Sex, sideways… (Image: Roger Jones, London)

If you’re going through a dry patch, it’s nothing compared to the entire animal kingdom – which appears to have gone millions of years without copulating. A new analysis of 380-million-year-old fossils tucked away in boxes in museums is rewriting the textbooks on the origins of sex and genitalia. It shows genitals started out bony, were used sideways, and then copulation went out of fashion for tens of millions of years.

John Long from Flinders University in Adelaide, Australia, and colleagues have found fossil evidence that one of the earliest jawed vertebrates called Microbrachius dicki – from a group known as gnathostomes – reproduced via internal fertilisation. This suggests that all gnathostomes were doing it too.

The find shows that vertebrates lost and regained the ability to efficiently deliver sperm internally, many times over. Copulation was such fun, evolution discovered it again and again.


It also shows that the first jawed vertebrates were copulating. But close descendants of Microbrachius have been found with clear evidence showing that they used external fertilisation, Long says. So the evolution of both external and internal fertilisation must have happened repeatedly.

“Among the roughly 50,000 species of extant vertebrates, we have no evidence that internal fertilisation has ever reverted to external fertilisation,” says Daniel Blackburn from Trinity College in Hartford, Connecticut, who was not involved in the study. “Once a lineage has evolved a way for males to introduce sperm into the reproductive tract of the female, they tend to retain that mode of fertilisation.”

Missing, no more

Apparently, not, since Long’s work provides this missing evidence, Blackburn says. “Under this interpretation, internal fertilisation must have been lost prior to the evolution of the two major lineages of living jawed fishes.” From them evolved the cartilaginous fishes – modern day sharks, skates, and rays – and the bony fishes and their descendants – including us.

Around the time the bony fishes and sharks evolved, internal fertilisation went AWOL, says Long. And then nobody was doing it until internal fertilisation re-evolved about 20 to 40 million years later. And when that happened, animals adopted a different way of locking on to each other.

Long says there are genetic clues as to how the ability could be lost and then come back. “The HOXD13 gene can develop limbs and genital organs in mammals and in sharks as well,” he says. “Early fish probably originated the capability of evolving these things and then they were lost. But once that gene was set in the vertebrate body plan, it could come back later.”

Examining fossil specimens of the earliest known jawed fish, M. dicki, Long and colleagues found both male and female genitalia that had gone unnoticed. On the male they found bony structures that spread out on each side of the fish, with a groove that would have delivered the sperm. On the female, there were spiny plates that would have acted like Velcro, holding the male in place.

Video: Oldest genitals reveal how ancient fish had sex

The real clincher showing that the fish went for internal fertilisation is that their genitals are nearly identical to those of later fish, where females have been found complete with embryos, Long says. “There’s no other interpretation of what they could be,” he says. The new find shows that it was a feature of the very earliest ones.

It even reveals how they did it (see video, above). “Fundamentally they couldn’t have done it in a missionary position,” says Long, pointing out that the genital structures are bony, immobile and are on the sides of the fishes. It also explains why the fish have spiny arms: they were probably used to hold hands, to help lock the genitals in place, as they did it side-by-side. “We’ve wondered for over 100 years what these tiny little jointed arms were used for in these peculiar fishes,” Long says. “The very first act of copulation was done sideways, square-dance style.”

Blackburn, who himself studies reproductive anatomy, says he finds the analysis of how the genitals were used convincing. “It is most surprising to find evidence for a loss of internal fertilisation in a fossil lineage,” he says.

Journal Reference: Nature, DOI: 10.1038/nature13825