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.

Advertisements