Transgenerational plasticity in a zooplankton in response to elevated temperature and parasitism

Organisms are increasingly facing multiple stressors, which can
simultaneously interact to cause unpredictable impacts compared to a
single stressor alone. Recent evidence suggests that phenotypic plasticity
can allow for rapid responses to altered environments, including biotic
and abiotic stressors, both within a generation and across generations
(transgenerational plasticity). Parents can potentially ‘prime’ their
offspring to better cope with similar stressors, or, alternatively, might
produce offspring that are less fit because of energetic constraints. At
present, it remains unclear exactly how biotic and abiotic stressors
jointly mediate the responses of transgenerational plasticity, and whether
this plasticity is adaptive. Here we test the effects of biotic and
abiotic environmental changes on within- and trans-generational plasticity
using a Daphnia-Metschnikowia zooplankton-fungal parasite system. By
exposing parents and their offspring consecutively to the single and
combined effects of elevated temperature and parasite infection, we showed
that transgenerational plasticity induced by temperature and parasite
stress influenced host fecundity and lifespan; offspring of mothers that
were exposed to one of the stressors were better able to tolerate elevated
temperature, compared to offspring of mothers that were exposed to neither
or both stressors. Yet the negative effects caused by parasite infection
were much stronger, and this greater reduction in host fitness was not
mitigated by transgenerational plasticity. We also showed that elevated
temperature led to a lower average immune response and that the
relationship between immune response and lifetime fecundity reversed under
elevated temperature: the daughters of exposed mothers showed decreased
fecundity with increased hemocyte production at ambient temperature, but
the opposite relationship at elevated temperature. Together, our results
highlight the need to address questions at the interface of multiple
stressors and transgenerational plasticity, and the importance of
considering multiple fitness-associated traits when evaluating the
adaptive value of transgenerational plasticity under changing
environments.

生物正日益面临多重胁迫因子，与单一胁迫因子相比，这些因子可同时发生交互作用，产生难以预测的影响。近期研究表明，表型可塑性（phenotypic plasticity）可使生物对环境变化做出快速响应——包括应对生物胁迫与非生物胁迫，且该响应可发生于当代之内，亦可跨代传递，即跨代可塑性（transgenerational plasticity）。亲代可通过预致敏子代，使其更好地应对同类胁迫；但另一方面，受能量约束影响，亲代也可能产生适合度更低的子代。目前，学界尚不清楚生物与非生物胁迫如何共同调控跨代可塑性的响应过程，也不确定该可塑性是否具有适应性。本研究以水蚤-梅奇酵母（Daphnia-Metschnikowia）浮游动物-真菌寄生虫系统为研究对象，探究生物与非生物环境变化对当代可塑性及跨代可塑性的影响。通过依次让亲代与子代分别暴露于高温、寄生虫感染的单一胁迫及其复合胁迫下，我们发现：由温度与寄生虫胁迫诱导产生的跨代可塑性，会影响宿主的繁殖力与寿命。与未经历任何胁迫或同时经历两种胁迫的母代所产后代相比，仅经历过单一胁迫的母代所产后代对高温的耐受能力更强。但寄生虫感染所造成的负面影响更为显著，且跨代可塑性并未缓解宿主适合度的大幅下降。此外我们还发现，高温会使宿主的平均免疫响应水平降低；且在高温条件下，免疫响应与终身繁殖力之间的关系发生了逆转：在常温环境下，经历过胁迫的母代所产雌性后代的血细胞数量越多，其繁殖力越低；而在高温环境下，二者的关系则恰好相反。综上，本研究结果表明，学界亟需厘清多重胁迫与跨代可塑性之间的交互关系；同时，在评估变化环境下跨代可塑性的适应性价值时，需综合考量多个与适合度相关的性状。