffolds (Sharakhova et al 2019;Artemov et al 2018b) are detailed for A. albimanus (Artemov et al 2017), A. atroparvus Neafsey et al 2015;Artemov et al 2018a), A. stephensi (SDA-500) , A. stephensi (Indian) (Jiang et al 2014), and A. sinensis (Chinese) (Wei et al 2017). A. funestus mapping built on previous results (Sharakhov et al 2002(Sharakhov et al , 2004Xia et al 2010) with additional FISH mapping (Supplementary Online Material: Figure S9) to further develop the physical map by considering several different types of mapping results.…”

“…The Anopheles 16 Genomes Project (Neafsey et al 2013) produced assemblies ranging from a few hundred to several thousand scaffolds and used mapping data from four species to anchor Anopheles funestus (35%), Anopheles atroparvus (40%), A. stephensi SDA-500 strain (41%), and Anopheles albimanus (76%) genomes to chromosome arms . Additional physical mapping data for A. atroparvus subsequently improved this initial assembly to 90% chromosome anchoring (Artemov et al 2018a), and for A. albimanus to 98% (Artemov et al 2017).…”

“…Combining the synteny-based results with physical mapping data from a subset of the anophelines allowed for enhanced superscaffolding as well as independent validations of the synteny-based predictions and their consensus sets. Building cytogenetic photomaps and conducting extensive FISH experiments mapped 31 A. albimanus scaffolds(Artemov et al 2017), 46 A. atroparvus scaffoldsNeafsey et al 2015;Artemov et al 2018a), 202 A. funestus scaffolds(Sharakhov et al 2002(Sharakhov et al , 2004Xia et al 2010;Neafsey et al 2015) (including additional mapping for this study), 52 A. sinensis scaffolds (Chinese)(Wei et al 2017), 99 A. stephensi (SDA-500) scaffolds, and 118A. stephensi (Indian) scaffolds(Jiang et al 2014) (including additional mapping for this study) (seeMethods; Supplementary Online Material:…”