Thursday, 18 April 2019

Hagfish from the Late Cretaceous Hâdjula Lagerstätte of Lebanon.

Hagfish, Myxinoidea, are scavenging Jawless Fish, found in deep marine environments, noted for the prodigious production of sticky slime as a defence mechanism. They are one of only two surviving groups of Jawless Fish, along with the Lampreys, Petromyzontiformes, which are parasitic organisms that attach themselves to Fish with a toothy sucker, and have a reproductive cycle that involves breeding in freshwater environments then migrating to the sea. As the only surviving Jawless Fish these organisms are of great interest to taxonomists (scientists that study the relationships between organisms), for the evidence they can provide on the evolution of Vertebrates as a whole. The earliest taxonomic schemes placed the Hagfish and Lampreys along with a variety of Palaeozoic Jawless Fish in a single group, the Agnathia, with all jawed Vertebrates grouped together as the Gnathostomata. The development of cladistic classification systems (computerised analysis of relationships within the group based entirely upon shared common features rather than assumed relationships) has suggested that the Lampreys might be more closely related to the Gnathostomes than they are to Hagfish, making the Hagfish a very ancient member of the Vertebrate lineage, which branched off before the common ancestor of Lampreys and Gnathostomes. The advent of molecular genetic classification techniques has complicated this situation further, suggesting that the Hagfish and Lampreys are more closely related to one-another than either is to the Gnathostomes, with the two groups being collectively called the Cyclostomes, and the Hagfish thought to have lost many features found in Lampreys and Gnathostomes secondarily due to the extreme environments they inhabit and their specialised lifestyle. However, this did not end the debate on Hagfish classification as molecular taxonomy, whilst considered highly accurate for closely related organisms, is known to be less reliable with organisms only distantly related, with no surviving (or surveyed) intermediate relatives; in such cases a phenomenon called long-chain attraction can cause some distantly related organisms to appear more closely related than others, as random genetic drift causes them to share more DNA sequences by pure chance, something which could be the case with ancient groups such as the Hagfish, Lampreys, and Gnathostomes.

To date only three putative fossil Hagfish have been described, Gilpichthys greenei, and Myxinikela siroka, from the Carboniferous Mazon Creek Formation ans Francis Creek Shale of Illinois and Myxineidus gononorum, from the Carboniferous Montceau-les-Mines Lagerstätte of France, though of these only Myxinikela siroka is now thought likely to be a true Hagfish.

In a paper published in the journal PNAS on 5 February 2019, Tetsuto Miyashita of the Department of Organismal Biology and Anatomy at the University of Chicago, and the Department of Biological Sciences at the University of Alberta, Michael Coates, also of the Department of Organismal Biology and Anatomy at the University of Chicago, Robert Farrar and Peter Larson of the Black Hills Institute of Geological Research, Phillip Manning and Roy Wogelius of the School of Earth and Environmental Sciences at the University of Manchester, Nicholas Edwards, also of the School of Earth and Environmental Sciences at the University of Manchester, and of the Stanford Synchrotron Radiation Lightsource at the SLAC National Accelerator Laboratory, Jennifer Anné, again of the School of Earth and Environmental Sciences at the University of Manchester, and of the Children’s Museum of Indianapolis, Uwe Bergmann, also of the Stanford Synchrotron Radiation Lightsource at the SLAC National Accelerator Laboratory, and Richard Palmer and Philip Currie, also of the Department of Biological Sciences at the University of Alberta, describe a new species of Hagfish from the Late Cretaceous Hâdjula Lagerstätte of Lebanon.

The new species is named Tethymyxine tapirostrum, where ‘Tethymyxine’ means ‘Tethys Hagfish’, in reference to the ancient ocean in which the Hâdjula deposits were laid down, and ‘tapirostrum’ means ‘tapering snout’. The species is described from a single specimen preserved on a slab of lithographic limestone; this is a Hagfish 313 mm in length, preserved lying on its left side with its head twisted counter-clockwise to expose its underside. Like other specimens from the Hâdjula Lagerstätte the specimen shows excellent soft-tissue preservation, in this case including 133 slime glands, eight branchial pouches, and the tentacular cartilage.

Synchrotron rapid-scanning X-ray fluorescence mapping of the specimen revealed that the preserved tissues of the specimen were enhanced in Aluminium, Phosphorous, Sulphur, Manganese, Iron, Copper, Zinc, and Arsenic, relative to the surrounding matrix, while the matrix shows raised levels of Silicon, Calcium and Mercury relative to the preserved tissues, giving a very clear outline to the specimen. Some of the specimen is obscured by glue and paint, potentially making it hard to tell soft tissue features from curatorial artefacts, but these could be clearly distinguished using X-ray absorption spectroscopy, as neither contained any organic sulphur compounds, which were present in both the preserved tissues of the specimen and the matrix.

Tethymyxine tapirostrum, a fossil Hagfish from the Cenomanian of Lebanon. Specimen in right lateral view: (A) photograph; (B) interpretive drawing; (C) false-colour composite of distributions of three selected chemical elements (blue is calcium; green is iron; red is phosphorous) from synchrotron rapid-scanning X-ray fluorescence. The visceral anatomy of the specimen in composite photograph (D) and interpretive drawing (E) in the following colour codes: black for liver lobes; brown for branchial pouches; dark grey for intestine; light grey for preserved amorphous tissues; pink for slime glands; stippled grey for other soft tissues that are preserved with distinct outlines. The cranial anatomy of the specimen in interpretive drawing (F) in which preserved structures are indicated in grey shades and stipples. Abbreviations: ant, anterior; int, intestine; L, left branchial pouch; l, left side; lva, liver, anterior lobe; lvp, liver, posterior lobe; post, posterior; R, right branchial pouch; r, right side. Miyashita et al. (2019). 

The absence of a mineralized skeleton in the specimen rules out the possibility of the specimen being a Bony Fish, such as an Eel, while the absence of an oral sucker, tectal cartilages, branchial basket, dorsal fins, and other features rules out the possibility of it being a Lamprey, while it shows several clear features associated with Hagfish such as a long snout, branchial pouches behind the head and slime glands.

The head is shorter as a proportion of total body length than in living Hagfish, the snout more tapered, and the protruding nasohypophyseal tube appears to be absent. The keratinous tooth plates are preserved in association with the anterior lingual cartilages, though their number and shape are hard to define. The number of branchial pouches (eight) is greater than is found in most, but not all, living species. A structure the right position and shape to be the heart is also enriched in Iron, while the apparent intestine extends between the anterior and posterior liver lobes. The slime glands are clearly marked by their profile, and show elevated levels of chlorine, titanium, manganese, iron, copper, nickel, zinc, mercury, and particularly of calcium, phosphorous, and sulphur, consistent with the tightly coiled, mucin-coated α-keratin threads, which have a high calcium phosphatic content. The number of slime glands (133) is higher than in any living Hagfish, but not exceptionally so (the species Rubicundus eos typically has 128-130 slime glands on each side).

A cladistic analysis carried out including Tethymyxine tapirostrum and based entirely upon morphological, rather than genetic, features, suggests that this new species is a member of the crown group Hagfish (i.e. a descendent of the last common ancestor of all living Hagfish), while the Carboniferous Myxinikela siroka was found to be a stem group Hagfish (i.e. a member of the Hagfish lineage, but one which lived before the last common ancestor of all living Hagfish). Interestingly, and unlike previous attempts to classify Hagfish using only morphological features, Hagfish and Lampreys were found to be sister groups, grouped together as the Cyclostomes, with the Carboniferous Gilpichthys greenei and Myxineidus gononorum found to be stem group Lampreys.

This classification scheme also suggests that the Euconodonts are the sister group of the Cyclostomes, while the Anaspids (bony Jawless Fish from the Palaeozoic) are the sister group of the Cyclostomes plus the Euconodonts, the three groups together forming an Agnathian clade, which is the sister group of the jawed Gnathostomes.

A time-scaled phylogenetic tree of Cyclostomes. (A) Summary tree showing Cyclostome relationships. Maximum parsimony and Bayesian inferences converged onto each other in placing Tethymyxine within the Hagfish crown group and supporting Cyclostome monophyly. The precise topology is from the maximum parsimony analysis. Node ages represent median of 95% highest posterior density interval distribution in a Bayesian molecular clock analysis of mitogenomic sequences (16S and COI) under fossilized birth–death model. The crown group of Cyclostomes is united by at least two morphological characters (shown on each stem): keratinous tooth plates (yellow) and periocular position of trunk muscles (red). At Top Right, the nasohypophyseal profiles are compared in ventral view among three selected crown-group Hagfish (B) Tethymyxine tapirostrum; (C) Rubicundus eos; (D) Eptatretus stoutii. To show morphological divergence among the three major crown groups of living vertebrates (E) Myxinoids; (F) Petromyzontiforms; (G) Gnathostomes, each is accompanied by a chondrocranium in left lateral view (green: neural crest-derived nasohypophyseal skeleton; red: mesodermally derived neurocranium; blue: neural crest-derived pharyngeal skeleton). Filled squares represent occurrences of the terminal taxa. Crown nodes are each indicated by a filled circle, and total nodes by an empty circle. Abbreviations: nha,nasohypophyseal aperture; nhb, nasohypophyseal barbels; mo, mouth; ob, oral barbels. Miyashita et al. (2019). 

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