Recurrent evolution of two competing haplotypes in an insect DNA virus

Hosts and viruses are constantly evolving in response to each other: as hosts attempt to suppress the virus, the virus attempts to evade and suppress the host's immune system. This arms race results in the evolution of novel pathways in both the host and virus to gain the upper hand. Here we describe the coevolution between Drosophila species and a common and virulent DNA virus. We identify two distinct viral types that differ 100-fold in viral titer in infected individuals, with similar effects across multiple species. Our analysis suggests that one of the viral types appears to have recurrently evolved at least 4 times in the past ~30,000 years, including in another geographically distinct species, due to the high effective mutation rate which increases with titer. The higher titer viral type is associated with suppression of the host immune system and an increased transmission rate compared to the low viral titer type. Both types are maintained in all populations, likely due to an increased virulence in the high titer type creating a trade-off between effective transmission and virulence and resulting in nearly equal reproduction rates (R0) in both types. Together these results suggest that the reciprocal selective pressures caused by the co-evolution between host and virus has resulted in this recurrently evolving relationship.

宿主与病毒始终处于相互驱动的协同演化进程中：宿主会试图抑制病毒增殖，而病毒则会演化出策略以规避宿主的免疫防御并对抗宿主的免疫系统。这种演化军备竞赛（arms race）会促使宿主与病毒双方均演化出全新的通路，从而在相互对抗中占据演化优势。本研究描述了果蝇属（Drosophila）物种与一种常见高致病性DNA病毒之间的协同演化关系，我们鉴定出两种截然不同的病毒类型，二者在感染宿主后的病毒滴度（viral titer）相差可达100倍，且该效应在多个果蝇物种中均保持一致。我们的分析显示，其中一种病毒类型因病毒滴度越高其有效突变率也随之升高，在过去约3万年的时间里已至少4次独立反复演化，甚至在另一地理隔离的果蝇物种中也出现了该类型的演化事件。相较于低滴度病毒类型，高滴度病毒类型可抑制宿主免疫系统，并提升病毒传播速率。两种病毒类型在所有种群中均得以维持，这大概率是因为高滴度类型的致病力（virulence）更强，由此在有效传播与致病力之间形成了演化权衡（trade-off），最终使得两种类型的基本再生数（R0）近乎相等。综上，上述结果表明，宿主与病毒间由协同演化所引发的双向选择压力，造就了这种反复出现的演化关联。