Out of thin air, nature matters in selection!

A few weeks ago I watched a Bloggingheads diavlog between Carl Zimmer and Peter Ward, the latter a paleontologist at the University of Washington. I had been developing a deeper interest in the broader patterns of evolution across Deep Time, so I really enjoyed the discussion and learned quite a bit. When I saw Ward's book Out of Thin Air: Dinosaurs, Birds, and Earth's Ancient Atmosphere at the library, I had to pick it up! Overall it's a quick and breezy read; but nevertheless he manages to pack a pretty big scientific punch from what I can tell, the occasional interruptions of the narrative form with a restatement of his points as formal hypotheses were extremely well done. The structure managed to interject the author's clear intent into what might otherwise have been an enjoyable but somewhat shallow narrative.¹

At this point, I must admit that I approached this book from a peculiar angle. On the one hand I don't really bring a "thick" background of knowledge to the table when I read paleontology; like many scientifically inclined individuals my love of evolutionary biology derives from a fixation upon dinosaurs as a child, but I don't think I've read any dino-books since Robert Bakker's Dinosaur Heresies. In other words, my knowledge of natural history isn't trivial, but I am not immersed in the primary literature to the same extent as I am in topics related to evolutionary genetics. I certainly can't tell a femur from a tiba. To some extent I approach Out of Thin Air as a wide-eyed lay person; on the other hand I'm also someone with a deep appreciation and preoccupation with microevolutionary processes and dynamics and can't but help wonder how paleontology fits into it all. After all, I do subscribe to a general scale independence of evolutionary process.

Peter Ward's story is a big one. As a paleontologist he thinks in terms of geological time scale; a grounding physical science means that he is always aware of non-biological parameters. As one who generally focuses on temporal scopes of more modest dimension I have a tendency to ignore macro level dynamics which are the bread & butter of paleontology. Rather, I tend to focus on Charles Darwin's original idea that selection operates upon normal variation, the concept which resulted in the idea of evolution as phyletic gradualism. As a paleontologist Ward generally does not speak of intrapopulation level differences or competition, rather, his canvass encompasses whole taxa. Enormous variegated branches of the tree of life fly by with each paragraph. Instead of revisions on the margins, Out of Thin Air chronicles the pruning of entire phyla due to whims of nature. If one thinks of selection as operating so that it results in differential affects upon various individuals or taxa, this story is one of how some lineages may possibly be phylogenetically constrained so as to be inevitably hurtled toward extinction, or conversely predisposed toward radiation due to nature's caprice. This does not negate parameter of within population variation, but that is contingent upon exogenous environmental disruptions. The hypothesis at the center of Out of Thin Air is simple: variation in the atmospheric oxygen level have been responsible for a great deal of the details of natural history which we see within the extant fossil record. More specifically, Peter Ward contends that low oxygen levels tends to reduce species richness (through extinction) as well as spur elevated rates of body plan innovation (as the remaining species rapidly shift toward new adaptive peaks).

Today about 21% of our atmosphere consists of oxygen. Ward suggests that inferences from various geochemical data sets imply that over the past billion years (since the rise of photosynthetic organisms) the proportion of oxygen has varied from as low as ~10% to as high as ~30%. In other words, our environment has shifted from a hypo to hyper oxygenated world many times over the course of our planet's history. One does not need to have a deep scientific education to know that oxygen is important. It is one of the basic ingredients necessary for the biochemical reactions which generate energy and synthesize the raw materials which are essential for life.

It takes no great powers of perception to realize how this might shape the course of evolution. For example, Ward has argued that the reduction in oxygen levels 400 million years ago resulted in the retreat of animals from land, only to reappear when the levels increased once again. An "oxygen-centric" viewpoint does seem to make many paleontological phenomena more intelligible. Why were insects once so large compared to today? Ward points out that the respiratory system of insects is inefficient and does not scale well; but with higher oxygen levels the outer limits of insectoid architecture are pushed up. Some of the inferences might also surprise you. He suggests that lower oxygen levels during the Triassic might have worked against warm-blooded metabolisms. An analogy to higher altitude is widely used. Consider that during the Triassic the levels of oxygen at sea level were equivalent to what we might experience at 5,000 feet! Today no birds can breed above 18,000 feet, and that is because their eggs can not obtain enough oxygen from the air above that point. Similarly, the levels of oxygen required for mammalian fetuses is higher than for their mothers because of the mixing of arterial and venous blood. During periods of low atmospheric oxygen one might model the earth's surface as dissected by nearly uninhabitable massifs. This would obviously resulted in fragmentation of breeding populations of species which up to that point might have been united by anagenetic processes.

Out of Thin Air has many fascinating details and case studies. The first two chapters lay out the general physical and biological parameters, but most of the text is devoted to interpreting natural history through the lens of variation in oxygen levels. But I believe that the most interesting assertion that the author makes is that the origin and rise to dominance of the dinosaur lineage was caused by low oxygen levels. Even I remember from schoolboy readings that one of the features of dinosaurs which differentiated them from modern reptiles (and to a lesser extent their mammal-like reptile competition) was that their stance was upright as opposed to sprawled. In other words, their legs were situated underneath the carriage of their body as opposed to the sides. The biomechanical implications are clear for locomotive efficiency, but another point that Ward makes is that the early dinosaurs also tended to be bipedal. As bipedal mammals we might not comprehend how strange this stance is, but in the dinosaur lineage it was very common, and early on it was one of the characteristics of the clade (even the ancestors crocodiles were bipedal!). The author argues that the upright stance and bipedalism were critical because quadrupedal sprawling reptiles can not breath when they run. You read that right! It helps to know a little anatomy I suppose; it was certainly something that was a surprise to me. Obviously this is a constraint upon modern day reptiles, which is apparently one reason why they are ambush & burst predators, they simply can't take in oxygen while they're on the chase and so that serves as a limit in terms of their energy budget. Imagine a world were oxygen levels were much lower! Yes, Ward argues that the dinosaur body plan was an innovative solution to the dilemma of low levels of oxygen, a way for the early carnivorous dinosaurs to be the tireless wolves of their world.

But that wasn't the only trick up their sleeve. The next piece of the story requires some exposition about bird anatomy and physiology. Ward explains that birds are more efficient respirators than mammals. The likely reason is that they have air sacs which super-charge the flow of oxygen through their system as a one way pump. Details aren't necessary, what is important is that birds get more bang for their buck than a typical mammal all things controlled. Obviously the next step is to wonder about the clade within which birds are nested: the dinosaurs. Did they have air sacs? This is a controversial topic. Many dinosaurs have bone structures which do not resemble reptiles, but do resemble birds. Some scientists argue they were not air sacs, while others do; the author of Out of Thin Air comes down strongly in the latter camp. In fact, he comes close to declaring the former deluded after the compelling research which he recounts in loving detail that supports the contention that dinosaurs, especially the basal and Saurischia lines, did have air sacs. The inference from this is that dinosaurs were more efficient extractors of oxygen from the atmosphere. Ward also notes that the ornithischian lineage of dinosaurs, which may not have had air sacs (the anatomical evidence is much weaker), diversified only after oxygen levels had increased. Finally, there is also the suggestion that dinosaurs may have been homeothermic due to their large size, that is, their body temperatures were stable simply due to the fact that their low surface area to volume ratio meant that there would be very little relative radiation. Remember that in low oxygen environments endothermic warm-blooded organisms are at a disadvantage because they have higher needs in terms of raw materials for their constantly churning metabolic processes. In sum, the rise of the dinosaurs may be attributable to three traits which were perfectly adapted toward a low oxygen environment: more efficient locomotion (upright stance), more efficient extraction of oxygen (they could breathe when they ran because of their stance and bipedalism, as well as air sacs) and a possible shift away from endothermy (less need for oxygen).

The argument presented above is a tall tale; one I find in compelling, but then again I don't know the paleontology in great detail. The overall thesis is bold, and again I am drawn to it. Nevertheless, there is an unfortunate air to it all of finding a nail because one has a hammer. Paleontology is a historic science which rests upon vectors converging upon probable inferences and likely hypotheses, but we can't do macroevolutionary experiments. To be fair, Out of Thin Air is laced with the sort of developmental and physiological data from extant lineages which paleontologists rely on to fill in the gaps in lieu of time machines. But big bold hypotheses need to settle in and be validated by other researchers; the method of calibrating oxygen levels which the author depends upon to make his case seems to be relatively new, so we'll see if the numbers hold steady as more data comes in. Additionally, as I allude to above Ward also comes down strongly on particular sides in scientific controversies, if by chance the wind blows in contrary directions then some of the vectors which point to his hypothesis must be removed from the equation, and his argument becomes proportionately weaker. But in the end I am blown away by the interdisciplinary scope of the argument marshaled in Out of Thin Air, and I'm left to mull over the implications of the sweeping action of geology across the tree of life.

1 - This is not to say that the content would have been shallow, but a looser exposition in a classic narrative essay format does not, I think, foster a systematic understanding of the broader scientific issues. Rather, it highlights a sequence of facts as opposed to their contingent relations.