High-temperature exposure induces sexually dimorphic immune and metabolic responses in the spleen of Micropterus salmoides

Experimental studies have found substantial biological differences between male and female largemouth bass (Micropterus salmoides) under high-temperature conditions. To gain an in-depth understanding of these differences, this study compared the spleen transcriptomes of male and female under high-temperature and ambient-temperature conditions. The results indicated that the high-temperature group (C32) showed significant differences in both metabolism- and immunity-associated terms compared with the ambient-temperature group (C22). Differential analysis was subsequently performed on male and female samples under identical temperature conditions. KEGG enrichment analysis revealed that high-temperature exposure induced stronger immune and inflammatory responses between males and females, including enrichment in males in pathways such as the intestinal immune network for IgA production and autophagy. These responses were associated with growth inhibition and potential sexual dimorphism in immune defense. Differential analyses were conducted separately for male and female samples. The DEGs differed significantly between males (C22-M vs. C32-M) and females (C22-F vs. C32-F), primarily for DEGs associated with organic nutrient metabolism and apoptosis. KEGG enrichment analysis showed that only 16.7 % of pathways were jointly enriched. In males, over 70 % of enriched DEGs were associated with immune- and inflammatory-related pathways. Sankey diagrams analysis further linked these to multiple immune and metabolic-related pathways. We deduced that high-temperature affects multiple metabolic and immune pathways, thereby inducing autophagy and intestinal immune responses. Under high-temperature conditions, markedly different response strategies were adopted by males and females, with males showing stronger immune and inflammatory responses, with multiple immune pathways affected via immune regulatory networks. These findings suggest that males may possess a greater adaptive advantage under high-temperature stress, especially in metabolism or energy supply. Under high-temperatures, estrogenic pathway may be activated in females, thereby influencing certain immune and metabolic pathways and in turn affecting the adaptability to high-temperature. These findings offer new insights for future mono-sex breeding strategies. • High temperature altered multiple metabolic and immune pathways in largemouth bass, triggering autophagy and intestinal immune responses. • Under high-temperature conditions, male and female largemouth bass exhibited distinct response strategies.Males exhibited stronger immune and inflammatory responses through multiple regulatory pathways, suggesting a higher adaptive advantage, particularly in metabolism and energy supply. • Under high temperatures, activation of the estrogenic pathway in females may modulate immune and metabolic processes, thereby affecting their thermal adaptability.