Gill remodelling during terrestrial acclimation in the amphibious fish Polypterus senegalus

Abstract

Fishes are effectively weightless in water due to the buoyant support of the environment, but amphibious fishes must cope with increased effective weight when on land. Delicate structures such as gills are especially vulnerable to collapse and loss of surface area out of water. We tested the ‘structural support’ hypothesis that amphibious Polypterus senegalus solve this problem using phenotypically plastic changes that provide mechanical support and increase stiffness at the level of the gill lamellae, the filaments, and the whole arches. After 7 d in terrestrial conditions, enlargement of an inter‐lamellar cell mass filled the water channels between gill lamellae, possibly to provide structural support and/or reduce evaporative water loss. Similar gill remodelling has been described in several other actinopterygian fishes, suggesting this may be an ancestral trait. There was no change in the mechanical properties or collagen composition of filaments or arches after 7 days out of water, but 8 months of terrestrial acclimation caused a reduction in gill arch length and mineralized bone volume. Thus, rather than increasing the size and stiffness of the gill skeleton, P. senegalus may instead reduce investment in supportive gill tissue while on land. These results are strikingly similar to the evolutionary trend of gill loss that occurred during the tetrapod invasion of land, raising the possibility that genetic assimilation of gill plasticity was an underlying mechanism.

Plastic loss of motile cilia in the gills ofPolypterusin response to high CO2or terrestrial environments

“…Considering that the cilia play essential roles in efficient respiration, excretion of the carbon dioxide, etc ., it makes sense that cilia disappear under conditions where water is unavailable. Previous studies have revealed a reduction in the volume of mineralized bone in the internal gills after 8 months of rearing on land, suggesting that Polypterus may reduce investment in its internal gills when in a terrestrial environment (Turko et al, 2019). Importantly, the loss and regeneration of the cilia are plastic in response to the environmental change (Fig.…”

Terrestrial acclimation and exercise lead to bone functional response inPolypteruspectoral fins

“…This would be consistent with a hypothesis that fin bones exhibit adaptive plasticity in response to gravitational loading. A stiffening effect of terrestrial acclimation has also been demonstrated in the gill arches of the amphibious mangrove rivulus (although, interestingly, not in Polypterus) (Turko et al, 2017(Turko et al, , 2019. Conversely, the increased length of bones potentially reduces their strength in bending.…”

Evolutionary and cardio‐respiratory physiology of air‐breathing and amphibious fishes

“…The loss of buoyancy in the air also impacts gill structures. Gill remodelling in two amphibious species, K. marmoratus and bichir, Polypterus senegalus , involved an increase in the height of the interlamellar mass, which was associated with a reduced gill surface area in air‐acclimated fish, possibly to fortify delicate lamellar structures or to reduce water loss. As well, air exposure stiffened the gill skeleton of K. marmoratus with increased expression of proteins responsible for bone mineralization and more densely packed collagen fibrils in gill arches and filaments .…”