One-billion-year-old epibionts highlight symbiotic ecological interactions in early eukaryote evolution

Abstract

Symbiosis represents close and long-term interactions—which can be mutualistic, commensalistic, or parasitic—between two different taxa. Symbiotic associations play a pivotal role in accelerating eukaryotic evolution and diversification. However, the Proterozoic fossil record of symbiosis is rarely documented despite the abundance of Proterozoic eukaryotes and their accelerated diversification in the Neoproterozoic. The scarcity of direct fossil evidence for symbiosis impedes our understanding of the ecological impact of symbiosis on the evolution and diversification of early eukaryotes. Here we report abundant dark discoidal, semicircular, or ovate structures preserved on the early Neoproterozoic eukaryotic fossils Tawuia and Sinosabellidites from North China. Our systematic analyses show that these dark structures were originally spheroidal organisms, which are interpreted as eukaryotic epibionts that lived on the surface of and may have benefited from an association with their Tawuia and Sinosabellidites hosts, representing a case of ectosymbiotic commensalism. The new material represents some of the earliest known fossil evidence of eukaryotic symbiosis which, together with other contemporaneous evolutionary innovations, may have contributed to the ecological expansion of eukaryotes in the Neoproterozoic. This study opens the door to new investigation of ecological interactions in Proterozoic marine ecosystems.