Department of Biology, Tufts University, Medford, Massachusetts, USA.
Department of Integrative Biology, Michigan State University, East Lansing, Michigan, USA.
J Anim Ecol. 2022 Nov;91(11):2192-2202. doi: 10.1111/1365-2656.13803. Epub 2022 Aug 29.
Infectious disease is an important potential driver of population cycles but must occur through delayed density-dependent infection and resulting fitness effects. Delayed density-dependent infection by baculoviruses can be caused by environmental persistence of viral occlusion bodies (OBs), which can be influenced by environmental factors. Specifically, ultraviolet radiation is potentially important in reducing the environmental persistence of viruses by inactivating OBs. Delayed density-dependent viral infection has rarely been observed empirically at the population level although theory predicts that it is necessary for pathogens to drive population cycles. Similarly, field studies have not examined the effects of ultraviolet radiation on viral infection rates in natural animal populations. We tested if viral infection is delayed density-dependent with the potential to drive cyclic dynamics and if ultraviolet radiation influences viral infection levels. We censused 18 Ranchman's tiger moth (Arctia virginalis) populations across 9° of latitude over 2 years and quantified the effects of direct and delayed density and ultraviolet radiation on proportion infected by baculovirus, infection severity and survival to adulthood. Caterpillars were collected from field populations and reared in the laboratory. Baculovirus has not previously been described infecting A. virginalis, and we used genetic methods to confirm the identity of the virus. We found that proportion infected, infection severity and survival to adulthood exhibited delayed density dependence. Ultraviolet radiation in the previous summer decreased infection severity, which increased caterpillar survival probability. Structural equation modelling indicated that the effect of lagged density on caterpillar survival was mediated through proportion infected and infection severity and was 2.5-fold stronger than the indirect effect of ultraviolet. We successfully amplified polh, lef-8 and lef-9 viral genes from caterpillars, and BLAST results confirmed that the virus was a nucleopolyhedrovirus. Our findings provide clear evidence that delayed density-dependent mortality can arise through viral infection rate and severity in insects, which supports the role of viral disease as a mechanism, among others, that may drive insect population cycles. Furthermore, our findings support predictions that ultraviolet radiation can modify viral disease dynamics in insect populations, most likely through attenuating viral persistence in the environment.
传染病是种群循环的一个重要潜在驱动因素，但必须通过延迟的密度依赖感染和由此产生的适应性效应来实现。杆状病毒的延迟密度依赖感染可由病毒包埋体（OB）的环境持久性引起，而 OB 的持久性会受到环境因素的影响。具体而言，紫外线辐射可能通过使 OB 失活而在减少病毒的环境持久性方面发挥重要作用。尽管理论预测延迟的密度依赖感染对于病原体驱动种群循环是必要的，但在种群水平上，这种感染很少被经验观察到。同样，野外研究也没有检测紫外线辐射对自然动物种群中病毒感染率的影响。我们测试了病毒感染是否具有延迟的密度依赖性，这种依赖性有可能驱动周期性动态，以及紫外线辐射是否影响病毒感染水平。我们在 2 年的时间里，横跨 9 个纬度，对 18 个牧场虎蛾（Arctia virginalis）种群进行了普查，并量化了直接和延迟密度以及紫外线辐射对杆状病毒感染比例、感染严重程度和成虫存活率的影响。我们从野外种群中收集毛毛虫，并在实验室中进行饲养。杆状病毒以前没有被描述过感染 A. virginalis，我们使用遗传方法来确认病毒的身份。我们发现，感染比例、感染严重程度和成虫存活率都表现出延迟的密度依赖性。去年夏天的紫外线辐射降低了感染严重程度，从而增加了毛毛虫的存活概率。结构方程模型表明，滞后密度对毛毛虫存活的影响是通过感染比例和感染严重程度介导的，其间接影响比紫外线辐射强 2.5 倍。我们成功地从毛毛虫中扩增了 polh、lef-8 和 lef-9 病毒基因，BLAST 结果证实该病毒是一种核多角体病毒。我们的研究结果提供了明确的证据，表明昆虫中通过病毒感染率和严重程度导致的延迟密度依赖性死亡率可能会出现，这支持了病毒疾病作为一种机制的作用，可能会驱动昆虫种群循环。此外，我们的研究结果支持了紫外线辐射可以改变昆虫种群中病毒疾病动态的预测，最有可能是通过削弱病毒在环境中的持久性。
