Department of Entomology, the Fralin Life Sciences Institute, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA.
Kurchatov Genomics Center, the Federal Research Center, Institute of Cytology and Genetics, Novosibirsk, Russia.
BMC Biol. 2023 Apr 10;21(1):63. doi: 10.1186/s12915-023-01538-w.
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.
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.
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.
对密切相关的蚊子物种进行系统发育分析，对于更好地了解有助于传播病媒传播疾病的特征的进化很重要。世界上 41 种主要疟疾病媒蚊子中有 6 种属于按蚊属的 Maculipennis 组，该组分为两个近北极亚组（Freeborni 和 Quadrimaculatus）和一个北极亚组（Maculipennis）。尽管先前的研究认为近北极亚组是祖先，但有关它们与北极亚组的关系，以及它们从北美到欧亚大陆的迁移时间和路线仍存在争议。目前，Palearctic 物种 An. beklemishevi 被归入近北极 Quadrimaculatus 亚组，这增加了蚊子系统发育的不确定性。
为了重建 Maculipennis 组的历史关系，我们基于 1271 个直系同源基因的序列，对 11 种北极和 2 种近北极物种进行了系统基因组分析。分析表明，北极物种 An. beklemishevi 与其他欧亚物种聚在一起，代表它们中的一个基群。此外，An. beklemishevi 与栖息在美国西部的 An. freeborni 关系更为密切，而不是与栖息在美国东部的 An. quadrimaculatus 关系更为密切。时间校准的树表明，大约 20-2500 万年前，蚊子从北美迁徙到欧亚大陆，通过白令陆桥。杂种检查分析表明，所有生境物种 An. labranchiae 和 An. beklemishevi 之间存在高度显著的基因渗入事件的特征。该分析还确定了其近北极亲缘种 An. sacharovi 与 An. freeborni 之间的祖先基因渗入事件，尽管它们目前地理上是隔离的。重建的系统发育表明，在 Maculipennis 组的不同谱系中，媒介效能和在冬季进入完全滞育的能力是独立进化的。
我们的系统基因组分析揭示了全北极疟疾病媒的迁移路线和辐射时间，并强烈支持将 An. beklemishevi 归入 Maculipennis 亚组。对 Maculipennis 亚组进化历史的详细了解为研究与生态适应和对人类病原体易感性相关的基因组变化提供了框架。这些基因组变异可以为研究人员提供有关未来类似变化的信息，为了解欧亚大陆疾病传播模式提供了信息。
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