SexyPlac: love in the time of placoderms.

At the beginning of last week, fossil fish made a rare appearance in the news. Although I secretly cling onto the futile hope that this was because the world just can’t get enough of placoderms, it was probably actually because the story was about sex – dirty, Devonian sex – with a Nature paper from Long et al. revealing the earliest evidence of vertebrate internal fertilisation in the appropriately named fish Microbrachius dicki. Microbrachius (first described in 1888 by the palaeoicthyological machine Ramsay Traquair) is a placoderm from the Devonian (about 419-359 Mya) of Scotland, and said evidence comprises pelvic claspers, similar to those used for internal fertilisation in modern sharks. While the traditional view of the evolution of internal fertilisation is that it evolved from external fertilisation, Long et al. argue that Microbrachius shows that it was in fact the other way around: the modern spawning of many bony fish is derived from an internally fertilising ancestral state. Either way Microbrachius adds an interesting chapter to the story of the placoderms.

Placoderms

Phylogeny showing the various placoderm morphophologies (note that here they’re monophyletic, and sister group to extant jawed vertebrates). (From Palaeos.com)

Placoderms were a group of heavily-armoured jawed fish from the Devonian with a diverse range of morphologies; these included flattened ray-analogues such as the rhenanids, the holocephalan-like ptyctodontids, and the more conventionally fish-shaped arthrodires, which included massive predators such as Dunkleosteus. Antiarchs, the group to which our hero Microbrachius belonged, have a particularly weird bodyplan that led to them initially being described as arthropods: a box-like, plated body with jointed, armoured pectoral fins and closely-set eyes. The phylogenetic relationships of placoderms are still poorly understood, but they lie somewhere on the gnathostome stem as the closest group to modern jawed fish. Historically they have been thought of as a monophyletic group, ie. comprising all of the descendents of a single common ancestor. More recent finds, such as Entelognathus – a placoderm with osteichthyan-like facial bones – suggest they may form a paraphyly, with some groups and taxa (eg. Entelognathus) more closely related to modern gnathostomes than others.

Phylo

Diagram illustrating (a) monophyletic placoderms, where placoderms are all descendants of a single common ancestor, and the sister group to living jawed vertebrates, and (b) paraphyletic placoderms, where some groups of placoderm are more closely related to living gnathostomes than others.

Many aspects of placoderm anatomy are of great interest to palaeontologists due to the information they provide about the ancestral state for vertebrates, and those pertaining to their sex-life are no different. In addition to live birth in the ptyctodontid placoderms (Materpiscis), structures described as pelvic claspers have been described in both ptyctodontid (Austroptyctodus) and arthrodire (Incisoscutum) placoderms. The closest analogue to these claspers in modern vertebrates is the pelvic claspers of cartilaginous fish. Male sharks and rays have an extension of the pelvic fin pointing backwards, which is used to channel sperm into the female whilst mating, while male holocephalans go one further and have two claspers in addition to their pelvic ones: one anterior pair further forward on their body, and one single clasper on the midline of their head. While both placoderm and chondrichthyan claspers are grooved structures and are found in roughly the same place, they have important differences, which suggest they aren’t actually homologous: the claspers of sharks are made of cartilage and attached to the pelvic fin, whereas those of placoderms were made of dermal bone (like their armour) and were completely separate from any other structure.

Sexyplac male2

a-c are the pelvic clasper (with reconstruction) of male Microbrachius. d-g are claspers in other placoderms, and h-i show the fossil Microbrachius with claspers in situ. From Long et al.

The claspers of male Microbrachius are like those of other placoderms in that they are grooved dermal plates separate from the pelvic fin. Like the claspers of ptyctodonts, those of Microbrachius are hook-shaped (arthrodire claspers are thin rods), and would have been immobile. Female Microbrachius have also been described with blade-like plates in the same region, with ornamentation (ie. bumps and ridges) on the surface that would have faced inwards. The authors interpret these as genital plates, which would have received and gripped the males’ claspers whilstmating. With this interpretation, the presence of claspers can be used to infer the presence of internal fertilisation, reconstructed by the authors as a form of side-by-side copulation apparently akin to square dancing.

Sexyplac female2

Female Microbrachius with genital plates labelled (from Long et al.)

This is all very well, but if we already know that claspers are widespread in both placoderms and modern sharks, why do we care about Microbrachius? One reason is that in a scenario of placoderm paraphyly (ie. where the various groups are arrayed along the gnathostome stem), antiarchs are likely to be the most rootwards group, ie. least closely related to living gnathostome. Long et al. argue that if placoderms are paraphyletic then internal fertilisation, present in chondrichthyans and in multiple placoderm groups including the most ‘primitive’, is likely to be the ancestral state of jawed vertebrates. This would in turn mean that the spawning behaviour of today’s bony fish and amphibians, where females lay eggs and the males fertilise them externally, is actually secondarily derived from internal fertilisation, completely changing how we understand the evolution of internal fertilisation in vertebrates.

Sexyplac phylo

Figure showing the presence and absence of pelvic claspers through (paraphyletic here) placoderms and other vertebrates. (From Long et al.)

While this would be an exciting, paradigm-shifting set of circumstances,it remains far from firmly established. One issue, which the authors acknowledge, is that placoderm paraphyly is far from definite. While it has been repeatedly found to be the case in various recent analyses, the various taxa and groups tend to switch position a lot between analyses suggesting that the result isn’t very stable. If placoderms, or even just placoderm groups with claspers, were monophyletic then internal fertilisation with pelvic claspers could just be a synapomorphy (uniting character) of this group, derived independently from that of chondrichthyans. It’s also possible that the various placoderm claspers aren’t homologous at all. Structurally they appear (to my untrained eye, at least) quite different and in some antiarch taxa, such as Bothriolepis, no direct evidence of claspers has been found despite there being thousands of known specimens. If the claspers aren’t homologous, it doesn’t actually mean that the internal fertilisation isn’t, but it would reduce the argument’s weight somewhat.

Sexyplac

Microbrachius apparently loves an audience. Mandatory listening. (From Long et al.)

Whatever the answer, this new description of Microbrachius offers an intriguing glimpse into the sex life of a 400 million-year-old fish. Its significance will ultimately come down to the resolution of placoderm phylogenetic relationships, as well as a better understanding of the homology of the claspers in various placoderm taxa. At the very least we can be thankful for the serendipity of the first fish known to have sex coincidentally having the species name dicki.

 

References

Long et al. (2014) Copulation in antiarch placoderms and the origin of gnathostome internal fertilisation. Nature.

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Announcing the official TDS Facebook page.

Afternoon to all readers of The Dino Sirs. Richard and I have an announcement to make, TDS has an official Facebook page! Either click like on the sidebar widget or follow the link (click me). We’ll announce all our future posts as well as post amusing (vaguely) palaeontological tidbits, as well as our pictures etc. from conferences etc.

Obligatory related humorous tidbit.

Taxon of the Week: Hauffiopteryx

In keeping with Richard’s aquatic theme for the previous TotW, this week the ichthyosaur Hauffiopteryx typicus has the honour of being the last TotW of January 2014. It also has the honour of being the first post to announce some exciting work (unpublished at time of writing) being carried out by Ryan on the first 3D reconstruction of an ichthyosaur (amongst other firsts, see below!).

During the Mesozoic, marine environments were very different. In modern oceans, marine reptiles (turtles, sea snakes, marine iguanas, saltwater crocs etc.) aren’t hugely important in the grand scheme of things, with only around 100 species around today (compared to the 30,000 ish species of teleost fish swimming about). However, take it back to the Mesozoic (especially from the Jurassic onwards, for everything except ichthyosaurs) and marine reptiles dominated the higher trophic levels, with 5 big groups (ichthyosaurs, plesiosaurs, pliosaurs, mosasaurs and thalattosuchians) emerging by the Cretaceous. We see a huge range in morphological diversity, from long necked plesiosaurs (e.g. Elasmosaurus,  and the amazingly named Attenborosaurus), pliosaurs with heads reaching over 2.5m in length, crocodiles trying to be sharks, and finally ichthyosaurs.

marinrep

TIL: pliosaur taxonomy consists of just ‘pliosaur’ and ‘big pliosaur’.

nessieseadragon

A more useful figure detailing different Mesozoic marine reptiles (Motani 2010).

Whilst ichthyosaurs seem a little less awesome than ‘shark crocs‘, Predator X and the Loch Ness Monster, ichthyosaurs have a wealth of published literature that makes them really cool. Looking at the organisms’ gross anatomy, it looks fish-like, and true, it is the first tetrapod to adapt a fish-like body plan, allowing them to adopt (over the course of the Triassic and the early Jurassic) a more thunniform body plan, aiding more efficient swimiming. This has led ichthyosaurs to conquer both shallow sea and open ocean environments.  Ichthyosaurs also have incredible eyesight (see Motani 1999), allowing them to be efficient deep-water predators. Speaking of feeding, they also may adopt suction feeding (although heavily debated). Shastasaurus is also the largest marine reptile ever described (take that Predator X). They’ve also been shown to give birth to live young, as modern whales and some sharks do. As well the aforementioned cool stuff, ichthyosaurs have made a splash (heh) in Nature recently, with an ichthyosaur (along with a mosasaur) providing the first direct evidence of skin pigmentation in the fossil record which aren’t feathers. This has lead to the conclusion that ichthyosaurs may have been dark coloured all over (rather than countershading, seen in some modern cetaceans, for example).

the_dapper_ichthyosaur_conundrum_by_robthedoodler-d4uh3vs

If you’re not convinced yet that ichthyosaurs are cool, here are some dapper gentlemen ichthyosaurs. (From RobTheDoodler, DeviantArt).

However, poor little Hauffiopteryx, as yet, has received little attention. Up until 2008 the genus Hauffiopteryx was previously described as just another species of Stenopterygius (S. hauffianus, von Huene 1931). In 2008, Maisch et al. redescribed S. haffianus specimens, leading to the establishment of a new genus, Hauffiopteryx , with H. typicus being the only species within it. H. typicus has significantly larger orbits and a much more slender rostrum (snout) than S. hauffianus (amongst other apomorphies).

Hauffiopteryx_NT

Reconstruction of Hauffiopteryx typicus, (c) N. Tamura.

More Hauffiopteryx trivia:

  • Up to 3m long
  • From the Toarcian (early Jurassic, 182.7-181.8 Ma) of England, Luxembourg and Germany.
  • Small size thought to possibly indicate ventures into shallower waters to feed.

Yet, in 2011 Caine & Benton described 8 rediscovered specimens (initially from Somerset, England), all infants and juveniles. These 8 individuals (both H. typicus and S. triscissus) are all remarkably preserved (with some soft tissue preservation). One specimen in particular, M1399, may well turn out to be incredibly important. 

hauff_caine&benton

Skull of M1399, right lateral view.

As you can see from the pictures of M1399, it is exceptionally preserved in 3D, which is uncommon in the usually laterally compressed ichthyosaur fossil material. This is extremely exciting, because it means we can CT scan it and explore the cranial anatomy of ichthyosaurs in three dimensions. Which by the way, has never really been done before (aside for some work on ichthyosaur teeth, see references), and is even more amazing considering M1399 is a wee juvenile. And that’s exactly what I’ve been up to lately. For the past few months I’ve been beavering away in the tomography lab, attempting to create M1399’s (which I’ve come to affectionately call ‘The Hauff’) 3D cranial reconstruction. So far results have been really interesting, we’ve seen some things which (according to my research so far) has never been seen in ichthyosaurs before. Due to the great 3D preservation, we’re hoping to reconstruct one of the first ichthyosaur endocast (and maybe alongside some more functional/musculature stuff). Unfortunately that’s all I can say right now, as it’s still a long way off from being published (hopefully later this year/2015). As soon as I can tell you guys more, I’ll post right here on TDS.

M1399_after_a_web_0

M1399 (left lateral view). What a beauty. From JESBI collection page.

References

Motani, R. et al. (1999). Large eyes in deep diving ichthyosaurs. Nature 402, 747.

Lindgren, J. et al. (2014). Skin pigmentation provides of convergent melanism in extinct marine reptiles. Nature doi:10.1038/nature12899.

Motani, R. (2005). Evolution of fish-shaped reptiles (Reptilia: Ichthyopterygia) in their physical environments and   constraints. Annu. Rev. Earth Planet. Sci. 33, 395–420.

Motani, R. (2009). The Evolution of Marine Reptiles. Evo Edu Outreach 2, 224-235.

Fröbisch, N., B. et al. (2013). Macropredatory ichthyosaur from the Middle Triassic and the origin of modern trophic  networks. PNAS, 110(4), 1393-1397.

Sanders, P., M. et al. (2011). Short-Snouted Toothless Ichthyosaur from China Suggests Late Triassic Diversification of Suction Feeding Ichthyosaurs. PLoS ONE 6(5): e19480.

Motani R. et al. (2013) Absence of Suction Feeding Ichthyosaurs and Its Implications for Triassic Mesopelagic Paleoecology. PLoS ONE 8(12): e66075. doi:10.1371/journal.pone.0066075

Caine, H. & Benton M., J. (2011). Ichthyosauria from the Upper Lias of Strawberry Bank, England. Palaeontology 54 (5), 1069-1093.

Motani, R. (2005) Detailed tooth morphology in a durophagous ichthyosaur captured by 3D laser scanner,
Journal of Vertebrate Paleontology, 25:2, 462-465, DOI: 10.1671/0272-4634(2005)025[0462:DTMIAD]2.0.CO;2