Wednesday, February 13, 2008

A Tyrannical Romance

By Olivia Judson

Olivia Judson's The Wild Side Blog
(Credit: Charles Rex Arbogast,
Associated Press)

If Charles Darwin were alive today, he’d be turning 199: like Abraham Lincoln, he was born on Feb. 12 1809.

I considered observing their joint birthday with a discussion of slave making in ants, but rejected that idea in favor of another. For later this week is another Big Day: the feast of St. Valentine. With apologies to Lincoln, I’ve decided to hold a Darwin-Valentine celebration by revealing one of my more tyrannical romantic fantasies.

I should say, by way of preamble, that Darwin contributed far more to biology than the “Origin of Species,” in which he laid out how evolution by natural selection works, and the evidence for it at the time. He also wrote (and this list is not complete): a treatise on the formation of coral reefs, which is still held to be correct; a landmark work on carnivorous plants; a definitive treatise on barnacles, extinct and extant; a study of how earthworms plow and aerate soil; and a fascinating speculation on the evolution of emotion in humans and other animals.

And that’s not all. One of his other major works, “The Descent of Man, and Selection in Relation to Sex,” includes a huge compilation of the sexual decorations and displays of animals, from the jaws of stag-beetles to the tail of the Argus pheasant, which far exceeds that of the peacock in absurd magnificence. From his study of all this, Darwin began to elucidate systematic patterns and principles of the evolution of courtship and sexual behavior. In particular, he developed the concept of sexual selection, which is the idea that cumbersome ornaments like big tails can evolve, even if they make the bearer less likely to survive, if the opposite sex (usually the female) finds them attractive.

In doing so, he founded one of the most important and successful branches of evolutionary research. We now have a robust understanding of how sexual pressures — the pressures to find, impress, and seduce a mate — influence the evolution of males and females. So much so that if you tell me a fact, such as the average size difference between males and females in a species, or the proportion of a male’s body taken up by his testes, I can tell you what the mating system is likely to be. For example, where males are much bigger than females, fighting between males has been important — which often means that the biggest males maintain a harem. If testes are relatively large, females probably have sex with several males in the course of a single breeding episode.

These forces are so reliable that, if only we could determine the sex of dinosaur fossils, we could begin to infer their mating habits. But alas. Unless the animal died while heavy with eggs, as one oviraptor obligingly did, determining the sex of a dinosaur is close to impossible. At one point, it was thought that the shape of a particular bone at the base of the tail might indicate sex; but a recent analysis has shown it does not. Now the best guesses come from subtle differences in structure of the bone in the hind legs. For the time being, then, fossils are stonily silent about the dinosaurs’ private lives, their methods of wooing, the exuberance of their song-and-dance routines.

Which brings me to my tyrannical fantasy. I want to take a journey 68 million years back in time to see a Tyrannosaurus rex couple mating. What was it like? Did they trumpet and bellow and stamp their feet? Did they thrash their enormous tails? Did he bite her neck in rapture and exude a musky scent? Somehow, I imagine that when two T. rex got it on, the earth shook for miles around.

And if I could only take this journey, I could answer a question that sometimes bothers me. Did T. rex have a penis? Did he even, as lizards do, have two?

I ask the question not out of prurience, but because it’s a matter of scientific interest. There are a couple of reasons why. First, the penis is another important indicator of the mating system. In species where females usually mate with a single male during a breeding episode, penises tend to be small and uninteresting. In those where females mate with several males (whether by choice or by force), penises are typically larger, and come with fancy decorations such as grooves, nobbles, and spikes. Second, the question of the dinosaur penis provides an exercise in evolutionary inference.

The reason we don’t know whether T. rex had one is that the organ is generally too soft to leave a fossil trace. (There’s an exception to this: some mammals have a bone in their penis, the os penis or baculum. This can fossilize. Humans are unusual among primates in not having one; in case you’re wondering, it’s not clear whether the bone plays a role in maintaining erections.)

Moreover, whether a male has a penis at all varies from one group to the next. Male salamanders, for instance, don’t: they deposit sperm on the ground and the female collects it. Among birds, penises are rare: ostriches, emus, ducks, geese and swans are among the few. The rest just have a cloaca — an all-purpose opening also used for urination, defecation and, in the female, laying eggs. To copulate, two birds bring their cloacae together in what’s called a cloacal kiss.

So what can we say about dinosaurs? My guess is that the males had members — but it’s an educated guess. It’s based on an analysis of dinosaur relations.

Two living groups are most closely related to dinosaurs. One is the crocodiles. Male crocodiles have a penis — just one — which, most of the time, they keep tucked inside their cloacae. (In most species of crocodile, it’s hard to determine the sex of living animals without an intimate exam, never mind dead ones.) Compared with the mammalian penis, the crocodile’s has an oddity: sperm is transported along an external groove, rather than through an internal tube.

The other group related to dinosaurs is the birds. Indeed, to be strict about it, birds are dinosaurs. If you look at a family tree of dinosaurs, birds, and other reptiles, you see that the lineage that evolved into dinosaurs split off from the lineage that evolved into crocodiles. Birds, in contrast, evolved directly from a dinosaur lineage. Birds are more closely related to T. rex than they are to any living form.

Birds themselves divide into two main groups, formally known as the palaeognathous and the neognathous. The palaeos comprises the big flightless birds such as ostriches, emus, rheas, and cassowaries, as well as kiwis and an obscure (but flying) group of south American birds, the tinamous; the neos covers everything else. The palaeos have penises; like crocodiles, they keep them tucked into their cloacae. Again like crocodiles, the organ has an external groove for sperm. What’s more, the lineage leading to the other endowed birds, the ducks, geese, and swans, appears to have split off from that of the other neos relatively early.

This strongly suggests that the ancestor of all birds had a penis, and that at some point early in the evolution of the neognathous birds, the penis got lost. Since crocodiles have one, and ancestral birds almost certainly did, and since the two groups have such similar genital morphology, I think it’s a safe bet that the lineages between crocodiles and birds — that is, dinosaurs — had one, too.

Now, the next question — what did it look like? Was it large or small? Fancy or plain? I wouldn’t like to guess. The blue-billed duck (Oxyura australis) is just a little fellow — he weighs less than one kilogram (two pounds) — but his penis measures 28.5 centimeters (11 inches), and it’s covered with knobs. In contrast, the mighty ostrich (Struthio camelus), which can weigh as much as 160 kilograms (350 pounds), has a penis that’s a mere 20 centimeters (8 inches) long. But at least it’s bright red.

If I only had that time machine . . .



The text of The Descent of Man, and Selection in Relation to Sex, along with many of Darwin’s other works, is available from Project Gutenberg.

The relationship between male body size and fighting, and between relative testes size, penis morphology, and female mating patterns, is well known and can be found in any recent book on animal sexual behaviour, including my own (see chapters 1, 2 and 4, and the references therein).

For difficulties in sexing dinosaurs, and for the uselessness of the bones at the base of the tail, see Erickson, G. M., Lappin, A. K., and Larson, P. 2005. “Androgynous rex — the utility of chevrons for determining the sex of crocodilians and non-avian dinosaurs.” Zoology 108: 277-286. For a female dinosaur heavy with eggs, see Sato, T., Cheng, Y-N., Wu, X-C., Zelenitsky, D. K., and Hsiao, Y-F. 2005. “A pair of shelled eggs inside a female dinosaur.” Science 308: 375. For a method of sexing dinosaurs through differences in legbone structure, see Schweitzer, M. H., Wittmeyer, J. L., and Horner, J. R. 2005. “Gender-specific reproductive tissue in ratites and Tyrannosaurus rex.” Science 308: 1456-1460.

The relationships between crocodiles, birds, and dinosaurs are well known; but see, for example, Padian, K., de Ricqlès, A. J., and Horner, J. R. 2001. “Dinosaurian growth rates and bird origins.” Nature 412: 405-408. For ducks, geese, and swans having an early split from the other neognathous birds, see Livezey, B. C., and Zusi, R. L. 2007. “Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and Discussion.” Zoological Journal of the Linnean Society 149: 1-95.

For the penis of crocodiles see the extended version of: Ziegler, T. and Olbort, S. 2007. “Genital Structures and Sex Identification in Crocodiles.” Crocodile Specialist Group Newsletter 26:16-17. For the distribution of the penis in birds, for a description of its structure, and for the measurements of various ducks, see Coker, C. R., McKinney, F., Hays, H., Briggs, S., and Cheng, K. M. 2002. “Intromittent organ morphology and testis size in relation to mating system in waterfowl.” The Auk 119: 403-413.

Author notes:

Olivia Judson's The Wild Side Blog

Olivia Judson, an evolutionary biologist, is the author of “Dr. Tatiana’s Sex Advice to All Creation: The Definitive Guide to the Evolutionary Biology of Sex,” which was made into a three-part television program. Ms. Judson has been a reporter for The Economist and has written for a number of other publications, including Nature, The Financial Times, The Atlantic and Natural History. She is a research fellow in biology at Imperial College London.

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