Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity

Abstract

The maximum size of organisms has increased enormously since the initial appearance of life >3.5 billion years ago (Gya), but the pattern and timing of this size increase is poorly known. Consequently, controls underlying the size spectrum of the global biota have been difficult to evaluate. Our period-level compilation of the largest known fossil organisms demonstrates that maximum size increased by 16 orders of magnitude since life first appeared in the fossil record. The great majority of the increase is accounted for by 2 discrete steps of approximately equal magnitude: the first in the middle of the Paleoproterozoic Era (approximately 1.9 Gya) and the second during the late Neoproterozoic and early Paleozoic eras (0.6-0.45 Gya). Each size step required a major innovation in organismal complexity--first the eukaryotic cell and later eukaryotic multicellularity. These size steps coincide with, or slightly postdate, increases in the concentration of atmospheric oxygen, suggesting latent evolutionary potential was realized soon after environmental limitations were removed.

Fig. 1.

Sizes of the largest fossils through Earth history. Size maxima are illustrated separately for single-celled eukaryotes, animals, and vascular plants for the Ediacaran and Phanerozoic. The solid line denotes the trend in the overall maximum for all of life. Increases in the overall maximum occurred in discrete steps approximately corresponding to increases in atmospheric oxygen levels in the mid-Paleoproterozoic and Ediacaran–Cambrian–early Ordovician. Sizes of the largest fossil prokaryotes were not compiled past 1.9 Gya. Estimates of oxygen levels from Canfield (38) and Holland (37) are expressed in percentage of PAL. Phan., Phanerozoic; Pz., Paleozoic; Mz., Mesozoic; C, Cenozoic. Red triangles, prokaryotes; yellow circles, protists; blue squares, animals; green diamonds, vascular plants; gray square, Vendobiont (probable multicellular eukaryote).

Fig. 2.

Phanerozoic trends in size maxima for selected animal phyla and plant divisions. (A) Animal phyla. (B) Vascular plant divisions. Historical maxima differ by <2 orders of magnitude among phyla and divisions, although the timing of those historical maxima differs across clades. 1, Pteridophyta; 2, Lycopodiophyta; 3, Pinophyta; 4, Ginkgophyta; 5, Cycadophyta; 6, Magnoliophyta; 7, Equisetophyta; E, Ediacaran; Cm, Cambrian; O, Ordovician; S, Silurian; D, Devonian; C, Carboniferous; P, Permian; Tr, Triassic, J, Jurassic; K, Cretaceous; Pg, Paleogene; N, Neogene.