Tetrapod Zoology

At a vertebrate palaeontology workshop held in Maastricht in 1998, some colleagues and I sat in a bar, lamenting the fact that nobody cared about anatomy any more, and that funding bodies and academia in general were only interested in genetics. Given the poor to non-existent coverage that anatomy gets in many biology courses and textbooks, you might think that anatomy has had its day and that - as some molecular biologists told us in the 1980s and 90s - all the anatomical work worth doing had been published in the days of Owen and Huxley. Nothing could be further from the truth, and if you don't believe this you only have to consider the fact that a thousand basic questions of everyday anatomy have never really been studied, let alone answered. As demonstrated at the Centre for Ecology and Evolution workshop 'Modern Approaches to Functional Anatomy' (held at the Natural History Museum in London on April 23rd), we are in the midst of a new anatomical revolution, and these are very, very exciting times...

Organised by John Hutchinson of the Royal Veterinary College (with help from the NHM's Adrian Lister), the meeting combined new work on primates, dinosaurs, elephants and other tetrapods with contributions on fishes and insects. The application of new computational approaches was at the fore as a major theme. I was honoured and surprised when, during the opening welcome, John mentioned the bloggers who were in attendance: specifically Darren Naish of Tetrapod Zoology and Mike P. Taylor of SV-POW! Wow, what an accolade.

The talks opened with Robin Crompton's plenary lecture on locomotor ecology and locomotor evolution. Primates can be distinguished from other mammals by way of their elongate hindlimbs and divergent big toes (still evident in humans, as demonstrated by a video of a person able to play the guitar with their feet), and the main locomotor dichotomy that we see in anthropoid primates - that between pronogrades and orthogrades - occurred round about 20 million years ago during the Early Miocene. But even many of the 'key' adaptations linked to locomotion are controlled by the life history of the individual: an excellent example being the bicondylar angle of the knee joint, the development of which is governed by the animal's post-natal development (Shefelbine et al. 2002). Chimps forced for whatever reason to adopt a bipedal gait during growth have ended up being obligate bipeds: Oliver is the example most people have heard of, but there's also Poko, a bipedal chimp who spent the first ten years of his life in a tall and narrow parrot cage and was never able to develop normal quadrupedal walking. The bent-hip, bent-knee walking (BHBK) practised occasionally by normal gorillas and chimps is less efficient (in terms of wattage per kilo) than the striding bipedality of modern humans, but orangutan bipedality is highly efficient and more so than that of humans. Orangutans can and do walk bipedally on the ground, but it's mostly practised arboreally, yet rather than practising their bipedal gait on strong, robust branches, orangutans use bipedality to access small, flexible branches. They use the compliancy of such supports to their advantage, walking on them with a stiff-legged gait that is very reminiscent of what we do on the ground (Thorpe & Crompton 2006, Thorpe et al. 2007a, b: for data on arboreal bipedality in chimps see Stanford 2006). In view of the fact that pongines are basal relative to African hominids (which include us hominins), it is tempting to infer from this that hominid bipedality evolved in an arboreal context, and was later exapted for terrestriality [bipedally walking orangutan shown above; reconstructed bipedal Australopithecus below].

Why did primates evolve long hindlimbs and a grasping hallux (big toe) in the first place? Basal primates were small arboreal animals, well within the predation range of raptors and other predators (raptors might take as much as 20% of the annual birth population of some small extant primate species), so the impressive leaping allowed by long powerful hindlimbs and grasping feet probably had an important role in predator avoidance. Among Madagascan primates, Prof. Crompton suggested that the evolution of fossas (Cryptoprocta) might have driven the evolution of both large body size and diurnality in lemurs.

Modelling of australopithecines like Lucy now indicates that these primates were capable bipedal walkers (at least over short distances), and similar in their abilities to modern human children. This view matches new work on the famous Laetoli tracks, which were produced by australopithecines walking at a speed similar to that practised by modern humans. The Laetoli trackmakers had a clear medial arch, a hallux more divergent than that of modern humans, and also produced high-pressure areas of impact both at the heel at in the area of the metatarsal heads. That last point is significant because this can only be produced by erect walking, and not by BHBK walking. Even further down the hominid tree, frequent terrestrial bipedality was very probably practised by Orrorin and Australopithecus anamensis, both of which were denizens of fully wooded habitats (an observation indicating that hominid bipedality did not evolve as a result of the opening of woodland). As you might have gathered from this long write-up, this was a very data-heavy talk, and a great overview of primate locomotor evolution and ecology. Mary Blanchard, who you might remember from my brief congratulatory article from December 2007, is part of Prof. Crompton's research group. The subject of primate anatomy, its evolution and diversity, and how we can study it, was to be revisited by several other speakers during the meeting.

Moving on, John Hutchinson discussed his work on dinosaur biomechanics, urging the importance of an integrated approach that incorporates work on living animals. A nice photo of a researcher about to vomit over a toilet bowl accompanied the message that there are so many unknowns that we're likely to be wrong about most or all of our assumptions. But what we're now learning about extant animals means that we're approaching an 'interpretative asymptote' and are soon to have enough data to make more confident assertions about palaeobiomechanics. Sexy work on gigantic bipeds like Tyrannosaurus has gone hand in hand with an effort to better understand form and function in large ground-birds like ratites: two really important components of bipedal walking and running - the role of anti-gravity muscles and of limb posture - have been poorly studied and are poorly understood, so John and colleagues have been doing pioneering work on ostriches and chickens. For more on this sort of thing see Carrano & Hutchinson (2002), Hutchinson (2001a, b, 2002), Hutchinson & Garcia (2002) and Hutchinson & Gatesy (2000, 2006) [many available for free here]. New modelling on Cretaceous theropods like Microraptor and Velociraptor is underway, and eventually we should have enough models to reliably extrapolate biomechanical behaviour up and down the archosaur cladogram: John suggested that this technique be termed Quantitative Anatomical Phylogenetic Optimisation, or QAPO. Nice acronym [image below shows range of possible hindlimb postures in a model tyrannosaur (from Hutchinson & Gatesy 2006); image above is Luis Rey's painting of running tyrannosaur and giant chicken.... it's a long story].

Renate Weller spoke about the different three-dimensional imaging tools that are now available for anatomical work (and hence not so much about animals), but I was particularly impressed with and/or shocked by the fact that MRI scanners have such strong magnetic attractivity that they can literally pull big metal objects, like radiators and hospital trolleys, across the room, the results being both spectacular and expensive. Renate also spoke about her work in producing a 3D reconstruction of Eclipse (1764-1789), the famous British thoroughbred racehorse (he won every race he took part in, fathered over 320 foals at least, and is thought to have made a genetic contribution to over 80% of all modern thoroughbreds). Kept at the Natural History Museum for about a century, his mounted skeleton is now back at the Royal Veterinary College.

Going back to fossil taxa, Jenny Clack reviewed the new ideas and interpretations that she and her colleagues have developed about the famous Devonian tetrapod Ichthyostega, traditionally imagined as a rather nondescript salamander-like animal but now known to have been more bizarre than anyone ever thought [new reconstruction shown here, with Acanthostega too]. The polydactyly and paddle-like hindlimbs of Ichthyostega suggest both that pentadactyly was not primitive for tetrapods, and that basal forms like Ichthyostega were still predominantly aquatic. Less well known is that Ichthyostega has a somewhat differentiated vertebral column, with a short neck, weird tall neural spines in the pelvic region, and a tail which is proportionally shorter than long imagined (Ahlberg et al. 2005). The orientation of the zygapophyses in the 'lumbar' region suggest that some dorsoventral motion was possible, and that lateral flexion wasn't really possible. Perhaps Ichthyostega worked something like a pinniped. Whatever, the new picture of this iconic animal is very different from the conventional one developed by Jarvik. Mike P. Taylor asked afterwards if the possibility of secondary adaptation to aquatic life has been considered for Ichthyostega: in fact it has (Henderson 1999), the main problem being that there are no known terrestrial ancestors for aquatic Ichthyostega.

More to come in part II, to be published tomorrow.

Refs - -

Ahlberg, P. E., Clack, J. A. & Blom, H. 2005. The axial skeleton of the Devonian tetrapod Ichthyostega. Nature 437, 137-140.

Henderson, D. M. 1999. Late Devonian amphibians as secondarily aquatic tetrapods. In Hoch, E. & Brantsen, A. K. (eds) Secondary Adaptation to Life in Water. University of Copenhagen, p. 18.

Hutchinson, J. R. 2001a. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131, 123-168.

- . 2001b. The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131, 169-197.

- . 2002. The evolution of hindlimb tendons and muscles on the line to crown-group birds. Comparative Biochemistry and Physiology Part A 133, 1051-1086.

- . & Garcia, M. 2002. Tyrannosaurus was not a fast runner. Nature 415, 1018-1021.

- . & Gatesy, S. M. 2000. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26, 734-751.

- . & Gatesy, S. M. 2006. Beyond the bones. Nature 440, 292-294.

Shefelbine, S. J., Tardieu, C. & Carter, D. R. 2002. Development of the femoral bicondylar angle in hominid bipedalism. Bone 30, 765-770.

Stanford, C. B. 2006. Arboreal bipedalism in wild chimpanzees: implications for the evolution of hominid posture and locomotion. American Journal of Physical Anthropology 129, 225-231.

Thorpe, S. K. S. & Crompton, R. H. 2006. Orangutan positional behaviour and the nature of arboreal locomotion in Hominoidea. American Journal of Physical Anthropology 131, 384-401.

- ., Crompton, R. H., Alexander, R. McN. 2007a. Orangutans use compliant branches to lower the energetic cost of locomotion. Biology Letters doi:10.1098/rsbl.2007.0049 [free pdf, and others, here].

- ., Holder, R. L. & Crompton, R. H. 2007b. Origin of human bipedalism as an adaptation for locomotion on flexible branches. Science 316, 1328-1331.