External gills: first appearance, radiation, disappearance

Curiosity drove this blogpost.
Where did external gills first appear? How widespread are external gills?

According to Wilkipedia:
“External gills are exposed to the environment, rather than set inside the pharynx and covered by gill slits, as they are in most fishes. The respiratory organs are set on a frill of stalks protruding from the sides of an animal’s head.”

Figure 1. Hemidactylum scutatum larval amphibian. Note the several (3 tan gills per side) external gills, plus that blue one on the left.

The first chordates,
lancelets like Branchiostoma, have internal gills as juveniles and adults. Sturgeon and their larvae, like Acipenser, have internal gills.

Larvae of the banded houndshark
(Triakis) have poorly organized external gills (Fig 2) prior to hatching, still attached to their yolk sac.

Figure 2. External gills appear in taxa from sharks to amphibians.

According to NotesOnZoology.com:
“External gills, though rare in fishes, are found in some larval forms of lampreys, Polypterus (bichir) has one pair of external gills. Dipnoi (Lepidosireri) have four pairs of filamentous external gills attached to the outer edges of the branchial arches.”

Figure 3. Lamprey embryo. Arrow points to possible external gills. Still not sure. Larvae do not have external gills. They have seven shark-like tall gill slits. Adults reduce these gill slits to small circular openings.

Larval and neotonic adult amphibians,
like Hemidactylum scutatum (Fig 1) display the most commonly known examples of external gills. Larval fish close to the fin-to-finger transition also have external gills (Figs 2, 4). Examples include Polypterus (Fig 2), the extant Nile bichir with one large pair of external gills.

Figure 3. Polypterus adult and larval forms. 1 pair of external gills are present in the juvenile, completely absent in the adult. This may be the post primitive example of external gills. Phylogenetically this grade of taxa was present in the Early Devonian, perhaps Late Silurian.

Polypterus bichir
(Geoffroy Saint-Hilaire 1802) is the extant Nile bichir. Given that it breathes air and can walk on land, early scientists were unsure whether this was a fish or an amphibian, then later unsure whether this was a crossopterygian or an actinopterygian. Here it nests between the Early Devonian dipnomorph, Powichthys and the mid-Devonian tetrapodomorphs, the lobefins that eventually developed fingers and toes.

Stundi et al. 2019 reported,
“This type of gill is most commonly observed on the aquatic larva of most species of salamanders, lungfish, and bichirs (which have only one large pair), and are retained by neotenic adult salamanders and some species of adult lungfish. They are present on non-transforming salamander species, such as most members of the family Proteidae (the olm and mudpuppies) and the family Sirenidae, which naturally never metamorphose into an air-breathing form.”

“The embryos of frogs and caecilians also develop external gills at some point in their development, though these are either resorbed before or disappear shortly after hatching. Fossils of the distant relatives of modern amphibians, such as Branchiosaurus and Apateon, also show evidence of external gills.”

Figure 1. Apateon overall and the skull in palatal and dorsal views. This taxon nests between Doleserpeton and Gerobatrachus in the LRT.
Figure 4. Apateon overall and the skull in palatal and dorsal views.

“The external gills commonly consist of a single stalk (rami) protruding from a gill arch behind the head of the animal, above an associated gill slit. The stalk usually contains muscle tissue, and may be moved by the animal as a free appendage, in order to stir up stagnant water. The stalk is lined by many thinly walled filaments (fimbriae), containing the majority of blood vessels used in gas exchange. Animals usually have one external gill originating on each gill arch (except the hyoid), which leads to there being three pairs of external gills in salamanders, and four in the gilled larvae of lungfish.”

“Polypterid bichirs represent the earliest diverged living group of ray-finned (Actinopterygian) fishes and they are often referred to as the most relevant species for studying character states at the dichotomy of ray- and lobe-finned fishes.”

The large reptile tree (LRT, 2155 taxa) does not recover that relationship. Bichirs are not the earliest diverging living group of ray-finned fish in the LRT, but among the latest, just before the fin-to-finger transition.

“This places bichirs in a unique phylogenetic position among vertebrates, which can be exploited for evolutionary and developmental comparative studies. Adult bichirs possess several intriguing characteristics that have been associated with air-breathing during the transition from water to land, such as ventral paired lungs or spiracular openings on the head. Moreover, bichirs also share several key larval features with lungfishes or amphibians, such as cranial adhesive organs, and larval external gills.”

That’s because bichirs are closely related to taxa in the fin-to-finger set of transitional taxa in the LRT.

“The external gills of bichirs represent prominent adaptive structures, and constitute major breathing organs of their free-living embryos and early larvae. Strikingly, while external gills of amphibians and lungfishes derive from branchial arches as a rule, those of bichirs have historically been considered as unique hyoid arch derivatives due to their blood supply from the hyoid aortic arch. Importantly, the external gills of bichir embryos represent the first cranial structures to appear, emerging before the eyes or mouth are evident.”

Stundi J et al.(8 co-authors) 2019. Bichir external gills arise via heterochronic shift that accelerates hyoid arch development. eLife 8:e43531. https://doi.org/10.7554/eLife.43531



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