Animal evolution at the ocean’s water-air interface

Innovation is a key to evolutionary success and entrance into novel ecosystems. Species that float freely at the ocean’s surface, termed obligate neuston (also called pleuston, here referred to simply as neuston), include highly specialized taxa from distinct evolutionary lineages that evolved floating morphologies. In 1958, Soviet scientist, A.I. Savilov, stated that floating animal species are derived from benthic ancestors, rather than species from the adjacent pelagic zone, and that floating morphologies are homologous to benthic attachment structures. To test Savilov’s hypothesis, we constructed molecular phylogenies and ancestral states for all major floating groups for which molecular data were available. Our results reveal that four of the five clades examined arose directly from a substrate-attached ancestor, although that substrate was not necessarily the benthos, as Savilov stated, and instead included epibiotic and rafting ancestors. Despite their diverse evolutionary origins, floating animals use gas-trapping mechanisms to remain at the surface, and many of these gas-trapping structures appear to be homologous to substrate attachment structures. We also reconstruct the trophic habits of floating mollusks and their sister species, revealing that prey preference remains conserved upon entering the ocean’s surface ecosystem. Colonization of the ocean’s surface seems to have occurred through successive evolutionary steps from the seafloor. Our results suggest that these steps often included transitions through epibiotic (where species attach to other living organisms) or rafting (where species attach to floating debris) habits. The water-air interface, despite its unique properties, may, in some ways, be just another substrate