Loss of the benthic life stage in Medusozoa and colonization of the open ocean

Abstract

In marine environments, life cycle strategies strongly impact species dispersal and their ability to colonize new habitats. Pelagic medusozoans (jellyfish and siphonophores) exhibit various reproductive strategies, variations of meroplanktonic and holoplanktonic life cycles. In the ancestral meroplanktonic life cycle, a benthic polyp stage alternates with a pelagic medusa stage. During the course of evolution, some medusozoans lost their benthic stage, leading to a holoplanktonic life cycle. The ecological consequences of these losses have not been addressed at global scale. Here, integrating metabarcoding and environmental data from Tara Oceans into a phylogenetic framework, we show that each convergent transition toward a holoplanktonic life cycle is associated with a more offshore distribution compared to meroplanktonic medusozoans. Our analyses showed that holoplanktonic medusozoans are more globally distributed and relatively more abundant than meroplanktonic medusozoans, although they are less diversified and occupy a more peripheral position in a global plankton community interactome. This suggests that holoplanktonic medusozoans have acquired a greater tolerance to biotic and abiotic conditions. Overall, our results demonstrate the relationship between medusozoan life cycles, distribution, and biotic interactions, suggesting that the loss of the benthic stage promoted colonization of the open ocean.