Phylogenomics revealed migration routes and adaptive radiation timing of Holarctic malaria mosquito species of the Maculipennis Group

Abstract

Background Phylogenetic analyses of closely related species of mosquitoes are important for better understanding the evolution of traits contributing to transmission of vector-borne diseases. Six out of 41 dominant malaria vectors of the genus Anopheles in the world belong to the Maculipennis Group, which is subdivided into two Nearctic subgroups (Freeborni and Quadrimaculatus) and one Palearctic (Maculipennis) subgroup. Although previous studies considered the Nearctic subgroups as ancestral, details about their relationship with the Palearctic subgroup, and their migration times and routes from North America to Eurasia remain controversial. The Palearctic species An. beklemishevi is currently included in the Nearctic Quadrimaculatus subgroup adding to the uncertainties in mosquito systematics. Results To reconstruct historic relationships in the Maculipennis Group, we conducted a phylogenomic analysis of 11 Palearctic and 2 Nearctic species based on sequences of 1271 orthologous genes. The analysis indicated that the Palearctic species An. beklemishevi clusters together with other Eurasian species and represents a basal lineage among them. Also, An. beklemishevi is related more closely to An. freeborni, which inhabits the Western United States, rather than to An. quadrimaculatus, a species from the Eastern United States. The time-calibrated tree suggests a migration of mosquitoes in the Maculipennis Group from North America to Eurasia about 20–25 million years ago through the Bering Land Bridge. A Hybridcheck analysis demonstrated highly significant signatures of introgression events between allopatric species An. labranchiae and An. beklemishevi. The analysis also identified ancestral introgression events between An. sacharovi and its Nearctic relative An. freeborni despite their current geographic isolation. The reconstructed phylogeny suggests that vector competence and the ability to enter complete diapause during winter evolved independently in different lineages of the Maculipennis Group. Conclusions Our phylogenomic analyses reveal migration routes and adaptive radiation timing of Holarctic malaria vectors and strongly support the inclusion of An. beklemishevi into the Maculipennis Subgroup. Detailed knowledge of the evolutionary history of the Maculipennis Subgroup provides a framework for examining the genomic changes related to ecological adaptation and susceptibility to human pathogens. These genomic variations may inform researchers about similar changes in the future providing insights into the patterns of disease transmission in Eurasia.

Two Nested Inversions in the X Chromosome Differentiate the Dominant Malaria Vectors in Europe, Anopheles atroparvus and Anopheles messeae

“…melanoon. Only one autosomal inversion became fixed after the split between the European clade and the Northern Eurasian clade about 10.5 million years ago [8]. According to our reconstruction, the X chromosome of An.…”

“…Two nested inversions were identified in the X chromosome, which were fixed in the An. messeae lineage after its separation from other species of the Maculipennis subgroup about 7.9 million years ago [8]. The comparison of gene orders in the BRs with those in outgroup species has shown that An.…”

“…Iterative physical mapping was conducted in multiple steps. In the first step, we selected 17 gene markers spaced by about 1 Mb from each other [8]. These An.…”

“…For example, chromosomal phylogeny has identified ancestral and derived karyotypes in malaria mosquitoes of the Anopheles gambiae complex [4][5][6][7]. A recent combination of the whole-genome and inversion-based approaches reconstructed the phylogeny of mosquito species of the Maculipennis subgroup [8].…”

“…The Maculipennis subgroup comprises species of malaria mosquitoes found in northern Eurasia. According to a recent multi-gene phylogeny reconstruction, supported by cytogenetic analysis, the ancestral species of these mosquitoes migrated from North America to Eurasia through Bering Land Bridge about 20 million years ago and were later divided into three clades: the Southern Eurasia clade, the European clade, and the Northern Eurasian clade [8]. Anopheles atroparvus is the dominant vector in much of Europe and to a lesser extent in the western part of Russia [10,11].…”