Pharyngula

Yanoconodon, a transitional fossil

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The latest Nature reveals a new primitive mammal fossil collected in the Mesozoic strata of the Yan mountains of China. It’s small and unprepossessing, but it has at least two noteworthy novelties, and first among them is that it represents another step in the transition from the reptilian to the mammalian jaw and ear.

Here’s the beautiful little beast; as you can see, it’s very small, and we need to look very closely at some details of its morphology to see what’s special about it.

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Main part of the holotype (Nanjing University-Paleontology NJU-P06001A). b, Skeletal restoration (dorsal view). Abbreviations: ag, angular (ectotympanic ring); am, acromion (scapula); as, astragalus; at, atlas (cervical vertebra, c1); ax, axis (c2); c?, canine?; c5-7, cervical vertebrae 5-7; ca3 and ca8, caudal vertebrae 3 and 8 (distal caudals are missing); cl, clavicle; cm, calcaneum; cod, coronoid process (dentary); cos, coracoid process (scapula); cp, carpals; dc, dentary condyle; dpc, deltopectoral crest (humerus); ec, ectepicondyle (humerus); en, entepicondyle; ep, epipubis; fe, femur; fi, fibula; hu, humerus; hy, hyoid elements; i1-2, incisors 1 and 2; il, ilium; in, incus; is, ischium; j?, jugal?; l1 and l8, lumbar vertebrae 1 and 8; lr2-7, lumbar ribs 2-7; lt, lesser tubercle (humerus); m1-4, lower molars 1-4; ma, malleus; mc, Meckel’s cartilage (ossified); mg, Meckel’s groove (dentary); mp, metacarpals; mt, metatarsals; mx, maxillary; p1-2, premolars 1 and 2; pb, pubic; ph, phalanges; ra, radius; sc, scapula; sq, squamosal; stb, sternum and sternabrae; s1-3?, sacral vertebrae 1 and 2 (and possibly sacral vertebra 3?); t1, t10 and t18, thoracic vertebrae 1, 10 and 18; ti, tibia; tr1-2, tr6 and tr15-18, thoracic ribs 1, 2, 6 and 18; ti, tibia; ul, ulna.

The first significant feature to examine is the jaw. This animal is from the Mesozoic, and a time when evolution was generating some radical changes in the feeding and sensory structures of the mammalian lineage. So first, a little background.

The primitive tetrapod jaw is a compound structure built up from multiple bones. In embryonic development, a rod-like structure called Meckel’s cartilage is first to form; in modern mammals, it is resorbed later in development, and really only forms a temporary scaffold. The dentary, as you might guess from the name, is the tooth-bearing portion. Farther back are several bones, including the angular and the articular, which contribute to the body of the structure and its articulation with the skull. One of the roles of these bones is to connect to the auditory apparatus of the cranium—the jaw conducts vibrations to these bones, which then transmits them to the organs of hearing. This is not a particularly sensitive way to sense sound, since it means sound waves traveling through the air (or the ground) are going to have to be picked up by a high impedance element, the bulky jaw, before being transmitted to the ear.

In the early mammalian lineage, there is a pattern of progressive reduction of the various secondary jaw elements and an expansion of the dentary bone to take over the whole job of the jaw. We have an excellent record of the transformation of the jaw and skull elements in mammalian evolution — in short, what we see is that everything but the dentary gets smaller and smaller, and gets pushed farther and farther back towards the skull. We have transitional forms that have double articulations of the jaw with the skull—one between the old articular bone and the quadrate bone of the skull, and another between the dentary and the squamosal (the current jaw joint in modern mammals)—and then forms where the old hodge-podge of bones have been cast free of the jaw altogether.

In us, the old articular and quadrate bones have completely lost their role in supporting the jaw as a joint and instead have become imbedded in the middle ear of mammals, suspended with the stapes between two delicate membranes to specialize in conducting sound vibrations to the inner ear. What does the hearing apparatus look like in Yanoconodon?

Start by looking at a, b, c, and d in this diagram. Highlighted in blues and purples at the back of the jaw are these small bones in Morganucodon (a) and Yanoconodon (b). In d is the jaw of Repenomamus, a large Cretaceous mammal. Don’t miss c—that small object is the collection of middle ear bones from Ornithorhyncus, better known as the platypus.

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a, Mammaliaform Morganucodon (medial view); a-1 and a-2 label schematic transverse sections at the levels of the malleus and the ectotympanic. In Morganucodon, the middle ear maintains both an anterior connection to the mandible via the Meckel’s cartilage, and a mediolateral contact to the mandible. b, Eutriconodont Yanoconodon (medial view, composite restoration of mandible and middle ear from NJU-P06001A and B). b-1 and b-2 label transverse sections at the levels of the malleus and the ectotympanic. The middle ear retains the anterior connection to the mandible via ossified Meckel’s cartilage (yellow), but is mediolaterally separated from the posterior part of the mandible because of the twist and curvature of Meckel’s cartilage (red arrows in b). c, the ectotympanic (blue), malleus (green) and incus (brown) of modern Ornithorhynchus: the shape and proportion of the ear bones are similar in Ornithorhynchus and Yanoconodon. d, Eutriconodont Repenomamus: ossified Meckel’s cartilage connected anteriorly to the mandible (similar to Yanoconodon). e, Ossified Meckel’s cartilage of Repenomamus (ventral view, isolated). f, Ossified Meckel’s cartilage of Yanoconodon (ventral view, isolated, composite restoration of both the left and the right elements). g, Middle ear of Yanoconodon (composite restoration, ventral view): the ectotympanic and malleus are connected anteriorly to the mandible via ossified Meckel’s cartilage; but these are mediolaterally separated from the posterior part of mandible, facilitated by curvature of the Meckel’s cartilage (yellow). h, Middle ear bones of adult Ornithorhynchus (ventral view) and similarity to those of Yanoconodon. i, Embryonic Ornithorhynchus: the tympanic ring and the partially developed manubrium and goniale (‘prearticular’) of the malleus are anteriorly connected via Meckel’s cartilage to the mandible, but separated mediolaterally from the posterior region of mandible, facilitated by the curved cartilage (red arrow). Yanoconodon retains the embryonic pattern of Ornithorhynchus owing to the timing change of earlier ossification of Meckel’s cartilage, but otherwise its ectotympanic, malleus and incus are nearly the same as in adult Ornithorhynchus.

What we see here is that the three Mesozoic mammals all retain Meckel’s cartilage as a slender, ossified splint clinging to the inner side of the jaw. In b and c, we can see that middle ear bones of both Yanoconodon and the platypus are remarkably similar, but there is one significant difference. In the platypus, those bones are not connected to the jaw at all—they have the standard mammalian middle ear, with the bones suspended remotely from other bones of the jaw and skull. In Yanoconodon, we are almost at that point. The middle ear bones are clearly delicate and specialized for function in hearing, but they retain one last tentative, delicate connection with the jaw through a contact with Meckel’s cartilage. In this animal, we’ve caught the mammals just before they’ve taken that last step of fully separating the middle ear bones from the jaw.

This animal is from that time just before the hearing apparatus has let loose of its last bony mooring and said bon voyage to the jaw. It’s a significant moment in history, I think.

Also look at g. This is a ventral view of the left jaw of Yanoconodon, and again you can see the middle ear bones connected by that tiny strut to the jaw. h is a drawing of the middle ear bones of the platypus in the same orientation, and i is especially neat: that’s the jaw of a platypus embryo, before Meckel’s cartilage is resorbed, and you can see that the middle ear bones are connected in the same way, transiently. It’s one module in development that flaunts a lovely example of embryonic recapitulation of evolutionary history.

I said there were two novelties in this specimen. One is the beautiful connection between the middle ear bones and the jaw; the other is a curiosity in the number of vertebrae. Compare yourself to Yanoconodon, for instance:

# vertebrae
Region You Yanaconodon
Cervical 7, no ribs 7, no ribs
Thoracic 12, with ribs 18, with ribs
Lumbar 5, no ribs 8, with floating ribs

Not only is the total number of vertebrae very much on the high end of what we see in any modern mammals, making for a rather sinuous and flexible body, but there’s that odd business of the lumbar (our lower back) vertebrae having riblike bones attached to them. The authors make the point, too, that the boundary between thoracic and lumbar in Yanoconodon is somewhat arbitrary—there’s a continuous gradation rather than a sharp delineation. Gain and loss of lumbar ribs seems to be a fairly common event in these early mammalian clades, as illustrated below.

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a, Homoplastic distribution of lumbar ribs in Mesozoic mammal taxa preserved with vertebral column: lumbar ribs are present in gobiconodontids and Yanoconodon but absent in closely related Jeholodens (node marked 2), present in Akidolestes but absent in closely related Zhangheotherium and the more inclusive theriiforms (node 1). b, Patterning of vertebral structure (development of lumbar ribs) in modern laboratory mice by homeobox genes. A separate loss of lumbar ribs in Jeholodens among eutriconodontans is hypothesized to be correlated with an independent activation of Hox10 patterning of thoracolumbar vertebrae (node 2). An isolated occurrence of lumbar ribs in Akidolestes among most spalacotheroids without lumbar ribs is hypothesized to be the effect of an independent loss of Hox10 gene function. The loss or gain of Hox gene function to pattern the vertebral identities is a plausible mechanism for homoplasy of lumbar ribs in early mammals, and for variation of thoracolumbar vertebral counts among eutriconodontans. tr, numbered thoracic ribs.

The inset diagram illustrates an experiment in mouse embryos: knocking out the three Hox10 genes in mice produces a transformation just like that seen in Yanoconodon, with all the lumbar vertebrae also producing small ribs. That’s very cool, in that it suggests a molecular mechanism in that the evolution of the Hox10 genes was probably responsible for the morphological variation we see in Mesozoic fossils.


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

Comments

  1. #1 Robert
    March 16, 2007

    Good thing God doesn’t have to show your “pathetic” level of detail in explaining his creation. That would be a lot of work.

  2. #2 Stuart Coleman
    March 16, 2007

    Hooray science!

  3. #3 Geral
    March 16, 2007

    “That makes two new gaps in the fossil record.”

    HAHAhahahaa… sad, sad but true. We’ll be hearing that one soon.

    Interesting post PZ. It’s unfortunate time travel really is impossible/extremely unlikely, it would be amazing to see these ancient critters in their habitat with their unfossilized peers who we may never learn about.

  4. #4 David Marjanovi?
    March 16, 2007

    Would Yanocondon have been a monotreme?

    Nope. Look at the tree: Tachyglossus is the echidna*, and Ornithorhynchus is the platypus**. These are the only two monotremes in the tree. Thus, Yanoconodon is more closely related to us*** than to the monotremes.

    Which means that the “mammalian” middle ear evolved (at least) twice within mammals.

    But we knew that already. It was shown two years ago**** that the oldest known monotreme, Teinolophos, retained the condition represented above by Morganucodon!

    Reality is always stranger than fiction. :-)

    * Originally called Echidna in Scientific, but then that name turned out to be preoccupied.
    ** Originally called Platypus in Scientific, but then… DAMN BEETLES!!! Sorry. Ornithorhynchus “bird beak” is a better name. :-)
    *** The closest relative of us shown in the tree is Eomaia, one of the first eutherian mammals. Eutheria includes Placentalia and everything closer to it than to Marsupialia. The beastie next to it, Sinodelphys, is the oldest known metatherian — Metatheria includes Marsupialia and everything closer to it than to Placentalia. :-) Together, Metatheria and Eutheria form Theria, which you’ll need in the next footnote:
    **** Thomas H. Rich, James A. Hopson, Anne M. Musser, Timothy F. Flannery & Patricia Vickers-Rich: Independent Origins of Middle Ear Bones in Monotremes and Therians, Science 307, 910 — 914 (11 February 2005)

  5. #5 David Marjanovi?
    March 16, 2007

    Uh, or were you maybe just asking if it laid eggs? That we don’t know. But we don’t have a reason to expect that only monotremes among mammals lay eggs, considering the vast extinct diversity between Monotremata and Theria (hinted at in the tree).

    It is too bad we don’t have good access to dinosaur DNA, since they seem to have a great deal of variability in numbers of different vertebrae and the relationship between verts and ribs.

    In mammals, abnormalities like ribs on the last neck vertebra have a strong correlation to early-onset cancer and malformations. This is thought to explain why mammals are so extremely conservative in regards of vertebra numbers.

    Birds don’t get cancer as easily as mammals. It’s still mysterious why.

  6. #6 David Marjanovi?
    March 16, 2007

    Which means that the “mammalian” middle ear evolved (at least) twice within mammals.

    Stupid me! At least three times! Repenomamus is a triconodont like Yanoconodon (see tree), but has the “mammalian” condition.

    Unless of course Y. represents a reversal. But I have a hard time imagining natural selection for this.

  7. #7 Bob Dog
    March 16, 2007

    I’ve never understood the purpose or meaning of the phrase, “transitional fossils”.

    *All* fossils are transitional, since there is no “end product” to evolution (except for worldwide extinction, of course).

  8. #8 David Marjanovi?
    March 16, 2007

    Compare yourself to Yanoconodon, for instance:

    I’ve just read the article. Y. has ribs in the neck, and they’re not even fused to the vertebrae (as they are e. g. in birds). Repenomamus has the same number of thoracics + lumbars.

    The ear condition of Y. is argued to be a reversal, connected to other paedomorphic (childlike) features of the skeleton like the loss of separate epiphyses in all triconodonts. And Hadrocodium, a not-quite-mammal-under-the-strictest-definition, is said to have a “mammalian” middle ear. Curiouser and curiouser!

  9. #9 rmp
    March 17, 2007

    Kseniya, you hit the nail on the head with nature being awe-inspiring. Unfortunately, for many people they assume the next logical step to be there must be a God. Not because there is evidence for it, simply because, ‘gosh, isn’t this just amazing’. As Leon said, we just don’t tend to think in terms of a scale of billions of years. What I don’t understand is why someone who thinks that nature is too amazing to have happened without a God (it would be too amazing), has no problem believing in something that is much more amazing (a being that can manipulate nature at will).

  10. #10 DaveX
    March 17, 2007

    This is a fantastic post. I’ll freely admit that I don’t follow a lot of it, though– all the names become mushy for me, sadly. I really need to bone up on my classification system. What would be a good online resource for someone wishing to do this– something accurate, but maybe of a high school/early college level biology understanding?

    I’d enjoy it to show EVERYTHING– I’ve forgotten far too much, I can’t even recall all the kingdoms properly. *sigh* Feel free to send me e-mail: I have a gmail account: malty1

  11. #11 Azkyroth
    March 17, 2007

    DaveX:

    Have you taken a look at the Tree of Life project?

  12. #12 Stephen
    March 17, 2007

    DaveX:

    I once put together a page about scientific names of birds. It may help you to get a bit of feel for scientific names in general:

    http://www.xs4all.nl/~sbpoley/scinames.htm

  13. #13 David Marjanovi?
    March 17, 2007

    I just did… have things changed a lot?

    In the last 20 years? Yes. People started to do phylogenetics as a science instead of as an art. They discovered that having three cusps in a row on the molars is the normal state, so not everything with such teeth can be lumped into “Triconodonta”, and that having three cusps in a triangle was just the next step, so not everything with such teeth can be lumped into “Symmetrodonta”. And they figured out where the monotremes come from, thanks to bits and pieces from the southern hemisphere and China.

    Then came discoveries of new fossils: we used to have a grand total of zero spalacotheroid (true symmetrodont) skeletons — just jaw fragments and isolated teeth –, now we have complete skeletons (with hair) of three species. We used to have one true triconodont skeleton, now we have at least seven (most of them complete and with hair). We used to have half a docodont, now we have a whole one in addition (complete and with hair). We have the intriguing Fruitafossor (mentioned in the tree above) from the US Late Jurassic, a highly modified termite specialist (known from a largely complete skeleton). And then there’s Hadrocodium, and a complete lower jaw of Haramiyavia (which belongs to a group known otherwise only from teeth), and so on…

  14. #14 David Marjanovi?
    March 17, 2007

    I just did… have things changed a lot?

    In the last 20 years? Yes. People started to do phylogenetics as a science instead of as an art. They discovered that having three cusps in a row on the molars is the normal state, so not everything with such teeth can be lumped into “Triconodonta”, and that having three cusps in a triangle was just the next step, so not everything with such teeth can be lumped into “Symmetrodonta”. And they figured out where the monotremes come from, thanks to bits and pieces from the southern hemisphere and China.

    Then came discoveries of new fossils: we used to have a grand total of zero spalacotheroid (true symmetrodont) skeletons — just jaw fragments and isolated teeth –, now we have complete skeletons (with hair) of three species. We used to have one true triconodont skeleton, now we have at least seven (most of them complete and with hair). We used to have half a docodont, now we have a whole one in addition (complete and with hair). We have the intriguing Fruitafossor (mentioned in the tree above) from the US Late Jurassic, a highly modified termite specialist (known from a largely complete skeleton). And then there’s Hadrocodium, and a complete lower jaw of Haramiyavia (which belongs to a group known otherwise only from teeth), and so on…

  15. #15 David Marjanovi?
    March 17, 2007

    And then I had a look at the Tree of Life site, and found that nothing of this business is up there. The tree shown is outdated, and even the nomenclature is wrong (palaeoryctoids are eutherians). Well, the Tree of Life accepts only the most qualified contributors, who are invariably those with the least spare time. *sigh*

    The best site on the web about Mesozoic mammals is here.

    I haven’t mentioned Volaticotherium, the gliding mammal (complete skeleton with hair and flight membrane) with no known close relatives except maybe two or three isolated teeth…

  16. #16 SEF
    March 17, 2007

    The best site on the web about Mesozoic mammals is here.

    I’m sure Trevor would be very pleased to receive any fictional award you might care to make up to go with that verbal accolade :-D – as long as any accompanying attention doesn’t end up constituting a denial of service attack.

  17. #17 David Marjanovi?
    March 17, 2007

    I’m sure Trevor would be very pleased to receive any fictional award you might care to make up to go with that verbal accolade :-D

    What for? If he wins in the lottery as many times per day as I do — and chances are he wins twice as often –, he has no use for anything I can make up.

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    May 7, 2009

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  19. #19 Brian
    December 15, 2009

    Thnks fr tkng ths. Gd blg pst n yr st. I ws chckng yr mssg nd I hv bkmrk yr blg dn.

    [remove the comment registration requirement, and time to first spam? Two minutes. --pzm]