Environmental and genetic drivers differentially shaped resident and transient gut microbiota during the Macaronesian chaffinch radiation

Abstract

Disentangling whether gut microbiome diversification reflects host evolutionary history or spatial processes remains challenging because these factors are often confounded. The Macaronesian chaffinch (Fringilla) radiation provides a replicated natural experiment to separate these effects. Using long-read 16S sequencing, diet metabarcoding, and whole-genome data, we evaluated competing models of community assembly, testing host-mediated dispersal versus neutral assembly, and environmental filtering versus host control. We show that microbiome alpha diversity across host species was largely shaped by island size and isolation, aligning with Island Biogeography Theory, rather than host colonisation history. This indicates that microbial dispersal occurs independently of their hosts. Moreover, spatial and host factors influenced different aspects of the microbiome: geography and diet primarily predicted which taxa were present, whereas host genetic relatedness and heterozygosity were associated with the abundance of established residents. Notably, we show that inbreeding compromises a host's ability to regulate microbial abundance, leading to highly variable microbiomes. While we detected phylosymbiosis (closely related hosts harboring similar microbiomes), we found no evidence of co-diversification between birds and microbes. Instead, associations likely arise from convergent ecological filtering, where shared host traits filter similar bacteria from the local environment. Together, our results show that avian microbiomes are shaped by distinct spatial and host-mediated processes, and that separating microbial presence from abundance is important for understanding the mechanisms driving microbiome assembly.