Shark gill slits: their genesis and multiple coverups with an operculum

Dolce and Wilga 2013 wrote about gill slits in sharks,
“One of the defining characteristics of Elasmobranchii is the external gill slits, through which water is expelled during exhalation.

Starting off with this “Pulling a Larry Martin“ (defining a clade based on a short list of traits rather than a last common ancestor) is not a good way to start, even if this statement is more than ninety per cent true.

“The evolution of gill slit morphology and the relationship to behavior and ecology is not clear.

Dolce and Wilga only studied traditional extant sharks. Missing from their study are all fossil taxa, a non-shark outgroup taxon, all rays, skates, paddlefish and ratfish. In the large reptile tree (LRT, 2181 taxa) Entelognathus (Fig 1) is the non-shark outgroup taxon and the above listed taxa, some with opercula (paddlefish and ratfish).

“The relative length of each slit, relative distance between adjacent pairs of slits, and number of slits positioned over the pectoral fin were quantified in 289 preserved specimens representing 185 species in 69 genera, 28 families, and 8 orders of sharks.

That’s indeed a large number, but still a restricted cherry-picked gamut because it does not include the several clade members listed above.

“Six character states of relative gill slit length, five character states of relative inter-gill slit spacing, and five gill slit positions over the pectoral fin were identified. Character mapping onto a phylogeny reveals that the basal state for extant Selachii is to possess slits of similar relative length and spacing with no slits over the pectoral fin.

Adding taxa, including fossil taxa, should confirm, refute or modify this conclusion.

“Multiple character states in various combinations evolved within the Carcharhiniformes, which is the most speciose extant group. Ontogenetic differences in gill slit morphology were found in the 12 genera in which adult and juvenile data were collected.

To the extent of their chosen taxon list, this was indeed an all inclusive study. Nevertheless, the LRT indicates taxon exclusion was an issue in Wilga and Dolce.

“Macropelagic types are ram ventilators with a longer first slit length, similar slit spacing in most, and no slits over the pectoral fin. Most littoral types are ram ventilators, with decreasing slit length and spacing and with one slit over the fin. Benthic types are suction ventilators with decreasing slit length and spacing and up to four slits over the fin. Bathic and micropelagic types are suction ventilators with no slits over the fin and most having similar slit length and spacing.”

Missing are taxa with gill slits below the pectoral fins and those with opercula. This was made possible by using invalidated analyses that united all rays with all skates under the clade Batoidea. The LRT does not support the monophyly of the traditional Batoidea.

Let’s start over with Entelognathus to recover the origin of gill slits
This late Silurian traditional placoderm, nests in the LRT at the base of the shark, ray, ratfish, paddlefish clade, aka the Chondrichthyes. Entelognathus is the last common ancestor and it lacks gill slits. Instead all respiration takes place in the skull = atrium with a single hard, slit-like opening over the pectoral fins for water exhalation.

Also from the Late Silurian, Loganellia
(Fig 1) appears to document several gill slits posterior to the hyomandbular arch and above the pectoral fins. This arrangement is confirmed in Middle Devonian Gladbachus (Fig 1). Larger taxa with less surface area-to-volume ratio seemingly require improved respiration because deeper tissues become further separated from surrounding oxygenated waters as overall size increases.

Paddlefish opercula
In the LRT ocean-going basking sharks (Cetorhinus) are closely related to river-dwelling paddlefish (Polyodon ). The former has the largest gill slits of all. The latter covers their similar large multiple gill slits with an elongate operculum (Fig 2, see video here). According to Ohio State University, “Another distinct feature is a long operculum flap which may aid in protecting the gills while feeding. Their skin is smooth and isn’t scaled, resembling that of a shark. Like sharks, they have a cartilaginous skeleton that consists mostly of a spinal cord and lack bones.”

University textbooks ally spoonbills with sturgeons.
The LRT does not support that hypothesis of interrelationships.

Another subclade within the Chondrichthyes is the Chimaeridae
This clade (Fig 4) also has a gill cover, or operculum, but it is not supported by bone, as in bony fish.

Yet another clade within Chondrichthyes: the Iniopterygidae,
also had an operculum covering the narrow area between the skull and pectoral girdle. This clade included member genera like Gregorius and Iniopteryx.

Gill slits below the pectoral fins
Several bottom-dwelling members of the Chondrichthyes (sawfish, guitarfish, rays, skates, torpedoes and the manta ray all have gill slits below the enlarged pectoral fins, all converging with each other an converging with an osteostracan morphology.

Nesting very near the split
of Chondrichthyes and Placodermi, but on the bony fish clade, is the spiny shark, Brachyacanthus (Fig 5). This tiny fish has two sets of gills, one above the other. The more dorsal set are like those of a shark, arranged serially with several openings. The more lateral set are covered with a single operculum or gill cover, as in bony fish.

References
Dolce JL and Wilga CD 2013. Evolutionary and Ecological Relationships of Gill Slit Morphology in Extant Sharks. Bulletin of the Museum of Comparative Zoology 161(3), 79-109. https://doi.org/10.3099/MCZ2.1

wiki/Chondrichthyes
wiki/Gill_slit
wiki/Operculum_(fish)