1_MonitorLizard_AnatomyFlow

Image courtesy of Emma Schachner.

Gotta say, I did not see that coming.

Today sees the publication of a new paper by Emma Schachner and colleagues in Nature, documenting for the first time that unidirectional, flow-through breathing–previously only known in birds and crocodilians–happens in freakin’ monitor lizards. The image above, which is most of Figure 1, pretty much tells the tale.

Some quick background: until the early 1970s, no-one was quite sure how birds breathed. Everyone knew that birds breathe, and that the air sacs had something to do with it, and that the bird lungs are set up as a series of tubes instead of a big array of little sacs, like ours, but the airflow patterns had not been worked out. Then in a series of nifty experiments, Knut Schmidt-Nielsen and his students and colleagues showed that birds have unidirectional airflow through their lungs on both inspiration and expiration. Amazingly, there are no anatomical valves in the lungs or air sacs, and the complex flow patterns are all generated by aerodynamic valving. For loads more information on this, including some cool animations, please see this page (the diagram below is modified from versions on that page). For a short, eminently readable summary of how undirectional airflow in birds was first discovered (among many other fascinating things), I recommend Schmidt-Nielsen’s wonderful little book, How Animals Work.

Avian breathing

After 1972, biologists had almost four decades to get used to the idea that birds had this amazing miraculous lung thingy that was unique in the animal kingdom. Then in 2010, Colleen Farmer and Kent Sanders of the University of Utah blew our collective minds by demonstrating that alligators have unidirectional flow-through lungs, too. That means that far from being a birds-only thing, unidirectional flow-through lung ventilation was probably primitive for Archosauria, and was therefore the default state for non-avian dinosaurs, pterosaurs, the other ornithodirans and the hordes of croc-line archosaurs.

Crocodilian breathing - Schachner et al 2013a fig 10

Diagrammatic and highly simplified representation of airflow through the dorsobronchi and ventrobronchi during inspiration (A) and expiration (B) in the crocodilian lung, and inspiration (A) and expiration (D) in the avian lung. The avian model is a modification of the Hazelhoff loop (Hazelhoff, 1951). Arrows denote direction of airflow, white arrows show air flowing through the parabronchi, blue arrows show air entering the trachea, the red circled “X” demonstrates the location of the aerodynamic inspiratory valve (i.e., air does not flow through this location during inspiration). Colors represent hypothesized homologous regions of the lung in both groups. Abbreviations: d, dorsobronchi; P, parabronchi; Pb, primary bronchus; v, ventrobronchi. [Figure 10 and caption from Schachner et al. 2013a.]

The birdy-ness of crocodilian lungs was further cemented earlier this year when Schachner et al. described the lung morphology and airflow patterns in Nile crocs, which have lungs that are if anything even more birdlike than those of gators. I got to review that paper and blogged about it here.

Now…well, you read the headline. Monitor lizards have unidirectional airflow through their lungs, too. This falls at about the halfway point between “whatisthisIdonteven”–I mean, dude, unidirectional airflow in friggin’ lizards!–and “yeah, that makes a weird sort of sense”. Because to sum up a lot of science unscientifically, monitors just kick a little more ass than other squamates. They have crazy high aerobic capacities for animals that aren’t birds or mammals, they’re ecologically versatile and geographically widespread, they get waaay bigger than any other extant lizards (Komodo dragons) and until recently got even bigger than that (Megalania). Is it going too far to link the success of varanids with their totally pimpin’ flow-through lungs? Maybe, maybe not. But it seems like fertile ground for further study.

Schachner_fig3_labels

Phylogeny for Diapsida showing lungs of representative taxa.
Greyscale images are modified from Milani and transected. The coloured
three-dimensional images are the bronchial tree (right lateral view). Images are
not to scale. a, Diapsida. b, Sphenodon punctatus. c, Crocodile sp. (left) and
Alligator mississippiensis (right). d, Squamata. e, Iguana iguana (left) and
Polychrus marmoratus (right). f, Gekko gecko. g, Lacerta viridis. h, Python sp.
in dorsal view . i, Varanus bengalensis (left) and V. exanthematicus (right).
The blue regions of the phylogeny reflect the hypothesis that unidirectional
airflow evolved convergently; the green arrow shows the alternative hypothesis
of an ancestral origin. [Figure 3 and caption from Schachner et al. (2013b).]

Now, obviously the gigantic question looming over all of amniote biology like one of those monoliths from 2001 is: does this mean that unidirectional flow-through lung ventilation is primitive for all diapsids? That is a super-interesting possibility, and in the new paper Schachner et al. advance some evidence both for and against. On the “for” side, well, hey, there’s uniflow in monitors, crocs, and birds, and in all three cases, air flows down the primary bronchus into a sac at the caudal end, and then back cranially through series of interconnected sacs or tubes. On the “against” side, the patterns of airflow in varanids are similar to those in archosaurs but not identical: in archosaurs, the caudal-to-cranial flow goes through dorsal, tube-shaped secondary bronchi, whereas in varanids it goes through ventrolateral, sac-like bronchi. Also, varanids and archosaurs are phylogenetically distant, so if uniflow was primitive for diapsids, it would seem to have been lost in a lot of other lineages–potentially, all the non-varanid lepidosauromorphs.

On the gripping hand, uniflow would seem to have been lost in all those other lepidosauromorphs, but maybe it wasn’t. Maybe some of them are in the same state varanids were in until this year: they’ve had uniflow lungs forever and we don’t know because no-one has looked yet. And this is one of the concluding points in the new paper: we need to go look more at how living animals actually work.

A small sample of monitor lung diversity, from Becker et al. (1989).

A small sample of monitor lung diversity, from Becker et al. (1989).

In fact, we don’t just need to look at more critters in general, we specifically need to look at more monitors. I have been casually throwing around the terms “monitors” and “varanids” as if the findings of Schachner et al. (2013b) apply to all of them. They may not–the new paper is only about airflow in the savannah monitor, Varanus exanthematicus (same species as Mike’s “sauropod” Charlie), and monitor lungs are sufficiently diverse in form to have been used as taxonomic characters (Becker et al. 1989). So monitors may actually provide multiple windows into the evolution of unidirectional, flow-through lung ventilation. This is especially tantalizing because extant monitors cover a much wider range of body sizes and ecologies than extant crocs, so–just maybe–we can find out if and how diversity in lung structure and ventilation is related to body size and mode of life. Somebody get on that, stat.

Hypothetical bird lung intermediates - Perry 1992 fig 6

Figure 6 from Perry (1992).

My favorite part of all this? Something virtually identical to how monitor lungs work was proposed just over two decades ago by Steve Perry, as a hypothetical stage between saccular lungs and bird-like lungs. See the “Euparkerian grade” lung in the above figure, with perforations between adjacent chambers? Compare that to the diagram of the monitor lung in the image at the top of the post–they’re pretty darned similar. Now, two caveats. First, Steve was suggesting this as a plausible ancestral state for archosaurs, not monitors, and as mentioned above, monitors do things a little differently than archosaurs. Second, there are some things in this figure that are now known to be incorrect, primarily the lack of unidirectional airflow in the crocodilian lung. In fact, on the page opposite this figure, Steve explicitly discounted the possibility of unidirectional airflow in croc lungs. Still, he recognized that croc lungs and bird lungs share profound structural similarities, that they are really points on a spectrum of plausible intermediate conditions, and that crocs had the potential to shuttle air around their lungs because of the complex connections between chambers. So if Steve was not completely right, neither was he completely wrong; it might be most accurate to say that he was less wrong than anyone else at the time, and for about 20 more years after. Which is pretty darned good; I’ve had to rebut myself within the space of five years (Wedel 2007: prosauropod pneumaticity is equivocal. Yates et al. 2012: oh no it’s not!).

Here are the thoughts that have been tumbling through my head since I first learned about this. Obviously structures can be simplified or lost through evolution. Birds and turtles lost their teeth, numerous tetrapods have lost one or both pairs of limbs, and, heck, the platypus lost its stomach. But I rarely see hypotheses of derived simplification entertained for organs like hearts and lungs. There seems to be an unstated but widespread assumption that complex = better when it comes to core physiological processes like breathing.

Reptilian lung morphospace - Perry 1992 fig 2

Figure 2 from Perry (1992)

But it ain’t necessarily so. Following Steve Perry’s diapsid-lung-continuum diagrams, I have often wondered if croc lungs are derived from bird lungs instead of the reverse; maybe the ancestral archosaur had a fully bird-like lung/air-sac system and the non-diverticular, not-super-aerobic lungs of crocs represent a simplification of that system to suit their more sedate lifestyle as semiaquatic ambush predators. That’s pretty much what Seymour et al. (2004) suggested for crocodilian hearts, and it seems plausible given that so many early crocodylomorphs were long-legged, terrestrial, and possibly cursorial (e.g., sphenosuchians). In other words, maybe extant crocs are secondarily ectothermic, with secondarily and possibly paedomorphically reduced air sac systems.

Heck, maybe even bird lungs are simplified compared to their ancestral condition. Most birds have nine air sacs: paired cervical, anterior thoracic, posterior thoracic, and abdominal sacs, and an unpaired clavicular air sac. Some have reduced the number further through loss or fusion of adjacent air sacs. But they all start out with 12 embryonic air sacs (the extras fuse together, IIRC almost all of them becoming part of the clavicular sac), which suggests that the ancestors of birds might have had more than the standard nine.

If we assume that there was some diversity in respiratory anatomy in Mesozoic dinosaurs–which is not much of a stretch, given the diversity we see within (let alone among) monitors, crocs, and birds–it would be an awfully big coincidence if the only dinosaur clade to survive the end Cretaceous extinction just happened to have the fanciest lungs. As far as I know, no-one has proposed that birds survived because they out-breathed everyone else. If anything, the decent-to-high survival rates of mammals, crocs, and turtles across the K-Pg boundary, and the complete extinction of air-sac-equipped pterosaurs and non-avian saurischians, suggests that lung ventilation had nothing to do with survivorship. So what are the chances that crown birds have the most complex lungs among ornithodirans? (Don’t say “flight” because enantiornithines and pterosaurs had air sacs and died out, and bats don’t have air sacs and fly just fine.)

I’m not saying these “awesomeness came first” hypotheses are currently more parsimonious than the standard view. But they’re plausible, and at least potentially testable, and if nothing else an antidote to the idea that birds sit at the top of some physiological Great Chain of Being.

Back to the homology-vs-convergence question. If flow-through lungs are primitive for diapsids, maybe they’ll turn up in a few more critters. But maybe evolving undirectional airflow just isn’t that hard, and only requires poking some holes through the walls of adjacent lung chambers–as stated above, we need to go check more critters. But either way, the form and function of the lungs in V. exanthematicus are not only fascinating in their own right, they give us a window into what the early evolution of archosaurian–and maybe even early diapsid!–breathing might have been like. And that’s phenomenal.

I have some more thoughts on this, particularly the implications for sauropods and other dinosaurs, but those will have to wait for another post.

Images and figures from Schachner et al. (2013b) appear here courtesy of Emma Schachner (website), who kindly offered to let me look under the hood before the paper came out. She also created a cool video showing the 3D lung anatomy of V. exanthematicus. Thanks, Emma, and congratulations!

References

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Schachner et al 2013 fig-13-full

Schachner et al. (2013: Figure 13): Diagrammatic representations of the crocodilian (A) and avian (B) lungs in left lateral view with colors identifying proposed homologous characters within the bronchial tree and air sac system of both groups. The image of the bird is modified from Duncker (1971). Abbreviations: AAS, abdominal air sac; CAS, cervical air sac; CRTS, cranial thoracic air sac; CSS, caudal sac-like structure; CTS, caudal thoracic air sac; d, dorsobronchi; GL, gas-exchanging lung; HS, horizontal septum; IAS, interclavicular air sac; L, laterobronchi; NGL, non-gas-exchanging lung; ObS, oblique septum; P, parabronchi; Pb, primary bronchus; Tr, trachea; v, ventrobronchi.

Gah! No time, no time. I am overdue on some things, so this is a short pointer post, not the thorough breakdown this paper deserves. The short, short version: Schachner et al. (2013) is out in PeerJ, describing airflow in the lungs of Nile crocs, and showing how surprisingly birdlike croc lungs actually are. If you’re reading this, you’re probably aware of the papers by Colleen Farmer and Kent Sanders a couple of years ago describing unidirectional airflow in alligator lungs. Hang on to your hat, because this new work is even more surprising.

I care about this not only because dinosaurian respiration is near and dear to my heart but also because I was a reviewer on this paper, and I am extremely happy to say that Schachner et al. elected to publish the review history alongside the finished paper. I am also pleasantly surprised, because as you’ll see when you read the reviews and responses, the process was a little…tense. But it all worked out well in the end, with a beautiful, solid paper by Schachner et al., and a totally transparent review process available for the world to see. Kudos to Emma, John, and Colleen on a fantastic, important paper, and for opting for maximal transparency in publishing!

UPDATE the next morning: Today’s PeerJ Blog post is an interview with lead author Emma Schachner, where it emerges that open review was one of the major selling points of PeerJ for her:

Once I was made aware of the transparent peer review process, along with the fact that the journal is both open access and very inexpensive to publish in, I was completely sold. […] The review process was fantastic. It was transparent and fast. The open review system allowed for direct communication between the authors and reviewers, generating a more refined final manuscript. I think that having open reviews is a great first step towards fixing the peer review system.

That post also links to this one, so now the link cycle is complete.

Reference

Schachner, E.R., Hutchinson, J.R., and Farmer, C.G. 2013. Pulmonary anatomy in the Nile crocodile and the evolution of unidirectional airflow in Archosauria. PeerJ 1:e60 http://dx.doi.org/10.7717/peerj.60