Unveiling the co-phylogeny signal between plunderfish Harpagifer spp. and their gut microbiomes across the Southern Ocean.

Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. Yet, closely related hosts are valuable models for deciphering the contribution of host evolutionary history to microbiome assembly, through the underscoring of phylosymbiosis and co-phylogeny patterns. Here, we hypothesized that the recent allopatric speciation of Harpagifer across the Southern Ocean (1.2-0.8 Myr) will promote the detection of robust phylogenetic congruence between the host and its microbiome. We characterized the gut mucosa microbiome of 77 individuals from four field-collected species of the plunderfish Harpagifer (Teleostei, Notothenioidei), distributed across three biogeographic regions of the Southern Ocean. We found that seawater physicochemical properties, host phylogeny and geography collectively explained 35% of the variation in bacterial community composition in Harpagifer gut mucosa. The core microbiome of Harpagifer spp. gut mucosa was characterized by a low diversity, mostly driven by selective processes, and dominated by a single Aliivibrio taxon detected in more than 80% of the individuals. Almost half of the core microbiome taxa, including Aliivibrio, harbored co-phylogeny signal at microdiversity resolution with Harpagifer phylogeny. This suggests an intimate symbiotic relationship and a shared evolutionary history with Harpagifer. The robust phylosymbiosis signal emphasizes the relevance of the Harpagifer model to understanding the contribution of fish evolutionary history to the gut microbiome assembly. We propose that the recent allopatric speciation of Harpagifer across the Southern Ocean may have generated the diversification of Aliivibrio into patterns recapitulating the host phylogeny. ImportanceAlthough challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it allows highlighting potential intimate associations between the hosts and ecologically relevant microbial symbionts. Through a natural system consisting of closely related fish species of the Southern Ocean, our study provides foundational information about the contribution of host evolutionary trajectory on gut microbiome assembly, that represents an important yet underappreciated driver of the global marine fish holobiont. Notably, we unveiled striking evidence of co-diversification between Harpagifer and its microbiome, demonstrating both phylosymbiosis of gut bacterial communities, and co-phylogeny of specific bacterial symbionts, in patterns that mirror the host diversification. Considering the increasing threats that fish species are facing in the Southern Ocean, understanding how the host evolutionary history could drive its microbial symbiont diversification represents a major challenge to better predict the consequences of environmental disturbances on microbiome and host fitness.