Exposing the intimate details of the sex lives of placoderms

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The media is getting another science story wrong. I keep seeing this discovery of an array of fossil placoderms as revealing the origins of sex, and that's not right. Sex is much, much older, and arose in single-celled organisms. Come on, plants reproduce sexually. A fish is so far removed from the time of origin of sexual reproduction that it can't tell us much about its origins.

Let's get it right. These fossils tells us about the origin of fu…uh, errm, mating in vertebrates.

What we have are a set of placoderm fossils from the Devonian (380 million years ago) of Western Australia (The Aussies are going to be insufferable, now that they can claim to be living in the birthplace of shagging) that show two interesting features: some contain small bits of placoderm armor that show no signs of digestion, and so are not likely to be relics of ancient cannibal feasts, but are the remains of viviparous broods — they were preggers. The other suggestive observation is that the pelvic girdle has structures resembling the claspers of modern sharks, an intromittent organ or penis used for internal fertilization.

These animals are placoderms, an extinct group (which may be paraphyletic) of fish characterized by a massively armored skull. They are thought to belong on the gnathostome stem — that is, somewhere among this motley and diverse and successful collection of animals lies the ancestor to all the jawed vertebrates, such as sharks, bony fish, and tetrapods like us. That makes them an important focus of interest in understanding our own origins, and learning that they used internal fertilization, i.e., were shtupping each other, suggests that this is a very ancient practice.

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Here are some photos of two of the fossils. You may not find them particularly exciting, because most of what you see below is a jumble of bony plates, the disarticulated pieces of the bony skull and scales. What was found was that, among the larger pieces of the adult fish, there were smaller pieces of the same species, in a state of early development. That only this species was found inside, and that they are in a consistent state (unlike a jumble of partially digested meals), suggests strongly that these are embryos.

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a, c, d, P50934; b, e, f, P57640. AMV, anterior median ventral; l.AL, left anterolateral; l.AVL/r.AVL, left and right anterior ventrolaterals; l.Ifg, left inferognathal; l.Mg, left marginal; l.PDL, left posterior dorsolateral; l.PVL/r.PVL, left and right posterior ventrolaterals; l.Sp, left spinal; MD, median dorsal; PMV?, posterior median ventral?; r.ADL, right anterior dorsolateral; l.PNu/r.PNu, left and right paranuchals; r.PDL, right posterior dorsolateral; l.PRO/r.PRO, left and right preorbitals; r.PSO, right postsuborbital; rad, radialia; Scc, scapulocoracoid; wc, worm casts.

The fins of some of the adults also show traces of a distinctive feature that all of us who have done shark dissections will find familiar: an extension of the pelvic fin to form a kind of paired penis called a clasper. That structure is a giveaway that these animals were copulating in those distant Devonian seas.

i-610815cd8460d38187ec91eb6afa4314-arth_pelvic.gif
The phyllolepid Austrophyllolepis ritchiei (MV P160746) showing pelvic girdle in ventral and dorsal aspects, and compared, after being restored (d), with the shark Cobelodus (e). h, Pelvic fin structures restored in dorsal view showing restored fin cartilages in white. art.fac, articular facet for additional pelvic elements; art.rad, radial articulations; bas, basipterygium; bas.art, basipterygial articulation facet; cart, cartilage distal to basipterygium; clas, clasper; j,car, junction cartilages; pel.f, pelvic fin; pel.g, pelvic girdle; pel.sy, pelvic symphysis; rad, radialia.

All this raises some interesting questions. We mammals, of course, use internal fertilization. The ancestral bony fish, the animals that gave rise to modern bony fish and modern tetrapods, are thought to have been spawners that practiced external fertilization, like salmon today. Modern sharks use internal fertilization. Placoderms, down there at the base of the family tree, are now known to have some members that used internal fertilization.

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a, Reproductive modes mapped onto a gnathostome phylogeny, simplified from ref. 7. 'C' marks the gnathostome crown-group node: the part of the tree that lies below this node is the gnathostome stem group; that above it is the crown group. In this scheme, both osteichthyans and chondrichthyans are clades (groups comprising all descendants of a single common ancestor), but the 'placoderms' and 'acanthodians' are not — hence the inverted commas. Examples of placoderm groups are the antiarchs, ptyctodonts and arthrodires, the latter including Incisoscutum (the antiarchs are placed as the lowest placoderm branch and the arthrodires as the highest). b, A conventional consensus phylogeny: placoderms and acanthodians are interpreted as clades.

Now the question is where our reproductive practices came from. Did internal fertilization come first, then our bony fish ancestors threw it away (hard to imagine…), and we then re-evolved the ability independently? Or was it retained in the line that led to us, and bony fish secondarily lost it (given the ubiquit of spawning in fish, this seems unlikely)? Clearly, what we need now are more revealing fossils that expose ancient reproductive behavior.


Long JA, Kate Trinajstic K, Johanson Z (2009) Devonian arthrodire embryos and the origin of internal fertilization in vertebrates. Nature 457:1124-1127.

Ahlberg PE (2009) Birth of the jawed vertebrates. Nature 457:1094-1095.

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Is Ray Comfort opposed to this? Evolution + sex = fundy nightmare.

"The Aussies are going to be insufferable now"

Yes. Yes we are.

Nothing like a little after lunch science paper. Good brain food.

By Nerd of Redhead, OM (not verified) on 26 Feb 2009 #permalink

These fossils tells us about the origin of fu...

Uh fun? Fudge? Fundies? C'mon, out with it, man!

I seem to remember an article suggesting that penises have evolved independently at least three times in vertebrates, and another about basal amniotes possibly having been live-birthers. Evolution uses what is currently available and throws it out if something more useful for the environment at hand comes along, so why not internal fertilization too?

By Sclerophanax (not verified) on 26 Feb 2009 #permalink

Oh great, we'll never hear the end of this.

By Patricia, OM (not verified) on 26 Feb 2009 #permalink

Internal fertilization would seem to be a necessary preadaptation for a fully terrestrial lifestyle. Seeing as some of our closest tetrapod relatives fertilize externally to this day, I wonder if internal fertilization might have been *the* adaptation that allowed dryland life.

Placoderms, down there at the base of the family tree, are now known to have some members that used internal fertilization.

Or, "...some that used members for internal fertilization."

By Richard Smith (not verified) on 26 Feb 2009 #permalink

Or was [internal fertilization] retained in the line that led to us, and bony fish secondarily lost it (given the ubiquit of spawning in fish, this seems unlikely)?

It wouldn't be that unlikely if all Actinopterigians had a common ancestor that reproduced by spawning. However, since modern Sarcopterigian fishes (lungfish) also reproduce by spawning, as well as modern amphibians, it would seem that internal fertilization evolved separately in amniotes. I don't actually know my arthropods that well, but i imagine sex evolved independently a few times within that group, as well. Fascinating stuff, anyway. Thanks for the post-lunch brain wake-up, PZ!

By cactusren (not verified) on 26 Feb 2009 #permalink

The media is getting another science story wrong.

The media that I've listened to has been getting it right....but I'm in Melbourne, and I've been listening to interviews with the paleontologists.

Yep, we're insufferable alright.

Mayby its a matter of semantics, but wouldn't any reproductive process be "sex" or is it that "sex" requires genitalia?

"Did internal fertilization come first, then our bony fish ancestors threw it away (hard to imagine…), and we then re-evolved the ability independently?"

Lungfish and most frogs have external fertilization (even the fully terrestrial ones). Salamanders technically have internal fertilization, but no intromittent organ (they deposit spermatophores, so are somewhere in between). Caecilians, coelocanths and tailed frogs have internal fertilization. Not only that, but bony fish have internal fertilization in some groups as well. I think given the impressive evolvability of this trait in fish and amphibians, I would be surprised if we haven't lost and gained internal fertilization a couple times since it initially evolved.

@12: "sex", i believe, is any reproductive process that involves recombination of genetic material from more than one parent. some of this may also involve, ahem, recreational gymnastics, but that's not a requirement.

By Nomen Nescio (not verified) on 26 Feb 2009 #permalink

The origin of fugu? I thought they evolved much later, what with their squeaky clean genome and whatall.

By Greg Peterson (not verified) on 26 Feb 2009 #permalink

Sex is much, much older, and arose in single-celled organisms..... Let's get it right. These fossils tells us about the origin of fu…uh, errm, mating in vertebrates.

Well, a good clearing of the throat back atcha. I go through this every year, multiple times, whenever the topic of sex comes up....because, of course, in a high school biology course, they use the word 'sex' in the text, but pretty much fail to explain that the term does not, in a biological context, imply internal fertilization, much less copulation. As you might imagine, terms like 'copulation' and 'mating' don't make it into text either. Even an excellent test like Ken Miller's, which mentions the evolution of sexual reproduction, fails to clarify the difference between the way biologists and the popular culture uses it, which is to say to denote either gender or copulation.

So every year I have the same conversation with my classes, details omitted in the interest of avoiding hassles. I duel with creationists publicly and....well, fu..uh, errm, errm.

Ray Comfort makes a stupid remark about sex in 3,2....

By Feynmaniac (not verified) on 26 Feb 2009 #permalink

PZ -

Thanks for a great post. It's incredible that internal fertilization and reproduction occurred so early in the history of gnathostomes. Moreover, this suggests that this may be a "primitive trait" for chondrichthyan fishes. Absolutely amazing.

By John Kwok (not verified) on 26 Feb 2009 #permalink

To see if fishies copulate, thus little fishies born,
We need some "more revealing fossils" (i.e., fossil porn)

A clear fossil pic o' flagrante delicto
would really be reason for bragging--
A stone preservation of fish copulation,
A petrification of shagging!

A fossil find of such an act would surely take some luck
But think... for all eternity, preserved in stone, mid-fuck!

"I never drink water. Fish fuck in it." W. C. Fields

Wow! I actually reach a paleontology thread in time! :-)

Now the question is where our reproductive practices came from. Did internal fertilization come first, then our bony fish ancestors threw it away (hard to imagine…), and we then re-evolved the ability independently? Or was it retained in the line that led to us, and bony fish secondarily lost it (given the ubiquit of spawning in fish, this seems unlikely)?

Must have been lost and regained, because:

1) Claspers are not homologous with amniote penes (not all of which are necessarily homologous with each other, BTW). They are homologous with legs.
2) See arguments from phylogenetic bracketing above.

Salamanders technically have internal fertilization

Neither cryptobranchoids (cryptobranchids and hynobiids) nor apparently sirenids do, though there is apparently evidence that the sirenids have lost it.

Caecilians, coel[a]canths and tailed frogs have internal fertilization.

And the (suddenly) interesting thing about this is that the "tailed" frogs* are the sister-group of all other extant frogs...

* Guess what that "tail" really is. Hint: only males have it.

Not only that, but bony fish have internal fertilization in some groups as well.

Which ones?

The origin of fugu?

Not even close. Fugu are teleost actinopterygian osteichthyans.

I assume this is ovovivipary. Would it be possible to determine if it is?

They actually found the (mineralized) umbilical cord in Materpiscis the ptyctodont, so...

By David Marjanović, OM (not verified) on 26 Feb 2009 #permalink

BTW, in the first illustration, numbers 10 and 11 are not "placoderms", but sarcopterygian osteichthyans (10 looks like a lungfish, and 11 like something closer to us... Gogonasus perhaps?), and 12 is, I suppose, an actinopterygian osteichthyan. 8 and 9 could be chondrichthyans, but I'm not sure.

By David Marjanović, OM (not verified) on 26 Feb 2009 #permalink

I guess the clasper did not evolve to become the clapper to turn off the lights.

By NewEnglandBob (not verified) on 26 Feb 2009 #permalink

Bravo Cuttlefish!

I am in awe of your varied use of meter.

By cactusren (not verified) on 26 Feb 2009 #permalink

Oooh, oooh, I know one!

"Not only that, but bony fish have internal fertilization in some groups as well.
- Which ones?"

Poecilids (mollies) have a modified fin structure called a gonopodium (well, the males do) used for internal fertilization. They are actinops.

By ctenotrish (not verified) on 26 Feb 2009 #permalink

And I used to think I moved here for the beer (and the beaches).

Now after almost 28 years I finally figure it out.

Go figure.

By marc buhler (not verified) on 26 Feb 2009 #permalink

Bravo Cuttlefish! Bravo!

By Patricia, OM (not verified) on 26 Feb 2009 #permalink

Ray Comfort makes a stupid remark about sex in 3,2....

Ten to one it won't involve anything obviously designed to curve toward his mouth.

Figure h is clearly a Native American headdress. Finally, scientific evidence for intelligent design!

@12: "Mayby its a matter of semantics, but wouldn't any reproductive process be "sex" or is it that "sex" requires genitalia?"

Sex implies male and female (or call them A and B if you like) types within a species and that they have haploid germ cells and exchange/combine genetic material in reproduction.

Bacteria (without two types) do exchange DNA; and some call this "sex." I think this muddies the term; and that "gene exchange" is better for bacteria.

In this case (this post, placoderms), the innovation appears to be internal fertilization of eggs and "live" birth of the offspring (as opposed to external fertilization of eggs in the water and subsequent egg hatching -- think salmon spawning.) This is inferred from external structures that appear to correlate to claspers, which perform the function of a penis and the apparent presence of fetal placoderms within the body of adult(s).

Anyway, surprising and cool, given the time frame.

One might imagine that internal fertilization would be highly advantageous in pelagic fish - do it here, then find a spot in the shallows for the eggs, rather than get both sexes to the egg-layin' spot. There's some advantage to delaying the laying of eggs, to let them develop a bit inside the female, which would further protect the brood as well.

Aussie fish are mad rooters*! Yeah!

*Yes, in Australia that's what that word means; it's certainly nothing to do with cleaning drains. Well, unless you're being figurative.

By Wowbagger (not verified) on 26 Feb 2009 #permalink

@Wowbagger (#36)

Does that make male pigs roto-rooters?

By Richard Smith (not verified) on 26 Feb 2009 #permalink

Did internal fertilization come first, then our bony fish ancestors threw it away (hard to imagine…), and we then re-evolved the ability independently?

Careful how you phrase that PZ. Some stupid morons may misunderstand that as though there were some kind of selective consciousness at work directing the fish to keep or discard genes. It reminds me of the misdirected criticism Richard Dawkins received after releasing the Selfish Gene. Some ignorant fucks actually believed that there was a similar kind of deterministic selective consciousness that was "selfish" within a gene.

By Helioprogenus (not verified) on 26 Feb 2009 #permalink

Really you should cut them a break here. Certainly in popular writing, the word sex usually refers to the act of sexual congress. After all, when they say "Sex Sells," they don't mean that people have an abiding interest in meiosis.

Heidi:

I think the Trophy Wife™ has come to accept that being a science god always means there's a bevy of groupies waiting in the wings.

Oh, gack! Please don't start with the male pigs.

By Patricia, OM (not verified) on 26 Feb 2009 #permalink

(The Aussies are going to be insufferable, now that they can claim to be living in the birthplace of shagging)

Shagging? We aren't british. It's 'rooting' here.

The living Coelacanth, Latimaria, has internal fertilization. Amongst modern teleost fishes, some catfishes, sculpins, characins, surfperches, killifishes, etc., have internal fertilization while others in the group may not. Some cichlids do oral sex. Fishes do sexual reproduction in about anyway you can think of.

By Jim Thomerson (not verified) on 26 Feb 2009 #permalink

Did internal fertilization come first, then our bony fish ancestors threw it away (hard to imagine…), and we then re-evolved the ability independently?

Hard to imagine, yes, but that's what it looks like on the new gnathostome phylogeny.

Surprises like this are pretty common, actually. Did you know that there's a good chance that the poison spur of the platypus is not a special feature of monotremes, but an ordinary mammalian feature that the marsupial + placental clade happens to have lost? Here's the pdf -- and here is the pdf that argues that this only holds for the spur, but not for the venom.

Oh, gack! Please don't start with the male pigs.

Too late.

By David Marjanović, OM (not verified) on 26 Feb 2009 #permalink

Cuttlefish is my hero!

(Wow, three links, and it got through immediately! Maybe because two are to the same journal, and the third is to ScienceBlogs... ~:-| )

So it sounds like internal fertilization evolved lots of times within teleosts, but is not ancestral for actinopterygians. Hm. Sturgeons have external fertilization, IIRC. How do the bichirs go about business?

By David Marjanović, OM (not verified) on 26 Feb 2009 #permalink

"Neither cryptobranchoids (cryptobranchids and hynobiids) nor apparently sirenids do, though there is apparently evidence that the sirenids have lost it."

Shoot! I knew that at one point. Just goes to show that you better check a few times before you make generalizations about reproductive life history traits in amphibians.

Just about any trait linked with sex evolves a lot faster than other traits, so it shouldn't be that surprising that it reproductive mode changes frequently. Penises evolve willy-nilly, if you need one its not hard to get one.

Note to self:
Older ladies who have given birth share a common problem sometimes when laughing explosively. I must never, never read something like that from Cuttlefish on a full bladder.

By Lee Picton (not verified) on 26 Feb 2009 #permalink

I think PZ needs a new category for his posts, something like "Awesome Australia" maybe... just to help people, of course.

I always love the fundy kicking that goes on here, but get you guys wound up on the pure science and the discussion is amazing! (I am but humble I.T.)

SCIENCE!

By Charlie Foxtrot (not verified) on 26 Feb 2009 #permalink

The media is getting another science story wrong.

I chalk this up to an annoyingly anthropocentric (or at least mammal-centric) point of view.

By Longtime Lurker (not verified) on 26 Feb 2009 #permalink

These fossils tells us about the origin of fu…uh, errm, mating in vertebrates.

Oh fu...

By Shaden Freud (not verified) on 26 Feb 2009 #permalink

This kind of science is too abstract and far-removed for me.

Any insight into the origins of masturbation?

going to be insufferable?
sandgropers going to be insufferable?

i thought we already were.

#30 wins! Best line in a long time.

By Nancy France (not verified) on 26 Feb 2009 #permalink

Well Pony, Oz has just won my eternal gratitude. Be as insufferable as you like.

By Pete Moulton (not verified) on 26 Feb 2009 #permalink

Here's a thought. Perhaps 'sex' is much older than even with just single-celled organisms. It could have happened with strands of proteins floating and interacting with each other in that primordial soup?

In which case, the birth of sex happened in America!! Afteralll, where else can you find a lot of useless floating shit endlessly exchanging rants in that sewage soup known collectively as right-wing talk radio!

By Teddydeedodu (not verified) on 26 Feb 2009 #permalink

Richard Smith:

Does that make male pigs roto-rooters?

Indeed, and My question, since it has already clearly been evolved by the time of these placoderms is: who were the proto-rooters?

I'll get me hat.

I think it more likely that internal fertilization evolved in at least one placoderm line, but then that line died out without the internal fertilization trait continuing on. Some times groups die out completely, with no descendants.

Quoting David Marjanovic:

So it sounds like internal fertilization evolved lots of times within teleosts, but is not ancestral for actinopterygians. Hm. Sturgeons have external fertilization, IIRC. How do the bichirs go about business?

Chondrichthyans are basally without intromittant organs (e.g. Cladoselache) but gained them relatively early. Same goes for arthrodires, apparently. Modern polypterids engage in external fertilization, as do modern dipnoans, so it is probably reasonable to assume that both basal tetrapods and basal osteichthyans engaged in external fertilization as well. Acquisition of internal fertilization in frogs, salamanders, and caecilians is probably associated with adaptations to water stress in more highly terrestrial lineages, of which we see numerous forms in frogs, salamanders, and caecilians.

OK I am Australian and I am seriously using this story on the next impressionable girl I meet in a hostel in Europe. PZ mate you are the best.

Alternatively to having internal fertilization as an ancestral feature of crown-group gnathostomes, it either emerged independently in ptyctodonts and arthrodires, or my phylogenetic analysis is wrong in placing arthrodires as the sister group of crown-group gnathostomes. However, if it's wrong, then a bunch of braincase characters found in arthrodires are convergently evolved with crown-group gnathostomes.

By Martin Brazeau (not verified) on 26 Feb 2009 #permalink

Chondrichthyans are basally without intromittant organs (e.g. Cladoselache) but gained them relatively early. Same goes for arthrodires, apparently.

Wow.

By David Marjanović, OM (not verified) on 27 Feb 2009 #permalink

@Patricia, OM (#41)

Sorry, I guess I'm just a male pig chauvinist.

@Aaron (#55)

Well, since (normally) soft tissue rarely fossilizes, perhaps T-Rex wasn't so angry after all...

By Richard Smith (not verified) on 27 Feb 2009 #permalink

What's the relation between this and an adaptive immune system?

My understanding is that today, jawed vertebrates are precisely those animals with an adaptive immune system; and that one of the problems with that is that internal fertilisation exposes haploid cells to an immune system reaction - human embryos are supposed to make use of something called the eu-FEDS, and human sperm express universal marker molecules, probably to avoid immune system reaction (the universal marker molecules, if that they are, also appear to be mimicked by some pathogens trying to trick their way past the human immune system).

No doubt, at this point, some creationist will be perking up and ready to go into his (women being subject to their husband in all things, and confined to the household, we can safely assume the creationist is male) speech: "A-ha! So internal fertilisation cannot have evolved with the immune system already present, unless the immune system had, in God-like premonition, made arrangements for universal markers and so on but the adaptive immune system cannot have evolved with internal fertilisation already in place, unless the internal fertilisation mechanisms had already provided for a defence system for the immune system which was yet to come. Irreducible complexity! God did it! Stone all gays!" and so on.

That's nonsense, of course, but it would be interesting to know what the current speculation is on whether the two co-evolved, in which order they evolved, or whether there might have been more than one back-and-forth.

And while this might just be an expression of my extraordinary stupidity, I don't really see how we can find out: the adaptive immune system, as it currently is, doesn't survive from one generation to the next, and I don't think anything in it fossilises. But surely that hasn't stopped someone from speculating about it during their lunch breaks?

Wasn't there a Disney song about this?

(Sung to "March of the Pink Elephants" from Dumbo)

I can stand the sight of worms
And look at microscopic germs
But fornicating placoderms
Are really too much for me.

Maybe Cuttlefish can expand on this.

As its name says (I'll have to fix the stupid, stupid, stupid sentence in the Wikipedia article when I get home), the eutherian fetoembryonic defense system is something peculiar to placental mammals. Other live-bearing gnathostomes presumably use different methods (I don't think this has been researched).

Marsupials, the idea goes, are simply born before the mother's immune system notices.

By David Marjanović, OM (not verified) on 27 Feb 2009 #permalink

@64 Quoting JDM:

Chondrichthyans are basally without intromittant organs (e.g. Cladoselache) but gained them relatively early.

The absence of intromittant organs in Palaeozoic chondrichthyans is only recorded in Cladoselache and thus, along with it having once been known as the oldest chondrichthyan, comes the belief that it is somehow "primitive". However, a number of recent analyses show that Cladoselache is anything but primitive, and may even be in the stem group of holocephalans (chimaeras, etc.), together with all kinds of clasper-bearing sister groups. If claspers are genuinely absent in Cladoselache it's probably a derived feature.

All this, of course, even assumes the fossils of Cladoselache were correctly interpreted . . .

By Martin Brazeau (not verified) on 27 Feb 2009 #permalink

Well, a good clearing of the throat back atcha. I go through this every year, multiple times