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亲代抚育对箭毒蛙皮肤微生物群落组成的影响。

Effects of parental care on skin microbial community composition in poison frogs.

作者信息

Fischer Marie-Therese, Xue Katherine S, Costello Elizabeth K, Dvorak Mai, Raboisson Gaelle, Robaczewska Anna, Caty Stephanie N, Relman David A, O'Connell Lauren A

机构信息

Department of Biology, Stanford University, Stanford, United States.

Division of Microbial Ecology, University of Vienna, Vienna, Austria.

出版信息

Elife. 2025 Jul 31;14:RP103331. doi: 10.7554/eLife.103331.


DOI:10.7554/eLife.103331
PMID:40742751
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC12313234/
Abstract

Parent-offspring interactions constitute the first contact of many newborns with their environment, priming community assembly of microbes through priority effects and shaping host health and disease. Microbe acquisition during parental care is well studied in humans and agriculturally relevant species but remains poorly understood in other vertebrate groups, such as amphibians. Here, we investigate vertical transmission of skin microbiota in poison frogs (), where fathers transport tadpoles piggyback-style from terrestrial clutches to aquatic nurseries. We found that substantial bacterial colonization of embryos begins after hatching, suggesting that the vitelline envelope acts as a microbial barrier. A cross-foster experiment demonstrated that poison frogs performing tadpole transport serve as a source of skin microbes for tadpoles on their back. To study how transport impacts skin communities of tadpoles in an ecologically relevant setting, we sampled sympatric species that do or do not exhibit tadpole transport in their natural habitat. We did not find a higher degree of similarity between microbial communities of tadpoles and adults in species that transport their offspring compared to those that do not. Similarly, communities of tadpoles were no more similar to their caregiver than to unrelated adults, indicating that most caregiver-associated microbes do not remain in tadpole communities long-term. Nonetheless, some taxa persisted on tadpoles over development. This study is the first to demonstrate that offspring transport facilitates transmission of parental skin microbes in anurans.

摘要

亲子互动是许多新生儿与外界环境的首次接触,通过优先效应启动微生物群落的组装,并塑造宿主的健康与疾病状态。在人类和农业相关物种中,亲代抚育期间的微生物获取已得到充分研究,但在其他脊椎动物群体,如两栖动物中,这方面仍知之甚少。在此,我们研究了箭毒蛙皮肤微生物群的垂直传播情况,在箭毒蛙中,雄性亲代会将蝌蚪以背负的方式从陆地巢穴转移到水生保育场所。我们发现胚胎在孵化后才开始有大量细菌定殖,这表明卵黄膜起到了微生物屏障的作用。一项交叉寄养实验表明,参与运输蝌蚪的箭毒蛙会成为其背上蝌蚪皮肤微生物的来源。为了在生态相关环境中研究运输对蝌蚪皮肤群落的影响,我们对在自然栖息地中表现出或未表现出蝌蚪运输行为的同域物种进行了采样。与不运输后代的物种相比,我们并未发现运输后代的物种中蝌蚪和成年个体的微生物群落之间有更高的相似度。同样,蝌蚪的群落与其照料者的相似度并不高于与无关成年个体的相似度,这表明大多数与照料者相关的微生物不会长期存在于蝌蚪群落中。尽管如此,一些分类群在蝌蚪发育过程中持续存在。这项研究首次证明了后代运输促进了无尾两栖类动物亲代皮肤微生物的传播。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/51072e3c4aa4/elife-103331-fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/9b2ef7ef8606/elife-103331-fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/9676f30e2fd4/elife-103331-fig1-figsupp1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/75fdc441836d/elife-103331-fig1-figsupp2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/8d757c422203/elife-103331-fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/7fbf1d1b4452/elife-103331-fig2-figsupp1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/11030a7d32e9/elife-103331-fig2-figsupp2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/7a81acb225bc/elife-103331-fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/51072e3c4aa4/elife-103331-fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/9b2ef7ef8606/elife-103331-fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/9676f30e2fd4/elife-103331-fig1-figsupp1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/75fdc441836d/elife-103331-fig1-figsupp2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/8d757c422203/elife-103331-fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/7fbf1d1b4452/elife-103331-fig2-figsupp1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/11030a7d32e9/elife-103331-fig2-figsupp2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/7a81acb225bc/elife-103331-fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3f1a/12313234/51072e3c4aa4/elife-103331-fig4.jpg

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Effects of parental care on skin microbial community composition in poison frogs.

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本文引用的文献

[1]
Absolute quantification of prokaryotes in the microbiome by 16S rRNA qPCR or ddPCR.

Nat Protoc. 2025-5-19

[2]
Developments in Amphibian Parental Care Research: History, Present Advances, and Future Perspectives.

Herpetological Monographs. 2020-7-15

[3]
What Amphibians Can Teach Us About the Evolution of Parental Care.

Annu Rev Ecol Evol Syst. 2023-11

[4]
A comparative table for staging anuran embryos from terrestrial clutches based on the Brilliant-thighed Poison Frog, (Anura: Dendrobatidae).

Herpetol Notes. 2022-10-20

[5]
Paternal and induced gut microbiota seeding complement mother-to-infant transmission.

Cell Host Microbe. 2024-6-12

[6]
Priority effects alter microbiome composition and increase abundance of probiotic taxa in treefrog tadpoles.

Appl Environ Microbiol. 2024-6-18

[7]
Something in the water: aquatic microbial communities influence the larval amphibian gut microbiota, neurodevelopment and behaviour.

Proc Biol Sci. 2024-2-28

[8]
Microbial underdogs: exploring the significance of low-abundance commensals in host-microbe interactions.

Exp Mol Med. 2023-12

[9]
Early-life microbiota-immune homeostasis.

Front Immunol. 2023

[10]
Ongoing declines for the world's amphibians in the face of emerging threats.

Nature. 2023-10

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