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Endgame for the fish model


For someone not familiar with the modern systematics of vertebrates, acanthomorphs are simple fishes. They are viewed as primitive beings possessing a simple anatomy and odd behaviours, their study being only worthy of interest for economic purposes or to understand the origin of “more complex” animals. Acanthomorphs are then considered as “awaiting” species, announcing future transformations ... leading of course to our species. In that perspective, when they do not announce us, they are considered as evolutionary dead-end species, some sort of culs-de-sac. Humorously, the American ichthyologist Gareth Nelson wrote in 1969 that if teleosteans had classified tetrapods, they would have considered them as terrestrial ... culs-de-sac !


Evolutionary stepping stones or culs-de-sacs, these visions are outdated... the “stepping stone” vision is in fact a scalist representation which would try to become evolutionist and where fishes were a link in a chain “going” to four-limbed vertebrates (tetrapods) and then to mammals and then to Man ... When this vision admits the existence of lateral branches, these ones are viewed as culs-de-sac, because they do not “go” to mammals. It is a manner to magnify our “evolutive destiny”. But our understanding of Evolution has radically changed, with no more stepping stones, no more culs de sac nor tops of the Evolution. Its representation is a tree of relationships, where species are equivalent and not reduced by the presence of other ones. 

Simplified tree of interrelationships between jawed vertebrates (= gnathostomes), modified from Chanet (1998).

Acanthomorphs and mammals are in different positions in this tree. They share a 420 millions years old common ancestor. From this ancestor, both groups diversified independantly, acquired original and new features (that is, innovations). Consequently, acanthomorphs and mammals share common characteristics inherited from the common ancestors, but both present peculiarities which have to be considered as specificities of each group, and not as rough shapes or drafts.

Among many features, acanthomorphs and mammals share :
a bilateral symmetry, inherited from their bilateria shared ancestor, around 680 millions years ago,
a rigid and dorsal body axis, inherited from their chordate shared ancestor, around 530 millions years ago,
a skull, inherited from their craniate shared ancestor, around 500 millions years ago,
vertebrae, inherited from their vertebrate shared ancestor, around 500 millions years ago,
- jaws and nervous fibers with a myelin sheat, inherited from their gnathostome shared ancestor, around 430 millions years ago,
- enchondral bone, inherited from their osteichthyan shared ancestor, around 420 millions years ago,
 

New structures in both groups

* Innovations in the skeleton

 

In mammals:

Each half-mandible of a mammal is composed by a single bone, the dentary.

Bony head of a young cow. Image: C. Guintard (ENVN).

In other gnathostomes, the half-mandible is composed of at least 2 bones: dentary and angulo-articular (see the page dedicated to the osteology of the tuna head).

  • In acanthomorphs :

The premaxilla of acanthomorphs possesses a developped ascendant process (as.pr)  associated to a large rostral cartilage (r.ca).

Premaxilla of Bodianus diplotaenia (Labridae). Image: S. Tercerie.
Rostral cartilage (r.ca, stained in blue) of a young turbot (Scophthalmus maximus, Scophthalmidae), after a Cleared & Stained protocole.
Image: F. Wagemans (Univ. Liège).
These two structures are only present in  acanthomorphs.

* Innovations in soft organs

Mammals are the sole animals to possess lacteal glands producing milk.

glandes lactéales d'une vache

in a cow (Bos taurus, Bovidae). Image: C. Guintard (ENVN).

In acanthomorphs, the palato-vomerine ligament — uniting the palatine to the vomer  — is divided in two independant ligaments , while there is only one in the other teleosteans.

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Ventral view of the vomer region of an acanthomorph.
Drawing: B. Chanet, modified from Stiassny (1986).
 
The blue structure (r.ca) is the rostral cartilage. Bones (pal : palatine and vo : vomer) are in white.
Palato-vomers ligaments  are  indicated in orange.
 

* Innovations in the  proteins

Four types  of hemoglobin exist in acanthomorphs, with the rare exception of the species with no hemoglobin.


A dozen of different hemoglobins exist in mammals.


* Innovations in the chromosomes

The caryotype of acanthomorphs is simpler than the caryotype of mammals. However, actinopterygians or ray-finned fishes — the clade to which acanthomorphs belong — underwent several events of complete duplications, with multiplications of the number of chromosomes.

Tetraodon nigroviridis (Tétraodontidés)Same phenomena occured in the genome. Even if there are some very compact genomes,  like the one of the green spotted puffer, Tetraodon nigroviridis (Tetraodontidae), many acanthomorphs have genome larger than mammals.


* Innovations in the genes controling developpment

The study of the developement of the pectoral fin of the zebrafish (Danio rerio, Cyprinidae) provided data to understand the molecular events occuring during the formation of this fin and the anterior limb of tetrapods. Similar genes play important roles in the developpment of both.

Recently, Zhang et al. (2010) demonstrated that some genes (actinodin) controling the formation of this fin are completely absent in tetrapods. The setting-up  of the pectoral fin appears to be more complex and more "controled" as to the number of implicated genes. 

Convergent features

Homeothermy — the ability to keep constant the body temperature— is the rule among mammals, with the exception of hibernating species such as the Alpine marmot (Marmotta marmotta, Sciuridae). But several acanthomorph species — like opah opah(Lampris guttatus, Lamprididae), bluefin tunaThunnus thynnus (Thunnus thynnus, Scombridae) and swordfish Xiphias gladius (Xiphias gladius, Xiphiidae) — have a warmer body (at least the temperature of the eyes and brain) . By this way, their internal temperature is constant and  higher than the water where they swim (Runcie et al., 2009). This ability appeared independantly at least three times in acanthomorphs (opah, tuna and swordfish are not closely related) and exists in some sharks as well.

Mammals are viviparous ! Yes ... but not all of them - platypus and echidnea lay eggs. On the other hand, acanthomorph species giving birth to live youngs are not so rare.

Seahorses (Syngnathidae) and several species of halfbeaks demi-becs(Hemiramphidae) are viviparous. In the eel pout, Zoarces viviparus loquette(Zoarcidae), embryos (from dozens to hundreds) develop in the body of the female and receive nutriments through materno-fetal exchanges. Gaz exchanges are even facilitated by the presence of a fetal hemoglobin with high affinity to O2. The same phenomena exist in  Embiotoca lateralis (Embiotocidae) as well.


poissons clowns
Drawing: B. Chanet.

Mammals take care of their youngs ! But so do numerous acanthomorph species !
Several species of tilapias (Cichlidae) protect their eggs and youngs by keeping them in their mouth (image to the right). Many species, like clownfishes (Pomacentridae)combattants or fighting fishes (Osphronemidae, left image) take care, protect and provide O2 to their eggs.

Image: B. Chanet



Conclusion

The study of acanthomorphs can help to understand the biology of mammals: some features illuminate several characteristics - the study of the first steps of the development of vertebrates for instance -. But acanthomorphs are not  simply models to understand the biological features of some animals falsely considered to be more evolved. Studying their biology, at every level from ecosystems to molecules, is fundamental to understand the biodiversity around us. We have to consider them not as relics, but as organisms which have undergone a different path in evolution, a path as long as and as complex as the one of mammals and all living beings.


References

  • Mank, J.E. et J. C. Avise (2006). Cladogenetic correlates of genomic expansions in the recent evolution of actinopterygiian fishes.Proc. R. Soc. (B), 273 : 33-38.
  • Nelson, G.J. (1969). Origin and diversification of teleostean fishes. Annals of the New York Academy of Sciences, 167(1):18-30.
  • Runcie, R.M., Dewar H., Hawn D.R., Frank L.R. et K.A. Dickson (2009). Evidence for cranial endothermy in the opah (Lampris guttatus). The Journal of Experimental Biology, 212: 461-470.
  • Stiassny, M.L.J. (1986). The limits and relationships of the acanthomorph teleosts. J. Zool. (B) 1 : 411-460.
  • Zhang J., Wagh P., Guay D., Sanchez-Pulido L., Padhi B.K., Korzh V., Andrade-Navarro M.A. et M.A. Akimenko (2010). Loss of fish actinotrichia proteins and the fin-to-limb transition. Nature, 466(7303) :234-7.