The ancient fish that first had sex

When back-boned animals get down to business, they do it in one of two ways. Either females release eggs to be externally fertilised as do many fish and frogs. Or the male fertilises eggs inside the female’s body as do reptiles, birds and mammals. Because fish evolved first, it’s always been assumed that external fertilisation was invented before copulation, perhaps as an adaptation to living on land.

Now, the discovery of penetrative sex organs in an ancient fish is rewriting that story. In a study published in Nature, palaeontologists report finding them in fossils of the very earliest placoderms, armour-plated fish that dominated the seas 440–360 million years ago. These fish are the likely ancestors of bony fish and all other vertebrates. The finding suggests, bizarrely, that copulation preceded external fertilisation.

“It throws a cat among the pigeons because we always thought it was impossible to go from a complex thing like internal fertilisation back to external fertilisation,” says John Long of Flinders University in Adelaide, Australia, who led the study. “But that seems to be what happened.”

There have long been hints that all was not quite as it seemed. Some fish for instance do copulate. Cartilaginous fish such as sharks do so using “claspers” – a pair of flexible rods located on the underside of their pelvic fins, used one at a time to deliver sperm into the female cloaca. In some species the young develop inside a uterus. Even some species of bony fish like guppies do it, having adapted their anal fin to deliver sperm, although the eggs are then laid rather than developing inside a womb. “It happened 13 different times within teleost fishes. There are lots of bizarre ways bony fish have adopted copulation,” says Long.

So which species was the first to copulate?

Six years ago Long and his colleagues made a startling discovery in the Kimberley region of Western Australia when they unearthed what appeared to be a mother placoderm with an embryo inside her. Over the past five years palaeontologists have come to appreciate that placoderms were not just weird armoured oddities in the fossil record. They developed the defining features of vertebrates such as jaws, paired hind limbs and an advanced hind brain that provides the connection between the spinal cord and the rest of the brain.

Long’s findings suggested they might also have figured out how to copulate. The researchers found the males had what seemed to be bony, L-shaped sperm-transferring claspers located close to the pelvic fins. These claspers were different to shark claspers – not a part of the pelvic fin but more like an extra pair of limbs.

Was this unique to the Kimberley species or had placoderms generally invented copulation?

Long’s answer came when he examined fossils of an even earlier group – the antiarch placoderms that were the first to develop jaws and paired hind-limbs. The moment of discovery came when Long was shown a box of broken-up fossils of a group called Microbrachius unearthed in Estonia. Scientists had been looking at these fossils for more than a century, but Long saw something no one else had noticed – a tiny bony clasper.

To make sure it was what he thought it was, Long searched the world’s museums and tracked down some complete specimens unearthed on the Orkney Islands. These had massively big bony curved claspers containing a deep groove that likely carried sperm. Females, meanwhile, showed a series of ridges and grooves inside their armour, perfectly placed and well shaped to accommodate the clasper. The species was named Microbrachius dicki.  (“Purely fortuitous. I didn’t name it.” says Long. The species was named after Robert Dick, the 19th-century fossil collector.)

“We’ve discovered the moment when a whole new form of mating first evolved in our distant ancestors,” says Long. “It was pretty wacky and weird. They must have mated sideways with their bony pectoral fins interlocked like they were dancing the do-si-do.”

Matt Friedman, a palaeobiologist at Oxford, says the evidence that antiarch placoderms had copulatory claspers is “pretty compelling”. What’s more, he says, “clasper-like appendages are invariably associated with internal fertilisation, so there’s not much to debate here”.

It seems our vertebrate ancestors were the first to copulate. But that ability was not necessarily taken up by all their descendants. Sharks and other fish developed independent ways to do it. But though it may have remained dormant for millennia, Long suspects that when animals started land-dwelling, those old genetic plans may have been revisited. “There’s genetic evidence the blueprint was dusted off and put back to work to make penises.”

This article appeared in Cosmos 60 – Dec-Jan 2015 under the headline “The ancient fish that first had sex”