Transient increase in abundance of B lineage but not myeloid-lineage cells in anterior kidney of sockeye salmon during return migration to the natal grounds

Abstract

As anadromous fish, sockeye salmon undergo complex endocrine changes when they return to their natal grounds to spawn. This is correlated with major immunological changes that will affect their response to pathogens. In spite of these challenges, salmon need to maintain sufficiently robust immunity to survive until spawning is complete, but the nature of immune adaptations during the spawning stage remains poorly understood. Our central question is to determine if sockeye salmon stimulate their immune system during the return migration and if so, whether this is a protective response. To begin answering this question, here we characterized the nature and timing of potential changes in anterior kidney immune fingerprints between salmon collected from seven different sites along the Kenai river, including the mouth of the river and two spawning sites. Our results revealed significant changes in abundance of B lineage, but not myeloid lineage cells during the spawning journey. This included early, transient and significant increases in abundance of both IgM+ and IgT+ B cells soon after fish entered the river, followed by a transient, significant increase in abundance of IgM++ secreting cells in fish caught mid-river, and ending with a return to base levels of both cell populations in fish caught at spawning sites. Further, males appeared to have higher immune activation than females, as reflected by higher abundance of IgM++ secreting cells, higher spleen index, and higher titers of serum IgM. Although roles for these newly generated IgM++ secreting cells remain unclear at this time, the data complement our previous work which supported roles for long-lived plasma cells to protect returning salmon from pathogens at their natal grounds. We conclude that sockeye salmon are capable of inducing B cell responses during their spawning journey, with males having stronger responses compared to females. B cell activation during the return journey may provide returning adults with additional protection against pathogens not encountered as juveniles.