Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp.
Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp.
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DOI：
10.1371/journal.ppat.1005629
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发表时间：
2016-06
期刊：
影响因子：
6.7
通讯作者：
King KC
中科院分区：
文献类型：
--
作者：
Parratt SR;Frost CL;Schenkel MA;Rice A;Hurst GD;King KC
可遗传的微生物共生体对其节肢动物宿主的生物学具有深远的影响。虽然我们目前对这些共生体动态的理解通常只在垂直传播的框架内进行，但在许多情况下已经观察到水平传播。例如，几种共生体可以水平传播，当它们的寄生宿主与未受感染的同种共享产卵补丁时，这种现象称为超寄生。尽管如此，水平传播，和主机接触结构，促进它，没有被认为是遗传共生流行病学。在这里，我们测试了主机接触的重要性，并由此产生的水平传播，在寄生蜂宿主的男性杀死遗传共生体（砷螨nasophonus）的流行病学。我们观察到，通过过寄生的寄主接触是该共生体在其主要寄主丽蝇蛹集金小蜂种群中传播的必要条件，因此当过寄生率高时，丽蝇蛹集金小蜂A。nasopharyngeal几乎达到固定，导致高度女性偏向的人口性别比，从而导致当地主机灭绝。我们进一步测试，如果自然种间变异的超寄生行为预测共生动态寄生蜂物种。我们发现A.在实验室种群的一组密切相关的Nasonia物种，但下降，在其他更远的相关pteromalid主机nasophilus保持。一个物种的自然倾向，以过寄生是决定共生持久性的主要因素。因此，我们的研究结果表明，主机接触行为是一个关键因素，可遗传的微生物动态时，水平传播是可能的，和“生殖寄生虫”的表型，如男性杀死，可能是次要的动态共生体感染。大多数昆虫都有可遗传的共生体，这些共生体是它们生物学的重要组成部分，既可以作为配偶传递有益的特性，如防御天敌，也可以作为拮抗剂操纵宿主的繁殖。对这些细菌的研究大多假设这些表型的进化主要是为了促进共生体从亲本到后代的垂直传播。然而，一些这样的细菌也在不相关的个体之间水平移动。在这里，我们表明，男性杀死共生体实际上取决于其传播和维护水平传输。我们观察到，砷螨nasarcophonus仅保持在寄生蜂种群时，允许的路线，使水平传播，过寄生蝇蛹。当过寄生现象普遍到足以引起A.其次，由于缺乏雄性，宿主种群灭绝。我们的研究表明，过寄生行为可能是决定哪些黄蜂物种在自然界中维持这种共生体的关键因素。这为确定物种内和物种间可遗传共生体频率的因素提供了新的见解，并突出了这种共生体对其宿主种群的极端影响。这些数据还表明，雄性杀戮可能会进化并维持作为一个额外的，而不是主要的，遗传共生体健身的驱动程序。
Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont’s spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that ‘reproductive parasite’ phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections. Most insects house heritable symbionts and these represent an important component of their biology, both as partners conveying beneficial traits such as defence against natural enemies, or as antagonists manipulating their hosts’ reproduction. Work on these bacteria mostly assumes that such phenotypes have evolved primarily to facilitate the symbiont’s vertical transmission from parent to offspring. However, several such bacteria also move horizontally between unrelated individuals. Here, we show that a male-killing symbiont actually depends upon horizontal transmission for its spread and maintenance. We observed Arsenophonus nasoniae was only maintained in parasitoid wasp populations when the route enabling horizontal transmission, superparasitism of fly pupae, was allowed. When superparasitism was common enough to cause epidemic spread of A. nasoniae, host population extinction occurred due to lack of males. Our study indicates that superparasitism behaviour is likely to be the key element determining which wasp species maintain this symbiont in nature. This provides new insights into the factors determining heritable symbiont frequency within and amongst species, and highlights the extreme effects such symbionts can have on their host populations. The data also indicate that male-killing may evolve and be maintained as an additional, rather than primary, driver of heritable symbiont fitness.