In 3.5 billion years, life on earth went from single microscopic cells to giant sequoias and blue whales. Scientists have now documented quantitatively that the increase in maximum size of organisms was not gradual, but happened in two distinct bursts "tied to the geological evolution of the planet," said Michal Kowalewski, professor of geosciences in Virginia Tech's College of Science.

Jonathan L. Payne, assistant professor of geological and environmental sciences at Stanford University; Jennifer A. Stempien, a recent Virginia Tech Ph.D. graduate now a research associate and science teaching fellow in geological sciences at the University of Colorado, Boulder; and Kowalewski are principal investigators on a project to document the increase of body size through time, funded by the National Evolutionary Synthesis Center. Ten additional researchers joined the study, including another Virginia Tech Ph.D. graduate Richard A. Krause Jr., now an Alexander von Humboldt fellow at the Museum für Naturkunde der Humboldt-Universität zu Berlin. Krause and Stempien also contributed body size data from their dissertation research at Virginia Tech.

The researchers report their findings in the week of Dec. 22, 2008, early on-line issue of the Proceedings of the National Academy of Science (PNAS) in the article, "Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity."*

"Searching for the largest organisms, we have reviewed the existing knowledge on the history of life on our planet from the oldest, and still controversial, fossil bacteria in 3.5-billion-year-old rocks to the largest animals and plants that live today," said Kowalewski. "The idea was to see if we could reconstruct how maximum size of organisms -- as measured in terms of biovolume -- increased."

Size is one of the fundamental characteristics of organisms and an important parameter for studying their ecology, evolution, and behavior. And yet, "before our study, the understanding of how maximum body size of organisms changed through time was primarily based on the seminal graph J.T. Bonner put together more than 40 years ago. Moreover, Bonner's curve was neither tied directly too empirical data nor presented in the rigorous taxonomic and temporal contexts," Kowalewski said.

"A common thought was that size will increase as animals and plants become more complex or change through time," said Stempien. "But, in fact, in most cases we did not know how the size changed over the entire time span of a group of organisms. Did it increase quickly after the first appearance and then taper off, or vice versa?"

"Our study had been thus motivated by a purely exploratory question regarding the first order pattern of changes in maximum size of organisms through time," Kowalewski said. "And we wanted to be able to answer the question in a rigorous, quantitative way."

But as they pulled together data from the fossil record, the scientists noted a remarkable pattern. "During out second working group meeting, we brought together the datasets collected by different working group members for individual groups of organisms," recalls Payne. "Once we brought these datasets together and plotted them against geological time, the basic pattern presented in the paper became very clear. For me, this is always the most exciting part of doing science, seeing your data for the first time, especially when the implications of your results are immediately apparent," said Payne.

"We were surprised to observe that nearly all of the increase in size occurred in two distinct time-intervals. And what is more, those intervals followed two major oxygenation events," Kowalewski said.

Payne said, "The realization that the episodes of size increase correlated with the oxygenation events was essentially immediate, in large part because the stepwise increase in maximum size looks so similar to our current understanding of the history of oxygen increase. The history of atmospheric oxygen concentrations has been an area of active research for several decades, and has experienced a great deal of recent attention and refinement. So, many of us were quite familiar with the oxygen curve from our reading of the geological literature and it was not hard to see that connection."

"What is really interesting is that each of these 'steps' correlate with a time in life’s history where there is innovation in the complexity of life, the first one being the eukaroytic cell and the second is the mulitcellularity of life," said Stempien, who was so impressed with the discovery that she included it in material about the fossil record for the introductory course she was teaching about geologic history.

Here is what the research team learned

During the first 1.5 billion years of the recorded history of life -- from about 3.5 billion to 2 billion years ago -- only bacteria-like fossils are found. Maximum size to which a bacteria cell can grow is severely limited. Consequently, the maximum size of life could not, and did not, change until the arrival of more complex organisms, which happened somewhere around 2 billion years ago.

But before that occurred something else happened that changed the planet. Way back in Archean times, more than 3 billion years ago, some primitive bacteria invented a metabolism that allowed them to use the sun's energy and carbon dioxide for nourishment; that is, they invented photosynthesis. These bacteria thrived in oceans devoid of oxygen. The atmosphere also lacked oxygen then. Like today's plants, the bacteria released oxygen back into the ocean and eventually into the atmosphere. The appearance of free oxygen, even as scarce as it was, had numerous consequences, including biological ones. Free oxygen made it possible for the evolution of a more complex cellular structure. Organisms developed a nucleus to contain their genetic material and incorporated other intra-cellular machinery.

The eukaryotic cell arrived on earth -- still a single cell organism, but able to develop much larger single-celled structures than any bacteria. In about two hundred million years, organisms went from cells not visible to the naked eye to macroscopic organisms, some about the size of a dime.

"In a way, thus, an increase in size and complexity was a consequence of geobiological interactions between life and earth. Life itself enabled life to become more complex," Kowalewski said.

Life languished as single cells for another billion years or so, until just before the Precambrian-Cambrian transition about 540 million years ago, when atmospheric oxygen again increased notably reaching as much as 10 percent of its current concentration.

Many scientists argue that the second increase in oxygen levels was a key prerequisite for evolution of yet more complex, multi-cellular (tissue-forming) life. Once this new level of complexity was achieved, body size limits imposed on single-celled organisms were removed and larger organisms started appearing in the fossil record. Relatively quickly in evolutionary terms – in about one hundred million years – largest life forms transitioned from dime-size, single-celled forms to giant marine animals such as Ordovician cephalopods, tens of feet in length. Dinosaurs, which came much later, come to mind, although not mentioned in the PNAS paper. "At the time they existed, they were indeed the largest life forms on land, but they were not much larger than giant cephalopods that existed in the oceans already in the Ordovician," said Kowalewski.

Incidentally, marine animals and vascular plants can attain even larger body size than the largest of dinosaurs. Today, such enormous organisms include blue whales and the giant sequoia, the latter being the largest life form known.

The scientists report in their PNAS article that through the 3.5 billion years of the documented history of life, maximum body size of organisms increased by 16 orders of magnitude. But most of that increase was realized in two relatively short intervals representing less than 20 percent of the total recorded history of life.

Stempien, one of the three principal investigators for the NESCent working group that authored the PNAS paper, noted that this effort is just a starting point for the team. "Each individual chose a topic for a manuscript, so there will be more exciting papers soon about size and evolutionary history, from origination to extinction and across different groups," she said.

*Authors of the PNAS article are: Payne, Alison G. Boyer, recent Ph.D. graduate, and James H. Brown, professor of biology, both at the University of New Mexico; Seth Finnegan, postdoctoral research fellow in the Department of Geological and Environmental Sciences, Stanford; Kowalewski; Krause ; S. Kathleen Lyons of the Smithsonian Museum of Natural History; Craig R. McClain of the Monterey Bay Aquarium Research Institute; Daniel W. McShea, associate professor of biology, Duke University; Philip M. Novack-Gottshall, assistant professor of geosciences, University of West Georgia; Felisa A. Smith, associate professor of biology, University of New Mexico; Stempien; and Steve C. Wang, associate professor of statistics, Swarthmore College.

Data used in the paper will be posted on the NEScent website, said Stempien, who is writing an introduction. Educational material is also being created by the center.

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