Maternal gut microbes shape the early-life assembly of gut microbiota in passerine chicks via nests

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Maternal gut microbes shape the early-life assembly of gut microbiota in passerine chicks via nests Cheng-Yu Chen1, Chih-Kuan Chen1,2,3, Yi-Ying Chen1, Andrew Fang4, Grace Tzun-Wen Shaw1, Chih-Ming Hung1* and Daryi Wang1*

Abstract Background: Knowledge is growing on how gut microbiota are established, but the effects of maternal symbiotic microbes throughout early microbial successions in birds remain elusive. In this study, we examined the contributions and transmission modes of maternal microbes into the neonatal microbiota of a passerine, the zebra finch (Taeniopygia guttata), based on fostering experiments. Results: Using 16S rRNA amplicon sequencing, we found that zebra finch chicks raised by their biological or foster parents (the society finch Lonchura striata domestica) had gut microbial communities converging with those of the parents that reared them. Moreover, source-tracking models revealed high contribution of zebra finches’ oral cavity/ crop microbiota to their chicks’ early gut microbiota, which were largely replaced by the parental gut microbiota at later stages. The results suggest that oral feeding only affects the early stage of hatchling gut microbial development. Conclusions: Our study indicates that passerine chicks mainly acquire symbionts through indirect maternal transmission—passive environmental uptake from nests that were smeared with the intestinal and cloacal microbes of parents that raised them. Gut microbial diversity was low in hand-reared chicks, emphasizing the importance of parental care in shaping the gut microbiota. In addition, several probiotics were found in chicks fostered by society finches, which are excellent foster parents for other finches in bird farms and hosts of brood parasitism by zebra finches in aviaries; this finding implies that avian species that can transfer probiotics to chicks may become selectively preferred hosts of brood parasitism in nature. Keywords: Avian microbiota, Host-microbiome interactions, Maternal effects, Gut microbiota assembly, Maternal microbial transmission

* Correspondence: [email protected]; [email protected] 1 Biodiversity Research Center, Academia Sinica, Taipei 115201, Taiwan Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directl