Fossils of the antiarch Microbrachius dicki show males with large bony L-shaped claspers for transferring sperm, whereas females bore small paired bones to help dock the male organs into position.
These discoveries, published today in the journal Nature, represent the first appearance of sex involving copulation in vertebrates (back-boned animals). It’s also the first time in vertebrate evolution that males and females appear with distinct differences in their physical appearance.
Little arms, big genitals
Microbrachius means “little arms” from its small paired pectoral limbs. It inhabited ancient rivers and lakes about 385 million years ago. Its species name dicki honours Robert Dick, an avid fossil collector in the late 19th century who first found its fossils in the north of Scotland.
The new discoveries began late last year when I was working at the University of Technology in Tallinn, Estonia, with my colleague Elga Mark-Kurik. She handed me a box of isolated Microbrachius bones from Estonia to examine. I found a tiny plate, less than 2cm long, which had a tube of bone attached to it that I couldn’t identify.
Eventually I realised it was a clasper; a primitive vertebrate sexual organ. Claspers are found in male sharks and rays and used for copulation. It was one of those sublime eureka moments as the discovery was profound: it basically meant a complete rethinking of the evolution of sexual strategies in jawed vertebrates.
Antiarchs had never before shown any evidence for this type of reproduction. We had long assumed they simply spawned in water, like many living fishes. The new discovery meant they had the ability to copulate, so internally fertilised their eggs. As antiarchs are the most primitive jawed vertebrates (gnathostomes) it meant that highly complex sexual reproduction first appeared at more or less the same time as jaws and paired hind limbs appeared.
We began searching other museum collections in Europe, Australia and the USA for more evidence. Eventually some amazing complete specimens of Microbrachius held in private collections by UK and Dutch collectors were revealed to us, showing distinct male and female features. These were then donated to the Natural History Museum, London, so we could complete our study.
First vertebrates copulated ‘square-dance’ style
It’s bizarre that these tiny fishes mated from a sideways position, the male and female resting alongside each other. They likely intertwined their bony jointed pectoral appendages (arms) using the rows of hooks on their inside edge. The outside arms could have helped them manoeuvre their large claspers into the mating position. With their hooked “arms” interlocked, the act of copulation in these fishes somewhat resembled square dancing the do-si-do.
The female’s paired genital plates bore a roughened surface, a bit like a cheese grater, for the male claspers to latch on to. Once the male’s clasper was in the mating position only the tip could be inserted inside the cloaca of the female to deposit sperm.
Despite their awkward looks, Microbrachius were highly successful little fishes whose species are found in UK, China and Estonia. The antiarchs could have all mated in this way as other forms such as Bothriolepis show similar genital structures preserved.
Bothriolepis was the most ubiquitous vertebrate known in the Devonian period, with more than 150 species found. It lived on every continent, including Antarctica. Such antiarchs were probably the world’s first truly widespread vertebrates. We now think it likely that their movable bony arms which facilitated copulation were the key to their migratory success.
Placoderm sex and live birth
The new discovery follows on the heels of a string of recent finds elucidating how the oldest backboned animals mated. In 2008 we discovered the oldest evidence for live birth (viviparity) in a placoderm fish fossil from Gogo, Western Australia.
It showed a 3D embryo fossil attached by a mineralised umbilical cord. We named it Materpiscis attenboroughi, meaning “Attenborough’s mother fish”.
This discovery was followed in 2009 by another equally unexpected find, more placoderm embryos inside another group of placoderms, the “arthrodires”.
The arthrodires were the most diverse clade of placoderms. Yet despite thousands of specimens in museum collections, none had shown any evidence for how they reproduced. Our discovery proved they used internal fertilisation and that males had bony claspers for mating.
Earlier this year we added to this by showing that placoderm claspers did not develop in the same way as shark claspers, as part of the pelvic fin, but evolved more or less like an extra pair of limbs.
Placoderm claspers were at first fixed rigidly to their body plates as in Microbrachius so the fish had to move its entire body around to mate. More advanced placoderms such as the arthrodire Incisoscutum evolved flexible bony claspers capable of rotating forwards and becoming erect for mating.
The rise and fall and rise again of male intromittent organs
Our new research implies something that was thought impossible in biology - that fishes went from using copulation (internal fertilisation) to reverting back to external fertilisation (spawning in water), the default primitive condition seen in jawless fishes such as lampreys.
This must have occurred when bony fishes (Osteichthyes) first evolved from placoderms as none of the primitive fossil or living species (such as Polypterus) show any evidence for internal fertilisation.
We know that coelacanths mate using internal fertilisation even though they lack copulatory structures. Some families of advanced bony fishes, the teleosts, evolved different kinds of internal fertilisation. Guppies, for example, use a modified anal fin spine to transfer sperm (a gonopodium), although none of these teleosts ever developed paired claspers similar to those in placoderms or sharks.
Our study concludes that the most primitive jawed vertebrates originally evolved copulation as the main way of mating, then lost it early on in their evolution. Later it reappeared again and again in many different animal groups.
Snakes and some lizards have hemipenes (paired penises), but crocodiles, tortoises, mammals and some birds all have a single penis. The Argentine Lake Duck has the longest penis relative to body size for any living vertebrate (43cm for an average-sized duck). The penis was secondarily lost in many lineages of flying birds.
We humans thus mate in a way that first evolved in crocodiles and tortoises back in the age of dinosaurs. We can thank our distant ancestors, the placoderms, for first evolving this unique method of reproduction.
John Long receives funding from The Australian Research Council and Flinders University.