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A Kink in the History of Sex

The first act of copulation in vertebrates

The first act of copulation in vertebrates was in these 385 million-year-old antiarch fishes from Scotland (Microbrachius dicki). The male (right) uses his bony L-shaped claspers to inseminate the female (left). Credit: Brian Choo

By John Long

The discovery of the first vertebrate to have copulated reveals not only the genesis of different male and female forms but also some surprising kinks in how sex has evolved.

The evolutionary origin of the intimate act of copulation has been discovered in ancient armoured placoderm fishes called antiarchs. Fossils of the 385 million-year-old antiarch Microbrachius dicki show males with large bony L-shaped claspers for sperm transfer, while females bore small paired bones to help dock the male organs into position.

Our discoveries, published in Nature in October, represent the first appearance of sex involving copulation in vertebrates. It’s also the first time in vertebrate evolution that males and females appear with distinct differences in their physical appearance.

The new discoveries began late last year when I was working at the University of Technology in Estonia with my colleague Dr Elga Mark-Kurik. She handed me a box of isolated Microbrachius bones from Estonia to examine. I found a tiny plate, less than 2 cm long, which had a tube of bone attached to it. I couldn’t identify what it was for.

Eventually I realised that it was a bony clasper – a primitive vertebrate sexual organ. Claspers are found in male sharks and rays, and are used solely for copulation. It was one of those sublime eureka moments as the discovery was profound: it basically required a complete rethinking of the evolution of sexual strategies in jawed vertebrates.

Antiarch placoderms had never before shown any evidence about how they reproduced. We had long assumed they simply spawned in water, just like many living fishes, but the new discovery meant they had the ability to copulate, and therefore fertilised their eggs internally. As antiarchs are the most primitive jawed vertebrates, 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 with fully formed male and female sexual structures were located in private collections owned by UK and Dutch collectors. They were keen to help us publish this important discovery so they willingly donated the most significant specimens to the Natural History Museum, London, and to the South Australian Museum in Adelaide so that studies of them could be completed.

Sideways Copulation, Square-Dance Style

Reconstructing how these extinct fishes must have mated was not hard. Bearing large bony L-shaped reproductive organs, the males could only do it one way. It’s bizarre that these tiny fishes must have copulated from a sideways position, with 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 edges. 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 small paired genital plates bore a roughened surface like a cheese grater to help the male claspers latch on. 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 the UK, China and Estonia from about 400–384 million years ago. The antiarchs could have all mated in this way because other forms like Pterichthyodes and the ubiquitous Bothriolepis have similar female genital structures preserved.

Bothriolepis was the most abundant and speciose 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, with their migratory ability capable of spanning oceans and invading freshwater rivers and lakes.

Because their fossilised remains occur in mostly freshwater deposits but also some marine sites, it’s likely they invaded freshwater to breed like many modern fishes do (e.g. salmon). This could also explain some mass mortalities of them in freshwater sites if they died immediately after mating. We now think it likely that their movable bony arms not only facilitated copulation but were also the key to their migratory success.

Adding to the Story of Placoderm Sex

The new discovery follows on the heels of a string of finds in the past 10 years that elucidated 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 discovery of more embryos inside another group of placoderms, the “arthrodires”. The arthrodires were the most diverse clade of placoderms, with well over 350 known species. Yet, despite thousands of specimens in museum collections, none had shown any evidence for how they reproduced. Our discovery proved that they used internal fertilisation and that males had bony claspers for mating.

Earlier this year we added to this by showing in a paper in Biological Reviews 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 in the zone behind the paired pelvic fins.

Placoderm claspers were at first fixed rigidly to their body plates, as observed in Microbrachius, so the fish had to move its entire body around to mate. More advanced placoderms such as the arthrodire Incisoscutum later 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 reverted from internal fertilisation through copulation to external fertilisation by spawning in water, the default primitive condition seen in jawless fishes like lampreys. This must have occurred when bony fishes first evolved, presumably from placoderms like the recently discovered Entelognathus (from China 425 mya), as none of the primitive fossil or living species show any hard evidence for internal fertilisation.

Coelacanths (primitive lobe-finned fishes) mate using internal fertilisation even though they lack copulatory structures. We still do not know how they mate as they are rarely seen alive in their natural environment. Lungfishes, which are closer on the evolutionary ladder to the tetrapods, still spawn externally in water.

Some families of advanced bony fishes, the teleosts, evolved different kinds of internal fertilisation. Guppies, for example, use a modified anal fin spine (a gonopodium) to transfer sperm, although none of these teleosts or lobe finned fishes 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 in their evolution. Later it reappeared again and again in many different animal groups. For example, snakes and some lizards have paired penises, but crocodiles, tortoises, mammals and some birds all have a single penis. The penis was lost in many lineages of flying birds that copulate without using male sexual organs by using a “cloacal kiss” to transfer sperm to the female.

We humans thus mate in a way that first evolved using a single penis in crocodiles and tortoises, from back in the age of dinosaurs. We can thank our distant ancestors, the placoderms, for first evolving this unique method of reproduction.

John Long is Strategic Professor in Palaeontology at Flinders University’s School of Biological Sciences.