Target-capture and 16S amplicon sequences of Red Sea Haplosclerida

Understanding how microbiomes evolve in concert with their hosts is crucial for understanding biological individuality and the evolutionary dynamics of complex holobionts. Phylosymbiosis describes a pattern in which microbial community relationships parallel host phylogeny. Although often interpreted as evidence for host–microbiome co-diversification, phylosymbiosis can also arise from ecological filtering through phylogenetically conserved host traits. Here, we test these alternative hypotheses in marine sponges (Order Haplosclerida) from the Red Sea. We inferred a robust host phylogeny using 1,153 target-captured genome-wide loci from 144 specimens and characterised their prokaryotic microbiomes via V4 16S rRNA gene amplicon sequencing. Host clade identity explained roughly 50% of microbial community variation (PERMANOVA R² = 0.498, P = 0.001), demonstrating host-specific microbiome structuring. However, topological analyses revealed high incongruence between host phylogeny and microbial dendrograms (nRF > 0.89), and phylogenetic distance was only weakly correlated with microbiome dissimilarity (Mantel r = 0.177). Partial Mantel tests confirmed geography did not affect this signal. Trait-based analyses revealed that high versus low microbial abundance (HMA–LMA) classification was a better predictor of microbiome composition than phylogenetic distance (Mantel r = 0.230 vs. r = 0.177, respectively). Furthermore, phylogenetically distant clades with convergent HMA morphology harboured similar microbiome profiles but had unique ASV compositions, with between-trait dissimilarity exceeding within-trait dissimilarity. These findings show that sponge–microbiome associations are more likely to occur due to ecological filtering through convergent functional traits than host–microbe co-diversification, suggesting that sponge-holobionts may be better understood as ecological consortia than as co-evolved units.