Host association drives significant genetic divergence in the bed bug, Cimex lectularius

Genetic differentiation may exist among sympatric populations of a species due to long-term associations with alternative hosts (i.e., host-associated differentiation). While host-associated differentiation has been documented in several phytophagus insects, there are far fewer cases known in animal parasites. The bed bug, Cimex lectularius, a wingless insect, represents a potential model organism for elucidating the processes involved in host-associated differentiation in animal parasites with relatively limited mobility. In conjunction with the expansion of modern humans from Africa into Eurasia, it has been speculated that bed bugs extended their host range from bats to humans in their shared cave domiciles throughout Eurasia. C. lectularius that associate with humans have a cosmopolitan distribution, whereas those associated with bats occur across Europe, often in human-built structures. We assessed genetic structure and gene flow within and among populations collected in association with each host using mtDNA, microsatellite loci, and knock-down-resistance gene variants. Both nuclear and mitochondrial data support a lack of significant contemporary gene flow between host-specific populations. Within locations human-associated bed bug populations exhibit limited genetic diversity and elevated levels of inbreeding, likely due to human-mediated movement, infrequent additional introduction events per infestation, and pest control. In contrast, populations within bat roosts exhibit higher genetic diversity and lower levels of relatedness, suggesting populations are stable with temporal fluctuations due to host dispersal and bug mortality. In concert with previously published evidence of morphological and behavioral differentiation, the genetic data presented here suggest C. lectularius is currently undergoing lineage divergence through host-association.

物种的同域种群（sympatric populations）之间可能存在遗传分化，该分化源于其与不同宿主的长期关联，即宿主关联分化（host-associated differentiation）。尽管已有多项研究在植食性昆虫（phytophagus insects）中记录到宿主关联分化现象，但在动物寄生虫中已知的相关案例却少得多。温带臭虫（Cimex lectularius）作为一种无翅昆虫，可作为研究流动性相对有限的动物寄生虫宿主关联分化过程的潜在模式生物。伴随现代人类从非洲向欧亚大陆的扩张，有推测认为温带臭虫曾在欧亚大陆的共享洞穴居所中，将宿主范围从蝙蝠拓展至人类。与人类关联的温带臭虫种群呈全球性分布，而与蝙蝠关联的种群则分布于欧洲各地，且常出现在人类建造的建筑中。我们依托线粒体DNA（mtDNA）、微卫星位点（microsatellite loci）以及击倒抗性基因（knock-down-resistance gene）变异，对两种宿主关联种群内部及种群间的遗传结构与基因流进行了评估。核基因与线粒体数据均表明，宿主特异性种群间不存在显著的当代基因流。在同一采样地点内，与人类关联的臭虫种群遗传多样性有限且近交水平升高，这可能源于人类介导的种群扩散、单次侵染事件中额外引入事件稀少，以及害虫防治措施的影响。与之形成对比的是，蝙蝠栖息处的臭虫种群遗传多样性更高且亲缘关系水平更低，这表明其种群结构稳定，仅因宿主扩散以及臭虫死亡而出现随时间变化的波动。结合此前已发表的形态与行为分化相关证据，本文呈现的遗传数据表明，温带臭虫当前正通过宿主关联过程发生谱系分化。