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

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!

What do beetles, cuttlefish, and orangutans all have in common?

Alternative mating strategies!

When we learn about sexual selection theory, we usually learn about it as a binary system:  Females choose males, and males try to be chosen. Female peahens choose male peacocks with the most and prettiest eyespots because it’s an indicator of their health, and she wants healthy offspring.  Female deer choose bucks who are able to fight and win against other bucks because it means that her offspring will be better fighters.  Male gorillas fight other male gorillas for the opportunity to rule over a harem of females, and females go along with it because the male is probably a good protector.

Look at this beautiful, flanged male!

But sometimes, even the small males who don’t stand a chance in direct competition get to mate.  As an anthropologist, one of the most obvious examples is the orangutan.  Male orangutans come in two different morphs:  Flanged and unflanged.  The unflanged males look a lot like female orangs or immature males in their facial characteristics.  The flanged males, on the other hand, develop a huge set of secondary sexual characteristics once they reach puberty.  Their cheecks swell out to form the eponymous flange.  Their body hair becomes long.  They form a throat pouch which allows them to make low, loud calls called long-calls because they travel over long distances.  Those long-calls are used to communicate with other orangutans.  They either say, “Stay away, I’m a big mature male!” to other males, or “Come here, I’m a big mature male!” to receptive females.  Hence, primatologists call their mating strategy the “call and wait” strategy.  These guys can successfully defend a territory from other males through fighting, and that makes them highly desirable to females looking to have healthy, fit offspring.

The unflanged males may eventually develop into flanged males.  In captivity, they all do.  Nobody’s really sure why, but they think it may have something to do with those long-calls.  The hyopthesis says that if there is a male in the area making those long-calls, the unflanged male will suppress his development.  He’ll only continue developing once the he starts to hear fewer long-calls in his area, meaning that there are fewer flanged males around, and he has a greater chance of becoming a dominant, territory-defending male.  The unflanged males do have lower levels of certain hormones than the flanged males (testosterone and luteinizing hormone), but levels are sufficient so that they are indeed sexually mature.

There must be some sort of cost associated with being a flanged male, or else everyone would do it.  Observers have reported that, while flanged males often engage in heavy fighting with high rates of injury, unflanged males rarely fight, so fighting could be one cost.  Another could be that, in an area of the world where there really isn’t that much food for large-bodied apes, maintainging gigantic cheek flanges and large body size is just too calorically expensive.  You’d only want to develop fully if you could ensure that the females around would choose you to be their mate.  So, you’d wait around in your small, feminine body  until the other guys die or leave, and then half the battle would already be won!

So we’ve established that the flanged guys are more attractive to females than their unflanged counterparts, so we’d expect a majority of the offspring to be sired by these flanged males, right?  Well, that’s what I’d expect, but it turns out not to be true!  Unflanged and flanged males have very similar reproductive success!  It turns out that these unflanged males have adopted a different strategy, called the “sneak and rape” strategy.  Flanged males can’t really tell if the unflanged males are males or females, so they don’t attack them if they’re in their territory.  The hypothesis here is that orangutans evolved from a gorilla-like social system, where one dominant, flanged male ruled the roost.  During the Miocene, the rainforests of Southeastern Asia dried up, leaving their habitat more fragmented, and their food more dispersed. It became necessary for the orangs to spend a lot of their time as solitary creatures because the forests simply couldn’t support large groups of large primates all eating in the same place at the same time.  Becuase females spend so much time alone and unprotected by the dominant male, it became a worthwhile strategy for the subordinate males to find these solitary females and force copulations with them.

In the primatology world, we think, “Oh man!  Those orangutans are crazy, with their alternative mating strategies!”  because it’s pretty rare for primates with alternative strategies to be almost as successful as the dominant, normal-strategy males.  Sure, we may get a few sneak copulations here and there so that the dominant male has fathered only 50% of the offspring in a group.  But the other 50% is split amongst 7 or 8 or even 12 other males.  In orangs, dominant males father about 50% of the offspring, and the rest are split between 2-4 other males (Caveat:  This research is based on a necessarily low sample size, so take it with the appropriately sized grain of salt).  But anyway, we primatologists think this is weird.

But it’s really not all that strange!  Animals from pretty much every single taxa on earth do this!  Male dung beetles will sit at the opening of a burrow with a female inside, defending it from other males.  Sometimes a male will come along and pick a fight with that male, and if he’s a formiddable opponent, he may win.  But other times, a male knows he can’t win, so he just makes another burrow, bypassing the fight at the opening and sneaking down to mate with the female.

Male horseshoe crabs cling to the backs of their mates so that when she lays her eggs, they can immediately fertilize them.  Older, larger horseshoe crabs have a hard time clinging on to the females, so they just wait on the beach for a mating pair to arrive.  Once they do, he scurries over and tries to fertilize their eggs at the same time.  Sometimes it works, sometimes it doesn’t.

And the coolest example, in my opinion, is in cuttlefish.  Giant Cuttlefish males court females by producing an elaborate courtship display consisting of dark zebra-type stripes which flicker and flash across the mantle.  Sometimes males will get into display fights with each other, which may eventually escalate into physical combat!  At the same time, the female display is a white background with brownish blotches.  After mating, the female lays eggs by passing them through the sperm pouch that the male has given her, and the male sticks around to make sure that all the eggs that she lays are fertilized by his sperm pouch and no one else’s.  Males who know that they can’t win in display or physical combat will sometimes display the brown and white pattern of the female while two other males are display fighting over a female.  This allows him to get close to the female and slip her a sperm sac while the other guys are fighting!  He cross-dresses in order to mate successfully!  Watch it on NOVA, if you get a chance.

It all makes such wonderful sense.  In a world where mating is usually status-dependent, and you are low-status, you aren’t going to be able to mate unless you can excel at something that isn’t status-dependent.  Any old beetle can dig a burrow, and any old cuttlefish can make a mottled brown pattern.  If you can’t beat a high-status male at his own game, you’ve got to find a way around the game.  If you can’t beat him, cheat him!

Those of us who study primates  and humans are often sequestered away in anthropology departments, which is really an artifact of our historical development than a useful distinction.  Biological anthropologists are just biologists who study a specific group of animals, just like the cuttlefish biologists and entomologists.  When I read about things like this in other animals, which are so incredibly pertinent to the field of primatology, it makes me wish that I could spend more time with other biologists, taking classes in marine biology or insect sociality instead of archaeology and cultural anthropology.  Harumph.

Mark D. Norman, Julian Finn, & Tom Tregenza (1999). Female impersonation as an alternative reproductive strategy in giant cuttlefish Proceedings of the Royal Society B, 266, 1347-1349
HARRISON, M., & CHIVERS, D. (2007). The orang-utan mating system and the unflanged male: A product of increased food stress during the late Miocene and Pliocene? Journal of Human Evolution, 52 (3), 275-293 DOI: 10.1016/j.jhevol.2006.09.005
Hunt, J., & Simmons, L. (2001). Status-dependent selection in the dimorphic beetle Onthophagus taurus Proceedings: Biological Sciences, 268 (1484), 2409-2414 DOI: 10.1098/rspb.2001.1758

Bats in my house!

Last night, I was sleeping soundly.  I don’t have AC, so the windows were open and my ceiling fan was on.  I woke up rather suddenly, and it took me a minute to realize that there was something else in my room… something really flappy and kind of loud.  A bat!

I’m doing some work with bats for my thesis, so even in my sleepy stupor, I was thrilled!  A real live bat!  In my house!  I watched him for about 30 seconds to a minute, but then I realized that the little guy or gal was distressed.  Here it was in a room with walls and a ceiling fan, when probably 5 minutes earlier it had been swooping around catching bugs in the meadow out front.  It wasn’t having any luck with the lights off, so I turned them on and closed all of the doors upstairs.  We made our way downstairs together, where I opened the door and waited for it to leave.  It swooped around my living room for awhile, always on the diagonal.  Just when I thought I was going to have to help it out somehow, it made a sharp 90 degree turn at the door and left.

In celebration of my little visitor, I’ll share with you some interesting sexual selection stuff related to bats.  I’m sure you’ve heard about the paper about the Tiger Moths who respond to the sonar of bats by emitting their own clicks, jamming up the bat’s detection.  Well, it turns out that some other species of moths are able to use these clicks to communicate with moths of the opposite sex.  It’s a form of sensory bias in sexual selection.  Sensory bias and exploitation is an hypothesis which explains the origins of some of the features which are sexually selected for in animals.  In Wax moths, the females already have the equipment to sense the ultrasonic clicks because they are predated upon by bats.  Natural selection has resulted in a moth which is able to detect the bat clicks, so males who are able to exploit that suite of sensory mechanisms are able to mate more successfully.

In one species of moth, the response to the clicks emitted by bats is to stop flying and fall out of the sky- a sort of self-paralyzing strategy.  The males emit the clicks, the females fall out of the sky, and copulation begins!

We see sensory bias and exploitation in lots of other animals, too.  Some populations of guppies in Trinidad like to eat bright orange fruit from the Cabrehash tree.  Females have been shown to prefer orange objects to non-orange objects, so males who have a bright orange dot on their tails are able to successfully mate with females more often than other males.  The interesting thing is that females prefer orange objects even in populations where the males don’t have the dot yet, suggesting that the preference for orange is a pre-existing bias which the males in the other population was able to exploit. Sensory bias and exploitation work has been done with frogs, fish, water mites, moths, and even cotton top tamarins. It’s an interesting field, and I will probably be writing about it more soon!

Ryan, M. (1998). Sexual Selection, Receiver Biases, and the Evolution of Sex Differences Science, 281 (5385), 1999-2003 DOI: 10.1126/science.281.5385.1999
Rodd, F., Hughes, K., Grether, G., & Baril, C. (2002). A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proceedings of the Royal Society B: Biological Sciences, 269 (1490), 475-481 DOI: 10.1098/rspb.2001.1891

Dinosaur Dads

A male ostrich with chicks. Art Wolfe- Stone/Getty Images

90% of bird species today receive care from their fathers.  This care can be the result of a two-parent model, with both mother and father contributing food and care to the offspring, or it can be the result of a father-only model.  When rare, seemingly disadvantageous strategies like this are adopted by so many species, it is probably wise to look for an adaptive reason for that behavior.  In the case of paternal care for offspring, the adaptation is for increased parental care of the young.  Instead of spreading their genetic material around, the male will invest in one set of his genetic material in order to insure that they survive into adulthood, hopefully to pass on his genes to subsequent generations.  It is the “quality over quantity” approach to parenthood.  So, when did this behavioral trait evolve?

One of the phrases that I find myself repeating a lot is “behavior doesn’t fossilize.”  It doesn’t, but sometimes there are clues in the biology that do fossilize, and can allow us to infer certain aspects of behavior.  Two clues that we can look at with regard to parental behavior in the ancestors of modern birds is the size of the clutches, and the structure of maternal bone.  A single clutch of eggs is usually laid over a period of time instead of contemporaneously.  A female can lay more or bigger eggs if she is allowed to go out and hunt and obtain nutrition than if she is stuck next to the clutch guarding her eggs.  We can look at the size of a clutch of eggs compared with adult body mass to see if the mother was more likely to be the brooding parent, or if she left the care of eggs with the father.  In extant crocodiles, the mother alone is responsible for protecting the eggs.  In one clade of modern birds, the neognathes (ducks, geese, finches, etc.), a two-parent model predominates.  In the other modern bird clade, the paleognathes (ostriches, emus, kiwis), paternal care is the predominant mode.

David Varricchio and his colleagues examined specimens of three different species of theropod dinosaurs to see what kinds of patterns were visible.  In these species, belonging to the geni Troodon, Oviraptor, and Citipati, adults have been found in association with nests.  The nests contained between 22-30 eggs each, and when compared with the clutch size/body mass ratio of 433 extant animals, matched most closely with modern birds exhibiting paternal care.

In order to form an eggshell and fetal skeleteon, females of many species have to extract phosphorus and calcium from their own skeletons.  Most of this bone comes from the inside of the long bones, next to the long, hollow medullary cavity where bone marrow is stored.  When this resorption happens, it leaves scars in the bone that can be observed when the bone is seen in cross-section.  Varricchio and his colleagues looked at cross-sections of the long bones of the dinosaurs found in association with the nests, and observed very little evidence of remodeling or resporption, indicating that these skeletons were not the ones who had laid the eggs.

This is a rather clever way to observe behavior in fossil species.  The clutch size/body mass ratio is consistent with birds that offer paternal care, like ostriches and rheas, and the bone histology is consistent with paternal care as well.  The authors suggest that this type of reproductive strategy may have evolved concurrently with larger eggs that were laid sequentially instead of all at once, along with the increased thermal needs that such large eggs would require.  By allowing the female to focus on her nutritional needs, the father ensures that his eggs will be bigger and his offspring stronger.  Paternal-only care in birds is thus the ancestral condition, with two-parent and maternal care being secondarily derived.

Citation:

Avian Paternal Care Had Dinosaur Origin. David J. Varricchio, Jason R. Moore, Gregory M. Erickson, Mark A. Norell, Frankie D. Jackson, and John J. Borkowski (19 December 2008)

Science 322 (5909), 1826. [DOI: 10.1126/science.1163245]