Three groups of fish are actually the males, females and larvae of one family

Blogging on Peer-Reviewed ResearchWhalefishes, bignoses and tapetails - these three groups of deep-sea fishes couldn't look more different. The whalefishes (Cetomimidae) have whale-shaped bodies with disproportionately large mouths, tiny eyes, no scales and furrowed lateral lines - narrow organs on a fish's flanks that allow it to sense water pressure.

The tapetails (Mirapinnidae) are very different - they also lack scales but they have no lateral lines. They have sharply angled mouths that give them a comical overbite and long tail streamers that extend to nine times the length of their bodies.

The bignoses (Megalommycteridae) are very different still - unlike the other two groups, they have scales, their mouths are small and their noses (as their name suggests) are very large.

Based on these distinct bodies, scientists have classified these fishes into three distinct families. Now, it seems they are wrong. Amazingly enough, the three groups are all just one single family - the tapetails are the larvae, the bignoses are the males and the whalefishes are the females. The entire classification scheme for these fishes needs to be reworked, as many distinct "species" are actually different sexes or life-stages of the same animal.

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Each form has such different lifestyles and diets that the larvae undergo dramatic transformations as they mature, completely remodelling their skulls and organs in order to prepare for their new lives. Males go through the greatest changes. Their jaw bones waste away, their mouths shrink, their intestines shrivel, and their food pipe and stomach disappear altogether. Once the transformation is complete, they will never feed again. Their chest cavity is filled with sexual organs and a massive liver that sustains them - they are little more than swimming sperm factories.

To power this lifelong fast, some young tapetails gorge on small crustaceans called copepods. They eat so many that they develop enormous potbellies and it's this stored food that creates the male's enormous liver. Tapetails that grow up to become female whalefishes don't need such extravagant stores - they continue to eat throughout their adult lives and as a result, they become the biggest of the three forms.

This metamorphosis is completely unparalleled among back-boned animals, and it has fooled biologists for decades. In retrospect, however, all the clues to this astonishing life cycle were there.

So far, 120 specimens of tapetails have been collected (five species in total) and all are sexually immature. In over 600 whalefish specimens across 20 species, no one had ever found any larvae or any males - all of them were sexually-mature females. And all the 65 specimens of bignoses (across four species) are male. Tapetails have only ever been found in the topmost 200m of ocean, while bignoses and whalefishes lives in lower waters of 1000m or deeper.

Based on the odd physical similarity, some scientists had suggested that these groups may be one and the same, but there wasn't any good evidence to back that up until 2003. Then, a Japanese group led by Masaki Miya found that a whalefish and a tapetail had almost identical genomes in their mitochondria (small structures within all animal cells). Now, David Johnson from the Smithsonian Museum, working with Miya's group, has settled the issue.

He found three specimens - two bignoses and one whalefish - that are clearly tapetails which have been caught mid-makeover. One bignose, Megalomycter teevani, still retains the vertically angled mouth of its former self and traces of pelvic fins, which the larval tapetails have but the adult bignoses don't. It's eponymous big nose is only half-grown. The other bignose species - Parateniophorus gulosus - is in a similar but earlier stage of transformation. The whalefish specimen belongs to the most common species, Cetostoma regani, and while none of the other 184 specimens have any pelvic fins, this one does.

Johnson backed up this physical evidence by sequencing the mitochondrial genomes of several species from all three groups. He used these to build a family tree, which clearly showed that P.gulosus is, in fact, the same species as C.regani.

Other species can also be merged together. For example, Johnson's family tree shows that Eutaeniophorus (a tapetail), Ataxolepis (a bignose) and Cetiomimus (a whalefish) are all actually the same genus. Clearly, the entire group's classification needs to be reviewed, and that can only be done by finding more specimens and taking more samples.

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If anyone wants to know more about deep-sea marine life, I wholeheartedly recommend heading over to Deep Sea News, a truly first-class blog that's just been recently set up on its own website.

Reference: Biology Letters; reference to be confirmed

Images by David Johnson

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Awesome. It's really crazy how much diversity evolution has created.

A living male sperm bank, only heard of something like this in bad science-fiction stories about (straw(wo)men) feminists. ;)

Btw. good article.

By student_b (not verified) on 20 Jan 2009 #permalink

If I am not wrong, many marine fishes (e.g. the spinous larvae of swordfish, the stalked eye larvae of Myctophum lanterfish) have quite bizarre larval forms worlds apart from their adult or even juvenile stages. Filamentous structures on their fins is another common trait. Could the whalefishes be said to be undergoing a kind of extended 'neotenic' stage?

Holy smokes Mr. Yong! That is a whalefish of tale! Thanks for the awesome shout out by the way, it means alot coming from a writer I truly admire.

@Mike - As a taxonomist (not a fish one), I wouldn't consider this an embarrassment. Taxonomies are hypotheses that can tested and falsified. To the classical taxonomist working anytime before 20-30 years ago, it would be likely the condition of the fish was horrid. Likely coming from trawls or dredges, or possibly even as a bycatch. New specimens an new information open the door to improved understanding.

Reminds me of a re-organization of pterosaurs that took place not too long ago. In some pterosaur examples, as many as 5 different forms, previously thought to be in different genera, were shown to be of the same species, having died at different ages. (You can find this in the wonderful book Pterosaurs From Deep Time )

Wow.. sounds like it could take a lot of work to update everything after this lot.
very interesting!

As ever, thanks for the comments folks.

Budak - my understanding of neoteny is that it's the retention of juvenile traits in a sexually mature individual. In which case, the term wouldn't apply here as the whalefishes are physically distinct from the tapetails.

Student_b - if you're impressed by this, then deep-sea anglerfishes will rock your world. When males find females, they bite them and eventually fuse to their bodies. The males slowly degenerate until they're nothing more than pairs of testes attached to the female. It's an extreme adaptation to a world where mates are hard to find.

Ed,
You did a fantastic job on this - really fun to read! I wanted to point out that the morphological part of this was a real collaboration between me and the second author, John Paxton, who has been studying whalefishes for most of his professional life - we, as the two "old fart" systematists, had great fun solving the mystery, and plan a larger more detailed paper describing various aspects of the morphology. One other thing - I only took the picture of the male - here are the credits for the others:

Upper images: Tapetail postlarval stage (ca. 6 cm + streamer) of cetomimid whalefish off Cozumel, Mexico; photo Donald Hughes.
Middle image: Adult male (5.8 cm) of cetomimid whalefish from Gulf of Mexico; photo G. David Johnson.
Lower image: Juvenile female (ca. 7-9 cm) of cetomimid whalefish Gyrinomimus from eastern North Pacific; photo Bruce Robison, courtesy of Monterey Bay Aquarium Research Institute.
Caption for individual figure
Tapetail postlarval stage (5.6 cm) of cetomimid whalefish off Kochi, Japan; photo Masanori Nakamachi, âSea fishes of Japanâ © YAMA-KEI Publishers Co., Ltd.

Cheers and keep up the good work!,

Dave

Dave, thanks for the praise and for the really, *really* cool study. And apols to John for leaving him out - just for stylistic reasons, I tend to focus on the first author, but obviously, that's not entirely fair in all cases. Good luck with the future work.

Ed,
Dave just passed me your blog and I wanted to thank you for putting this in both a form and forum that is so accessible.
We 'old farts' are most appreciative.
Best wishes, John

By John Paxton (not verified) on 21 Jan 2009 #permalink

Ed,

Thanks for your good job on our collaborative work! When I first found the identical sequences from Parataeniophorus (larva) and Cetostoma (female), Dave and John were very suspicious about my finding (mainly owing to a lack of voucher specimen). Subsequently they have found astonishing metamorphosis and proven that I was "correct." I am very happy to know that you enjoy the story!

Cheers,
Masaki

By Masaki Miya (not verified) on 21 Jan 2009 #permalink

so. cool.

This is so cool. I'm reading 'the origin' right now, and it's also asthonishing to see that Darwin already mentoined exactly these kinds of taxonomical problems and giving away the solution to the problemen (genealogy). To bad he didn't knew DNA.

That is amazing!

By Aphrodine (not verified) on 22 Jan 2009 #permalink

This might be a stupid question from an biology ignoramus:

But for what does the male need that much liver? Is that needed for sperm production?

nn: If I understand things correctly, the male doesn't feed once he reaches adulthood. It sounds as if the enlarged liver acts as an energy reserve, to keep the male going after he stops eating.

But of what benefit to the male is not eating?

Oh, loved the article. It's amazing how much we're still finding out about our own planet!

It's a distraction. One of the main challenges for deep-sea animals is finding a mate when the world around them is mostly empty and completely dark. Obviously, most species also need to find food too, which suffers from the same challenges and takes time away from the important business of getting it on. Take away the need to eat and you can focus your energies on finding a mate.

That's my assumption anyway - it's the same reason why the parasitic male anglerfish I mentioned earlier latch onto a mate permanently when they find her.

Maybe Dave, John or Masaki have their own theories?

Spot on, Ed! Nothing to add to that, really. Bulk up at the surface, and transform yourself into a pair of big testes and a big nose that has nothing to but try find a female before your liver runs out!
Incidentally, for whale of a story go to this URL ("As It Happens") and advance 16 minutes into the program.
Cheers,
Dave

By Dave Johnson (not verified) on 27 Jan 2009 #permalink

hey!!!!! seriously interesting to read.we have been knowing since ages that deep sea is a pandora's box but it wud reveal such secrets is really surprising.though a question mark in front of taxonomist, ur work is well done! thank you for the knowledge update.

By shruti.sawantdesai (not verified) on 29 Mar 2009 #permalink

Great post, and awesome to see the authors chime in like this as well. I love blogs!