Rise in atmospheric oxygen and patterns of mammalian evolution

In Science this week (9/30/05), there was an article by Paul Falkowski and colleagues, including Michael Novacek of the American Museum, which documented the rise in atmospheric oxygen over the past 205 million years and suggested that this rise may have allowed the evolution of large placental mammals.

The introduction is more informative than the abstract:

It has long been recognized that atmospheric oxygen levels play a key role in the evolution of metazoans (1), yet our understanding of precisely how oxygen concentrations influence specific animal evolutionary traits is limited. Although many metazoans are capable of acclimating to hypoxic conditions by lowering metabolic rates and/or operating the tricarboxylic acid cycle partially in reverse (2), these physiological modifications cannot be sustained indefinitely. Controls of atmospheric oxygen by the carbon and sulfur cycles (3, 4) have led to models based on analyses of the isotopic composition of carbonates and sulfur (3, 5) or on the relative abundance of different rock types (6), which suggest that atmospheric oxygen concentrations varied throughout the Phanerozoic, with a maximum 300 million years ago (Ma), a minimum 200 Ma, and an overall rise from 200 Ma to the present (5, 6). However, the range and underlying causes of these variations in oxygen are not well understood. Here, we provide an isotopic record for organic carbon, which we analyzed in conjunction with isotopic records for carbonates and sulfates for the past 205 million years (My). Our analysis suggests that ambient oxygen levels approximately doubled from 10% by volume (76 Torr) to 21% (160 Torr) over this period. Concurrent examination of the fossil record suggests that this change in oxygen tension was potentially a key factor leading to the evolution of large placental mammals in the Cenozoic (Falkowski et al. 2005:2202).

The main idea is that an increase in oxygen availability was essential to the evolution of large mammals, because the placental environment is hypoxic compared to the ambient air, placing limits on the metabolism and growth of developing fetuses, and because the density of capillaries scales with negative allometry with body size, so that larger animals benefit from higher atmospheric oxygen levels.

The authors don't attempt to correlate the dates with the evolutionary history of the globin genes. This seems to me to be an important comparison, since if it is true that the placental environment is more similar to the Jurassic atmospheric conditions, then the fetal hemoglobin molecule might be expected to be a closer functional analogue to the common ancestor of adult mammalian hemoglobin than are the current adult forms. The globin genes have undergone multiple duplications over vertebrate history, some of which have resulted in functionally different genes (the subunits of fetal hemoglobin included). They ought to fall into this story somehow.

Most of the increase in atmospheric oxygen is pre-primate, so it isn't exactly relevant to paleoanthropology. But there was an apparently rapid increase across the Eocene from around 18 percent to around 23 percent. This is possibly very relevant to primate evolution, because this was a time of radiation of today's primate lineages, including the living branches of prosimians (lemurs, lorises, and tarsiers) and the first anthropoids.

The paper relates the increase in oxygen to increases in body size, noting that the average mammalian body mass grew across this time period. But for primates, there was no great increase in body mass (although some lineages did ultimately include larger representatives), because arboreal adaptation ultimately imposes limits on how big primates are.

What may have changed in primates is the relative size of the brain. Primates today have larger brains for their size than most other mammalian lineages. This increase in relative brain size was not evident in the Paleocene relatives and ancestors of primates, such as the plesiadapids. Perhaps the Eocene increase in oxygen availability allowed the overall increase in metabolic rate that a larger brain would require in primates.

Of course, that leaves unanswered whether the subsequent decrease in atmospheric oxygen to today's 21 percent had any effect on our evolution. This decrease dominated the Miocene, which was not exactly a time of brain size or body size reduction. So maybe the whole thing is a red herring.

References:

Falkowski PG et al. 2005. The Rise of Oxygen over the Past 205 Million Years and the Evolution of Large Placental Mammals. Science 309:2202-2204. Full text (subscription)