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Deep-sea mystery solved: astonishing larval transformations and extreme sexual dimorphism unite three fish families.

Johnson GD, Paxton JR, Sutton TT, Satoh TP, Sado T, Nishida M, Miya M - Biol. Lett. (2009)

Bottom Line: Morphological and behavioural specializations necessary to occupy such contrasting environments have resulted in remarkable developmental changes and life-history strategies.Females have huge gapes with long, horizontal jaws and specialized gill arches allowing them to capture larger prey.Males cease feeding, lose their stomach and oesophagus, and apparently convert the energy from the bolus of copepods found in all transforming males to a massive liver that supports them throughout adult life.

View Article: PubMed Central - PubMed

Affiliation: Division of Fishes, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA. johnsond@si.edu

ABSTRACT
The oceanic bathypelagic realm (1000-4000 m) is a nutrient-poor habitat. Most fishes living there have pelagic larvae using the rich waters of the upper 200 m. Morphological and behavioural specializations necessary to occupy such contrasting environments have resulted in remarkable developmental changes and life-history strategies. We resolve a long-standing biological and taxonomic conundrum by documenting the most extreme example of ontogenetic metamorphoses and sexual dimorphism in vertebrates. Based on morphology and mitogenomic sequence data, we show that fishes currently assigned to three families with greatly differing morphologies, Mirapinnidae (tapetails), Megalomycteridae (bignose fishes) and Cetomimidae (whalefishes), are larvae, males and females, respectively, of a single family Cetomimidae. Morphological transformations involve dramatic changes in the skeleton, most spectacularly in the head, and are correlated with distinctly different feeding mechanisms. Larvae have small, upturned mouths and gorge on copepods. Females have huge gapes with long, horizontal jaws and specialized gill arches allowing them to capture larger prey. Males cease feeding, lose their stomach and oesophagus, and apparently convert the energy from the bolus of copepods found in all transforming males to a massive liver that supports them throughout adult life.

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(a) ML tree derived from analyses of whole mitogenome sequences from 15 specimens using RAxML v. 7.0.4. Numerals beside internal branches indicate bootstrap values (only 50% and above are shown) based on 1000 replicates. Scale indicates expected number of substitutions per site; red asterisks, larvae; blue asterisk, male. Long-finned whalefish C. regani Zugmayer, 1914: (b) USNM 391563; (c) MCZ 60609 (inset, enlarged nasal organ); (d) BMNH 1957.7.20.1.00, holotype of P. gulosus (inset, elongate nasal rachis); (e) USNM 392646; (f) USNM 391656. Photo courtesy of S. Raredon and G.D.J.
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fig2: (a) ML tree derived from analyses of whole mitogenome sequences from 15 specimens using RAxML v. 7.0.4. Numerals beside internal branches indicate bootstrap values (only 50% and above are shown) based on 1000 replicates. Scale indicates expected number of substitutions per site; red asterisks, larvae; blue asterisk, male. Long-finned whalefish C. regani Zugmayer, 1914: (b) USNM 391563; (c) MCZ 60609 (inset, enlarged nasal organ); (d) BMNH 1957.7.20.1.00, holotype of P. gulosus (inset, elongate nasal rachis); (e) USNM 392646; (f) USNM 391656. Photo courtesy of S. Raredon and G.D.J.

Mentions: Excellent new Gulf of Mexico megalomycterid specimens with closing-net data that placed them together with the cetomimids at 1500–2000 m depth led us to re-examine the problem. We discovered that the holotype and only known specimen of the megalomycterid Megalomycter teevani is actually a transforming mirapinnid, as evidenced by the remains of three small pelvic-fin rays, a slightly oblique mouth, a gut full of copepods and still-developing nasal organ anlagen. Subsequently, we found that the holotype of Parataeniophorus gulosus (figure 2d), one of the few mirapinnids collected at depths greater than 200 m, is in a similar, but earlier, state of transition. The identity of mirapinnids as larval megalomycterids was thus established. Fortuitously, a transforming specimen of the cetomimid long-finned whalefish Cetostoma regani (figure 2e) was captured shortly thereafter.


Deep-sea mystery solved: astonishing larval transformations and extreme sexual dimorphism unite three fish families.

Johnson GD, Paxton JR, Sutton TT, Satoh TP, Sado T, Nishida M, Miya M - Biol. Lett. (2009)

(a) ML tree derived from analyses of whole mitogenome sequences from 15 specimens using RAxML v. 7.0.4. Numerals beside internal branches indicate bootstrap values (only 50% and above are shown) based on 1000 replicates. Scale indicates expected number of substitutions per site; red asterisks, larvae; blue asterisk, male. Long-finned whalefish C. regani Zugmayer, 1914: (b) USNM 391563; (c) MCZ 60609 (inset, enlarged nasal organ); (d) BMNH 1957.7.20.1.00, holotype of P. gulosus (inset, elongate nasal rachis); (e) USNM 392646; (f) USNM 391656. Photo courtesy of S. Raredon and G.D.J.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2667197&req=5

fig2: (a) ML tree derived from analyses of whole mitogenome sequences from 15 specimens using RAxML v. 7.0.4. Numerals beside internal branches indicate bootstrap values (only 50% and above are shown) based on 1000 replicates. Scale indicates expected number of substitutions per site; red asterisks, larvae; blue asterisk, male. Long-finned whalefish C. regani Zugmayer, 1914: (b) USNM 391563; (c) MCZ 60609 (inset, enlarged nasal organ); (d) BMNH 1957.7.20.1.00, holotype of P. gulosus (inset, elongate nasal rachis); (e) USNM 392646; (f) USNM 391656. Photo courtesy of S. Raredon and G.D.J.
Mentions: Excellent new Gulf of Mexico megalomycterid specimens with closing-net data that placed them together with the cetomimids at 1500–2000 m depth led us to re-examine the problem. We discovered that the holotype and only known specimen of the megalomycterid Megalomycter teevani is actually a transforming mirapinnid, as evidenced by the remains of three small pelvic-fin rays, a slightly oblique mouth, a gut full of copepods and still-developing nasal organ anlagen. Subsequently, we found that the holotype of Parataeniophorus gulosus (figure 2d), one of the few mirapinnids collected at depths greater than 200 m, is in a similar, but earlier, state of transition. The identity of mirapinnids as larval megalomycterids was thus established. Fortuitously, a transforming specimen of the cetomimid long-finned whalefish Cetostoma regani (figure 2e) was captured shortly thereafter.

Bottom Line: Morphological and behavioural specializations necessary to occupy such contrasting environments have resulted in remarkable developmental changes and life-history strategies.Females have huge gapes with long, horizontal jaws and specialized gill arches allowing them to capture larger prey.Males cease feeding, lose their stomach and oesophagus, and apparently convert the energy from the bolus of copepods found in all transforming males to a massive liver that supports them throughout adult life.

View Article: PubMed Central - PubMed

Affiliation: Division of Fishes, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA. johnsond@si.edu

ABSTRACT
The oceanic bathypelagic realm (1000-4000 m) is a nutrient-poor habitat. Most fishes living there have pelagic larvae using the rich waters of the upper 200 m. Morphological and behavioural specializations necessary to occupy such contrasting environments have resulted in remarkable developmental changes and life-history strategies. We resolve a long-standing biological and taxonomic conundrum by documenting the most extreme example of ontogenetic metamorphoses and sexual dimorphism in vertebrates. Based on morphology and mitogenomic sequence data, we show that fishes currently assigned to three families with greatly differing morphologies, Mirapinnidae (tapetails), Megalomycteridae (bignose fishes) and Cetomimidae (whalefishes), are larvae, males and females, respectively, of a single family Cetomimidae. Morphological transformations involve dramatic changes in the skeleton, most spectacularly in the head, and are correlated with distinctly different feeding mechanisms. Larvae have small, upturned mouths and gorge on copepods. Females have huge gapes with long, horizontal jaws and specialized gill arches allowing them to capture larger prey. Males cease feeding, lose their stomach and oesophagus, and apparently convert the energy from the bolus of copepods found in all transforming males to a massive liver that supports them throughout adult life.

Show MeSH
Related in: MedlinePlus