OUP accepted manuscript

Abstract

The transition from benthos to plankton requires multiple adaptations, yet so far it remains unclear how these are acquired in the course of the transition. To investigate this process, we analyzed the genetic diversity and distribution patterns of a group of foraminifera of the genus Bolivina with a tychopelagic mode of life (same species occurring both in benthos and plankton). We assembled a global sequence data set for this group from single-cell DNA extractions and occurrences in metabarcodes from pelagic environmental samples. The pelagic sequences all cluster within a single monophyletic clade within Bolivina. This clade harbors three distinct genetic lineages, which are associated with incipient morphological differentiation. All lineages occur in the plankton and benthos, but only one lineage exhibits no limit to offshore dispersal and has been shown to grow in the plankton. These observations indicate that the emergence of buoyancy regulation within the clade preceded the evolution of pelagic feeding and that the evolution of both traits was not channeled into a full transition into the plankton. We infer that in foraminifera, colonization of the planktonic niche may occur by sequential cooptation of independently acquired traits, with holoplanktonic species being recruited from tychopelagic ancestors