Immune transcriptomic profile in adult female pigs: dominance status has more influence than environmental enrichment

Background: Assessing farm animals' welfare is crucial, yet practical physiological tools are still lacking. In this study, we tested whether the peripheral blood mononuclear cell (PBMC) transcriptome shows variations in association with sows' welfare. To do this, we compared animals whose welfare states were assumed to differ due to their lives in more or less enriched environments and to their different dominance statuses. Sows were housed in a conventional (C, n = 36) or enriched (E, n = 35) environments from gestation day 0 (G0) until three weeks before farrowing (G105), after which they were transferred to individual farrowing crates. From G99 to G103, behavioral analyses were conducted, and sows' dominance status was evaluated. A subset of 28 multiparous sows (C, n = 14 and E, n = 14) was selected for the collection of saliva on G35 and G98 and hair on G98 for cortisol measurement, and of blood samples for PBMC transcriptome analysis on G98 and on lactation day 12 (L12).

Results: Both environmental enrichment (EE) and dominance status influenced cortisol and variables related to social and exploratory behavior, indicating an influence on sows' welfare. In the transcriptomic analysis, among the 12,260 genes submitted to differential analysis on G98, EE impacted 31 genes, while dominance status impacted 449 genes. Compared with subordinate sows (SUB), dominant (DOM) sows exhibited an upregulation of genes related to inflammatory process and plasma cell function, and downregulation of genes related to B-cell activation. In groups of sows, dominance status is partly related to sows' parity; therefore, we compared the effect of dominance with that of parity. Some common genes emerged when comparing high-parity (HP) vs. low-parity (LP) sows (542 differentially expressed genes (DEGs), including 180 in common with dominance-related genes), indicating that some effects of dominance on the transcriptome during gestation were in fact more due to age or reproductive cycles than to dominance itself. EE and dominance effects appeared relatively short-term, as DEG numbers decreased on L12 (four DEGs for E vs. C, 25 for DOM vs. SUB).

Conclusions: Dominance status exerted a more pronounced influence on sows' PBMC transcriptome than did environmental enrichment. In particular, dominance status modulated genes associated with B cells and plasma cell functions. Some of the genes identified in this study could be tested in the future as potential molecular markers of well-being.