Developmental Plasticity and the Origin of Tetrapods
When Polypterus senegalus, an air breathing fish, was raised on land it showed environmentally induced plasticity. Fish raised on land walk with a more effective gait and have changes in their pectoral anatomy that resemble some key evolutionary changes in fossil stem tetrapods. This data presents evidence that environmentally induced developmental plasticity may have been present in the stem tetrapods and facilitated their successful transition onto land.
Polypterus are an air breathing fish from Africa. When they were first discovered they sparked a good deal of evolutionary interest because of their true paired lungs and were reported to have the ability to leave the water moving between ephemeral pools. We chose Polypterus as our study species for several reasons. Most importantly, Polypterus has several important morphological characteristics that is shares with stem tetrapods, the group of fossil fishes that appear to have led to the evolution of land vertebrates. Like Eustenopteron, an Elpistostegid fish, Polypterus has an elongate body form, rhomboid scales, ventro lateral pectoral fins and functional lungs. Similarity of body form allows for biomechanical comparison between Polypterus and fossil stem tetrapods. In addition, Polypterus has an appropriate phylogenetic placesment. All fishes are divided into two major groups, the Actinopterygians (ray-finned fishes) and the Sarcopterygians (lobe finned fishes). Although there has been some debate about Polypteruses phylogenetic placement, most recently they are considered to be the most basal of the ray-finned fishes. In this way they are the most closely related ray-finned fish to the common fish ancestor that led to the evolution of tetrapods. Although there are two extant groups of lobe finned fishes, they are very rare or highly derived. For example lungfishes have highly specialized spaghetti like limbs and the Coelocanth is extrememly rare and lives at 200m and has not been recorded interacting with the substrate at all.
What did we do?
Our experiment raised Polypterus senegalus for 8 months in a moist terrestrial environment. Fish ‘walked’ around on a wetted platform in a few millimeters of water but not suspended. To keep the air moist a misting system, much like you see at the supermarket keeping the lettuce fresh, continually sprayed water over the fish. After the fish had experienced this environment for a sufficient amount of time they were tested for their walking and swimming performance and their pectoral anatomy was imaged using microCT to quantify differences in the development of their bones.
Fish raised on land appear to walk more effectively. Terrestrialized fish planted their fins closer to their body midline, lifted their heads higher off the ground and their fins slipped less during the step cycle. These changes represent what one would expect to minimize friction with the body and the ground and maximize support and forward propulsion overland.
Land raised fish also showed changes in their pectoral anatomy. Their cleithrum and clavicle contact strengthened, the clavicle elongated suggesting a more supportive role. The border of the cleithrum with the operculum reduced making more space between the head and body and the contact between the supracleithrum and the skull reduced suggesting more head and neck mobility. These changes mirror what is seen in the fossil record as fish became tetrapods.
Environmentally induced plasticity in extant animals relates to evolutionary processes. Behaviour cannot be found in the fossil record, by using an animal that has a similar morphology we can help predict how those fossilized animals may have moved when they were living. In addition, because the environmentally induced anatomical changes reflect what we see in the fossil record we can hypothesize that similar behavioural changes may also have been present in the fossil fishes. Currently there is lots of interest in how plasticity contributes to plant and animal evolution and this data shows that environmentally induced plasticity may have been present in the stem tetrapods allowing evolution to act on existing building blocks and explaining how complex changes may have occurred in a relatively short evolutionary period of time.