Extant diversity, biogeography, and evolutionary history of Radiolaria.

Abstract

Since Ernst Haeckel and the Challenger expedition (1872-1876), Radiolaria have been known as ubiquitous and abundant star-shaped oceanic plankton. Their exquisite biomineralized skeletons left an extensive fossil record extremely valuable for biostratigraphic and paleo-environmental research. In contemporary oceans, there is growing evidence that Radiolaria are significant contributors to marine food webs and global biogeochemical cycles. Here we provide a comprehensive morpho-molecular framework to assess the extant diversity, biogeography, and evolutionary history of Radiolaria. Our analyses reveal that half of radiolarian diversity is morphologically undescribed, with a large part forming three hyper-diverse environmental clades, named Rad-A, Rad-B, and Rad-C. We suggest that most of this undescribed diversity comprises skeleton-less life forms or endosymbionts, explaining their elusive, yet abundant, nature. Phylogenetic analyses highlight the need for a major revision of high-level Radiolaria taxonomy, including placement of Collodaria within the order Nassellaria. Global metabarcoding surveys show that Radiolaria contributes more than 12% to the total eukaryotic community, displaying distinct biogeographic patterns with the skeleton-less lineages at depth and photosymbiont-bearing lineages in the surface. Fossil calibration of a molecular clock revealed the first appearance of Radiolaria ∼760 million years ago (mya), the development of the skeleton in the early Paleozoic (∼500 mya), and the onset of photosymbiotic relationships during the mid to late Mesozoic (∼140 mya), related to geological periods of oligotrophy and anoxia. The results presented here provide a robust framework for developing new perspectives on early eukaryotic diversification, paleo-environmental impacts on plankton evolution, and marine microbial ecology in rapidly evolving ecosystems.