Gene expression provides mechanistic insights into a viral disease in seabirds

Wild animals are exposed to a variety of anthropogenic stressors that may result in loss of physiological homeostasis. One main consequence of this stress exposure is the increased vulnerability to pathogens. We addressed the hypothesis that energetic unbalance and alterations of immune effectors are key proximate mechanisms underlying this vulnerability, by quantifying the gene expression of magnificent frigatebird Fregata magnificens chicks affected by a highly lethal viral disease, whose appearance is favoured by food limitation in this species. A comparison between chicks with and without visible clinical signs of the disease using strict threshold of significance (p-value adjusted<0.05 and log2 fold-change above 1 or below -1) revealed 86 upregulated and 9 downregulated genes in sick chicks. The main differentially expressed genes with several fold difference between healthy and sick chicks were linked to biotic and external stimuli, inflammation and antifungal/antibacterial activity, signaling, and hydrolase activity. We further followed the chicks for several weeks, to identify chicks that became sick over the course of the study, to assess how the gene expression profile of chicks may predict the response to the disease. A comparison between chicks that remained always healthy and chicks that showed the appearance of visible clinical signs of the disease revealed 4 upregulated and 8 downregulated genes in chicks that became sick. The main differentially expressed genes with several fold difference between the two phenotypes were linked to cell development and differentiation, metabolism, and immunity. The results of our study suggest that alterations of the energetic machinery and of specific immune effectors (e.g. toll-like receptor, tetraspanins) underlie the impact of a viral disease on a free-living vertebrate. Our study contributes to a more comprehensive understanding of the host-pathogen interaction in wild animals and the physiological pathways involved, and provides insights for effective wildlife disease monitoring and management strategies.