The earth has music for those who listen

As Stephen Jay Gould once put it, we have an earful of jaw. The small, sound-conducting bones of our inner ears – the incus, malleus, and stapes – got their start as jaw bones in our distant ancestors, and the modification of bits of jaw into intricate ear components is one of the classic examples […]
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As Stephen Jay Gould once put it, we have an earful of jaw. The small, sound-conducting bones of our inner ears – the incus, malleus, and stapes – got their start as jaw bones in our distant ancestors, and the modification of bits of jaw into intricate ear components is one of the classic examples of major evolutionary transformation. This was brilliantly demonstrated in a paper simply called “The Evolution of the Mammalian Ear” by paleontologist David Meredith Seares Watson in 1953, but, as Watson himself recognized, his transitional series was only a general outline of the change based upon the fossils available at the time.

Liaoconodon hui – a 133-120 million year old mammal from China’s rich Jehol fossil beds – adds a finer degree of resolution to Watson’s outline. Described by Jin Meng, Yuanqing Wang, and Chuankui Li in Nature last week, the ear anatomy of this small, Early Cretaceous creature had an intermediate arrangement. The bones present in our own inner ears were there, but they were not yet inside the skull.

Thanks to a combination of fossil discoveries and investigations of embryonic development, the correspondence between ancient jaw bones and the minute ossicles of the inner-ear has been well-established. While the stapes is actually an ear bone we share in common with other tetrapods – it is a modified version of the hyomandibular bone that was present in our fleshy-finned fish ancestors – the others are unique to mammals. The articular and prearticular bones in the jaws of our early synapsid cousins like *Dimetrodon *make up the malleus in our own ears, just as our incus is a modified quadrate and the bone which suspends our eardrum – the ectotympanic – is a transformed angular bone. Each of these started out as part of the lower jaw, but they gradually became reduced in size and associated with hearing rather than feeding.

What makes Liaoconodon remarkable is that several of these bones were suspended between the lower jaw and the inner ear. The tiny ectotympanic, malleus, and incus bones had lost their direct contact with the lower jaw, but they were supported on a splint of ossified cartilage that itself was connected to the mandible. The reason for this connection, Meng and co-authors hypothesize, might be attributable to the way the eardrum was supported. Most of the membrane was stretched over the ecotympanic bone, but it also attached to the malleus, meaning that the whole suite of bones would have required stable support in order for Liaoconodon to hear properly. Eventually, after the ectotympanic supported the entire eardrum and the malleus became anchored to the skull, the flange of supporting bone was lost in other mammals.

Close-ups of the jaw and auditory ossicles of Liaoconodon (bottom image a SEM of the right side). From supplement to Meng et al., 2011.

This finding was not unexpected. In 2007 a different team of paleontologists described a closely-related fossil mammal from the same deposits they named Yanoconodon allini. Though broken and not as well-articulated as in the Liaoconodon specimen, the small ear bones of Yanocodon were reconstructed as sitting on a flange of ossified cartilage. Likewise, in 2009 another collaboration of scientists described another Early Cretaceous mammal – Maotherium asiaticus – that had a preserved piece of ossified cartilage attached to its lower jaw. This was taken as an indication that Maotherium, too, may have had inner ear bones suspended between jaw and skull. The significance of Liaoconodon is that it is the first such specimen to be described with the delicate inner ear bones in place and unambiguously connected to the cartilage splint.

Liaoconodon, Yanoconodon, and Maotherium all inform our understanding of how the delicate ear bones of mammals evolved, but none of them were our direct ancestors. Both Liaoconodon and Yanoconodon belonged to a radiation of early mammals called eutriconodonts that has no living descendants. And, while it was more closely related to us, Maotherium was part of another group of prehistoric mammals called spalacotheroids that are among our various collateral cousins. What this boils down to is the fact that there was not one single, straight pathway of evolutionary improvement in terms of ear anatomy. The transitional features in these creatures were actually widespread and might indicate that the inner ear bones of modern mammals evolved more than once - the exigencies of life for early mammals may have caused the same arrangement to evolve in several lineages from a shared starting point.

How our inner ears evolved will undoubtedly remain one of the classic examples of evolutionary change, but we should not be fooled by the linear diagrams we create to illustrate these changes. Life was more varied and diverse than we could have ever imagined.

[For a little more detail on early mammals and the evolutionary inheritance they left us, see chapter 6 of my book Written in Stone.]

Top Image: The skeleton of Liaoconodon, from Meng et al., 2011.

A note about the title: The line "The earth has music for those who listen" has often been attributed William Shakespeare, but this appears to be a mistake. How this line turned into a meme credited to him is unclear. Still, I thought it fitting for a post about fossils and the evolution of hearing.

References:

Ji, Q., Luo, Z., Zhang, X., Yuan, C., & Xu, L. (2009). Evolutionary Development of the Middle Ear in Mesozoic Therian Mammals Science, 326 (5950), 278-281 DOI: 10.1126/science.1178501

Luo, Z., Chen, P., Li, G., & Chen, M. (2007). A new eutriconodont mammal and evolutionary development in early mammals Nature, 446 (7133), 288-293 DOI: 10.1038/nature05627

Meng J, Wang Y, & Li C (2011). Transitional mammalian middle ear from a new Cretaceous Jehol eutriconodont. Nature, 472 (7342), 181-5 PMID: 21490668

Watson, D. (1953). The Evolution of the Mammalian Ear Evolution, 7 (2) DOI: 10.2307/2405751