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Updated: Sep 10, 2025
Author Spotlight: Establishing Germ-Free Zebrafish for Microbiota-Host Relationship Studies
Published on: April 12, 2024
Paternal microbiota manipulation influences offspring microbial colonization and development in a sex role-reversed
Kim-Sara Wagner1, Frédéric Salasc2,3, Silke-Mareike Marten2
1Marine Evolutionary Biology, Zoological Institute, Kiel University, 24118, Kiel, Germany. kwagner@zoologie.uni-kiel.de.
Abstract:
Microbes are acquired through vertical and environmental horizontal transmission. Vertical transmission is directly linked to reproductive success and entails early transmission, facilitating coexistence of host and microbes over generations. The multiple potentially interacting routes of vertical transmission are challenging to be disentangled in conventional sex-role species, as they are mostly intermingled on the maternal side, i.e., through egg production, pregnancy, birth and postnatal care. The evolution of male pregnancy in syngnathids (pipefishes and seahorses) offers an opportunity to separate vertical microbial provisioning through the egg (maternal) from provisioning through pregnancy (paternal). We experimentally evaluated the existence and role of paternal vertical microbiota provisioning through male pregnancy on offspring development and microbial colonization. Male pipefish were exposed to antibiotics, and subsequently recolonized with bacteria of paternal, maternal, and environmental origin (spike treatment). After pregnancy, the microbiota of developing offspring was characterized using 16 S rRNA sequencing of the V3-V4 region. Paternal antibiotic and spike treatments influenced the microbial composition of the brood pouch and offspring microbiome development. Paternal spike treatment shortened pregnancy duration and enhanced offspring survival, underlining its beneficial effect for early life stages. Expanding on how distinct vertical microbial transmission routes shape the offspring microbiome will foster our understanding of holobiont function in health and disease.
Insights
Male pregnancy in pipefish allows separating maternal and paternal microbial contributions. Paternal provisioning via male pregnancy significantly impacts offspring microbiome development and survival.
Area of Science:
- Microbiology
- Evolutionary Biology
- Reproductive Biology
Background:
- Microbes are transmitted vertically (parent to offspring) and horizontally (environment).
- Vertical transmission is crucial for host-microbe co-existence, but routes are often maternal and complex.
- Male pregnancy in syngnathids offers a unique model to distinguish paternal from maternal microbial provisioning.
Purpose of the Study:
- To experimentally investigate paternal vertical microbiota provisioning in male pipefish.
- To assess the impact of paternal microbial provisioning on offspring microbiome development and survival.
Main Methods:
- Male pipefish were treated with antibiotics and then recolonized with specific bacteria (paternal, maternal, environmental).
- Offspring microbiome composition was analyzed using 16S rRNA gene sequencing.
- Pregnancy duration and offspring survival were monitored.
Main Results:
- Paternal antibiotic and bacterial "spike" treatments altered brood pouch and offspring microbial composition.
- Paternal "spike" treatment reduced pregnancy duration and increased offspring survival.
- Distinct vertical microbial transmission routes shape offspring microbiome.
Conclusions:
- Paternal provisioning of microbes during male pregnancy is a significant factor in offspring development.
- Understanding distinct vertical microbial transmission routes is key to holobiont health and disease research.
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