The origin and early evolution of complex organisms

Complex multicellular eukaryotic organisms (or complex organisms), including animals, land plants, fungi, and macroalgae, have dominated the Earth's biosphere since the Precambrian-Cambrian transition. Although fossil evidence and molecular clock estimates indicate that the early adaptive radiation of complex organisms occurred no later than the Ediacaran Period (similar to 635-539 Ma) or even the Cryogenian Period (similar to 720-635 Ma), the timing and dynamics of the evolutionary transitions from unicellular ancestors to different complex organisms remain largely elusive. This is mainly due to the deficiency of ancestral protists and transitional multicellular forms of complex organisms in the middle Proterozoic (similar to 1800-800 Ma), a period commonly known as the Boring Billion for a billion years of apparent environmental quiescence and evolutionary stasis in Earth history. However, recent paleontological and molecular clock advances have suggested that complex organisms have a deep root in the Boring Billion. In this review paper, we systematically scrutinized available fossil records, molecular clock estimates, and phylogenetic data regarding to the evolutionary mechanisms from unicellular ancestors to complex organisms. We propose that eukaryotic multicellularity may have originated through incomplete reproduction, where reproductive cells failed to liberate but retained in mother cells for ecological benefits. In addition, symbiosis, such as parasitism and mutualism, and horizontal gene transfer may have occurred multiple times among prokaryotes and protists during the Boring Billion, leading to the advent of differentiated cells, such as reproductive cells. Furthermore, the persistently stratified waters and stable environment during the Boring Billion have provided an unprecedented avenue for the trials of these evolutionary innovations. Although it is difficult to directly test all these hypotheses, integrated paleontological, molecular clock, and phylogenetic data suggest that single-celled ancestors may have diverged into major groups of complex organisms in the Boring Billion, setting up the basis for their adaptive radiations in the Ediacaran and ecological dominance at the Precambrian-Cambrian transition. Therefore, the Boring Billion is not boring at all in the perspective of early life evolution, it fostered the earliest divergence of complex life.

Automated summary

Complex multicellular eukaryotic organisms have dominated the Earth since the Precambrian-Cambrian transition, but the timing and dynamics of the evolutionary transitions from unicellular ancestors to complex organisms remain largely unclear. Recent advances in paleontology and molecular clock analysis suggest that complex organisms have deep roots in the "Boring Billion" period. This period, characterized by apparent environmental quiescence and evolutionary stasis, may have provided the conditions for the divergence of single-celled ancestors into major groups of complex organisms.