Mudskippers of the Tidal Mangrove Mudflats at the Sungei Buloh Wetland Reserve, Singapore

Habitats along the land-sea interphase provided the setting for evolution of vertebrate adaptations needed to move onto the land. Mangrove mudflats formed within the intertidal zone provide a fantastic array of habitat qualities that enable selection of amphibious traits. These gently sloping habitats can extend hundreds of meters between the land and the sea and are exposed to air on a regular basis following tides. The extensive root systems of the semi-aquatic mangrove trees stabilize the coasts, providing a dependable living space for specialized fish species like the amphibious Mudskippers.

Adaptations conferring the mobility on land and breathing air have evolved independently many times in fishes. For instance, in one of the earliest Devonian tetrapod fossils called “Tiktaalik”, the structural shift from fins to limbs shows a strikingly similar set of adaptations to those of Mudskippers. However, Mudskippers must have evolved these adaptations in a convergent fashion independently. Mudskippers belong to the goby family and are the largest group within the teleost fishes that have evolved to live an amphibious lifestyle. These googly-eyed fishes have accumulated an impressive set of amphibious adaptations that maximize their survival in mudflats. These include changes in refractive qualities of the eye which enhances aerial vision, higher ammonia tolerance associated to the anoxic burrow conditions, aerial respiration, immune responses against terrestrial pathogens, and land surface locomotion using pectoral fins. The genetic underpinnings of these adaptations have been elucidated by analysis of genome sequences from multiple Mudskipper fishes and evidence supported by gene expression studies.

Reversal of sex roles is a fascinating biological phenomenon seen in seahorses and pipefishes. In these fishes, males take over the fertilized eggs in their brood pouches and become pregnant. Paternal care in Mudskippers is another example for sex role reversal. Biologists are keenly interested in this type of reproductive strategy, because sexual selection continues to act on males after mating. Most of us are familiar with male characters evolved as a result of pre-mating selection such as the mane of lions or antlers of deer displaying male qualities. In Mudskippers, sexual selection operates continuously both before and after mating. Males not only have to fight for females, but also must be a successful father even after the eggs hatch. If you look closely, you can see the young fish swimming under the relative safety of their guarding father. It may take more than 50 days for the young fish to transition to amphibious life after hatching.

Observations made from inside the elusive mud burrows using endoscopic cameras developed for internal medicine have shown that males constantly assess the oxygen levels within the egg chamber. During low tides, while guarding the burrow, the male Mudskippers carry fresh air into the egg chamber in their mouths. They brood their eggs on the walls of burrows exposed to air, but allow the chamber to flood only when it is time for hatching.

Mudskippers provide a compelling anatomical demonstration for how fins became limbs. In Mudskippers, pectoral fins can propel the body of the fish similar to front wheel drive vehicles, and steer the springing action generated by the tail. The fin movements become evident during territorial aggressions among males. Some mudskipper species are carnivores and cannibalistic consumption of rival offspring is a possibility based on evidence from many other fish species in which males guard the nests.

Here, an opportunistic male makes an attempt to take over the nest of a resident. The resident male rushes back to intercept the intruder. The resident male immediately wallows in the pool covering his burrow entrance. The moisture of the skin is very important for cutaneous respiration which accounts up to 60 percent of the aerial respiration. In this way, he replenishes his reserves and gains strength before launching a counter attack to expel the intruder from his territory at an acceptable distance. Mudskippers are unique among fishes in that they carry out many of their key life activities on land. These include feeding, courting, and territorial defense. Their natural history provides a fantastic opportunity to observe how vertebrate adaptations may have evolved. Mudskippers help us draw parallels to understand our very own fish ancestor, which experienced similar pressures to transition to walk on land more than 380 million years ago during the Devonian Period.

References

Ishimatsu et al. 2007 Mudskippers brood their eggs in air but submerge them for hatching.
J. Exp.Biol. 210 (22): 3946-3954.

You et al. 2014 Mudskipper genomes provide insights into the terrestrial adaptations of amphibious fishes.
Nat. Commun. 5:5594.

Kim et al. 2021 Genetic adaptations in mudskipper and tetrapod give insights into their convergent water-to-land transition.
Animals, 11(2) 584.

Ziadi-Künzli et al. 2024 Anatomical insights into fish terrestrial locomotion: A study of barred mudskipper (Periophthalmus argentilineatus) fins based on μCT 3D reconstructions.
Journal of Anatomy 2024.