Kerckring’s Ossicle

I just “discovered” something new, and thought I’d spread the knowledge.

There are tons of teeny tiny bones scattered throughout the human body, and their location and development is highly variable.  Sesamoid bones are bones which develop inside a tendon (and actually don’t have to be teeny tiny- the patella is a sesamoid bone).  Accessory ossicles result when a bone has more than one center of ossification, and they just never fused.  Whether or not the centers of ossification fuse is one source of variation.  For example, most people have a secondary center of ossification in the talus, which may either fuse to the talus, or remain separate and be called the “os trigonum.”   But another source of variation is whether or not the center develops in the first place.

Most accessory ossicles are found in the postcranium, but they may be found in the skull, too!  The occipital bone is situated at the back and bottom of your skull.  The squamus is the part at the back, that extends from the foramen magnum like a big shelf.  There are two lateral portions which lie on either side of, or lateral to, the foramen magnum. A basilar portion lies in front of the foramen magnum and is named that because it forms the base of the occipital bone- and really the entire skull!

The squamus is further divided into the occipital plane and the nuchal plane.  The occipital plane develops intramembranously, which means that it ossifies (develops into bone) directly from collagenous membranes.  There are four centers of ossification in the occipital plane.  Ossification starts at these centers, and then spreads outward until the edges all meet up and fuse.  The nuchal plane, as well as the lateral and basilar portions all develop endocondrally, which means that a little cartilage model forms first, and is then replaced by bone throughout growth and development.

Here’s the new (to me) stuff:

In humans, there are usually two centers of ossification in the nuchal plane.  They lie on either side of the sagittal midplane.  However, in some humans, a third center develops directly on the posterior margin of the foramen magnum.  This is called Kerckring’s Center, after 17th Century Dutch anatomist Theodor Kerckring, who actually discovered it (as opposed to stumbling upon one and looking it up in his anatomy book).  The center develops at around the 16th week of gestation, and can remain visible into early adulthood.

Neat!

Bones and Genes

John Hawks has a nice post reviewing a recent article (itself a review) by Adam Seipel about the estimates for the chimp-human divergence.  Most of the estimates calculated in the past 5-10 years have put the split at less than 4.5 million years ago!  My brain would like it if that date were older, but Hawks discusses the many reasons why it just can’t be.  Among them is this:

To make the date older, you need to assume there was no demography — an extreme chuman bottleneck. But that would be inconsistent with the evidence of incomplete lineage sorting — those gorilla genes that we share. And it would take some magical rate discontinuities among genetic loci to get them the amount of interlocus variability that they have.

Well, shucks.

(P.S.- If anyone could send me the Seipel paper at amodernprimate AT gmail DOT com, I’d be forever greatful!)

I have the paper now!  Thank you!

The third trochanter and gluteus maximus of Ardipithecus

The femur can be an extremely informative bone when reconstructing the locomotor behaviors of fossil primates. The head and neck are particularly informative. The morphology of the head can tell you how flexible the hip joint is. If you can get a good CT scan, the distribution of cortical bone at the neck can reflect how the primate applied force to the skeleton during locomotion. If you look to the other end of the femur, the condyles can also tell you how a primate loaded the skeleton while moving around by way of the famous bicondylar angle.

Unfortunately, none of those characters were preserved in Ardipithecus. What we do have is a shaft, and as we’ll see, the shaft can give us some information about muscle attachments- especially the ever-important gluteus maximus.

First, a little background: In great apes, the insertion for the gluteus maximus is positioned further down and toward the midline of the femur relative to what we see in humans. A different muscle, the vastus lateralis, attaches to the femur a bit further up.  The two muscle attachment sites are separated from each other by a bump called the lateral spiral pilaster.

In humans, the gluteus maximus inserts onto the lateral aspect (outer edge) of the femur.  What we see is a third, very small trochanter that is part of the greater trochanter.  Immediately below that third trochanter is a bumpy depression in the bone  (a hypotrochanteric fossa).  Both of these characters are associated with our enlarged gluteus maximus. Apes never have either of them.

I bet everyone can guess that Ardi shares a more human-like femur morhpology (why else would we be talking about it?), and indeed it does have a third trochanter, as well as the depression below it.  What is surprising is who else has similar morphological characters.  Nacholapithecus has a third trochanter, as does Dryopithecus, and even primitive Proconsul! This is in addition to Orrorin tugenensis, Australopithecus afarensis and A. anamensis.

The femora of Australopithecus afarensis (A- the "Maka" femur) and Ardipithecus ramidus (B). The arrow indicates the third trochanter and the bracket indicates the hypotrochanteric fossa. (From Lovejoy et al. 2009)

Because the back of the African, large-bodied suspensory apes has been so drastically modified since Proconsul, the gluteus maximus also had to be moved around.  The gluteus maximus insertion diverged distomedially away from the vastus lateralus, and the gap was filled in by the lateral spiral pilaster.

…In both lineages!

The gluteus maximus in humans has changed, too.  By the time we get to Australopithecus, the insertion has moved back and to the midline (posteromedially).  The authors suggests that this is because the quadriceps has gotten bigger, while the hamstrings became smaller.

Clearly, we shouldn’t draw any conclusions about bipedality in Ardi from a third trochanter and hypotrochanteric fossa if even Proconsul had similar characters.  Enlargement of the quadriceps hasn’t happened yet, but if we’ve got an animal who was participating in bipedality only some of the time, I’m not sure if we’d expect it yet.  The take-away message here is that we have yet another anatomical detail that supports the idea that humans are more primitive than chimpanzees and gorillas in many aspects.  Using chimps (or bonobos) as an analog for early human behavior- locomotor or otherwise- is becoming less and less defensible.

Lovejoy, C., Suwa, G., Spurlock, L., Asfaw, B., & White, T. (2009). The Pelvis and Femur of Ardipithecus ramidus: The Emergence of Upright Walking Science, 326 (5949), 71-71 DOI: 10.1126/science.1175831

Skepticism is good, but…

Well-informed skepticism is the best!

Earlier this week, Eric Michael Johnson drew my attention to a post by psychologist Christopher Ryan at his blog Sex At Dawn.  Ryan attacks Lovejoy’s monogamous humans model by citing many different lines of evidence.

I became so distracted by the reported testes:body mass ratio of 1/160 in humans that I couldn’t stop until I had some answers.  I am a female human, but even I thought that 1 kg of testicles would be an awful lot to lug around.  So I got out my books and my calculator and did some math, wrote in, and it was fixed.  Peer review in action!

But then I clicked through to the actual post, and realized that it didn’t get much better from there.  Apart from characterizing Ardi as mere “bits of bone,” Ryan displays many instances of ignorance.

First, a few things that Ryan gets right:

1. Yes, reduced male-male competition can happen in promiscuous mating systems (but I do think that characterizing the Chimpanzee as having reduced competition is dubious).
2. Humans are probably able to produce more sperm per ejaculate than the number that Lovejoy cites.
3. Reproductive anatomy and physiology is particularly labile, so postulating about reproductive physiology 4.4 million years ago is a risky undertaking.

But then…

Lovejoy writes that “Humans have the least complex penis morphology of any primate.” Unfortunately, he never defines what he means by “complex;” nor does he discuss the fact that the human penis is, by most measures, the longest, thickest, most prominently displayed penis among primates. No mention of the unusual flared head or the external scrotum—both strong indications of sperm competition in our species.

Lovejoy clearly states that humans lack “keratinous penile surface mechanoreceptors” (known to you and me as penis spines and ridges) and an os baculum.  So there’s your complexity.

Lovejoy also states in the footnotes:

Flaccid human penis length (13 cm) is unusually great for a hominoid. Length is ~4 cm in Pongo and 3 cm in Gorilla. Its erect size is greater in the multimale Pan (8 cm), but this reflects specialized adaptation to penetrate seminal plugs. Short notes that “(e)ven the pubic hair in the male [human] seems designed to draw attention to the genitalia, rather than to conceal them as in the orangutan and gorilla.”

Lovejoy states these things in support of a rather weird argument against hand-to-hand combat in human ancestors, but why not in the discussion of sperm competition?  Because a huge penis does nothing if you don’t have the testes to back it up!  Clearly a large, pendulous, prominently-displayed penis is something special in humans, but it is not about sperm competition. The external scrotum- by itself- may be indicative of sperm competition, but combined with the fact that human testes are smaller and have fewer seminiferous tubules, that the human sperm midpiece volume is low, and that we have lost the physiology for creating copulatory plugs indicates that there may be something else at work here.

Perhaps the most glaring mistake lies in Ryan’s argument about canine teeth:

For example, much of his thesis hinges on the absence of pronounced canines teeth (fangs) in the fossils found. He writes that we can assume that both males and females lacked these canines (even if the teeth were from a female) because “The SCC [sectorial canine complex] is not male-limited; that is, it is always expressed in both sexes of all anthropoids….” But this is wrong. Male bonobos have long canines, while females don’t (2, 3). Lovejoy also claims an association between reduced canines and pair-bonding, but as this photo of the skull of a monogamous gibbon demonstrates, even this claim is suspect.

When anthropologists refer to the canine complex, they are not merely referring to canine length.  The Sectorial Canine Complex, or the CP3 complex, or the “honing” complex all refer to the way that the top canine tooth fits in with the lower canine and premolar.  It fits in this way in order to sharpen the canine tooth so that it acts as a blade.  In contrast to what Ryan states, both male and female anthropoids (including the bonobo) WILL have this trait if it is present at all.  Yes, the tooth will be longer in males (in many cases, much longer), but the sexual dimorphism here is in size, not in the actual way that these teeth occlude.

Teeth from more than 35 individuals have been found, and not one of them exhibits this Sectorial Canine Complex, so I think it’s safe to say that Ardi and her pals didn’t have it.

And then there’s that beautiful gibbon skull.  Unfortunately, the canine monomorphism in gibbons actually supports Lovejoy’s whole thesis:  In monogamous species, the canine teeth are no longer under strict sexual selection, and natural selection can take over and do its thing.  In gibbons, this has meant that not only do males have large canines, but females have them as well.  Both males and females defend their territory, and so both have enlarged canines.  In humans, the argument is that the energy that goes into maintaining large canine teeth and getting into the fights that result when you have them could be better spent by gathering food for your partner and offspring.  As a general rule for primates, the canines don’t have to be reduced to indicate pair-bonding, but if they are the same in both sexes, something is up.

Lovejoy’s hypothesis is controversial.  It’s a Theory of Everything, and that should raise flags in everyone’s head.  But at the end of the day, it’s really stinkin’ weird that human males abandoned their canine teeth, and it’s really stinkin’ weird that human females abandoned their ovulatory advertisement.  I think monogamous pair-bonding goes further than any other hypothesis in explaining those two weirdnesses of the human.  However, my little red flag pops up when we connect those things to bipedalism.

Zingeser, M. (1969). Cercopithecoid canine tooth honing mechanisms American Journal of Physical Anthropology, 31 (2), 205-213 DOI: 10.1002/ajpa.1330310210
Lovejoy, C. (2009). Reexamining Human Origins in Light of Ardipithecus ramidus Science, 326 (5949), 74-74 DOI: 10.1126/science.1175834
Frisch, J. (1963). Sex-differences in the canines of the gibbon (Hylobates lar) Primates, 4 (2), 1-10 DOI: 10.1007/BF01659148
Leutenegger, W., & Kelly, J. (1977). Relationship of sexual dimorphism in canine size and body size to social, behavioral, and ecological correlates in anthropoid primates Primates, 18 (1), 117-136 DOI: 10.1007/BF02382954

Genital Morphology and Social System

In primates, it has been noticed that if you live in a competitive mating system and you’re a male, you’ll have a very fancy penis.  Maybe some spines, or a few ridges here and there. These embellishments are keratinous structures and act to promote rapid ejaculation, which is useful if you’ve got nine other males lining up behind you, impatiently waiting for their turn.

In fact, the argument was made in the Ardi papers that humans have rather plain penises (except for their bigness).  They have no fancy spines.  Not even an os baculum.  In fact, the only remarkable thing about the human penis is that it’s so darn big!  But humans are another story for another blog post.  This one is about Mole Rats from Africa.

Mole rats are the only mammal that can be said to have a true eusocial system- that is, there is a queen and a few reproductive males, and all of the rest of the animals are non-reproductive “subordinates.”  In the female, the vagina remains imperforate until she becomes queen, so it’s impossible for one of these subordinate gals to have a family of her own.  Instead, she takes care of her sister’s babies by going out and finding them food, or defending the colony, or whatever else it is that baby naked mole rats need to be healthy.

Geintal Morphology in male and female mole rats. Males on the left, females on the right. From top to bottom: Naked mole rats, Damaraland mole rats, and Silvery mole rats.

In the naked mole rats (and in their cousins, the Damaraland mole rats), most individuals never become reproductive.  Wouldn’t it be a waste, then, to invest in maintaining elaborate genital morphology if you’re never going to use it?

As it turns out, yes.  If you’re a male naked mole rat, you barely even have a penis at all!  Your penis is merely a “genital mound” and can barely be distinguished from the genital mounds of the females. What’s more is that on the inside, you lack the typical mammalian “penile bulb,” which is a ventral expansion of the vascularized corpus spongiosum tissue that is typical for the shaft of the penis.

If you’re a male Damarland mole rat, who is eusocial, but slightly less so than the naked mole rats (there are smaller groups, and new colonies are started more frequently), things are a little better.  Your genital mound is a little longer than those in females.  You have a penile bulb, but it’s tiny.

So there are two mole rats who are eusocial.  The Silvery mole rat is a solitary animal.  If you’re a male and you’re wandering around the African savannah and you happen to bump into a female, you take the chance to mate with her.  There’s plenty of sexual dimorphism.  Your genital mound could now be rightly called a “phallus.”  Your penile bulb is three times as large as those in your Damaraland cousins.  And the muscles that attach all of those things to you are much bigger in volume.

Even though there are only three species represented here, and only two or two and a half social systems represented, these mole rats are an interesting illustration of the correlation between genital morphology and social/mating system in mammals.

Seney, M., Kelly, D., Goldman, B., Šumbera, R., & Forger, N. (2009). Social Structure Predicts Genital Morphology in African Mole-Rats PLoS ONE, 4 (10) DOI: 10.1371/journal.pone.0007477

The feet of Ardipithecus ramidus

We’ve already covered Ardi’s hands here, so let’s move on to what is possibly the most interesting aspect of her skeleton: The feet.

As humans, we have pretty special feet. They’re good at dissipating all of the force that comes with walking on only two feet. They’re also good at propelling us forward, since we’ve lost the mechanism that most quadrupedal animals use.

Chimps and gorillas have feet that are essentially hands. Compared to animals like Proconsul, the back of the foot was shortened, and the joints were modified to allow more flexibility at the ankle joint.  They also got rid of a teeny tiny little sesamoid bone embedded in the fibularis longus tendon called the os peroneum, which acts in old world monkeys to adduct the big toe and prevent twisting and buckling of the ankle joint.  Because the great apes have gotten rid of the little bone, their tendon can now grasp with the big toe, while the plantar surface of the foot can conform to whichever substrate they choose: Tree trunk or ground.

Most humans still have the little os peroneum, or at least a cartilaginous mass in the right place.  We clearly don’t use the associated muscle to adduct our big toe since it’s permanently in-line, but fibularis longus stabilizes our longitudinal arch.  We’ve moved fibularis longus to the outside and above the position of where it is in monkeys to aid in this function, and since we don’t need it for toe adduction anymore, the little os peroneum has been allowed to become almost vestigial.

In Ardi, the big toe is opposable, and the os peroneum is big.  In contrast to both the human morphology and the great ape morphology, it is comparable in size to what is seen in many old world monkeys, and probably Proconsul as well.  The fibularis longus muscle and tendon adducted the toe and flexed the foot as in OWM, but also added just a little bit of stabilization to the area of the foot that would become the arch in later hominids.

Now, to the lateral foot.  A second metatarsal was preserved, from which we can reconstruct the plantar base.  The second metatarsal articulates with the ankle bones at the tarsometatarsal joing.  In Ardi, there are small little dents in the proximal joint surface of the second metatarsal.  The proximal joint surface second metatarsal is mostly cartilage throughout development, and as such will preserve loading patterns from that time.  The indentations probably show us that these joints were experiencing regular pressure from the joint, which would happen during bipedality.

The third metatarsal has a big “gutter” at the junction of epiphysis and physis.  This gutter reflects loading during dorsiflexion at the ankle, and again, because it is mostly cartilage during development, can preserve important information about loading patterns.  The head shows that it had been consistently rotated during development, which would have occurred during bipedality.

The talus and tibia/fibula of Ardi form an angle (measured from the talus) that is within the range of OWM.  In hominids, this angle is considerably lower because of the angle of the valgus angle of the knee.  The talus in Ardi also preserves the flexor hallucus longus groove, which is shaped like a trapezoid tipped on its side and shows that the FHL approached the talus at an angle.  This is in contrast to the condition of Lucy and other hominids, where the FHL groove is a vertical parallelogram.  This means that, while Lucy was able to keep her knee rather straight during the stance phase of walking, Ardi’s knee was probably rotating.

Ardi's foot

These features, as well as some stuff in the pelvis that we’ll get to later, suggest that when Ardi was on the ground, she placed her foot along the midline of the body, with the big toe pointing inward and the front of the foot pointing outward.  In humans, most of the body weight rotates around the ball of the foot when we “toe-off,” but in Ardi, this pivoting occurred around a diagonal line drawn through the foot, with weight balanced both by the big toe and the fibularis muscle on the lateral edge of the foot.

Much like in the hand, the foot of Ardi suggests that, instead of modifying a foot that looks essentially like a chimpanzee foot, humans, chimpanzees, and gorillas have all taken a generalized Miocene ape foot and done our own special thing to it.

Lovejoy, C., Latimer, B., Suwa, G., Asfaw, B., & White, T. (2009). Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus Science, 326 (5949), 72-72 DOI: 10.1126/science.1175832

Climbing on the branches of the family tree: The hands of Ardipithecus ramidus

As everyone has already heard by now, the long-awaited Ardipithecus ramidus has finally been published, and boy is she a beauty!  So many “anatomical surprises”! There are so many strange and new things about this skeleton that it took an entire issue of Science to describe them.  Clearly then, it will take a few blog posts.  The first post will be about the hands.  Feet will be next, and we’ll move on from there.

But first, a few basics.  The papers report on over 35 individuals represented by various parts of the body.  Lots of teeth.  They were found in Aramis, Ethiopia and date to 4.4 million years ago.  For reasons that I’ll discuss below later, we think that Ardi was a facultative biped who spent most of her time in the trees.  When she was up there, she walked above the branches with her palms and plantar surfaces in contact with the branch.

That Ardi is a palmigrade, above-the-branch walker is surprising. Based on the apes that we have around today (chimps, humans, gorillas, and orangs), most anthropologists have always constructed the common ancestor to chimps and humans as an animal who was suspensory when in the trees (that is, hanging from the branches), and a kunckle-walker when on the ground.  There have been plenty of people who have called this scenario into question (in fact, I talked about one of them here a few weeks ago), but that hasn’t stopped many anthropologists from using the chimp as an analog for what the last common ancestor roughly looked and acted like.  Ardi shows us that the LCA probably looked nothing like either the chimpanzee or the human, but was more likely a generalized Miocene ape which lacked the specializations of either.

(As an aside, I’ve seen a rather questionable quote by Owen Lovejoy mentioned a few times– something like, “Humans didn’t evolve from apes.”  It is a very unfortunate thing for him to have said from the standpoint of science journalism, but taken in the context of the 11 articles that he and the rest of the team have written, as well as numerous other quotations, he clearly means that humans didn’t evolve from anything that looks like any of the extant apes.)

Anyway, on to some anatomy!

Because the extant African apes are knuckle-walkers, they have stiff, inflexible hands and wrists that allow them to support their body weight in sort of a weird position.  Because they also have to climb trees for food and protection, their hands are very long and powerful.  Humans, on the other hand, have pretty mobile hands and wrists which allows us what we call a “power grip.” We are very good graspers, and this has allowed us to become the dextrous tool-wielders that we are.  Because of our close genetic similarity to chimps, and the close morphological similarity between chimps and gorillas, it has been argued that certain features of the Australopithecine wrist- and even the human wrist- were “hold overs” from the period of time when we, too were knuckle-walkers who required a stiff wrist and hand.

Ardi's hand. The inset includes the capitate from a chimpanzee, Ardipithecus, and a human.

However, Ardi’s hand more closely approximates the human hand than the knuckle-walker hand.  It is very flexible.  The midcarpal joint in particular is striking in its flexibility.  Ardi could lay her palms flat on the tree branch and support her entire weight this way.  In this respect, Ardi resembles many generalized Miocene apes, such as Proconsul. Because this wrist is so generalized and resembles the wrist of so many other Miocene apes, it is probably the ancestral condition.

If we look at it that way, then human hands are only moderately derived when compared to those of chimps and gorillas.  Humans don’t enjoy quite the degree of flexibility at the midcarpal joint that Ardi does, and we’ve enlarged our thumbs and shortened our fingers a little.  Chimps and gorillas both had to modify their hands substantially to be able to move around the way that they do.

[Edited to insert link and fix a typo]

Lovejoy, CO., Simpson, S., White, T., Asfaw, B., & Suwa, G. (2009). Careful Climbing in the Miocene: The Forelimbs of Ardipithecus ramidus and Humans Are Primitive Science, 326 (5949), 70-70 DOI: 10.1126/science.1175827

Breaking News!

Ardipithecus is out!

More later.

In lieu of a regular post…

You should go visit these great posts written by other people!

Sarah Blaffer Hrdy writes about How humans became such other-regarding apes.  Has anyone read Mothers and Others?  What’d you think?

Eric Michael Johnson of The Primate Diaries has written a review of Frans de Waal’s new book, The Age of Empathy.

John Hawks has some funny discussion on naughty neandertals, magical morphometrics, and also points us to some magical dead fish who can detect the emotional states of humans.

Afarensis has compiled the 76th Four Stone Hearth, which is, as always, filled with good stuff.

The Open Dinosaur Project is really cooking along!  They’ve developed quite a few measurement protocols and are probably well past 300 entries by now.  Dave Hone also initiated the Paleo Paper Challenge, urging paleontologists to publish all of those languishing papers by the end of the year.  I wish I had one to add to the list!

Giving male monkeys color vision

Color Blindness Test- can you see the number?

On the back of the retina exist two types of photoreceptor cells: The famous rods and cones.  The rods are sensitive to light and dark, while the cones are sensitive to color.  Humans, apes, and old world monkeys are all trichromats, meaning that they have three different kinds of cones.  They have cones that are sensitive to long wavelengths (L) that we see as red or yellow, cones that are sensitive to medium wavelengths (M) that we see as green, and cones that are sensitive to short wavelengths (S) that we see as blue or violet.

Some people (and, I’d assume apes and monkeys as well) have recessive allele at the locus responsible for either L or M cones.  The recessive allele results in the photopigment in the cones not being expressed, meaning that the person is red-green color blind. The locus of interest happens to be on the X chromosome, which means that males are much more likely to express a recessive allele since they only have one copy of the X chromosome.  My father, for instance, is red-green color blind.  He passed this allele on to me, his daughter.  But luckily for me, my mother has two normal copies of the allele and gave me one of them, so I can see all the colors of the rainbow.  (Or, at least, all the ones that humans can normally see….)

New World Monkeys are very interesting with regard to their color vision.  There is only one gene locus for color vision in most NWM, and it’s on the X chromosome.  The gene allows for different kinds of color vision, but the only way to be a trichromat is to be a female who is heterozygous at this locus.  Males are always red-green color blind.

Until now!

Katherine Manusco and her colleagues injected a virus containing the L gene into the eyes of male spider monkeys and subjected them to behavioral tests of spectral sensitivity both before and after the treatment.  The results indicated that the monkeys could, indeed see more colors after treatment.  A subset of the M cones began to co-express both the L and M photopigments, which allowed them to detect longer wavelengths.

This is pretty exciting stuff, because these were adult monkeys who already had their brain circuitry all set.  There was no new “wiring” that had to be “installed,” other than switching the cones from M to L.  It’s exciting to me personally because my dad’s color blindness has always broken my heart.  Even when I was small, I remember feeling so bad that he couldn’t tell the difference between the red Sorry! piece and the green one and would occasionally grab the wrong one.  Of course, I know that a clinical treatment for humans is years and years and years away, but it’s very exciting to think that such a treatment could exist within my lifetime.