Phylogeography and population structure of the tsetse fly Glossina pallidipes in Kenya and the Serengeti ecosystem

Glossina pallidipes is the main vector of animal African trypanosomiasis and a potential vector of human African trypanosomiasis in eastern Africa where it poses a large economic burden and public health threat. Vector control efforts have succeeded in reducing infection rates, but recent resurgence in tsetse fly population density raises concerns that vector control programs require improved strategic planning over larger geographic and temporal scales. Detailed knowledge of population structure and dispersal patterns can provide the required information to improve planning. To this end, we investigated the phylogeography and population structure of G. pallidipes over a large spatial scale in Kenya and northern Tanzania using 11 microsatellite loci genotyped in 600 individuals. Our results indicate distinct genetic clusters east and west of the Great Rift Valley, and less distinct clustering of the northwest separate from the southwest (Serengeti ecosystem). Estimates of genetic differentiation and first-generation migration indicated high genetic connectivity within genetic clusters even across large geographic distances of more than 300 km in the east, but only occasional migration among clusters. Patterns of connectivity suggest isolation by distance across genetic breaks but not within genetic clusters, and imply a major role for river basins in facilitating gene flow in G. pallidipes. Effective population size (Ne) estimates and results from Approximate Bayesian Computation further support that there has been recent G. pallidipes population size fluctuations in the Serengeti ecosystem and the northwest during the last century, but also suggest that the full extent of differences in genetic diversity and population dynamics between the east and the west was established over evolutionary time periods (tentatively on the order of millions of years). Findings provide further support that the Serengeti ecosystem and northwestern Kenya represent independent tsetse populations. Additionally, we present evidence that three previously recognized populations (the Mbeere-Meru, Central Kenya and Coastal “fly belts”) act as a single population and should be considered as a single unit in vector control.

刺舌蝇（Glossina pallidipes）是非洲动物锥虫病的主要传播媒介，同时也是东非地区人类非洲锥虫病的潜在传播媒介，该区域因此承受了沉重的经济负担与严峻的公共卫生威胁。尽管媒介控制措施已成功降低了感染率，但近期采采蝇种群密度的回升引发了新的担忧：媒介控制项目亟需在更大的地理与时间尺度上优化战略规划。深入掌握种群结构与扩散模式，可为规划优化提供必要的信息支撑。为此，我们针对肯尼亚与坦桑尼亚北部大范围分布的刺舌蝇种群，采用对600个个体进行基因分型的11个微卫星位点，对其系统地理学与种群结构展开了研究。研究结果显示，大裂谷（Great Rift Valley）东西两侧存在显著的遗传聚类群，而西北部与西南部（塞伦盖蒂生态系统）的聚类群区分度相对较弱。遗传分化与第一代迁移的评估结果表明，即使在东部超过300公里的大范围地理距离内，各遗传聚类群内部仍存在高度的遗传连通性，但不同聚类群之间仅存在偶发的基因交流。连通性模式显示，遗传间断区域存在距离隔离效应，但在遗传聚类群内部则无此现象，这表明河流流域在刺舌蝇的基因流传播中发挥了关键作用。有效种群大小（effective population size, Ne）的估算结果与近似贝叶斯计算（Approximate Bayesian Computation）的分析进一步证实，在上个世纪内，塞伦盖蒂生态系统与西北部的刺舌蝇种群规模曾出现近期波动；同时研究也表明，东西两侧种群在遗传多样性与种群动态方面的差异，其完整形成过程可追溯至演化时间尺度（大致为数百万年量级）。本研究结果进一步支持塞伦盖蒂生态系统与肯尼亚西北部为独立采采蝇种群的结论。此外，我们发现此前被认定的三个种群（姆贝雷-梅鲁种群、肯尼亚中部种群与沿海‘蝇带’种群）实为单一种群，因此在媒介控制工作中应将其视为统一单元开展管理。