West Nile virus experimental evolution in vivo and the trade-off hypothesis.
West Nile virus experimental evolution in vivo and the trade-off hypothesis.
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DOI：
10.1371/journal.ppat.1002335
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发表时间：
2011-11
期刊：
影响因子：
6.7
通讯作者：
Ebel GD
中科院分区：
文献类型：
--
作者：
Deardorff ER;Fitzpatrick KA;Jerzak GV;Shi PY;Kramer LD;Ebel GD
在自然界中，节肢动物传播的病毒(虫媒病毒)通过在脊椎动物和无脊椎动物宿主中交替复制而永久存在。权衡假说提出，这些病毒在两个不同的宿主中保持足够的复制适应性，以换取在一个宿主中的优越适应性。因此，将病毒从两个宿主周期的限制中释放出来，应有助于适应单一宿主。这一理论已经在各种系统中得到了解决，但仍然知之甚少。我们试图使用活体模型系统来确定西尼罗河病毒(WNV)交替宿主复制的适合性。此前，西尼罗河病毒在小鸡或蚊子体内连续或交替传代20次，所产生的病毒具有遗传学特征。在这项研究中，这些测试病毒在体内与一种未通过的标记参考病毒进行适合性分析。在雏鸡和两个重要的西尼罗河病毒载体--淡色库蚊和致倦库蚊中进行了适合性分析。雏鸡专用病毒在雏鸡和CX中显示出明显的健康增长。但在CX中不存在。[医]五倍子属CX.蚊子特有的病毒在雏鸟身上的适合性降低，在两种蚊子中几乎没有变化。这些数据表明，当衡量鸟类的适合度时，权衡假说得到了支持；但在蚊子身上却没有得到支持。总体而言，这些结果表明，西尼罗河病毒的进化是由蚊子中基因扩张的交替周期驱动的，在蚊子中，净化选择较弱，产生遗传多样性，而在鸟类中，限制，净化选择较强。节肢动物传播的病毒，包括西尼罗河病毒(West Nile Virus，WNV)，长期以来一直被认为受到适合性“权衡”的影响，因为它们必须在至少两个分类上不同的宿主中复制才能持久存在。检验这一权衡假说的研究结果一直不一致，而且在很大程度上取决于研究的是哪个病毒家族和使用了哪个实验系统。因此，关于寄主交替如何影响病毒种群生物学，文献中存在相当多的含糊之处。因此，我们允许WNV适应它的每个主要宿主(蚊子和鸟类)20次连续传递，以确定宿主在自然界中的交替是否会像权衡假说所预测的那样带来适应性妥协。在宿主专门化之后，传递的病毒在蚊子和雏鸟体内与未传递的标记参考病毒竞争，以确定复制适合度是否发生了变化。我们的结果表明，权衡假设准确地预测了西尼罗河病毒在鸟类环境中的适应，而不是在蚊子中的适应。总体而言，我们的结果表明，西尼罗河病毒的适应是由允许蚊子环境中的基因扩张和鸟类中的限制交替循环控制的，在那里净化选择占主导地位。
In nature, arthropod-borne viruses (arboviruses) perpetuate through alternating replication in vertebrate and invertebrate hosts. The trade-off hypothesis proposes that these viruses maintain adequate replicative fitness in two disparate hosts in exchange for superior fitness in one host. Releasing the virus from the constraints of a two-host cycle should thus facilitate adaptation to a single host. This theory has been addressed in a variety of systems, but remains poorly understood. We sought to determine the fitness implications of alternating host replication for West Nile virus (WNV) using an in vivo model system. Previously, WNV was serially or alternately passed 20 times in vivo in chicks or mosquitoes and resulting viruses were characterized genetically. In this study, these test viruses were competed in vivo in fitness assays against an unpassed marked reference virus. Fitness was assayed in chicks and in two important WNV vectors, Culex pipiens and Culex quinquefasciatus. Chick-specialized virus displayed clear fitness gains in chicks and in Cx. pipiens but not in Cx. quinquefasciatus. Cx. pipiens-specialized virus experienced reduced fitness in chicks and little change in either mosquito species. These data suggest that when fitness is measured in birds the trade-off hypothesis is supported; but in mosquitoes it is not. Overall, these results suggest that WNV evolution is driven by alternate cycles of genetic expansion in mosquitoes, where purifying selection is weak and genetic diversity generated, and restriction in birds, where purifying selection is strong. Arthropod-borne viruses, including West Nile virus (WNV) have long been considered to be subject to a fitness “trade-off” because they must replicate in at least two taxonomically divergent hosts in order to perpetuate. Results of studies testing this trade-off hypothesis have been inconsistent and largely dependent on which virus family is studied and which experimental system used. Therefore, considerable ambiguity exists in the literature regarding how host alternation influences virus population biology. Accordingly, we allowed WNV to adapt to each of its main hosts (mosquitoes and birds) for 20 sequential passes in order to determine whether host alternation in nature imparts a fitness compromise, as predicted by the trade-off hypothesis. After host-specialization, passed viruses were competed in vivo in mosquitoes and chicks against an unpassed marked reference virus to determine whether replicative fitness gains or losses had occurred. Our results demonstrate that the trade-off hypothesis accurately predicts WNV adaptation in the avian environment but not in mosquitoes. Overall, our results suggest that WNV adaptation is controlled by alternating cycles of genetic expansion in a permissive mosquito environment and restriction in avians, where purifying selection is dominant.
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