The Teleost Fuse

A while back, I discussed the group of fish known as the Holostei, the gars and bowfin. The Holostei constitute one branch of the clade Neopterygii which includes the majority of living ray-finned fishes. However, their success in the modern environment pales in comparison to that of their sister group, the Teleostei.

Siemensichthys macrocephalus, an early teleost of uncertain affinities, copyright Ghedoghedo.

Teleosts are such a major component of ray-finned fishes that it is simpler to list those members of the modern fauna that do not belong to this clade: the aforementioned gars and bowfin, sturgeons and paddlefish, and the bichirs of Africa. Everything else belongs to the great teleost radiation, representing about 96% of all modern fishes. The earliest fishes generally recognised as teleosts come from marine deposits of the Late Triassic in the form of the Pholidophoridae of Europe. The earliest known members of the crown group are from the Late Jurassic (Nelson et al. 2016). Teleosts have been recognised as an apomorphy-defined clade; the crown clade has been dubbed the Teleocephala. Among the features that have been used to define the Teleostei are the presence of a mobile premaxilla. In my previous post, I explained how the mobile maxilla of neopterygians including bowfins improved feeding by creating suction when the mouth was opened. Having both the maxilla and premaxilla mobile enhances this process further. In some of the most advanced teleosts, such as dories and ponyfish, the connection between the jaws and the cranium is entirely comprised of soft, flexible tissue, allowing the jaw apparatus as a whole to be catapulted towards unwary prey. Other features that have been highlighted include a strongly ossified caudal skeleton with long uroneural spines derived from the neural arches of the vertebrae, and the lower lobe of the caudal fin supported by two plate-like hypural bones articulating with a single vertebral centrum (Bond 1996).

Leptolepis coryphaenoides, one of the earliest teleosts with cycloid scales, copyright Daderot.

Of course, not all these features necessarily appeared in lock with each other. A phylogenetic analysis of basal teleosts by Arratia (2013) identified the aforementioned features of the caudal skeleton as absent in some of the basalmost teleosts. The condition of the premaxilla is ambiguous in Prohalecites, the earliest stem-group teleost from the Middle-Late Triassic boundary. It appears to be absent in the Aspidorhynchiformes and Pachycormiformes, Mesozoic orders that are currently regarded as on the teleost stem but not part of the Teleostei. However, as was found with the mobile maxilla in gars, one can't help wondering whether this character has been affected by the uniquely derived upper jaw morphologies in these orders. Other features identified by Arratia (2013) as supporting the Teleostei clade include the presence of two supramaxillary bones, a suborbital bone between the posterior margin of the posterodorsal infraorbitals and the anterior margin of the opercular apparatus (subsequently lost in the teleost crown group), and accessory suborbital bones ventrolateral to the postorbital region of the skull roof.

The earliest teleosts in the Pholidophoridae and other basal lineages retained the heavy ganoid scales of thick bone that may still be seen in modern Teleostei. Lighter, thinner cycloid scales first appear with the Early Jurassic Leptolepis coryphaenoides (Arratia 2013) and are the basal scale type for the teleost crown group (in some derived subgroups, the scales would become further modified or even lost). The greater mobility permitted by these lighter scales may have been another significant factor in the teleost explosion. By the Cretaceous period, stem-teleosts had radiated into a variety of specialised forms such as the gigantic predatory Ichthyodectiformes (of which Xiphactinus grew up to four metres in length) and the deep-finned Araripichthys. The three major subgroups of the crown Teleostei—the Elopomorpha, Osteoglossomorpha and Clupeocephala—had diverged from each other by the end of the Jurassic. The stem-teleosts would disappear with the end of the Mesozoic; the crown teleosts would dominates the world's waters from that time on.

REFERENCES

Arratia, G. 2013. Morphology, taxonomy, and phylogeny of Triassic pholidophorid fishes (Actinopterygii, Teleostei). Journal of Vertebrate Paleontology 33 (6 Suppl.): 1–138.

Nelson, J. S., T. C. Grande & M. V. H. Wilson. 2016. Fishes of the World 5^th ed. Wiley.

To Drop Jaw or Not?

The vast majority of living ray-finned fishes (that is, all of them except for bichirs, sturgeons and paddlefishes) fall under the auspices of the clade Neopterygii. I have commented on this clade in earlier posts and in those posts I have noted that modern neopterygians can theselves be divided between three basal lineages. By far the largest of these is the teleosts with only a handful of species representing the other two: the seven or so species of gar in the Lepisosteidae, and the phylogenetically isolated bowfin Amia calva. However, the exact relationships between these three lineages have been the subject of debate.

Close-up on bowfin Amia calva head, from Big Fishes of the World. Note the membranous attachment of the back of the upper jaw.

Historically, the bowfin and the gars were recognised as a group Holostei in apposition to the Teleostei. When first established, this division was motivated primarily by the nature of their scales: the heavy, solid scales of the holosteans contrasted with the thinner, lighter scales of the teleosts. Hence the name 'Holostei' meaning 'entirely bone': the holosteans have both a completely bony skeleton on the inside (as opposed to the partially cartilaginous skeletons of more basal fishes) and a complete covering of bony scales on the outside. However, the heavy scales of the Holostei are a primitive feature, indicating that the two lineages diverged before the evolution of the lighter teleost scales but not indicating a direct relationship with each other.

With the increasing emphasis on evolutionary relationships as the primary informer of classifications, a different system was proposed. This saw the gars as the most divergent lineage of the Neopterygii with the bowfin being united with the teleosts as a clade Halecostomi. This time, the primary evidence for this division was in how their jaws worked. The ancestral condition for vertebrate jaws has them working much as our own still do. The upper jaw, the maxilla, is largely fixed in place against the base of the neurocranium (the brain-holding bit) while the movement of opening and closing the mouth is achieved by the lower jaw, the mandible, pivoting around its hinge towards the back of the skull. In the bowfin and teleosts, however, the maxilla is hinged with the skull at its anterior end and with the mandible at the back. When the mouth opens, the maxila pivots downwards from this anterior hinge, dropping the mandible as a whole downwards. The bowfin and teleosts also possess a bone in the cheek, the interopercular bone, that is not found in other fishes; a muscle attached to this bone rotates the gill operculum as the mouth opens (Lauder 1980). Functionally, the expansion of the mouth cavity in this manner of opening the jaws creates a suction that pulls prey or other food into the fish's mouth.

Though it was by no means universally accepted, it is probably fair to say that the halecostomes vs gars picture of neopterygian evolution became the majority view. But then came the advent of molecular phylogenetic analysis, all ready and willing to cast the proverbial spanner. Rather than confirming halecostome monophyly, molecular analyses pointed the other way, back towards a clade of the bowfin and gars. Following this, a detailed study of gar systematics published by Grande (2010) also supported a gar plus bowfin monophylum on morphological grounds and resurrected the concept of Holostei (albeit redefined on phylogenetic grounds).

Skull of a longnose gar Lepisosteus osseus, from Grande (2010). In the lower diagram, the maxilla is labelled 'mx' and the lacrimomaxillaries are labelled 'lmx'.

Gar jaws, it should be noted at this point, are a bit weird. Rather than being primarily composed of a single maxilla on each side, the upper jaws are made up of a series of tooth-bearing bones, each bone carrying just a few teeth, that have been dubbed the lacrimomaxillaries. When the jaws open, as well as the lower jaw opening in the standard manner, the flexible upper jaw also bends upwards. Rather than using suction to draw in their food like other neopterygians, gars capture prey by sneaking up to it then using a quick sideways jerk of the head to bring the open jaws around the prey (Lauder 1980). Gars were excluded from the Halecostomi on the basis of their lack of a long, mobile maxilla but, as explained by Grande (2010), a mobile maxilla is indeed present in gars but reduced to a remnant splint at the back of the jaw (in mature alligator gars Atractosteus spatula, the maxilla does not ossify). In very young juvenile gars, the mobile maxilla remains a significant part of the upper jaw with the lacrimomaxillaries being added in front of it as the jaw lengthens. As for the interopercular, this is genuinely absent in modern gars but it is present in close fossil relatives of gars such as semionotids. Rather than retaining a primitive jaw structure that was superseded in the bowfin and teleosts, it appears that gars evolved their own derived jaw structure from 'halecostome' ancestors.

Given that suction-assisted feeding is generally regarded as a major advance in fish evolution, how did gars end up abandoning it? That I can only speculate about. Is it related to the evolution of their elongate rostra? Long beaks are certainly a thing for a number of teleosts, but I don't know if any have a beak as long and robust as a gar's. Could it be that the greater precision of gars' snapping mode of feeding is an advantage in the low-oxygen, muck-filled waters in which gars thrive? Or could it be a side effect somehow of gars' more heavily armoured condition than other early-diverging neopterygians?

It's only fair to note that monophyly of Holostei is still not universally accepted; there are sill researchers who are inclined to think the bowfin closer to teleosts. But even if the 'Halecostomi' hypothesis was to rise once more to the surface, it would not be for the same reasons it did before.

REFERENCES

Grande, L. 2010. An empirical synthetic pattern study of gars (Lepisosteiformes) and closely related species, based mostly on skeletal anatomy. The resurrection of Holostei. Copeia 2010 (2A): iii–x, 1–871.

Lauder, G. V., Jr. 1980. Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. Journal of Morphology 163: 283–317.