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Microbiome Dynamics During Offspring Development in a Hemimetabolous Insect: The Role of Moulting and Maternal Care


Kernkonzepte
The bacterial microbiome of European earwig offspring undergoes substantial changes during development, which are not driven by moulting events but rather by stage-specific microbial niches. Maternal care also shapes the microbiome of offspring, with both short-term and long-term effects.
Zusammenfassung

The study investigated how the microbiome of the hemimetabolous European earwig changes during offspring development and whether these changes are driven by moulting events or influenced by maternal care.

Key findings:

  • The bacterial microbiome diversity and structure of earwig offspring changed substantially during development, but these changes did not occur during moulting events, except for the moult between the 3rd and 4th instar nymphs.
  • The changes in microbiome were associated with the colonization of new bacterial genera at certain developmental stages, likely reflecting stage-specific microbial niches.
  • Predicted bacterial functions also changed during development, suggesting potential benefits to the host, such as increased lipid synthesis during the egg-to-nymph transition and acquisition of essential vitamins during the 3rd instar.
  • Maternal care had both short-term and long-term effects on the microbiome of offspring, even though maternal presence is not required for offspring survival in this species. Offspring with maternal care had higher phylogenetic diversity and distinct bacterial communities compared to orphaned offspring.

Overall, the results provide new insights into the (in)stability of the prokaryotic microbiome in hemimetabolous insects and the role of maternal care in shaping offspring microbiomes, even when this care is facultative.

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Statistiken
"The 218 samples obtained showed that the microbiome diversity changed non-linearly during development and that these changes were associated with bacterial biomarkers." "We also found that access to maternal care affected the microbiome of both juveniles and adults, even when the last contact with mothers was two months before adulthood."
Zitate
"Surprisingly, these changes did not occur during moulting, but rather between the beginning and end of certain developmental stages." "Overall, these results provide new insights into our understanding of the (in)stability of the prokaryotic microbiome in hemimetabolous insects and its independence from moult."

Tiefere Fragen

How do the stage-specific microbial niches in earwig development arise and what are the underlying physiological or ecological mechanisms driving them?

In the context of earwig development, the stage-specific microbial niches likely arise from a combination of factors, including host physiology, environmental influences, and microbial interactions. During the early stages of development, such as eggs and newly hatched nymphs, the microbial community may be influenced by the initial colonization of bacteria from the environment and maternal transmission. Maternal care, such as grooming and egg protection, can introduce specific bacteria to the offspring, shaping the early microbial community. As the nymphs progress through different instar stages, physiological changes in the host, such as hormonal fluctuations and dietary shifts, can impact the microbial composition. For example, the decrease in microbial diversity observed in the 2nd instar nymphs could be linked to changes in the host's digestive system or immune responses during this developmental stage. Additionally, interactions between the host and specific bacterial species may lead to the establishment of stage-specific microbial niches. Ecological mechanisms, such as competition between bacterial species, environmental exposure, and host-microbe interactions, also play a role in shaping the microbial niches. Bacteria that are better adapted to the host's changing physiological and environmental conditions may outcompete others, leading to shifts in the microbial community structure at different developmental stages. Overall, the stage-specific microbial niches in earwig development likely arise from a complex interplay of host physiology, environmental factors, and microbial interactions, highlighting the dynamic nature of the host-microbiome relationship during development.

What are the potential fitness consequences, if any, of the microbiome changes observed in earwig offspring development, and how do they relate to the previously reported phenotypic effects of maternal care?

The microbiome changes observed in earwig offspring development could have several potential fitness consequences for the host. The diversity and composition of the microbiome play a crucial role in various physiological processes, including digestion, immunity, and metabolism. Therefore, alterations in the microbiome composition at different developmental stages could impact the host's ability to extract nutrients from the diet, resist pathogens, and regulate metabolic functions. For example, the decrease in microbial diversity observed in the 2nd instar nymphs may affect the host's digestive efficiency and nutrient uptake, potentially influencing growth and development. Changes in the microbiome structure could also impact the host's immune response, making them more susceptible to infections or diseases. These fitness consequences of microbiome changes are closely related to the phenotypic effects of maternal care reported in earwigs. Maternal care, such as grooming and food provisioning, can influence the transmission of beneficial microbes to offspring, shaping their microbiome composition. The presence of specific bacteria acquired through maternal care may enhance the host's ability to digest food, resist pathogens, and regulate physiological processes, ultimately contributing to improved fitness and survival. Therefore, the microbiome changes observed in earwig offspring development, influenced by maternal care, can have significant implications for the host's fitness and overall health, highlighting the importance of the host-microbiome interactions in shaping phenotypic traits and survival outcomes.

Could the microbiome-mediated effects of maternal care on offspring extend beyond development and into adulthood in other insect species where maternal care is more essential for offspring survival?

The microbiome-mediated effects of maternal care on offspring can indeed extend beyond development and into adulthood in insect species where maternal care plays a crucial role in offspring survival. Maternal transmission of beneficial microbes to offspring can have long-lasting effects on the host's health, immunity, and overall fitness throughout their lifespan. In insect species where maternal care is essential for offspring survival, such as provisioning of food, protection from predators, and grooming, the transmission of specific microbes from the mother to the offspring can have profound effects on the host's microbiome composition and function. These transmitted microbes can provide important benefits to the offspring, such as improved digestion, pathogen resistance, and overall health. Furthermore, the microbiome acquired through maternal care during early development can persist into adulthood and continue to influence the host's physiology and behavior. Studies have shown that the microbiome composition established during early life can have long-term effects on the host's immune system, metabolism, and reproductive success. Therefore, in insect species where maternal care is essential for offspring survival, the microbiome-mediated effects of maternal care can extend beyond development and into adulthood, shaping the host's health and fitness throughout their lifespan. This highlights the importance of maternal care in establishing and maintaining a healthy microbiome in insect offspring.
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