Offspring performance is well buffered against stress experienced by ancestors

Abstract

Evolution should render individuals resistant to stress and particularly to stress experienced by ancestors. However, many studies report negative effects of stress experienced by one generation on the performance of subsequent generations. To assess the strength of such transgenerational effects we used a strategy aimed at overcoming the problem of type I errors when testing multiple proxies of stress in multiple ancestors against multiple offspring performance traits, and applied it to a large observational data set on captive zebra finches (Taeniopygia guttata). We combined clear one-tailed hypotheses with steps of validation, meta-analytic summary of mean effect sizes, and independent confirmatory testing. With this approach we assess to what extent offspring performance in adulthood depends on (1) direct effects of own experiences during early development, (2) indirect condition-transfer effects of the early environment experienced by the parents and the grandparents, and (3) beneficial effects of a match between the environments experienced by the offspring and by its parents. Our study shows that drastic differences in early growth conditions (nestling body mass 8 days after hatching varied 7-fold between 1.7 and 12.4 gram) had only moderate direct effects on adult morphology (95%CI: r=0.19-0.27) and small direct effects on fitness traits (r=0.02-0.12). In contrast, we found no indirect effects of parental or grandparental condition (r=-0.017-0.002; meta-analytic summary of 138 effect sizes), and mixed evidence for small benefits of matching environments, as the latter was not robust to confirmatory testing in independent data sets. This study shows that evolution has led to a remarkable robustness of zebra finches against undernourishment and that transgenerational effects are absent. Author SummaryHow the early life conditions of your ancestors might influence your own life, an aspect of epigenetic inheritance, has become a popular topic among evolutionary biologists and has sparked much interest by the general public. Many theoretical and empirical studies have addressed this question, leading to theories of adaptive programming and condition transfer and ideas of epigenetic or genetic organization. Despite the popularity of this topic, however, there is a lack of a standard framework to guide empirical studies, which are at risk of over-interpreting the most significant effects that might emerge by chance alone when conducting a large number of tests. In this study, we used long-term observational data on multiple morphological and life-history traits of hundreds of male and female zebra finches with information on the early life conditions of both the focal birds and their parents and grandparents. This allows us to comprehensively quantify the magnitude of direct and transgenerational effects of early developmental conditions. Our study (1) proposes a standardized statistical framework for future investigations, (2) summarizes the average effect size (in zebra finches) and indicates the sample sizes needed to pick up such an effect, and (3) provides a counter statement to a growing faith in the ubiquity of transgenerational effects despite their limited evolutionary or mechanistic plausibility.