Q J Med 2004; 97: 109-110
© Association of Physicians 2004; all rights reserved.
Biologic |
Hearing the sermons in stones
In order to stay upright, or to lie down carefully, we have developed a well-defined system to ensure that we are aware of our position and orientation in three dimensions. This system depends on extracellular masses of proteins interleaved with inorganic crystals of calcium carbonate, lying over sensory hair bundles that are deflected by movements in the mass. There is a single large mass in the genus Pisces, the otolith, which rests above the gravity-sensing organ (the macula). In all other vertebrates (mammals, birds, reptiles and amphibians) each macula is signalled to by tiny masses (otoconia) of inorganic material embedded in a protein scaffold.
There are surprising differences in the details of these structures in the vertebrates, and differences are found at different developmental stages in the life of many of them. The crystals may be composed of calciuim carbonate, calcite, aragonite or vaterate, and the morphology of the sensing organ varies. The protein component of the matrix varies most. The major proteins of the otoconia in the utricles of amphibians, birds and mammals have high molecular masses, whereas the amphibia make do with a protein of less than a fifth the size. Sollner et al.1 have shown that the Zebrafish otolith switches from an aragonite polymorph to calcite polymorph with the knockout of a single 613-amino-acid protein ‘Starmaker‘, named for the bizarre and irregular type of otoliths formed when the amino acid sequence of the protein is changed. The calcium carbonate polymorph in these altered otoliths was still aragonite until Starmaker levels were reduced further—then what was formed was a collection of almost pure calcite crystals. Fish with these altered structures were unable to orientate themselves properly in flowing water, but recovered when the morpholinos (modified antisense oligonucleotides) that had been injected into the one-cell-stage embryos ceased to be effective in preventing proper protein expression.
Starmaker protein shares sequence homology with human dentin sialophosphoprotein (DSPP), a protein involved in the mineralization of teeth with hydroxyapatite (calcium phosphate) rather than calcium carbonate. In human dentogenesis imperfecta, which may be associated with hearing loss, it is tempting to imagine that a similar pathogenesis may operate.
This phylogenetic linkage is paralleled by developments from an unexpected area where the application of a modern technology to old collections of material has yielded important data—a matter of note, as these collections appear to be valued less and less. It is possible to examine fossils by computed tomography scans, and the technique has been applied to pterosaurs—very large reptiles with wingspans up to 10 m—to see whether information could be obtained about how well these animals might orientate themselves in the three dimensional world of flight. Pterosaurs have very large balance organs and, it appears, a well-developed part of the brain that is necessary to keep the retina looking precisely where you are going, very important in fish-catching flight (remember the scene in ‘Fantasia’?). Early primates (tiny) and whales have also been studied.
In general, animals that are agile have larger and wider-looped semicircular canals relative to their body mass (gazelle vs. hippopotamus, for example). So instead of looking at bone structures, muscle attachments and limb proportions as a way of guessing how animals moved, a study of the ear may give information on likely patterns of movement and head position, say. The lateral canal works best as a sensor when it is parallel to the ground; the pterosaur Anhanguera can thus be assumed to have flown with its head tilted down. It is also suggested that this type of technique may provide an answer to how the massive sauropods held their necks—did they graze high or low? In 1994, Spoor and colleagues first applied this technique to Homo erectus to show that the upright posture was accompanied by a ‘modern’ inner ear, but Australopithecus was less well adapted. Archaeopteryx was clearly a bird, not a dinosaur, the ostriches are like the crocodilians, and the whales and dolphins have small canals when compared with all other living mammals (this may be to stop them getting sea-sick when manoeuvring rapidly—the blue whale has an inner ear about the same size as ours).
Other applications of this type of study have yielded data on the evolution of hearing. If it is assumed that data on the size of the eardrum, and the size and arrangement of the ossicles, may allow conclusions to be drawn about frequencies that might be heard, then there is another field to be explored. In Icthyostega, a creature widely accepted to be a transitional fossil between fish and land vertebrates (say 400 million years ago) the stapes is thin and plate-like, and some believe that like the modern frog, the ear was adapted more for underwater hearing (perhaps Icthyostega was mainly a water dweller?).
Thus the conjunction of two very different modern techniques of investigation and imaging can tell us a great deal about evolution, may inform us about some pathways that when disrupted, lead to disease—and help us to understand better the value of collections.
References
1. Sollner C, Burghammer M, Busch-Nentwigh E, Berger J, Schwarz H, Riekel C, Nicolson T. Control of crystal size and lattice formation by Starmaker in otolith biomineralisation. Science 2003; 302:282–5.
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