Vertical transmission of sponge microbiota is weak and inconsistent

Classic evolutionary theory predicts that if beneficial microbial symbionts improve host fitness, they should be faithfully transmitted to offspring. More recently, the hologenome theory of evolution predicts resemblance between parent and offspring microbiomes, and high partner fidelity between host species and their vertically transmitted microbes. Here, we test these ideas for the first time in multiple host species with highly diverse microbiota, leveraging known-parent offspring pairs sampled from eight species of wild marine sponges (Porifera). Contrary to the hypothesis that vertical transmission is an adaptation that allows sponges to faithfully transmit intact microbial consortia to offspring, we found that vertical transmission is weak and incomplete. Further, we found no evidence that siblings consistently receive the same microbes from their parents, nor that vertically transmitted microbes show high degrees of host species fidelity. Finally, while we show that monophyletic groups of microbes with known symbiotic features and capabilities are more common among vertically transmitted microbes than in the consortia of horizontally acquired microbes, the signature of this vertical transmission is only detectable on the level of Porifera as a whole. Our study demonstrates that common predictions of vertical transmission that stem from species-poor systems are not necessarily true when scaling up to diverse and complex microbiomes.