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.

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, 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.

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.

Monogamy in Voles

Part of being an anthropologist is trying to figure out what exactly it is about humans that makes us unique.  Clearly we do some pretty neat tricks, but we have to go a little beyond “humans are the only animal that can make pesto.”

Many people have noticed that humans are more often monogamous than their ape relatives.  Sometimes we’re polygynous, too.  It’s hard to figure out what exactly the ancestral condition is for humans because we’ve got all of that culture mucking up the picture a bit, but a few of our special features make sense in light of monogamy.  In particular,  hidden ovulation encourages men to cooperate with us, because we look like we’re perpetually lactating.  The guy who risks it and copulates with a woman even though she looks like she’s already lactating will be more likely to father an offspring if she’s not actually lactating.  Now, how might such a seemingly counter-productive strategy evolve?  Well, to figure this out, we might have to look past some of our “uniqueness” as monogamous, intelligent animals in order to find some sort of analog.

Enter the humble vole.  Now, there are montane voles, who are like the chimpanzees of voles.  They mate with whomever is receptive, whenever they want.  And then, there are the prairie voles.  Prairie voles are extremely monogamous.  And we’re not just talking behavioral, pair-bonding monogamy that may or may not include a few extra-pair copulations here and there.  In prairie voles, the male is literally addicted to his female partner and wouldn’t dream of copulating with any other female.

Both of these voles produce the hormones oxytocin and vasopressin, and in similar amounts.  Oxytocin is a good hormone to have.  It downregulates stress hormones like cortisol, and might play some role in telling one person apart from another.  It might be the hormone that encourages you to hold the door open for people right after you meet a pretty girl, or maybe it helps you tell the difference between the two men with brown hair, a beard, and the name “Ted.”  Vasopressin, on the other hand, is usually associated with territoriality and aggression.  The two hormones are exactly identical, except for two little amino acids.

When our little voles first meet other little voles of the opposite sex, they sniff each other out to make sure they aren’t related, and if everything checks out, they mate for the next 24 hours.  During this time, tons of oxytocin is released.  Now- and here’s the tricky part- in our montane voles, much of that oxytocin goes unnoticed.  They meet, they mate, and it feels pretty good.  But after they’re done, they leave.   In prairie voles, a certain part of the brain is peppered with receptors for oxytocin so that it hits, and it hits hard.  It feels good, but that goodness is associated with this particular mate because it’s oxytocin and that’s in charge of their social memory.  And it’s the same with vasopressin:  In montane voles, most of it goes to waste, while in prairie voles, every last molecule is sucked up by receptors in the brain.    Both of these hormones set up a reward pathway in the little prairie vole so that the pair literally becomes addicted to each other.  They spend the rest of their lives raising their young together, defending their territory from dangerous invaders, and copulating like small little mammals are wont to do.

So what can these little love addicts tell us about human evolution?  Perhaps nothing, but perhaps studying these little voles can help us understand why we go back to that ex, even though we know that he’s bad news.  Maybe they can tell us why that first proto-hominid mated with that female with pendulous breasts, even though it went against that deeply engrained, 400 million-year-old urge to spread his seed around a little more.

I guess we’ll just have to wait and see!

Spatial packing of the skull

So, the academic year is in full swing and I. am. swamped.  Between taking classes, teaching classes, and beginning a new gig in a genetics lab, I barely have enough time left over to eat, let alone blog!  I had grand designs of blogging the papers that I’ve been reading for various classes and journal clubs, but by the time I get the paper read, highlighted and underlined, I have three more piling up.  And then, there is the research I need to do for my thesis!

At any rate, I have a few moments today, and I want to talk about spatial packing in the cranium.  Most anatomists divide the cranium up into three major modules:  First, the neurocranium- the big, vaulted area of the skull that sits on top of the brain.  Second is the face (a term we should all recognize).  Lastly, there is the basicranium, which is, in simplified terms, the bottom of the skull.  The basicranium is interesting because developmentally, it forms in a similar manner to bones like the radius and femur.  A cartilage model forms, and is then replaced by bone.  The basicranium has a number of immobile joints called synchondroses, and these continue to ossify after the original cartilage model is fully replaced.

The basicranium is even more interesting because of its centralized placement in the skull.  The brain grows on top of the basicranium, while the face grows underneath or lateral to it.  Because the skull is such a highly integrated part of the body, what happens to the brain affects what happens to the basicranium, which affects what happens to the face- and vice versa.

That brings us to the idea of spatial packing.  If the brain expands, it needs room in which to expand.  This can be accomplished by simply making the cranial base larger.  OR, you can put a little kink in it so that it folds down.  Then you’ve got a lot more surface area, and you can get a bigger volume of brain as well.

Putting a bend in the cranial base also sets up a situation in which the brain can become more of a sphere.  In a sphere, the length of different connections in different parts of the brain is shortened.  Putting a little bend in the angle of the brain sets the stage for a big, efficiently-connected brain.

And what about the face?  If you want a big face, the basicranium will straighten out, perhaps because if it doesn’t, you may shut off your pharynx.  Or perhaps because your head has to balance on the vertebral column.

Stephen Jay Gould made an argument for spatial packing as part of his infamous “humans are paedomorphic” argument because baby apes are born with a highly flexed basicranium, which then straightens out a little during ontogeny.  Humans retain the flexed basicranium into adulthood.  It may not be because of paedomorphy, but it does support the idea that larger brains relative to body size are correlated with a flexed basicranium.  Baby apes are born with relatively larger brains, with which their body must later catch up.

Okay, now let’s think about fossils.  Lots of times, anthropologists like to say that a particular fossil is bipedal because of the position of the foramen magnum (which is related to basicranial flexion).  In fact, Raymond Dart discovered the first Australopithecine and proclaimed it a hominid because of precisely that feature.  The Taung child has been vindicated, but is the foramen magnum really such a great marker of bipedality?  There are plenty of Australopithecus skulls out there.  Most of them have brains that are a little larger than a chimp’s, and all of them walk bipedally.  Where they are particularly variable is in the face.  The robust species (A. garhi, A. boisei), who have very robust, but very  short faces, have cranial bases which are awfully flexed.  The gracile species (A. afarensis, etc) are somewhat intermediate between chimps and humans.  Even when we compare Neandertals to modern humans, we find that modern humans have cranial bases which are more flexed- again, probably because of the interaction between brain size and face size.

Open Dinosaurs!

Apropos of the discussion that we’ve been having lately about paleo-databases, data sharing, etc, the fellas over at SV-POW and the Open Source Paleontologist have announced that they are creating The Open Dinsoaur Project.

From the blog:

We want to put together a paper on the multiple independent transitions from bipedality to quadrupedality in ornithischians, and we want to involve everyone who’s interested in helping out.  We’ll get to the details later, but the basic idea is to amass a huge database of measurements of the limb bones of ornithischian dinosaurs, to which we can apply various statistical techniques.  Hopefully we’ll figure out how these transitions happened — for example, whether ceratopsians, thyreophorans and ornithopods all made it in the same way or differently.

Sounds like a very neat project.  I wonder if we paleoanthropologists could ever make something like that happen?