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Will we ever find mating dinosaurs? No one knows, but the discovery of fossils showing dinosaur behavior—such as this nesting oviraptorosaur—hint that we may someday find dinosaur sex set in stone. Photo by Steve Starer, image from Wikipedia.

Earlier this month, I wrote a short article for Nature News about 47-million-year-old turtles that died at a very inopportune moment. Several pairs of prehistoric turtle were fossilized in the act of mating—the tragic consequence of sinking to the toxic depths of a prehistoric lake. An unfortunate fate for the reptiles, but a boon for the paleontologists who found the sexy fossils.

The discovery got me thinking about dinosaur sex. I’ve written quite a bit about the topic before—I ran a four-part series on what we know about dinosaur nooky earlier this year—but much of what we know about dinosaur reproduction only outlines the mating habits of Apatosaurus and company. There’s still a lot we don’t know. In fact, some of the most basic questions are the most persistent. What, exactly, “dinosaur style” looked like has been a subject of frequent speculation but very little rigorous research, and no dinosaurs have ever been found fossilized in the act to show us how it was done. But does this mean that we’ll never find dinosaur sex preserved in stone?

Copulation is typically a brief moment in time. For such an intimate snapshot to become part of the fossil record, exceptional circumstances are required. In the case of 320-million-year-old sharks preserved in what may be part of a mating ritual, a quick death and rapid burial in fine-grained sediment locked the fishy forms in rock. We also know a little about how prehistoric insects reproduced thanks to mating pairs trapped in amber. And as for the turtles, the copulating reptiles drifted down to a layer of water that not only killed them, but kept their bodies safe from scavengers as sediment settled on their bodies. For sex to make it into the fossil record, a quick death, rapid burial and high-definition preservation are all required.

Given these conditions, I’m not very hopeful that paleontologists are going to find mating dinosaurs. Even the smallest dinosaurs were too big to be trapped in amber, and as fully-terrestrial animals, dinosaurs did not copulate in the sort of aquatic environment where fast death and burial would have been possible. Dinosaurs just didn’t mate in the kind of habitats where there was a high potential for the amorous pairs to perish and be entombed in sediment. Good news for them, but frustrating for paleontologists.

Still, I shouldn’t be too hasty in saying that we’ll never find mating dinosaurs. I never expected that paleontologists would discover turtles caught in the act, for one thing. And the fossil record is full of surprises, including fossils that detail some aspects of dinosaur behavior. Paleontologists have previously discovered dinosaurs preserved in nesting and sleeping positions, and there’s the fighting dinosaur pair. Maybe someday a fortunate paleontologist will help us solve the prehistoric mating mystery by finding dinosaurs that made love, not war.

A pair of Tyrannosaurus restored in the act at Spain’s Jurassic Museum of Asturias. Photo by Mario Modesto, from Wikipedia.

Over the past few days I have written about the dinosaurian Kama Sutra, the idea that sauropods had sexy necks, and how to sex a Tyrannosaurus rex (Answer: very carefully). But there is one topic that I have saved for last: what the Tab A, Slot B reproductive anatomy of dinosaurs actually looked like.

Whenever I bring up dinosaur sex in conversation—which is probably far too often—questions about the anatomy of the dinosaurian penis arise almost immediately. I am not sure why this is. Maybe it’s because we expect such impressive, terrifying creatures to have equally scary gonads. Few things would be better nightmare fuel. Whatever the reason for this interest, though, the sad truth is that we don’t know very much about the reproductive organs of male dinosaurs. No one has yet found a fossilized impression or other vestige of a non-avian dinosaur’s penis, a discovery that would have a good shot at the cover of Nature or Science. Instead, restoring a dinosaur’s delicate bits requires some evolutionary context.

Male dinosaurs must have had the equipment for internal fertilization. This was a mode of reproduction passed on by their ancient ancestors. Around 375 million years ago, the first vertebrates with limbs, the early tetrapods, began to crawl along the water’s edge. These amphibious creatures had to stay wet to survive, and like their fish ancestors, they reproduced in the water. Females probably laid soft eggs in aquatic cradles and males squirted sperm over the egg clusters to fertilize them. By about 315 million years ago, however, the early radiation of amphibious vertebrates had produced a lineage of creatures capable of reproducing away from the water. These lizard-like animals, akin to Hylonomus from the Carboniferous strata of Nova Scotia, laid eggs that encompassed an internal pond surrounded by membranes and a tough outer shell. This was the amniotic egg—one of the most important evolutionary innovations of all time. But males could no longer fertilize eggs by excreting sperm over egg clusters in the water. Egg-laying on land required internal fertilization before the female deposited her eggs. All descendants of these creatures, from the dinosaurs to creatures that carry offspring inside the body (placental mammals like humans), continued this tradition.

A different set of evolutionary brackets is needed to narrow down what a dinosaurian penis might have looked like. Birds are living dinosaur descendants, and crocodylians are  the closest living relatives to dinosaurs as a group, and so we can expect that features shared between birds and crocodylians were also present in dinosaurs. One such trait is a cloaca. This charming-sounding orifice, from the Latin word for “sewer”, is the common opening for the reproductive, urinary and intestinal tracts in birds and crocodylians of both sexes. Dinosaurs almost certainly had cloacae, too, and this means that the genitals of Stegosaurus, Deinonychus, Argentinosaurus and all other dinosaurs were hidden away internally. You wouldn’t be able to watch Allosaurus walk by and see anything swinging around.

And that brings us to the thrilling details of size and shape. The difficulty is that, according to a 2006 estimate by Steve Wang and Peter Dodson, there may have been more than 1,850 genera of dinosaurs during a span of more than 150 million years. Almost any generalization about dinosaur sex organs is going to be wrong in some respect, and looking for modern analogs is a complicated task. If we look to modern avian dinosaurs for hints, we are met with a bizarre array of reproductive organs and strategies. Males of most bird species don’t have a penis at all and pass genetic material to females through a brief encounter given the cringe-inducing term “cloacal kiss.” Then again, the Argentine lake duck Oxyura vittata has the longest penis in relation to body length of any known vertebrate, and ducks in general have become infamous for having bizarre sex organs that have a lock-and-key arrangement. In general, though, it seems that the presence of a penis in male birds is the ancestral state, and that the loss of a penis is an evolutionary specialization.

Things are not so varied on the other branch of our evolutionary bracket. Male crocodylians have relatively small penises. This condition, combined with the fact that a penis seems to be the archaic state for male birds, means that male dinosaurs probably had penises as well. As paleontologist Kenneth Carpenter colorfully described, “[A]ssuming you were stupid enough to sneak up under a T. rex and pull the cloaca open, the last thing you would ever see during the last moments of your life would be a penis if it was a male, probably similar to that seen in a crocodile.” The organ probably would have had a single head and a runnel along the top for sperm to travel down, as seen in the closet living relatives of dinosaurs.

We will probably never know the full range of dinosaurian penis variation. I doubt that such diverse and disparate creatures would have had a one-size-fits-all anatomy, although I also doubt the horrifying idea—which comes up often in internet comment threads—that male dinosaurs might have had long, prehensile organs which allowed them to inseminate at a distance. No matter what their gonads looked like, though, male dinosaurs probably had to get very close to their female partners during sex. There were only a limited number of positions which would have worked for dinosaurs.

But we actually know a little more about the reproductive anatomy of female dinosaurs than male dinosaurs. Dinosaur penis anatomy is constrained by what we know about the evolutionary relationships of dinosaurs and what we are willing to imagine, but a few significant fossils have given paleontologists a general idea of the female dinosaur reproductive tract. The most fantastic of them is a pelvis of an oviraptorosaur—one of the feather-covered, beaked dinosaurs that were relatively close cousins of dinosaurs like Velociraptor—with two eggs preserved inside. Described in 2005 by Tamaki Sato and colleagues, the hips show that the female oviraptorosaur had died just before laying those eggs. This fortuitous discovery illustrated that at least some dinosaurs had a mix of bird- and crocodylian-like reproductive features.

While female birds have only one oviduct—thought to be an adaptation related to becoming light enough to fly—the presence of two eggs in the dinosaur suggested the presence of two oviducts, as in crocodylians. But the fact that there were only two eggs indicated the dinosaur laid a small number of eggs at a time. Instead of producing a large clutch of eggs and laying them all at once, like a crocodylian, the dinosaur only laid two eggs each round and arranged those pairs around the nest. (Oviraptorosaurs have famously been found preserved on top of nests which seem to show a ring of paired eggs.) The female dinosaur did not have a reproductive system just like that of a bird or a crocodile, but a combination of traits seen in the modern lineages.

Other eggs hint that some of the largest dinosaurs might have been more crocodylian-like. No one has yet found a Diplodocus with eggs preserved in the hip region, but paleontologists have found numerous eggs referred to sauropod dinosaurs. Some of these show a pathological condition in which eggs are coated with a second shell layer. According to Kenneth Carpenter, there are two possible ways for this to happen. One possibility is that the egg stalled while going through the shell gland and received a second covering because of the delay. But the other explanation is that some dinosaurs might have produced a larger number of eggs relatively rapidly, and sometimes so many eggs filled the reproductive tract of a mother dinosaur prior to laying that an egg might be pushed back up the oviduct where it would be coated in another shell coating. This pathology is often seen among crocodylians and other reptiles, but is rarer among birds, and the idea that sauropods laid eggs in large clutches seems to fit the nests attributed to these dinosaurs. Dinosaurs like Brachiosaurus and Mamenchisaurus laid nests of multiple eggs which were relatively small compared to their body size, so it is possible that they deposited entire clutches, while smaller dinosaurs such as oviraptorosaurs could lay a limited number of eggs at a time.

There is much we don’t know about dinosaur sex. From possible positions to anatomy, mysteries abound. But the subject has moved beyond silly speculation. A better understanding of dinosaur evolutionary relationships has given paleontologists a framework from which to hypothesize about different aspects of dinosaur reproduction, and those ideas have been tested by discoveries in the fossil record. Future finds and analyses will undoubtedly flesh out some of the remaining unknowns. We are only just beginning to discover some of the most intimate secrets of dinosaur lives.

This is the final installment of the dinosaur sex series. For more, please see my Smithsonian article “Everything you wanted to know about dinosaur sex” and the previous entries in the series:

How did the biggest dinosaurs get it on?

Sex and Dinosaur Necks

Intimate Secrets of Dinosaur Lives

References:

Brennan, P., Birkhead, T., Zyskowski, K., van der Waag, J., & Prum, R. (2008). Independent evolutionary reductions of the phallus in basal birds Journal of Avian Biology, 39 (5), 487-492 DOI: 10.1111/j.0908-8857.2008.04610.x

Brennan, P., Prum, R., McCracken, K., Sorenson, M., Wilson, R., & Birkhead, T. (2007). Coevolution of Male and Female Genital Morphology in Waterfowl PLoS ONE, 2 (5) DOI: 10.1371/journal.pone.0000418

Carpenter, K. 1999. Eggs, Nests, and Baby Dinosaurs. Bloomington: Indiana University Press. pp. 78-81

McCracken, K. (2000). The 20-cm Spiny Penis of the Argentine Lake Duck (Oxyura vittata) The Auk, 117 (3) DOI: 10.1642/0004-8038(2000)117[0820:TCSPOT]2.0.CO;2

Sato, T., Cheng, Y., Wu, X., Zelenitsky, D.K., Hsaiao, Y (2005). A Pair of Shelled Eggs Inside A Female Dinosaur Science, 308 (5720), 375-375 DOI: 10.1126/science.1110578

Wang, S., & Dodson, P. (2006). Estimating the diversity of dinosaurs Proceedings of the National Academy of Sciences, 103 (37), 13601-13605 DOI: 10.1073/pnas.0606028103

Did sexual selection cause sauropods, such as this Barosaurus at the Natural History Museum of Utah, to evolve ludicrously long necks? Photo by the author.

Yesterday I wrote about the possible mating mechanics of immense sauropod dinosaurs such as Brachiosaurus and Argentinosaurus. But there’s more to mating than the act itself. It is not as if two Diplodocus nonchalantly walked up to each other, had a quickie, and plodded off to feed on a nearby patch of ferns. There was probably some kind of behavioral lead-up to copulation—a way for one sex to strut its stuff and the other to be choosy about a mating partner. With this in mind, one paleontologist proposed that sex might hold the secret of why sauropods evolved such long, gorgeous necks.

The idea that mating behavior might have something to do with sauropod anatomy was inspired by giraffes. Scientists have been puzzling over why giraffes have such spectacular necks for over a century and a half. The most popular notion is that the long necks of the mammals are an adaptation for feeding high up in the trees where competing herbivores can’t reach, but in 1996 zoologists Robert Simmons and Lue Scheepers proposed something different.

Male giraffes fight each other in a peculiar form of combat called “necking.” It’s not as nice as it sounds. Male giraffes swing their long necks to batter each other with the stout ossicones on the tops of their heads. These bouts determine hierarchies among males, and dominant males mate more often than subordinate ones do. Since males with bigger, stronger necks would seem most likely to win the contests, Simmons and Scheepers argued, those males are more likely to pass on their traits to the next generation, and therefore necking might have been the reason why giraffes evolved longer necks. Female giraffes just happened to get evolutionarily carried along even though they don’t engage in the same behavior.

The “necks for sex” hypothesis has been controversial from the start. At present, the weight of the data supports the idea that giraffe necks primarily evolved as a way to sample a wide range of food, not as a weapon involved in battles for mating rights. Studies since 1996 have indicated that long necks really do help giraffes avoid competition with other species for the most nutritious food by going higher up, especially when food may be scarce, and studies of fossil giraffes hint that long necks may have began to evolve in response to changes involved with the spread of grasslands around 14 million years ago. Still, the idea proposed by Simmons and Scheepers has remained a sexy hypothesis, and in 2006 paleontologist Phil Senter applied the idea to Apatosaurus and kin in a paper called “Necks for sex: sexual selection as an explanation for sauropod dinosaur neck elongation.”

Without living sauropods to study, Senter proposed six predictions for what a sexually-selected sauropod feature would look like. For example, on the basis of previous theoretical work, Senter suggested that a feature that was primarily used for display or mate competition would provide no benefit to the survival of the animal and might, in fact, be a risk. In the case of sauropods, Senter argued that the long necks of sauropods would not have provided the dinosaurs with any major advantage over other herbivores in terms of accessing food. Just as Simmons and Scheepers proposed that the long necks of giraffes did not provide a feeding benefit, Senter suggested the same for dinosaurs like Camarasaurus. As a corollary to that, Senter also pointed out that predatory dinosaurs must have targeted the long necks of sauropods to quickly bring down the giants. “The evolution of more neck, and hence more vulnerability to a fatal bite, therefore incurred a survival cost for all but the longest-limbed sauropods [which would have carried their necks higher off the ground],” Senter wrote.

Senter only briefly entertained how fancy, flashy sauropod necks might have been involved in dinosaur mating behavior. Maybe males smacked necks when fighting for territory, or perhaps competitors simply eyed each other to see whose neck was bigger. There was no way to tell. Overall, though, Senter believed that the necks of sauropods were more consistent with what would be expected for a sexually-selected feature than an adaptation for feeding.

However, in a paper published last year, paleontologists Mike Taylor, Dave Hone, Matt Wedel and Darren Naish refuted Senter’s arguments. The long necks of sauropod dinosaurs certainly could have provided survival benefits, particularly in terms of accessing high-quality foods that were beyond the reach of smaller herbivores. Senter had assumed that sauropods held their heads low to the ground and therefore would not have been capable of much vertical reach, but there is osteological evidence to the contrary. Sauropods were physically capable of holding their heads high, and may have favored an elevated neck posture most of the time. More than that, the exceptionally long necks of many sauropods would have provided an energetic benefit by allowing the animals to stand in one place while sampling food over a wide range.

Senter also overstated the vulnerability of dinosaurs like Barosaurus to attack. As Taylor and co-authors pointed out:

The [sauropod] neck was not simply a mass of external blood vessels and nerves, but was constructed from tough elements including the often robust cervical ribs, bony laminae, ligaments and tendons. A theropod could hardly dispatch a moving apatosaur with one swift bite, and a raised neck would further reduce vulnerability.

That is assuming that predatory dinosaurs hunted adult animals at all. Like many modern predators, Mesozoic hunters like Allosaurus and Torvosaurus probably targeted young, relatively small sauropods more frequently.

Underlying all of this, though, was a conceptual flaw in taking a hypothesis proposed for one species—the evolution of necks for sex in giraffes—and applying it to a disparate, wide-ranging, and long-lived clade of vertebrates. If the long necks of sauropods were so costly to evolve and provided no significant survival benefit, then why did so many dinosaurs retain this feature for so long? Taylor and co-authors summarized the rhetorical flaw this way:

If the long necks of sauropods had negative survival value, their retention across the whole clade is analogous to a hypothetical situation where the maladaptively long tails of birds-of-paradise are found throughout Passeriformes [perching birds, about half of known bird species], or where the enormous antlers of the Irish Elk Megaloceros are ubiquitous in Artiodactyla [even-toed, hoofed mammals and descendant forms, including whales].

The proportionally long necks of sauropods must have had some adaptive advantage for the trait to be so widespread and persistent. This doesn’t mean that sauropod necks were only used for feeding, though. As Taylor and co-authors pointed out, traits used in mate competition may also provide survival benefits. As the researchers stated, “It remains possible that the sauropod neck originally arose either as a sexually selected feature or to help gather food, but it cannot be demonstrated that the necks remained monofunctional throughout their evolution, or that they could not be co-opted for a secondary function.” The neck of the giraffe is a perfect example. Male giraffes swing their necks in competition, but their long necks have also been shown to provide them with a competitive edge when it comes to reaching food resources other herbivores just can’t exploit. The question is which impetus was more important in the trait’s evolution.

For sauropod dinosaurs, feeding ecology was more important than sexual selection in the evolution of long necks. But once long necks had evolved, who knows how they might have been used for communication and display? Such prominent necks would have been elongated, fleshy billboards which could very well have been used to establish dominance, attract mates, or otherwise advertise an individual’s prominence. If adult sauropods were too big to be harried by predators, and therefore did not require camouflage, would sauropods have developed bright, striking color patterns along their necks to gain the attention of potential mates and show off that they were the healthiest, sexiest dinosaurs around? Those are the kinds of questions that can keep a paleontologist up at night.

For more on sauropods and the “necks for sex” debate, see these posts by Darren Naish, Dave Hone and Mike Taylor.

This post is the second in a short series of articles on dinosaur reproduction that will run through Valentine’s Day. Because nothing spells romance like dinosaur sex.

Previous Installments:

How did the biggest dinosaurs get it on?

References:

Senter, P. (2006). Necks for sex: sexual selection as an explanation for sauropod dinosaur neck elongation Journal of Zoology, 271 (1), 45-53 DOI: 10.1111/j.1469-7998.2006.00197.x

Taylor, M., Hone, D., Wedel, M., & Naish, D. (2011). The long necks of sauropods did not evolve primarily through sexual selection Journal of Zoology, 285 (2), 150-161 DOI: 10.1111/j.1469-7998.2011.00824.x

The backside of Diplodocus, photographed at the Utah Field House of Natural History. Photo by the author.

In 1991, the American Museum of Natural History unveiled one of the most fantastic fossil displays ever created. Placed at the center of the renovated Theodore Roosevelt Rotunda, an adult Barosaurus rears back to protect its offspring from an oncoming Allosaurus. The defending sauropod’s head is 50 feet up in the air, although whether or not such an immense, long-necked dinosaur could have pulled off such a feat has been a continuing point of contention. Even in a typical posture, Barosaurus must have had a powerful heart to pump blood along its 25-foot neck, and who knows how hard the dinosaur’s heart would have to work to continue bloodflow to the animal’s head if it reared up? Some paleontologists consider such a feat physically impossible, but as paleontologist William Gallagher pointed out while teaching my Paleontology 101 class at Rutgers University, male Barosaurus had a good reason to rear up. How else would the huge dinosaurs have positioned themselves to mate?

Exactly how dinosaurs got it on has inspired no small amount of speculation. The largest dinosaurs of all, the sauropods, have been especially perplexing. We often say that these dinosaurs “shook the earth” with their footsteps, but did they also make the bed rock with their lovemaking? (I apologize for that joke, and will keep the geology puns to a minimum. Promise.) Paleontologist Beverly Halstead famously wondered about dinosaur sex in public lectures and articles, and he suggested that standard “dinosaur style” was for a male to come alongside the female and throw its leg over the female’s back as she lifted her rump into the air to move her tail out of the way. In the case of sauropods such as Diplodocus, Halstead even imagined that the amorous dinosaurs might intertwine their tails. While other paleontologists have considered the tail-twisting aspect unlikely—sauropod tails were balancing organs and were too stiff to intimately coil around each other—the basic dinosaur position Halstead promoted has remained a prominent possibility for the dinosaur kama sutra.

But not everyone agreed that giants such as Apatosaurus and Brachiosaurus were capable of such nupital acrobatics. These animals were so immense—Apatosaurus, not even the largest sauropod, is estimated to have weighed more than 23 tons—that some researchers thought the kind of positions Halstead was promoting would give the dinosaurs fractured legs and broken spines. At a symposium of vertebrate morphologists held at the University of Chicago in 1994, biologist Stuart Landry, Jr. gave a short presentation entitled “Love’s Labors Lost: Mating in Large Dinosaurs.” He did not see how sauropods could have mated on land. A large, rearing sauropod, he told his audience, “would have to support 10 to 20 tons in a precarious position two or three meters off the ground.” A male Apatosaurus would be liable to tip over and possible take the female with him. Instead, Landry suggested that the largest dinosaurs looked for muholes or bodies of water to buoy themselves up. When a conference attendee asked if he was proposing that all dinosaurs mated in water, Landry responded, “I would say the very large ones must have.” Of course, this hypothesis required a large number of Jurassic and Cretaceous hot tubs of just the right depth for sauropods to reproduce, and scientific models of sauropods have suggested that these dinosaurs were actually quite buoyant and unstable in water. Sauropods were diverse, disparate and widespread animals that roamed in terrestrial habitats all over the world—there’s no reason to presume that the largest dinosaurs had to seek out the nearest deep lake when they got the itch.

Biomechanics expert R. McNeill Alexander also considered the weight problem in his 1989 book Dynamics of Dinosaurs & Other Extinct Giants, but came to a different conclusion. Even though a male sauropod would have rested a great deal of weight on the back of the female during mating, Alexander pointed out that the stresses and strains would not have been any more severe than those caused while the female dinosaur was walking. (After all, walking requires shifts in weight as the dinosaur balances and goes through each step cycle, and so a dinosaur’s skeleton had to be strong enough to cope with these shifts.) “If dinosaurs were strong enough to walk they were strong enough to copulate,” Alexander wrote. “They were presumably strong enough to do both.”

Without living specimens to observe, we will never know all the intimate details of sauropod sex. Still, there are only a limited number of positions that could have worked for the dinosaurs. For reasons that I’ll write about later this week, the consensus among paleontologists is that male dinosaurs probably had relatively small penises. (Shhh! Don’t tell Tyrannosaurus. He’s already upset about all those “useless forelimbs” jokes.)  An amorous male would have to position his cloaca—the orifice used for both expelling waste and mating in crocodylians, birds and probably dinosaurs—right up to the cloaca of a female, and the female’s tail would have undoubtedly presented an obstacle. Rather than simply leaning straight against the top of a female like an elephant or rhinoceros does, a male sauropod would probably have to rear up at a relatively oblique angle, and the female would have to assist by moving her tail (which is also a way in which female dinosaurs could have exerted mate choice and confounded any hot-under-the-collar males they would rather not mate with). Perhaps some museum will look into the problem and try to mount a pair of coupling sauropod skeletons—much like the mating Tyrannosaurus at Spain’s Jurassic Museum of Asturias—but even then we are limited by what we can imagine. Whether we want to imagine a pair of Brachiosaurus in flagrante delicto is another matter altogether.

This post is the first in a short series of articles on dinosaur reproduction that will run through Valentine’s Day. Because nothing spells romance like dinosaur sex.

References:

Alexander, R. M. 1989. Dynamics of Dinosaurs & Other Extinct Giants. New York: Columbia University Press. pp. 57-58

Anderson, J. The Perplexing Puzzle of Maladroit Mating. Chicago Tribune. August 30, 1994.