Chronic heavy metal exposure drives mitochondrial remodeling and metabolic reprogramming to enhance sperm velocity in wild tree sparrows.

Environmental pollution is widely assumed to impair reproductive performance, yet whether organisms can sustain reproductive function under chronic stress remains poorly understood. Here, using natural populations of tree sparrows from a heavy metal-contaminated site and a reference site, we reveal a paradoxical increase in sperm velocity despite clear physiological costs. Males from the polluted population exhibited reduced body condition and elevated cadmium and lead accumulation in reproductive tissues, but their sperm velocity parameters were significantly enhanced. Mechanistically, sperm from exposed birds showed coordinated mitochondrial optimization, including elevated mitochondrial membrane potential, enhanced complex I activity, and higher ATP content. In the testis, genes associated with mitochondrial biogenesis (TFAM) and mitophagy (BNIP3) were upregulated, indicating enhanced mitochondrial quality control during spermatogenesis. Functional inhibition using the oxidative phosphorylation uncoupler carbonyl cyanide 4-(trifluoromethoxy) phenylhydrazone (FCCP) confirmed that elevated sperm velocity depends on mitochondrial oxidative phosphorylation (OXPHOS). Integrated proteomic and metabolomic analyses further revealed a systemic metabolic reprogramming from glycolysis toward OXPHOS, characterized by upregulation of OXPHOS-related proteins and suppression of glycolytic pathways. Together, our findings demonstrate that chronic heavy metal stress can enhance sperm performance through mitochondrial and metabolic remodeling, revealing a key mechanism by which avian reproductive behavior responds to long-term environmental stress.