Understanding the factors that sculpt fish gut microbiome is challenging, especially in natural populations characterized by high environmental and host genomic complexity. However, 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 propose that the recent diversification of several
Harpagifer
species across the Southern Ocean would allow 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
Operational Taxonomic Unit (OTU) detected in more than 80% of the individuals. Nearly half of the core microbiome taxa, including
Aliivibrio
, harbored co-phylogeny signal at microdiversity resolution with host phylogeny, indicating an intimate symbiotic relationship and a shared evolutionary history with
Harpagifer
. The clear phylosymbiosis and co-phylogeny signals underscore the relevance of the
Harpagifer
model in understanding the role of fish evolutionary history in shaping the gut microbiome assembly. We propose that the recent diversification of
Harpagifer
may have led to the diversification of
Aliivibrio
, exhibiting patterns that mirror the host phylogeny.
IMPORTANCE
Although challenging to detect in wild populations, phylogenetic congruence between marine fish and its microbiome is critical, as it highlights intimate associations between hosts and ecologically relevant microbial symbionts. Our study leverages a natural system of closely related fish species in the Southern Ocean to unveil new insights into the contribution of host evolutionary trajectory on gut microbiome assembly, an 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 some specific bacterial symbionts, mirroring the host diversification patterns. Given
Harpagifer
’s significance as a trophic resource in coastal areas and its vulnerability to climatic and anthropic pressures, understanding the potential evolutionary interdependence between the hosts and its microbiome provides valuable microbial candidates for future monitoring, as they may play a pivotal role in host species acclimatization to a rapidly changing environment.
