Phylogeography and ecological niche shape the cichlid fish gut microbiota in Central American and African lakes

Abstract

Cichlid fishes, with their repeated colonization of lakes and subsequent radiations at different scales of phylogenetic and ecological diversification, offer an excellent model system to understand the factors shaping the host-gut microbiota association in nature. Here, we characterized the gut microbiota of the Amphilophus species complex from Central America (known as the Midas cichlid complex), encompassing 158 wild specimens (13 species) collected from seven Nicaraguan lakes, and combined these data with previously published data from two African lakes (spanning 29 species). Our aim was to comprehensively explore trends in microbiota variation and persistence along the large spatial and temporal scales of cichlid diversification (from the oldest radiation in L. Tanganyika, 9-12 My old, to young ones in Nicaraguan crater lakes, <0.5 My old), in allopatry and sympatry (within and across lakes), and across the range of dietary niches (from highly specialized to generalist feeders). Despite their extraordinary diversity, cichlids shared a remarkably conserved microbial taxonomic profile, which argues for a primary role of the host genetics in the assembly and maintenance of these microbial communities. Within this partly constrained microbiota profile, geographic isolation (continent and lake) represented the first level of discrimination. For the Midas cichlid, a partial congruency was found between host microbiota and genetic distances, suggesting that microbial communities have partly diversified along their cichlid phylogeographic history of crater lake colonization. In sympatry (within lakes), the young and poorly ecologically diversified cichlid assemblages of Central American lakes display largely unresolved gut microbiotas (in terms of both alpha and beta diversities), whereas the phylogenetically and ecologically diverse species found in African lakes showed greater microbial interspecific diversity. This pattern largely points to the level of habitat segregation, trophic niche overlap, and reproductive barriers as major modulators of the gut microbiota connectivity among sympatric species.