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Department of Vertebrate Zoology

Division of Fishes

Mirapinnidae, the group of fishes
that contains tapetails and hairyfishes
Sandra Raredon
© Smithsonian Institution

An Ichthyological Family Reunion

Meet the Family Members

Solving the Puzzle

Read the Scientific ArticleBiology Letters, 5(2): 235-239

The Breakthrough Discovery

How could the scientists put the pieces of this bizarre family tree puzzle together? First, Johnson and Paxton proposed that a transformation from tapetails to bignoses was conceivable. They based this suggestion primarily on two features: gill arches and jaw bones.

The gill arches of the two fishes are strikingly similar in structure and the researchers could easily see how they could transform from tapetail to bignose. The jaws posed more of a problem, but Johnson and Paxton determined a feasible trajectory for their modification during development. They noted that with a fairly minimal change, the two mobile, upturned upper jaw bones of the tapetail could move and fuse to form the immobile, horizontal mouth of the bignose.

Comparison of mouth orientations of bignose, tapetail and whalefish
Johnson and Paxton analyzed cleared and stained bignose (left), tapetail (middle), and whalefish (right) specimens. In their investigation of mouth orientation, they agreed that a relatively small change in structure would be required to transition between a tapetail and a bignose, but the transition from a tapetail to a whalefish was much more difficult to fathom.
Photo credit: Dave Johnson
Johnson and Paxton analyzed cleared and stained bignose (left), tapetail (middle), and whalefish (right) specimens. In their investigation of mouth orientation, they agreed that a relatively small change in structure would be required to transition between a tapetail and a bignose, but the transition from a tapetail to a whalefish was much more difficult to fathom.

But this still left the looming question why. What could possibly be the reason for the bignoses to have a mouth that appears to be so poorly adapted to feeding in the depths of the ocean, where food is so scarce?

A clue for that question lay within the fishes' abdomen. Since their first description, the largest specimens of tapetails have been documented as having a distended stomach that is full of recently eaten crustaceans called copepods. This characteristic goes along with the mobile, upturned mouth of the tapetails that seems ideally adapted for rapidly snapping up large quantities of small food items from the plankton.

Dissected abdomen of a bignose fish
When Johnson dissected the abdomen of a bignose specimen, he found no stomach and no esophagus, suggesting the bignose could not actively eat. Instead, the abdomen was full of testes, a narrow intestine full of copepods, and an enlarged liver.
Photo credit: Dave Johnson
When Johnson dissected the abdomen of a bignose specimen, he found no stomach and no esophagus, suggesting the bignose could not actively eat. Instead, the abdomen was full of testes, a narrow intestine full of copepods, and an enlarged liver.

On the other hand, very little attention had been paid to the abdomen of bignoses, aside from Paxton's observation that they almost always contain enlarged testes. When Johnson dissected an intact specimen of bignose, he found much to his surprise, that they have no stomach and no esophagus. In other words, they have no way to eat. Instead, the abdominal cavity of bignoses is filled with testes, a narrow intestine containing only fully-digested copepods, and an enormous liver!

From these findings, Johnson and Paxton hypothesized that the ball of copepods in the tapetails is converted into the enlarged liver of the bignoses and that the liver then provides the only source of nutrition for the bignose. The bignoses apparently then swim continuously, using their enlarged nasal organs to "sniff out" females to mate with before their livers fail.

Transitioning bignose fish
The one tapetail specimen collected below 200 meters (top) is actually a male transitioning from the larval tapetail phase to an adult bignose. Another transitional male (bottom) had been described in 1966 as a bignose species, Megalomycter teevani. Both transitioning specimens shared characteristics that might be expected in transitioning specimens, including a slightly enlarged nasal organ, an intermediate mouth orientation, and a few relatively short pelvic-fin rays.
Photo credit: Dave Johnson, Myers, G. S. & Freihofer, W. C. 1966
The one tapetail specimen collected below 200 meters (top) is actually a male transitioning from the larval tapetail phase to an adult bignose. Another transitional male (bottom) had been described in 1966 as a bignose species, Megalomycter teevani. Both transitioning specimens shared characteristics that might be expected in transitioning specimens, including a slightly enlarged nasal organ, an intermediate mouth orientation, and a few relatively short pelvic-fin rays.

If the bignoses are the adult males that have developed from immature tapetails, then why had no transforming specimens ever been found? In fact, as Johnson and Paxton soon discovered, they had.

As it turns out, during the original description of tapetails in 1956, only one specimen was described as having been collected below 200m (656 feet). That one unusual tapetail exhibited physical traits of both the tapetail and bignose, including an enlarged but not fully developed nasal organ, a mouth orientation that was intermediate between the upturned tapetail mouth and horizontal bignose mouth, a somewhat enlarged liver, and reduced pelvic fins. From these traits, Johnson and Paxton established this unusual tapetail as one in the process of transitioning from tapetail to adult male. Furthermore, a species of bignose originally named Megalomycter teevani that had been described in 1966 was also found to be a transitional male for similar reasons.

But there was still a missing link in the story – where were the female members of this strange tapetail-bignose family? That question was tentatively answered through modern analysis of mitochondrial DNA, which offspring inherit from their mother and provides positive identification of maternal offspring. In this case, the DNA analysis was published in 2003 by a Japanese team headed by Masaki Miya. Their results indicated that the mitochondrial genome of a female whalefish was almost identical to that of the single tapetail specimen they used in their study. With this evidence, those authors suggested that tapetails might be larval cetomimids. Unfortunately, the tapetail specimen used in the study was so small that it had to be completely used in the analysis, and it was never photographed. Thus, there was no "voucher specimen" to verify its identity, and Johnson and Paxton were skeptical that it was indeed a tapetail. They felt that concrete morphological evidence would be necessary to confirm the relationship between these two fishes.

Confirmation of that relationship was difficult to obtain. According to Johnson, "It was hard to imagine the transformations that would convert the upturned mouth of a tapetail into the gaping, horizontal mouth of a whalefish. There are also several other physical disparities between tapetails and whalefishes, including differences in the gill arch configuration, the orientation of the skull to the first vertebra in the backbone and other features."

Transitioning whalefish
The smallest available whalefish specimens (top) were found to have a wide mouth but still exhibited some features in their gill arches and skull that appeared to be transforming. However, the final proof for a relationship between tapetails and adult whalefishes (bottom) came from a transitioning specimen (middle) that shared characteristics of both types of fishes. The middle and bottom specimens here are actually stages of the same whalefish species, Cetostoma regani.
Photo credit: Dave Johnson (top), Sandra Raredon
The smallest available whalefish specimens (top) were found to have a wide mouth but still exhibited some features in their gill arches and skull that appeared to be transforming. However, the final proof for a relationship between tapetails and adult whalefishes (bottom) came from a transitioning specimen (middle) that shared characteristics of both types of fishes. The middle and bottom specimens here are actually stages of the same whalefish species, Cetostoma regani.

The first morphological clues for a relationship between tapetails and whalefishes came when Johnson and Paxton decided to examine the skeletons of the smallest available whalefish specimens. Although the jaws of these specimens appeared fully transformed into the wide mouth seen in the whalefishes, certain areas of the gill arches and, particularly the back of the skull clearly showed the clues they were hoping for – the morphology appeared to be transitioning between tapetails and whalefishes.

The final piece of the puzzle once again came from a transitional specimen that was captured fortuitously at a critical time in the progression of the study. That specimen was developing from a tapetail into a whalefish and exhibited shared characteristics between the two. This one specimen illustrated that the physical change between a tapetail and a whalefish – although drastic – was possible. This specimen was the link that pulled the team's story and their seminal analysis together.

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