Rutkowski Nicola-Anne J, McNamara Kathryn B, Jones Therésa M, Foo Yong Zhi
School of BioSciences, University of Melbourne, Biosciences 4, Royal Parade, Parkville, VIC, 3052, Australia.
Centre for Evolutionary Biology & School of Biological Sciences, University of Western Australia, 35 Stirling Hwy, Crawley, WA, 6009, Australia.
Biol Rev Camb Philos Soc. 2023 Aug;98(4):1100-1117. doi: 10.1111/brv.12946. Epub 2023 Mar 6.
Traditionally, only vertebrates were thought capable of acquired immune responses, such as the ability to transfer immunological experience vertically to their offspring (known as trans-generational immune priming, TGIP). Increasing evidence challenges this belief and it is now clear that invertebrates also have the ability to exhibit functionally equivalent TGIP. This has led to a surge in papers exploring invertebrate TGIP, with most focusing on the costs, benefits or factors that affect the evolution of this trait. Whilst many studies have found support for the phenomenon, not all studies do, and there is considerable variation in the strength of positive results. To address this, we conducted a meta-analysis to answer the question: what is the overall effect of TGIP in invertebrates? Then, to understand the specific factors that affect its presence and intensity, we conducted a moderator analysis. Our results corroborate that TGIP occurs in invertebrates (demonstrated by a large, positive effect size). The strength of the positive effect was related to if and how offspring were immune challenged (i.e. whether they were challenged with the same or different insult as their parents or not challenged at all). Interestingly, there was no effect of the ecology or life history of the species or the sex of the parent or the offspring primed, and responses were comparable across different immune elicitors. Our publication bias testing suggests that the literature may suffer from some level of positive-result bias. However, even after accounting for potential bias, our effect size remains positive. Publication bias testing can be influenced by diversity in the data set, which was considerable in our data, even after moderator analysis. It is therefore conceivable that differences among studies could be caused by other moderators that were unable to be included in our meta-analysis. Nonetheless, our results suggest that TGIP does occur in invertebrates, whilst providing some potential avenues to examine the factors that account for variation in effect sizes.
传统上，只有脊椎动物被认为能够产生获得性免疫反应，比如将免疫经验垂直传递给后代的能力（称为跨代免疫致敏，TGIP）。越来越多的证据对这一观点提出了挑战，现在很清楚的是，无脊椎动物也有能力表现出功能上等效的TGIP。这导致了大量探索无脊椎动物TGIP的论文涌现，其中大多数关注影响这一特性进化的成本、益处或因素。虽然许多研究都支持这一现象，但并非所有研究都如此，而且阳性结果的强度存在相当大的差异。为了解决这个问题，我们进行了一项荟萃分析来回答这个问题：TGIP在无脊椎动物中的总体效应是什么？然后，为了了解影响其存在和强度的具体因素，我们进行了一项调节因素分析。我们的结果证实TGIP在无脊椎动物中确实存在（通过一个大的、积极的效应量证明）。积极效应的强度与后代是否以及如何受到免疫挑战有关（即它们是否受到与父母相同或不同的刺激，或者根本没有受到挑战）。有趣的是，物种的生态或生活史、被致敏的亲本或后代的性别均没有影响，并且不同免疫激发剂的反应具有可比性。我们的发表偏倚检验表明，文献可能存在一定程度的阳性结果偏倚。然而，即使考虑到潜在的偏倚，我们的效应量仍然是积极的。发表偏倚检验可能会受到数据集中多样性的影响，即使在调节因素分析之后，我们的数据中这种多样性仍然相当大。因此，可以想象，研究之间的差异可能是由其他无法纳入我们荟萃分析的调节因素造成的。尽管如此，我们的结果表明TGIP确实存在于无脊椎动物中，同时提供了一些潜在的途径来研究影响效应量变化的因素。
