This site needs JavaScript to work properly. Please enable it to take advantage of the complete set of features!
Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation

Save citation to file

Add to Collections

Name must be less than 100 characters
Unable to load your collection due to an error
Please try again

Add to My Bibliography

Unable to load your delegates due to an error
Please try again

Your saved search

Would you like email updates of new search results?
Saved Search Alert Radio Buttons
()

Create a file for external citation management software

Your RSS Feed

. 2019 Feb 5;116(6):2146-2151.
doi: 10.1073/pnas.1814794116. Epub 2019 Jan 22.

Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological-molecular conflict in early vertebrate phylogeny

Affiliations

Affiliations

  • 1 Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637; tetsuto@uchicago.edu.
  • 2 Department of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada.
  • 3 Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637.
  • 4 Black Hills Institute of Geological Research, Hill City, SD 57745.
  • 5 School of Earth and Environmental Sciences, University of Manchester, M13 9PL Manchester, United Kingdom.
  • 6 Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, CA 94025.
  • 7 The Children's Museum of Indianapolis, Indianapolis, IN 46208.

Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological-molecular conflict in early vertebrate phylogeny

Tetsuto Miyashita et al. Proc Natl Acad Sci U S A. .
. 2019 Feb 5;116(6):2146-2151.
doi: 10.1073/pnas.1814794116. Epub 2019 Jan 22.

Affiliations

  • 1 Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637; tetsuto@uchicago.edu.
  • 2 Department of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada.
  • 3 Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637.
  • 4 Black Hills Institute of Geological Research, Hill City, SD 57745.
  • 5 School of Earth and Environmental Sciences, University of Manchester, M13 9PL Manchester, United Kingdom.
  • 6 Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, CA 94025.
  • 7 The Children's Museum of Indianapolis, Indianapolis, IN 46208.

Abstract

Hagfish depart so much from other fishes anatomically that they were sometimes considered not fully vertebrate. They may represent: (i) an anatomically primitive outgroup of vertebrates (the morphology-based craniate hypothesis); or (ii) an anatomically degenerate vertebrate lineage sister to lampreys (the molecular-based cyclostome hypothesis). This systematic conundrum has become a prominent case of conflict between morphology- and molecular-based phylogenies. To date, the fossil record has offered few insights to this long-branch problem or the evolutionary history of hagfish in general, because unequivocal fossil members of the group are unknown. Here, we report an unequivocal fossil hagfish from the early Late Cretaceous of Lebanon. The soft tissue anatomy includes key attributes of living hagfish: cartilages of barbels, postcranial position of branchial apparatus, and chemical traces of slime glands. This indicates that the suite of characters unique to living hagfish appeared well before Cretaceous times. This new hagfish prompted a reevaluation of morphological characters for interrelationships among jawless vertebrates. By addressing nonindependence of characters, our phylogenetic analyses recovered hagfish and lampreys in a clade of cyclostomes (congruent with the cyclostome hypothesis) using only morphological data. This new phylogeny places the fossil taxon within the hagfish crown group, and resolved other putative fossil cyclostomes to the stem of either hagfish or lamprey crown groups. These results potentially resolve the morphological-molecular conflict at the base of the Vertebrata. Thus, assessment of character nonindependence may help reconcile morphological and molecular inferences for other major discords in animal phylogeny.

Keywords: Myxinoidea; cyclostome; monophyly; soft tissue; synchrotron.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

A summary of hypotheses for…

Fig. 1.

A summary of hypotheses for cyclostome relationships. The hypotheses differ in cyclostome monophyly…

Fig. 1.
A summary of hypotheses for cyclostome relationships. The hypotheses differ in cyclostome monophyly or paraphyly (columns), and about relationships of fossil “agnathans” with respect to the cyclostome and gnathostome crowns (rows). Blue box = support from morphological data; red box = support from molecular data. Yellow box = compatible with both data types. (A) Noncladistic classification schemes based on morphological data with cyclostomes nested among agnathans. (B) Craniate hypothesis in early cladistic analyses based on morphological data, where hagfish and fossil agnathans become nested outside the crown vertebrate node. (C) Cyclostome hypothesis as supported by molecular data. Fossil agnathans are assumed on the gnathostome stem. (D) Craniate hypothesis in recent analyses of morphological data, where hagfish remain nested outside the crown vertebrate node. Fossil agnathans are placed on the gnathostome stem. (E) Updated cyclostome hypothesis supported by the analyses of morphological data presented in this paper. Hagfish and lampreys form a clade of cyclostomes as supported by the molecular inferences. However, some fossil agnathans are closer to the cyclostome crown than to the gnathostome crown.
Fig. 2.

Fig. 2.

Tethymyxine tapirostrum gen. et sp.…

Fig. 2.

Tethymyxine tapirostrum gen. et sp. nov, a fossil hagfish from the Cenomanian of…
Fig. 2.
Tethymyxine tapirostrum gen. et sp. nov, a fossil hagfish from the Cenomanian of Lebanon. Holotype (BHI 6445) in right lateral view: (A) photograph; (B) interpretive drawing; (C) false-color composite of distributions of three selected chemical elements (blue = Ca; green = Fe; red = P; Ca and Fe in HZ setup and P in LZ setup, 99.9% threshold) from SRS-XRF. The visceral anatomy of BHI 6445 in composite photograph (D) and interpretive drawing (E) in the following color codes: black = liver lobes; brown = branchial pouches; dark gray = intestine; light gray = preserved amorphous tissues; pink = slime glands; stippled gray = other soft tissues that are preserved with distinct outlines. The cranial anatomy of BHI 6445 in interpretive drawing (F) in which preserved structures are indicated in gray 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.
Fig. 3.

Fig. 3.

A time-scaled phylogenetic tree of…

Fig. 3.

A time-scaled phylogenetic tree of cyclostomes. ( A ) Summary tree showing cyclostome…

Fig. 3.
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 (SI Appendix, Fig. S6). Node ages represent median of 95% HPD distribution in a Bayesian molecular clock analysis of mitogenomic sequences (16S and COI) under fossilized birth–death model (see SI Appendix, Fig. S9 for a fully calibrated maximum clade credibility tree with node intervals). 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 hagfishes (B: Tethymyxine tapirostrum; C, Rubicundus eos; D, Eptatretus stoutii; the latter two based on ref. 29). 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.

References

    1. Janvier P. Early Vertebrates. Clarendon Press; Oxford: 1996.
    1. Janvier P. Homologies and evolutionary transitions in early vertebrate history. In: Anderson JS, Sues H-D, editors. Major Transitions in Vertebrate Evolution. Indiana Univ Press; Bloomington: 2007. pp. 57–121.
    1. Hardisty MW. Lampreys and hagfishes: Analysis of cyclostome relationships. In: Hardisty MW, Potter IC, editors. The Biology of Lampreys. Academic; New York: 1982. pp. 165–259.
    1. Yalden DW. Feeding mechanisms as evidence for cyclostome monophyly. Zool J Linn Soc. 1985;84:291–300.
    1. Braun CB, Northcutt RG. The lateral line system of hagfishes (Craniata: Myxinoidea) Acta Zool. 1997;78:247–268.

Publication types

LinkOut - more resources

Cite
Morty Proxy This is a proxified and sanitized view of the page, visit original site.