On a hot August day in 2005 my team and I were out hunting for fish fossils in the tall, grassy paddocks of Gogo Station, a vast cattle ranch located in the heart of northwestern Australia. Today the arid region is hardly suitable for aquatic creatures. But some 375 million years ago, during the Late Devonian period, a shallow sea covered the area and Gogo was home to an enormous tropical reef that teemed with marine life, including a plethora of primitive fishes. Luckily, many of their remains have survived across the ages. Nestled among the clumps of spiky Spinifex bushes and sleepy death adders lie softball-size nodules of limestone—the products of millions of years of erosion of the local shales—some of which harbor pristine fossils of the fishes that lived on the primeval reef. And so over the course of our terrestrial fishing expedition, we would spend our days cracking the nodules open, one after another, hoping to glimpse a treasure inside.
The most abundant of the fishes that patrolled the Gogo reef were armored creatures called placoderms (“plated skin”)—some of the first backboned animals with jaws. Though gone today, placoderms ruled the planet for nearly 70 million years, making them the most successful vertebrate group of their time. Scientists have long debated exactly how they are related to other backboned creatures, and we had come to Gogo to look for specimens that might help resolve this and other questions about fish evolution. On this particular day our efforts were rewarded with a nodule containing what appeared to be a fairly complete fish. It did not strike me as especially remarkable in its anatomy, though, just another placoderm fossil to add to our haul and take back to the lab for extraction from its limestone tomb at a later date. Little did I know that this seemingly modest find would upend scientists’ understanding of a very intimate aspect of vertebrate biology—the origin of sexual intercourse and internal fertilization.
Researchers used to believe that internal fertilization and the carrying of the young inside the mother’s body until birth together made up a specialized form of reproduction that first appeared in the sharks and their kin (a group known as the chondrichthyans) roughly 350 million years ago, some 70 million years after the first members of this group evolved. Before then, piscine procreation was supposedly limited to spawning, a decidedly impersonal affair in which the females deposit eggs into the water, the males then fertilize them and the embryos develop out in the open. But recent analyses of the fish we found back in 2005, along with other placoderms from Gogo and elsewhere, have revealed that copulation and live birth arose millions of years earlier than previously thought and in a vertebrate group more primitive than the chondrichthyans.
It is hard not feel astonished when some major trait turns out to have evolved much earlier than was thought. But the significance of the findings goes beyond mere surprise. It turns out that placoderms are directly on the long line leading to creatures with four limbs (the tetrapods, including humans). In the sexual equipment of these ancient placoderms, we can thus see the earliest rudiments of our own reproductive system and other parts of our body and gain a clearer idea of how the anatomy changed over time to become what it is today. The paired pelvic fins that in placoderms permitted the males to deposit sperm into the females eventually gave rise to the genitalia and legs of tetrapods. And jaws may have originally evolved to help male fish grab ahold of females and stabilize them during mating, only later taking on the role of food processing. Sex, it seems, really did change everything.
Mother Lode
Gogo fossils are famous for their extraordinary preservation. Unlike most fish fossils, which tend to be flattened, the ones from Gogo often exhibit pristine three-dimensional preservation. Fully exposing the skeletons is time-consuming business, however—we must painstakingly dissolve the limestone matrix by applying diluted vinegar (acetic acid), which leaves the fossilized bone unharmed. It was not until November 2007 that I got around to cleaning the specimen my team found on that hot August day two years earlier. Based on its robust jaws and teeth built for crushing, my colleague Kate Trinajstic, now at Curtin University in Australia, and I determined that the fossilized animal, which was about the size of a mackerel, belonged to the so-called ptyctodontid family of placoderms. This finding in and of itself was good news, because the ptyctodontids are a poorly known group and ours looked like it was probably a new species. But the discovery was about to get much more interesting.
As I removed more of the limestone, I spotted some unusual structures near the base of the animal’s tail. On closer examination under the microscope, I saw a set of delicate little jaws alongside a scattering of other tiny bones. Then the penny dropped, and I experienced one of those sublime eureka moments that scientists get once in a lifetime, if they are lucky. Typically I would have assumed these were the remains of the fish’s last meal. But the minute jaws bore exactly the same distinctive features as those of the larger animal, and they were undamaged and still partially articulated—all signs that the miniature bones were those of a developing embryo, not an entrée. Furthermore, I could see a twisted structure wrapped around the tiny skeleton. Using a scanning electron microscope, we were soon able to identify this feature as a mineralized umbilical cord, which would have supplied the embryo with nutrients from a yolk sac. The case was clear: we had found a 375-million-year-old expectant mother fish and the oldest vertebrate embryo on record. We named the new fish Materpiscis attenboroughi, meaning “Attenborough’s mother fish,” in honor of the great British nature presenter David Attenborough, who introduced the Gogo fossil sites to the world in the 1979 documentary series Life on Earth.
Materpiscis solved a long-standing mystery about ptyctodontids. Back in the late 1930s British anatomist D.M.S. Watson observed that males of a fossil ptyctodontid species from Scotland have long, cartilaginous extensions coming off the bony girdle that supports the animal’s pelvic fins. In life, these extensions would have been encased in flesh and skin, forming structures akin to the two claspers present in males of all living chondrichthyans, which insert one or the other into a female to transfer sperm during copulation. But the claspers on the Scottish ptyctodontid were covered in bony plates, which would have made them rigid and ungainly. Furthermore, although all chondrichthyan claspers are tipped with scalelike hooks that help to hold the claspers in place during mating, the ones in this ptyctodontid were so pronounced that they appeared to be more of a deterrent to mating than an aid.
Subsequent ptyctodontid discoveries showed the same features, leaving scientists to wonder whether these fish actually inserted their bizarre claspers into the females, or used them to grasp the females while mating, or whether they were just for show—spiky adornments used to attract a mate. At that point, based on the available fossil evidence, paleontologists could not say definitively whether the ptyctodontids mated through copulation or spawning. Our mother fish and her baby showed without a doubt that at least some ptyctodontids reproduced through internal fertilization and live birth.
The Materpiscis revelation prompted us to reexamine previously discovered Gogo ptyctodontid fossils to see if they, too, might harbor babies. This search led us to a specimen of a different genus of ptyctodontid, Austroptyctodus, that I had prepared 20 years earlier. Scrutinizing it under higher microscope magnification and using the first discovery of the embryo as our Rosetta Stone, I could see that features that I had originally interpreted as dislodged scales were in fact tiny bones belonging to embryos. We had found another ancient mother, one that had died at the prime of life with triplets inside her.
Following our discoveries of the pregnant ptyctodontids, which my colleagues and I published in Nature in 2008, we began to look at even more Gogo placoderms. Our work had determined that ptyctodontids copulated and gave birth to live young, but they were just one of seven groups of placoderms. How widespread was this novel means of reproducing? We turned our attention to a specimen of a placoderm in the genus Incisoscutum that had previously been identified as having “stomach contents” in the form of bones of a smaller fish. Both this fossil and another one in the same genus turned out to be carrying embryos.
Incisoscutum belongs to the largest placoderm group, the arthrodires. This group consists of more than 300 species, including the biggest placoderms that ever lived, such as the fearsome six-meter-long Dunkleosteus. Before our discovery, there was no evidence to indicate whether male and female arthrodires differed in their external anatomy nor to reveal how they mated. The embryos we found showed unambiguously that Incisoscutum reproduced by internal fertilization. Eventually we proved using examples from Gogo and other sites that arthrodire males also had claspers to facilitate this type of mating—findings that we published in two more Nature papers in 2009. Thus, at least two of the seven main groups of placoderms, including the most successful one, reproduced by copulation at least 25 million years before the sharks and other chondrichthyans did.
Sexual Revolution
In light of these finds, it now appears that placoderms were the originators of intimate sexual reproduction. We also now have a better understanding of where they fit on the vertebrate family tree. Previously the leading theory held that the placoderms gave rise to just one of the two living groups of jawed vertebrates, namely, the sharks and their chondrichthyan kin. But the new discoveries, along with analyses of evolutionary relationships among early vertebrates conducted in 2009 by Martin Brazeau, now at the Natural History Museum in Berlin, suggest placoderms could be ancestral to both early chondrichthyans and an extinct group of fishes called acanthodians. Some of these acanthodians are thought to be ancestral to the first bony fishes, the lineage that led to the four-limbed animals, including humans.
This revised scenario for the start of sex as we know it raised important new questions, however. My collaborators and I began to contemplate how the emergence of copulation as a reproductive strategy might have affected subsequent vertebrate evolution. From anatomical comparisons made by others and us, we already suspected the hind limbs and genitalia of the tetrapods evolved from the pelvic girdle (including the claspers) of early fishes. One of the most compelling pieces of evidence supporting this view came from studies led by Martin J. Cohn of the University of Florida, who showed in 2004 that the Hoxd13 gene, involved in the development of the pectoral and pelvic fins in modern-day jawed fishes, is also active in the developing limbs and genitalia of mammals, an indication that our legs and sex organs could both have been derived from the early fish pelvic girdle.
If the new work indicated that we descended from placoderms, then those features clearly also came from those fishes. But we wondered what other anatomical legacies we inherited from placoderms. Among modern-day sharks, males must court females before they can mate with them. In some species, such as the white-tipped reef shark, the male makes his overture by biting the female’s back, neck and then her pectoral fin—a move that then helps him to hold onto her while copulating. This observation led us to speculate that perhaps jaws first evolved not for food processing, as scholars have traditionally envisioned, but to improve mating success. Such an innovation would have then laid the ground for the jaws to become pressed into later service for chewing. Although most bony fishes reverted back to spawning and thus did not use their jaws for mating, they were preadapted to chewing, thanks to their placoderm ancestors. (Internal fertilization later reevolved in land animals using the pelvic-fin foundation established by the placoderms, a shift that freed them from having to return to the water to reproduce.) Knowing that internal fertilization first appeared in placoderms, not sharks, and that placoderms are ancestral to bony fishes helped us to draw this tentative connection between copulation and chewing in the line of animals leading to humans.
Looking at the bigger evolutionary picture, my colleagues and I could not help but notice that the new timing for the origin of copulation dovetailed with the explosion of diversity in the arthrodire fishes—the first big species radiation of any jawed animal in the fossil record. Could this early switch in reproductive biology in vertebrates from spawning to internal fertilization have been the main driver of this major evolutionary event? Our search of the scientific literature turned up some interesting clues. In 2004 Shane Webb of the University of St. Andrews in Scotland and his colleagues reported that a group of fishes known as goodeid fishes, which today inhabit freshwater streams in Nevada and west-central Mexico, split into two lineages around 16.8 million years ago. One continued to spawn in water and branched into just four species. The other evolved a form of internal fertilization and today comprises 36 species. Another group of fishes known as the Bythitoidei, which includes three lineages, exhibits a similar pattern. The one that evolved internal fertilization contains 107 species. Of the other two lineages, which maintained the spawning strategy, one contains 22 species and the other just three. The fact that in both these groups the lineages that switched to internal fertilization underwent much higher species diversification than spawners did is a hint that we might be on the right track with our hypothesis.
At first glance, the suggestion that internal fertilization drove the arthrodire radiation might seem counterintuitive. In theory, spawning—which involves laying tens of thousands of eggs—should yield many more offspring than internal fertilization and live birth, in which the mother invests a lot of energy into raising just a few babies at a time. And the greater the number of offspring, the greater the chances that one will inherit a mix of genes that could lead to the beginnings of a speciation event. But during the Devonian, most fishes fed on other fishes, and the tiny, weak hatchlings that resulted from spawning would have been easy targets. A reproductive method in which the mother nurtured fewer offspring with larger body size—equipping the babies with better odds of surviving to reproductive age themselves—might well have given arthrodires an evolutionary edge.
Getting in the Mood
Many questions about the origin and evolution of internal fertilization in vertebrates remain. For instance, scientists still do not know exactly how placoderms made the transition from spawning to internal fertilization. Lacking the ability to observe them in action, I can only speculate about the nature of this sea change. From a mechanical standpoint, it may have started with males and females spawning closer to each other to achieve a higher success rate for fertilization or to better protect the fertilized eggs. There might also have been an intermediate stage whereby rather than depositing the eggs in water, the female or male carried the egg mass, as do some fishes, such as seahorses, which brood their eggs in pouches. Perhaps the use of well-developed pelvic fins to transfer sperm more accurately to the egg mass then brought the male closer to the female, and this arrangement created natural selection pressure for larger, more elongated pelvic-fin lobes, which eventually became claspers.
As for the neurological factors that made males want to insert parts of their pelvic fins inside females for mating, perhaps this desire evolved as a by-product of natural selection acting to encourage fertilization of the eggs before the female had laid them, thus boosting the chances of beating other males to the punch. Further study of the chemical signals and neural triggers that govern mating behavior in sharks and other fishes may provide additional clues to how the first step toward the hookup evolved.
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