From environmental perception to reproductive allocation: the microbiome-membrane-mitochondria axis in poultry.

Abstract

Reproductive performance has traditionally been interpreted through the physiology of reproductive organs, endocrine regulation, and genetics. Although these approaches have substantially advanced poultry production, they do not fully explain why reproduction consistently reflects the overall physiological condition of the organism. This review proposes an integrative conceptual framework in which reproductive success emerges from the coordinated activity of the entire host-microbiome ecosystem, not from the reproductive system alone. We examine current evidence supporting the concept that the intestinal microbiome functions as a major ecological and metabolic partner that can contribute to whole-organism homeostasis through effects on intestinal barrier integrity, immunometabolism, endocrine signaling, microbial metabolite production, and mitochondrial bioenergetics. In this model, microbially derived signals, including short-chain fatty acids, bile acid metabolites, tryptophan derivatives, polyamines, vitamins, extracellular vesicles, and microbial-associated molecular patterns, form an extensive communication network linking the intestinal ecosystem with distant tissues. Central to this model is the recognition of mitochondria as major bioenergetic and signaling integrators within the host-microbiome system. Beyond ATP production, mitochondria participate in redox homeostasis, immune activation, metabolic adaptation, endocrine responses, steroidogenesis, and cellular quality control, thereby integrating microbial, nutritional, immune, and environmental signals into cellular responses. Diverse stressors, including dysbiosis, heat stress, pathogens, mycotoxins, oxidative stress, nutritional imbalance, and chronic inflammation, converge upon mitochondrial and immunometabolic pathways that can alter systemic resource allocation and reproductive resilience. Reproductive performance is therefore considered here as an emergent, condition-dependent physiological outcome rather than as a hierarchically superior biological function. The intestinal microbiome does not directly regulate reproduction; instead, it contributes to the systemic conditions that can support reproductive investment, whereas microbial communities within the reproductive tract may interact more directly with reproductive tissues and gametes. The revised framework further emphasizes reciprocal communication: endocrine and reproductive states can reshape metabolism, immunity, intestinal physiology, mitochondrial function, and microbial ecology. Finally, maternal programming and optimization of host-microbiome interactions are considered as potential strategies for strengthening reproductive resilience across generations.