Box 1 | The phylogenetic relationship of hagfish, lampreys and jawed vertebrates

From the following article:

Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup

Trevor D. Lamb, Shaun P. Collin & Edward N. Pugh, Jr

Nature Reviews Neuroscience 8, 960-976 (December 2007)

doi:10.1038/nrn2283

Controversy has long surrounded the interrelationship between hagfish, lampreys and jawed vertebrates. One view is that hagfish are basal, having diverged before lampreys split from gnathostomes, whereas an alternative view is that hagfish have degenerated from a lamprey-like ancestor, with hagfish and lampreys forming an agnathan clade, the cyclostomes (round mouths) (Fig. 1). Here we list evidence and arguments that support each view, together with several unresolved issues.

Support for cyclostome monophyly (i.e. hagfish and lampreys as a clade)

  • Molecular–genetic analysis of mitochondrial and nuclear genes has provided strong support for the notion that hagfish and lampreys are sister taxa56, 135, 136, 137, 138, 139.

Support for a hagfish basal position

  • Morphological data on the body plans of extant cyclostomes and their fossil relatives suggest that the unique features of hagfish are plesiomorphic (ancestral), and that these animals approach the condition of the common ancestor of all craniates11, 15, 16, 140, 141.
  • The hagfish 'eye' and retina are very simple, and resemble the pineal organ of vertebrates (see main text). Furthermore, during lamprey metamorphosis, the eye develops from a simple hagfish-like form to a vertebrate-like adult form.
  • Other examples of simplicity are: that the semicircular canals of the labyrinth number just one in hagfish, but two in lampreys and three in jawed vertebrates140, and that the hagfish heart is not innervated.

Unresolved issues that bear on the interpretation

  • The observed variability of molecular-clock rates19, 20, 21 might have implications for the above molecular–genetic estimates.
  • It is possible that the role of 'long-branch attractions' might have been underestimated in previous molecular phylogenies of hagfish.
  • Interpretation of the molecular–genetic differences will be greatly assisted once the entire genome of a hagfish is available. In the meantime, the identification of hagfish opsin genes might resolve the phylogenetic positioning.
  • Extant hagfish display the vertebrate characteristic of delaminating neural-crest-like cells142, but this does not distinguish whether hagfish are basal or a sister group of lampreys.
  • There is insufficient evidence to determine whether the hagfish eye has degenerated from a lamprey-like ancestor or is basal.
  • Degeneration implies that the loss of vision was advantageous to the animals, which were presumably exposed to light throughout their evolution. The daytime intensity of light available to hagfish is sufficient for vision in other deep-sea species143.
  • There is as-yet no report of a fossil agnathan that possessed a lens144. If an ancestor of hagfish did possess a lens, degeneracy would be supported.
  • During early development the hagfish appears to exhibit a 'lens placode', but the ancestral function of this structure might have been to prevent pigmentation of the overlying skin, rather than to induce lens formation145.
  • If a primordial image-forming eye existed in ancestral hagfish, with a lens and a three-layered retina, and which sent its output to the thalamus, then this eye appears to have reverted to a lensless, two-layered retina connected to the region of the brain that regulates circadian rhythm.

Our view

On balance, and in the face of recent interpretations of the molecular evidence, we favour the view that hagfish are basal. In the words of Janvier141 (see also Ref. 135): "All I can say is that, if cyclostomes are a clade, either hagfishes are the most extraordinary example of reversion among vertebrates, or lampreys and gnathostomes are the most extraordinary example of evolutionary convergence."

Whatever the phylogenetic relationship between hagfish and lampreys turns out to be, it is very likely that improved knowledge of the eyes and photoreceptors of these species will help to refine our understanding of the origin of the vertebrate eye.