Sex and the Primordial Ooze

The rise of copulation as a vertebrate reproductive strategy may have driven crucial evolutionary change and explosive species radiation.

By | January 1, 2013

THE UNIVERSITY OF CHICAGO PRESS, OCTOBER 2012Reproduction is without a doubt one of the most delightful parts of being a vertebrate. Unlike arthropods, whose mating rituals can range from seemingly perverse acts culminating in the death of the male (think praying mantises and certain spiders) to traumatic rape and insemination (think bed bugs), for us more civilized backboned animals, mating is mostly an act of great pleasure following courtship and foreplay. Without sex and the subsequent mingling of two individuals’ genetic material, gene pool transformation would not occur. Sex is therefore central to evolutionary change.

The rise of this most pleasurable and evolutionarily productive of all vertebrate behaviors is the focus of my latest book, The Dawn of the Deed.

There are many strange and interesting ways in which living vertebrates reproduce. The oldest and likely most primitive method is displayed by fishes, which typically spawn gametes into water: females lay eggs and males fertilize them by shedding sperm over them.

But some fishes—in particular sharks, rays, and their kin (called chondrichthyans)—perform a kind of copulation, which is necessarily preceded by mating behaviors such as ritual courtship. In some species of whaler sharks (Carcharhinus sp.) the males bite the females’ pectoral fins to prepare the females for mating and to properly position themselves for the act of copulation. Following their courtship rituals, chondrichthyan males insert erectile claspers derived from the pelvic fin skeleton into females’ cloacal openings to transfer sperm, usually bundled in discrete packages.

The origins of vertebrate copulation have for years been an enigma to paleontologists, as little fossil evidence existed to show how the oldest-known fishes mated. One group of extinct fishes, the armor–plated placoderms, which flourished 410–359 million years ago during the Devonian Period, provide the first insights into early vertebrate sexual behavior. One group of placoderms, the ptyctodontids, showed variation in their pelvic fins, leading English paleontologist D.M.S. Watson to suggest in the 1930s that they showed sexual dimorphism—major male-female differences in reproductive or other structures.

Recently my colleagues and I made a major discovery confirming that these ancient fishes did in fact copulate. In the Gogo Formation of Western Australia we found an unborn embryo inside a mother fish, perfectly fossilized in 3-D, and still attached by a mineralized umbilical cord. It was a new species, so naturally we named it Mater-
piscis, meaning mother fish.

Our findings strongly suggested that copulation in vertebrates first arose within this group, widely acknowledged as the most basal of all jawed vertebrates. Internal fertilization in vertebrates thus turns out to be coincident with the origins of jaws and teeth themselves.

This raises a very interesting but radical idea. Did jaws evolve mainly for feeding, as most scientists would surmise? Or did jaws and teeth evolve primarily to facilitate copulation, as seen in the courtships of those extant sharks who bite their mates’ pectoral fins to hold on while inserting their claspers?

An even broader question arises from our discoveries: Could a reproductive strategy have served as a potential driver of explosive evolutionary radiations? The placoderms underwent the first great species explosion for all vertebrates, with some species clades containing more than 50–100 closely related taxa distributed around the globe within a relatively short span of geological time. Such problems show why the study of early vertebrate anatomy and the pursuit of new fossil evidence from the field is still highly relevant for the study of evolutionary biology. 

John Long is a paleontologist at the School of Biological Sciences, Flinders University, South Australia. He previously served as Vice President of Research and Collections at the Natural History Museum of Los Angeles County. Read an excerpt of The Dawn of the Deed: The Prehistoric Origins of Sex.

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Avatar of: James V. Kohl

James V. Kohl

Posts: 194

January 5, 2013

I'm tempted to pair the study of vertebrate anatomy with the conserved molecular biology of vertebrate reproduction and species divergence. For example, Kochman (2012) writes: "The discovery of the fact that one decapeptide molecule, among the GnRHs, was constructed perfectly at the beginning of 400 million years evolution and that it is not possible to improve its physiological potency using the any natural amino acid is, in my opinion, important, fascinating and beautiful."

Further back, we have invertebrate juvenile hormone (JH) in a similar modulatory capacity. What's most telling, perhaps, is that a form of the GnRH molecule found in yeast species at the advent of nutrient chemical-dependent pheromone-controlled sexual reproduction alters LH in the cultured rat pituitary, and that mammalian GnRH is epigenetically effected by  pheromones.

This links species divergence to nutrient chemical-dependent pheromone-controlled reproduction in species from microbes to man. What's clearest, however, is that the role of nutrient chemicals in the adaptive evolution of the cricket mandible, preceeds the structural adaptation of the penis. That helps to establish the natural order of things, where Natural Selection is for food and Sexual Selection is for pheromones associated with sexually dimporphic physical features across an evolutionary continuum of ecological, social, neurogenic, and socio-cognitive niche construction.
 

Avatar of: Curculio

Curculio

Posts: 49

February 14, 2013

How do you define radiations? What about cichlids or the many lineages in the Amazon and other river basins? The question about radiations and copulation needs to be separated from how copulation leads to better ability to be terrestrial (not necessary since there are non-copulating invertebrates), which leads to greater population fragmentations, due to limitations in motility or distance/physical barriers.  It is hard to be plankton on land.

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