Sex, the Early Years

Sex is an ancient tradition. It’s older than today’s continents, older than dinosaurs, older than trees, dating back to a time when vertebrate life thrived in the seas but had not yet ventured onto land. Back then, over 435 million years ago, armored fish were among the first to try this new mode of perpetuating life.

Finding prehistoric creatures caught in the act is an exceptionally rare occurrence. For vertebrates, copulating turtles and courting sharks were among the very few ancient animals that died at a most inopportune moment. Fortunately, we don’t need such intimate associations to track the beginnings of sex. Ancient anatomy tells the tale.

The story starts with procreating placoderms. These archaic fish flourished between 435 and 360 million years ago, and are easily-recognized by having bony armor on the outside, flexible skeletons of cartilage on the inside, and some of the earliest jaws. And, as reviewed in a new paper by Western Australian Museum paleontologist Kate Trinajstic and colleagues, some placoderm fossils preserve both essential mating equipment and the end result of their underwater unions.

The idea that placoderms relied on internal fertilization isn’t new. In 1938, paleontologist D.M.S. Watson published a report on a placoderm called Rhamphodopsis that seemed to preserve claspers – the tubular, paired “intromittent organs” seen in male sharks and rays. If placoderms had claspers, Watson reasoned, then they probably mated the same way as sharks.

But, as Trinajstic and coauthors note, placoderms were thought to be too primitive to have done as the sharks do. Other experts reasoned that placoderms were egg-layers, relying on the same “spray and pray” method employed by many of today’s bony fish. It wasn’t until 2008, when paleontologist John Long and colleagues described a female placoderm with embryos inside, that Watson was shown to be correct. Carrying embryos inside required internal fertilization, marking the placoderm – named Materpiscis in honor of her developing little ones – as one of the earliest vertebrates to have sex.

Rhamphodopsis and Materpiscis weren’t the only placoderms to reproduce this way. Trinajstic and coauthors point out signs of prehistoric sex among a variety of placoderms with names such as Holonema, Campbellodus, and Coccosteus. And given that placoderms are so close to the root of where jawed vertebrates originated, they likely represent the ancestral mode of reproduction for the greater group of biting fish – the gnathostomes – that included our own fishy forebears. For our early ancestors with jaws, at least, sex was likely the norm.

Our ancestors probably didn’t retain the ability permanently. Various descendants of the early jawed fish retained internal fertilization, switched back to egg-laying, and even re-evolved internal fertilization. Among fish alone, internal fertilization has evolved at least 29 times! On an evolutionary  timescale, sex doesn’t always stick around.

And there’s another prehistoric point worth keeping in mind. Placoderms were not just like the sharks, ratfish, and rays that rely on the same mode of reproduction today. In these cartilaginous fish, the male’s claspers are formed from part of the pelvic fins. Not so for male placoderms. Their bony pelvic girdles and claspers were actually separate structures, each supported by struts of cartilage.

Such a separation between fin and clasper might not seem like much, but the disjunction questions one hypothesis about how fish fins – including the precursors of our own limbs – first formed. Pelvic fins are essentially copied pectoral fins, and pelvic fins were thought to mark the back border of where alterations to development could produce new paired structures. But the placoderm claspers were situated behind the pelvic fins, Trinajstic and coauthors explain, and another early fish belonging to a different line – named Euphanerops – had paired anal fins. Either evolutionary tweaks to development could produce paired structures further down along the body than scientists previously thought, or something else was going on during the Age of Fishes. Solving the mystery will help resolve what Long has called the “dawn of the deed“, a milestone preserved in bone.

Reference:

Trinajstic, K., Boisvert, C., Long, J., Maksimenko, A., Johanson, Z. 2014. Pelvic and reproductive structures in placoderms (stem gnathostomes). Biological Reviews. doi: 10.1111/brv.12118