Tadpole eyes swivel and cross during metamorphosis

Abstract

The changes that most animals experience during the transition from juvenile to adulthood can be disruptive and inconvenient, but pale into insignificance in comparison with the drastic metamorphosis that amphibians undergo. Denis Combes and colleagues from the University of Bordeaux, France, and the Ludwig-Maximilians-University Munich, Germany, describe how metamorphosing tadpoles have to adapt from a wriggling swimming style to a forward thrusting motion with each kick of their newly emerged hind legs. However, this transition is also accompanied by a change in the tadpoles’ vision. Wriggling tadpoles swivel their eyes in the opposite direction from their weaving bodies to hold their view of the world steady, while kicking froglets cross their eyes in time with each kick to maintain their view of objects as they appear to loom when the tiny amphibians surge forward. The nerve signals that drive these eye movements are coordinated by the signals that control the respective swimming movement, so Combes and his colleagues Géraldine von Uckermann, François Lambert, Hans Straka and John Simmers wondered how Xenopus tadpoles maintain gaze control during the critical transition period from one swimming style to the other.The team recorded the nerve signals controlling the eye movements and swimming muscles of tadpoles, in addition to filming the motion of the tadpoles’ eyes, at various stages of metamorphosis. After analysis of the nerve signal patterns, they discovered that the eye control signals gradually shift from regulating the eyes as they swivel to coordinating both swivelling and looming eye movement patterns simultaneously, until the eye swivel pattern dwindles away and the tadpoles switch exclusively to converging the eyes as they kick-swim at the end of the metamorphosis. The team also realised that the nerve signal pattern that coordinates the eye movements with the swimming action switches gradually from the signals that control the wriggling swim to those driving the adult-style leg kick, allowing the tadpole to transition seamlessly from one lifestyle to the other.